Follow-up of the NICU Patient 

Updated: Jun 22, 2021
Author: Naomi F Lauriello, MD; Chief Editor: Ted Rosenkrantz, MD 

Overview

In developed countries, follow-up for neonatal intensive care unit (NICU) patients is commonly performed at designated clinics.[1, 2] From their inception, NICU-related follow-up clinics have focused on outcomes of premature infants. Some clinics perform follow-up for medical conditions (eg, bronchopulmonary dysplasia,[3] posthemorrhagic hydrocephalus); however, the intent in all NICU-related clinics is to determine neurodevelopmental outcomes. (For example, some evidence suggests potential risk factors for autism in children who require NICU stays.[4] Separately, there may be an association between inotrope use and neurodevelopment outcomes [higher risk for sensorineural or mixed hearing loss] in preterm infants [< 29 weeks’ gestation]).[5] Many clinics do both, especially if the institution is part of a research network.[6, 7]

The intent of the NICU-related follow-up should be several-fold. Less-than-acceptable outcomes may result in practice changes within individual NICUs. Most importantly, professionals in the clinic should direct "NICU graduates" to appropriate rehabilitative or social services if they are not aligned with optimal care in their community.[8]

The growth of NICU-related follow-up clinics reflects the increase in a population of infants with complex needs.[9] Currently, many neonates born prematurely or term infants with major malformations or perinatal hypoxic insult survive, whereas just a few decades ago, neonates born with these birth defects died.

At the same time, pediatricians and family practitioners have less experience with the advances in NICU care than they did 2-3 decades ago. In addition, current clinical training schedules give pediatric and family practice house staff only limited time to spend in the follow-up care of NICU graduates. The evaluation of preterm and term infants with complex conditions requires the involvement of professionals from multiple medical, rehabilitative, psychological, and social-service subspecialties.[10, 11]

Follow-up of extremely low-birth-weight infants (ELBW), who have a birth weight of less than 1000 g, from infancy to adulthood has revealed subtle neurodevelopmental problems that require evaluations and interventions that are more complex than previously appreciated.[12, 13, 14, 15] A retrospective analysis of information on ELBW infants from the National Institutes of Child Health and Human Development revealed that these patients have high use of special outpatient services, and efforts to improve these services are needed.[16]

This article is intended to inform pediatricians, family practitioners, other health professionals, and families about the follow-up care of NICU graduates, focusing particularly on the needs of premature infants.

 

Benefits of Birth at Regional Centers

Published reports for many years have emphasized the benefits of preterm birth at regional centers with advanced perinatal and neonatal services. Regional centers for perinatal care are often an accepted referral institution that is periodically reviewed by state health care agencies.

Regional centers include level III-IV hospitals that must meet high standards of care, and these institutions have many obstetric and pediatric subspecialists. Care at these advanced perinatal facilities is associated with lower mortality and morbidity for very-low-birth-weight (VLBW) infants (< 1500 g body weight).

A meta-analysis documented the mortality risk for VLBW and very-preterm (VPT) infants who are born outside of a level III or IV hospital (the level of a NICU is defined by the Perinatal Section of the American Academy of Pediatrics). For VLBW infants, mortality for those born in level III hospitals was 21%, compared with 36% in lower-level hospitals; for infants weighing less than 1000 g, mortality was 32% versus 59%. For VPT infants, mortality was 7% versus 12%, respectively.[17]

At level I and level II hospitals, all perinatal caregivers are encouraged to refer pregnant women to a hospital with a higher level NICU for delivery if the labor occurs very prematurely, particularly if the infant is likely to have VLBW. This referral assumes safe transport of the mother and fetus so that delivery does not occur during transit. The mother and fetus must also be in a reasonable state of health to avoid complications during transport.

 

Patient Education

Individualize a structured teaching plan for the primary caregivers to educate them in the infant’s care. Each infant has unique needs; thus, the education program should be directed at those needs. A checklist is essential to accomplish all the required teaching needs (eg, cardiopulmonary resuscitation, gastrostomy feedings, total parenteral nutrition administration, monitor use). Identify the appropriate educators to provide the training. Research shows that training educators for this activity results in better training of the primary caregivers at home.[18]

The goal of this education is to ensure that the parents/caregivers are capable and confident in caring for their infant at home. It may be appropriate for caregivers to stay overnight and provide care with minimal staff interventions. The staff providing care should not appear overprotective.

Two or more caregivers in the home must receive this training. Having an additional caregiver allows respite for the primary caregiver. A young mother with other small children and no grandmother or husband can be particularly stressed. The role of confounding factors associated with siblings in the home must be considered in the teaching.

For extremely complicated care situations (eg, infants with a tracheostomy), parents should have a rooming-in experience before discharge occurs. This is probably a good practice for all families before they go home with their infant but is especially important for infants who have ongoing, complex problems. Home visits by experienced home health care professionals and/or follow-up telephone calls are essential for the success of the transition process.

 

Resources for Parents and Healthcare Professionals

To meet the complex needs of the neonatal intensive care unit (NICU) graduate, parents and other caregivers may require educational material that covers conditions that require special evaluation or care after the infant is discharged from the hospital. Diverse resources available to parents and caregivers; they include medical and lay journals, books and other print materials, videotapes and digital sources, and websites.

Articles in medical journals are usually peer reviewed (ie, evaluated and accepted by experts in the field) before publication. The accuracy of information provided in lay journals and on websites can be suspect. Consultant experts may not have reviewed these sources. Clinicians should always investigate the particular sites that caregivers are using to obtain information and ask caregivers to discuss with them any information from online sources.

Because of the emotional turmoil that having an infant in a NICU can cause, patients and caregivers often find benefit in joining a support group. Information about such groups is available, especially on the internet, and support by hospital personnel and other parents may be the best therapy. In addition, specialized units or hospitals (eg, Shriners Hospitals for Children, Variety Children's Hospitals) are available to manage some conditions. Caregivers should be aware that children’s hospitals, especially those supported by the Children’s Miracle Network, may have additional resources available that are not available at large general or university hospitals.

Books for parents and caregivers

The following is a short list of books for parents and caregivers available online and from other booksellers.

  • Davis DL, Stein MT. Intensive Parenting: Surviving the Emotional Journey through the NICU. Fulcrum Publishers: Golden, CO; 2013.

  • Gunter J. The Preemie Primer. Da Capo Press: Philadelphia, PA; 2010.

  • Hall SL. For the Love of Babies: One Doctor’s Stories About Life in the Neonatal ICU. WorldMaker Media: Newton, MA; 2011.

  • Maddens SL.The Preemie Parents’ Companion; The Essential Guide to Caring for Your Premature Baby in the Hospital, at Home, and Through the First Years. Harvard Common Press: Boston, MA; 2000.

  • Wechsler Linden D, Paroli ET, Wechsler Doron M. Preemies: The Essential Guide for Parents of Premature Babies. 2nd ed. Gallery Books: New York, NY; 2013.

Internet resources

The American Academy of Pediatrics (AAP) is a national organization of pediatricians that is devoted to the health and well-being of infants and children. The American Academy of Pediatrics website has many policy statements regarding the proper care of infants and children and also provides information about the care of premature infants and childhood immunizations, such as “A Parent’s Guide to Safe Sleep,” which explains the prevention of sudden infant death syndrome (SIDS). The AAP shop sells items by topic and by product, including an extensive collection of pamphlets and books that cover the medical and psychosocial care of infants and children. Brochures such as “Your Preemie’s Growth” may be helpful to patients and caregivers. “Early Arrival: Information For Parents of Premature Infants,” a pamphlet no longer offered at the AAP shop, may be found here.

The March of Dimes Foundation provides a webpage on preterm labor and premature birth for parents, and it offers products for sale to health professionals such as DVDs and/or flyers in English and Spanish about late preterm brain development, premature birth, preterm labor, and pregnancy after a premature birth.

Shriners Hospitals for Children offer care to infants and children who have qualifying medical conditions, such as burn care, spina bifida, cleft lip and/or palate, orthopedic or craniofacial anomalies, and especially cerebral palsy. Its website provides information on the location of Shriners Hospitals and on patient referrals. In addition, clinicians or parents may call a toll-free patient-referral line to determine if a particular child qualifies; the referral numbers are 1-800-237-5055 in the United States, and 1-800-361-7256 in Canada.

"When Your Baby's Born Premature" is from the KidsHealth for parents website, sponsored by medical experts at the Nemours Foundation. It summarizes special needs and care of, as well as conditions common to, premature infants. Resources are also available in Spanish.

Child Care Resources presents information for families on the selection of child care, child care options, and financial assistance, as well as for child care professionals regarding day care requirements needed to establish programs for special-needs children. The site provides insight into early childhood learning resources and offers information regarding COVID-19 (coronavirus disease 2019) child care initiatives.

Additional resources

To obtain additional information or help with finding support groups, parents can also ask the neonatologist, the nursing supervisor, and/or the social worker for resources in or near the hospital. Some facilities provide parents with a pamphlet that contains this information when their child is admitted to the NICU.

Community agencies, such as the March of Dimes, and religious organizations may offer support services. Local and national support groups exist for infants and children with certain conditions, including the Down Syndrome Foundation, the Cystic Fibrosis Foundation, and the Little People of America (addresses dwarfism). Many rare disorders present in newborn infants have parent support groups and can be found via an internet search.

 

Criteria for Hospital Discharge

In 1998, the American Academy of Pediatrics (AAP) published guidelines related to "Hospital Discharge of the High-Risk Neonate."[19] These guidelines were updated in November 2008[20] and reaffirmed in 2018. This information has been supplemented by discharge planning for late preterm infants,[21] the evaluation of extreme premature infants for discharge,[22] the special needs for discharging infants born at the limits of viability,[23] and the reasons for rehospitalization after discharge of very preterm infants.[24]

The AAP places high-risk neonates into the following four categories:

  • Preterm infants

  • Infants with special healthcare needs or dependence on technology

  • Infants at risk because of family issues

  • Infants with anticipated early death

Preterm infant

No set weight criteria for discharge have been established, and studies reveal that preterm infants can be discharged safely and well while weighing less than 2 kg,[25] although infants must be able to be safely transported in vehicles.[26, 27, 28] At this time, the lowest weight that car seats are certified for is 4 lb or 1.814 kg.

Discharge should be based on physiologic maturity and stability of the infant. A principal criterion for discharge is the resolution of medical or surgical problems that require continued hospitalization. Additional criteria generally involve the following:

  • Physiologic stability which includes weight gain on enteral feeds, temperature stability in open crib, and mature respiratory control
  • Training and comfort of parents and caregivers

  • Predischarge healthcare maintenance

  • Postdischarge environment

  • Support team and follow-up

These criteria for discharge are applicable to all ill neonates and not just those born prematurely.

Weight gain and feeding

Weight gain of 10-20 g/kg/day must continue over a reasonable time period (several days to 1 week) and should approximate fetal or early postnatal growth. In addition, weight gain must be associated with the patient's ability to feed by mouth or by other methods (eg, gavage tube, gastrostomy, intravenous nutrition). Feedings must be accomplished without any distress or problems. Parents/caregivers should demonstrate competence in using the method or technique selected for the infant’s nutrition.

Weight gain should occur while the infant is in an open environment (eg, crib). The infant must have been clothed appropriately, and the body temperature should be maintained in the normal range for at least 24-48 hours in this environment (ie, thermal stability achieved).

Training and comfort of parents and caregivers

Parents or other assigned caregivers must be trained adequately and must be comfortable in all aspects of the preterm infant’s care, including the administration of medications and the use of technical devices (eg, monitors, aerosol delivery equipment). Parents may pressure physicians to order a home monitor, but monitors are infrequently needed and unlikely to prevent a sudden infant death syndrome (SIDS) event.[29, 30] (See Apnea of Prematurity.) In the hospital, the parents' performance with their infant must be adequate before discharge.

Predischarge healthcare maintenance

Certain aspects of healthcare maintenance must be performed before discharge. Appropriate metabolic screening must be completed. Assess anemia, and establish its follow-up care.

Assess the need for respiratory syncytial virus (RSV) prophylaxis, and administer appropriately during RSV season.[31]

Patients who had prolonged stays may need to begin age-appropriate immunizations before discharge. Consult the AAP Red Book[32] ; the AAP Immunizations webpage, which provides information for parents and clinicians; or the Centers for Disease Control and Prevention (CDC) Vaccines & Immunizations webpage.[33]

All neonatal intensive care unit (NICU) patients should undergo a hearing test before they are discharged from the hospital. Schedule infants for an appointment with an audiologist soon after discharge if testing in the hospital is abnormal.

For preterm infants, revised criteria were published in 2013 regarding the assessment of retinal vascularization by a trained ophthalmologist.[34, 35] For transferred infants, a qualified pediatric eye specialist must be available at the accepting facility. For outpatients, the infants must be seen by a qualified ophthalmologist according to the designed schedule. In 2018, the criteria were further revised to include attributes of an effective program to detect and treat retinopathy of prematurity (ROP), including the timing of initial and follow-up assessments.[36]

Postdischarge environment

An assessment of the postdischarge environment, possibly including an onsite evaluation of the home, is emphasized as part of discharge planning. Unfortunately, this very effective evaluation is rarely performed.

The parents and the home environment must be suitable so that neither neglect nor physical abuse is likely to occur. Indicators of concern can include the frequency of parental visiting and the physical involvement of parents in the infant's care during the infant's hospital stay. Knowledge of poor parenting skills with other children, a history of marital discord, past or present substance abuse, or criminal activity requires that hospital and outside social services be involved.

Reports may be required for submission to local or state authorities. A contract may need to be signed by parents to set benchmarks of care.

All medical equipment, termed "special technologies," required at home should be in place and in working order. Training of the caregivers should be such that they are experts. The caregivers must have emergency numbers to call when equipment malfunctions or supplies become meager.

Support team and follow-up

A program of parental support, including in-home visits by healthcare professionals and assistance by family and friends, should be in place before discharge occurs. Community services should be informed and willing to help.[16]

Prior to discharge, the NICU program must be responsible for coordinating visits among different consultants that will occur after discharge. A primary care physician (PCP) should have been identified during the mother's pregnancy; if not, one should be chosen early in the patient's hospital stay. The PCP should be familiar with the care of high-risk neonates and should help coordinate subsequent visits to subspecialists. The PCP also provides ongoing healthcare maintenance.

The most important tasks of the PCP are ensuring adequate nutrition and proper growth and development of the patient. These duties may be performed in conjunction with follow-up programs of the NICU from which the patient graduates or with follow-up programs of private or governmental agencies that specialize in infant development.

Obstetric and neonatal attending physicians should begin verbal and written communication with the PCP, and vice versa, shortly after the baby's birth. Team members should periodically provide the PCP with verbal and written reports about the progress of the future NICU graduate so that information is available in the outpatient record. An organized system must exist to assess the physical and psychological outcome of the NICU graduate.

Infant with special healthcare needs or dependence on technology

With the emergence of managed care, early discharge of infants with active medical and/or surgical conditions is common.[37, 38] Infants may leave the hospital with many unresolved issues, such as a need for nutritional assistance (eg, feeding by means of gavage or intravenous alimentation); for respiratory support ranging from supplemental oxygenation to assisted ventilation through a tracheostomy; and for maintenance of indwelling or external medical devices (eg, ventriculoperitoneal shunt, cardiorespiratory monitor, urinary catheter).

For patients requiring nutritional assistance, the ability of parents to provide adequate nutrition by the appropriate method is vital to success, as is their ability to prevent or recognize complications of gavage or gastrostomy feedings. Caregivers who must give home parenteral nutrition to their infant require special training to avoid infection and other complications (eg, hepatocellular liver disease).

Some infants, such as those with myelodysplasia, may require repeated urinary catheterizations. Caregivers must be trained in appropriate catheterization techniques and prevention of complications.

In patients with tracheostomies, the PCP must know the risks of clinically significant neurologic morbidity or mortality associated with the home care of tracheostomies during infancy.[39, 40, 41] Tracheostomy care may also involve assisted ventilation at home. In this circumstance, care by the PCP should involve consultation with a pediatric pulmonologist.

Home oxygen therapy may allow earlier discharge and avoid growth failure and chronic pulmonary hypertension. The infant must receive sufficient oxygen to accomplish these goals; therefore, these infants require a functional home oxygen saturation monitor. Care by a physician experienced in weaning oxygen in an appropriate manner is essential.

Parents usually do not anticipate complex home medical care for their infant at the beginning of a pregnancy. When the infant's medical condition requires extensive care in the home, the parents may be in need of a respite to perform other family duties or to have some leisure time. Planning for respite care for the parents should be part of the discharge process.

Infant at risk because of family issues

Problems with bonding between parents and their infant are reported with prolonged hospitalizations.[42, 43] The NICU is a stressful environment for parents, and the environment itself may hinder bonding. Infants who are born prematurely, have congenital defects, or have a chronic disease are all at increased risk for experiencing physical harm or neglect.

Other parental/caregiver risk factors for an adverse outcome in the home environment include the following[44] :

  • Low educational level

  • Lack of family help

  • Unstable marriage or relationship

  • Sporadic or no medical care during pregnancy

  • Use of illicit substances or alcohol abuse during pregnancy

  • Infrequent family visits during the infant’s hospitalization

The problem of adverse outcomes in the home environment has led to the widespread use of foster homes for the care of NICU graduates. If the foster home environment is a transitional approach, continuing medical care should be available after discharge.

Child protective services should monitor visitation by the natural parents. The parents' participation in a rehabilitation program is essential in planning to reunite infants with their parents. The likelihood of success in reuniting infants with their parents increases if the parents comply with a structured rehabilitation program.

If an infant is to be discharged to a home where illicit substances were used, a home visit before discharge and many home visits after discharge are necessary to protect the infant's health and well-being. Child protective services must be involved continuously in the care and treatment of infants in this situation.

Infants with anticipated early death

Home hospice and palliative care options for neonates with life-threatening or lethal conditions (eg, trisomy 13) are increasingly available, but several factors are needed for their success.[45, 46, 47, 48] With the advent of prenatal ultrasound examinations and genetic studies of the fetus, families may discuss neonatal palliative care before birth.[49] Initiating a hospice plan following a conference that includes the family, invited visitors (eg, clergy, friends), caregivers, and social workers is appropriate. Neonatal ethics has offered an opinion about more aggressive treatment of these infants, and it is recommended that parents’ rights be respected in the decision-making process.[50, 51]

If the parents request hospice or palliative care, discharge of the baby to home with supportive care is often the best option. Set in place a "do not resuscitate" (DNR) order before discharge.[52] Parents should have multiple copies of a letter that explains that the infant has a condition for which resuscitation would be futile and a DNR order is in place. Identify one or more contact physicians for the infant.

Establish a multidisciplinary approach before discharge. If available, skilled professionals experienced in the hospice care of infants should be present in the home. Daily home visits may be needed just after discharge and near the terminal event. Promptly alleviate distress or discomfort, if possible. Arrangements must be made for the family’s needs, including the process of bereavement. Social services and/or clergy must be involved.

 

Discharge Planning

From the initiation of intensive care, high-risk neonates should have an identified primary care physician (PCP). This person should become part of the discharge planning team. Unfortunately, finding a PCP and the degree of the PCP's involvement are problems in neonatal intensive care units (NICUs) throughout the United States.

Medical insurance coverage for the infant may make identifying a PCP difficult for parents or caregivers early in the hospital stay. Moreover, the parents' education may result in a lack of aggressiveness in securing the services of a PCP or the involvement of other community resources.

Most importantly, the PCP should have training and experience in caring for various problems associated with high-risk neonates. A significant number of NICU graduates require the services of a PCP, a neurodevelopmental follow-up clinic, and pediatric medical or surgical subspecialists after discharge. A common example is the medical follow-up of the extremely low-birth-weight (ELBW) infant who has ongoing bronchopulmonary dysplasia and requires a pediatric pulmonologist to work with the PCP.

The ideal follow-up clinic has clinicians that can perform assessments of ongoing medical problems and a neurodevelopmental team that undertakes psychological evaluations and appropriate interventions (eg, team consisting of a neonatologist or pediatrician, psychologist, dietitian, physical therapist, occupational therapist, speech therapist, social worker).

Each NICU should have a discharge-planning group consisting of designated professionals. The members should include at least the following:

  • A discharge planner or case manager

  • One or more social workers

  • Nursing representatives (eg, nurse manager, clinical nurse educator, neonatal nurse practitioners)

  • Physicians (always the attending neonatologist plus others)

  • Community service representatives (eg, home health nurses, Medicaid case workers, protective services case workers, personnel from private or government-funded neurodevelopmental follow-up clinics)

Because of rules related to the protection of patients' information, certain participants (eg, Medicaid and protective services case workers) may need to discuss their cases first and then leave when other patients are being discussed.

NICUs that maintain a high census and that care for high-acuity patients may have a discharge planner, a neonatologist, one or more nursing representatives, dietitians, physical therapists, occupational therapists, speech therapists, respiratory care practitioners, and representatives from the NICU follow-up clinic. On occasion, surgical subspecialists, pediatric subspecialists, or the PCP may be invited to the meetings to offer advice regarding infants with complex problems.

A busy office practice often precludes the PCP from attending these meetings. Nevertheless, PCPs should be given periodic reports on the progress of their future patients after every meeting, and they must be willing to assume care upon discharge.

The time of day, the designated day of the week, and the frequency of the meetings associated with discharge planning depend on the needs of a given NICU. For NICUs with large populations, the frequency, day, and time depend on having an optimal number of team members present. For small NICUs, formal discharge-planning rounds may be inefficient.

One summary of the discharge-planning process is the 2008 policy statement from the American Academy of Pediatrics (AAP) Committee on Fetus and Newborn.[20]

Hospital discharge guidelines

The 2008 (reaffirmed 2018) AAP Guidelines on Hospital Discharge indicated six critical components of the discharge-planning process, as follows[20] :

  1. Parental education

  2. Completion of appropriate elements of primary care in the hospital

  3. Development of management plan for unresolved medical problems

  4. Development of a comprehensive home care plan

  5. Identification and involvement of support services

  6. Determination and designation of follow-up care

Completion of appropriate elements of primary care

The implementation of primary care includes more than just identifying a PCP within the first week of the patient's hospitalization. In and out of the hospital, primary care involves a range of responsibilities, including the following:

  • Assessment of the infant's nutrition and growth

  • Immunizations before and after discharge

  • Indicated respiratory syncytial virus (RSV) prophylaxis

  • Car and home safety

  • Neurodevelopmental outcomes (including hearing and vision screening)

Among the most important follow-up items are monitoring for serious anemia and continuing assessment of retinopathy until its resolution. In-depth nutritional evaluation is mandatory for infants who received prolonged parenteral nutrition, who had gastrointestinal anomalies, and who may have either an inborn error of metabolism or other metabolic/biochemical disorders.

Development of management plan for unresolved medical problems

A list of unresolved problems must be developed during the patient's hospital stay, and this list must be made available to the PCP. Ongoing conditions should have been completely diagnosed, and a management plan for diseases that persist must be established at the time of discharge.

The plans for ongoing care by the PCP must be transmitted in detail. The current treatment plan and all medications the infant is receiving should be conveyed to the home health professionals and the PCP before discharge. Resolved problems should also be identified at the time of discharge because some unanticipated complication may arise. Individual infants have received the best in-home and follow-up care with this method.

Development of a comprehensive home care plan

The AAP guidelines for technology-dependent infants are helpful in the discharge-planning process.[20] Publications about the care and outcomes of NICU graduates requiring complex technology are limited.[16, 53, 54] The plan of care in the home should have the following elements:

  • Identification and training of the in-home caregiver

  • Planning for optimal nutrition and follow-up (eg, total parenteral nutrition, gastrostomy feeds)

  • A list of equipment, supplies, and resources that are needed at home

  • Referrals to home healthcare professionals and community resources that can provide ongoing assessments and care after discharge and the full knowledge that the PCP understands what resources have been initiated

  • An assessment of the home environment to determine that it is suitable for care and to determine what improvements must be made before the infant's discharge

  • A plan for emergency care and transport should the need arise

  • Assessment of financial resources identified by using either indemnified insurance or governmental programs to finance future hospital, office, and home healthcare needs

When appropriate, Social Security Income (SSI) must be applied for during the hospital stay; applications for other free services (eg, care at a Shriners hospital) must be underway at discharge. PCPs must be aware of the elements in the plan of home care. This is especially true when the PCP does not participate in their implementation.

Identification and involvement of support services

Assess the ability of the primary caregiver and other family support members to deliver care before discharge. Establish ongoing assessment of the caregiver's physical and emotional abilities to continue providing care at home.

Before discharge, initiate in-home evaluations regarding the availability of supplies, medications, complicated technologies, and nutritional support. Healthcare workers who provide ongoing home evaluations and who can identify new problems are essential for a favorable long-term outcome for the NICU graduate.

Determination and designation of follow-up care

The discharging neonatologist has overall responsibility for follow-up care at discharge. Ongoing communication between the neonatologist and the PCP during the hospital stay and at discharge improves outcomes for the infant.

Early identification of a PCP is important. In the ideal circumstance, the PCP reviews the records, examines the infant, and meets with the family before discharge. In the era of managed care, the busy office practice of a pediatrician or family practitioner may not allow for such a review before discharge.

In some cases, the skills of the PCP are limited relative to the complex problems of the infant. Therefore, appropriate follow-up care with surgical and pediatric subspecialists is necessary. Teamwork is the key to success regarding discharge planning and follow-up.

Most important among the subspecialist visits is a follow-up appointment with a neurodevelopmental specialist. Although such an appointment may be in the distant future, make a list of scheduled and unscheduled (but anticipated) appointments and give it to the parents and PCP before discharge.

The discharge-planning process is usually well established at tertiary NICUs; however, level II nurseries should also conduct such activities. Infants may be transported close to their home for convalescent care, and the staff at the level II nursery is responsible for determining the infant's health status (eg, the absence of potentially blinding retinopathy of prematurity) before discharge. If retinal pathology is still active, formulate an appropriate discharge plan or the outcome may be preventable visual disability.[55]

Arrangements for follow-up appointments may be made locally; however, this is not always possible. Some level II nurseries may be in relatively rural areas, and the infant still needs to return to the tertiary care center for certain services (eg, ophthalmologic examinations, hearing assessments, developmental follow-up). In rural areas, home services may also be limited, which means that the PCP has additional responsibility in evaluating the transition to home care.

Finally, the NICU staff is responsible for assessing the performance of a home healthcare agency and of its workers' abilities to provide quality care to the infant who is technology dependent. If an agency's staff does not perform properly, the agency should be so informed. If the quality of care does not improve, alternative arrangements for care must be sought.

In addition to the guideline components discussed above, the 2008 AAP guidelines also contain recommendations for infant readiness for hospital discharge, family and home environmental readiness, and community and healthcare system readiness. Caregivers, whether they are hospital-based or home-based, should be familiar with these summary guidelines.

 

Long-Term Monitoring

The major goals of the pediatrician or family practitioner who monitors a neonatal intensive care unit (NICU) graduate include the following:

  • Provide an ongoing assessment of growth

  • Evaluate the adequacy of nutrition

  • Deliver preventive care

  • Periodically examine the infant's, child's, or adolescent's motor, intellectual, and behavioral development

This section mainly covers the assessment of growth and nutrition and the delivery of preventive care. Periodic examination of development is discussed in the "Developmental Follow-up" section. Another important aspect of healthcare maintenance of the NICU graduate is health supervision and anticipatory guidance.

Assessment of growth

The first duty of the primary care physician (PCP) is to accurately monitor the growth of the NICU graduate.[56, 57, 58] Therefore, the patient's weight, length, and head circumference must be plotted on appropriate growth charts and evaluated over time.

Any infant with a growth rate in the lower percentiles of the curve or whose growth curve flattens or decelerates should have the causes assessed. If improved nutritional support does not reverse the growth pattern or if diagnostic studies do not reveal an obvious cause, referral to an endocrinologist, gastroenterologist, and/or dietitian is indicated.

Growth rates

For infants who were born prematurely, growth should be plotted after it is corrected for the patient's gestational age at birth. Special growth charts are available for this purpose.[59] Growth charts for term infants hospitalized in the NICU are also available.[60] Graduates of the NICU often have accelerating growth patterns after discharge. This is particularly true for preterm infants.[61]

In the first 3-4 months after birth, normal weight gain averages 15-40 g/day and then declines, reaching about 5-15 g/day by the age of 12-18 months. From a postmenstrual age of approximately 40 weeks until month 4 of postnatal life, weight proportionally increases more in infants who were born prematurely than in those who were born at term.

The rate of accelerated growth in preterm infants is still larger than that in term infants, but the magnitude is far less. In the months after preterm infants are born, the crown-heel length may incrementally increase by 0.8-1.1 cm/wk, whereas term infants gain a mean of 0.7-0.75 cm/wk. By the age of 12-18 months, the gain in length declines to 0.75-1.5 cm/mo.

Long term, infants who are born prematurely often catch up their growth relative to their full-term peers. However, that growth is impacted by any comorbidities, and small-for-gestational-age (SGA) infants may always remain smaller.[62, 63]

Head growth

Measurement and documentation of head growth, a predictor of future outcome,[64, 65] is especially important in this high-risk population. In preterm infants, head growth correlates with magnetic resonance imaging (MRI) findings and neurodevelopmental outcome.[66] An assessment of head growth is especially important in patients with a history of a chromosomal disorder, brain insult secondary to hypoxic-ischemic encephalopathy, or a metabolic disease.

The largest frontal-to-occipital plane is used to determine the patient's head circumference. For preterm infants, the increase in head circumference is in the range of 0.7-1 cm/wk, whereas the increase in term infants averages about 0.5 cm/wk during the immediate postnatal period.

Increases in head circumference of more than 1.25 cm/wk suggests ventricular dilatation (ie, hydrocephalus or other causes of increased intracranial pressure [eg, subdural hematoma]). If ultrasonography reveals that ventricular size is stable or declining after intraventricular hemorrhage, the risk of posthemorrhagic hydrocephalus is small. This issue is generally resolved before the patient is discharged from the NICU. Other causes of accelerated head growth include autism or genetic or metabolic disorders. A rapid deceleration in head growth occurs by age 12-18 months. Beyond that age, the increase is 0.1-0.4 cm/mo.

Growth failure

Growth failure is a concern among preterm babies who weigh less than 1500 g at birth (very low-birth-weight [VLBW] infants), and particularly those who weigh less than 1000 g at birth (extremely low-birth-weight [ELBW] infants). The National Institute of Child and Human Development (NICHD) Neonatal Research Network has reported that 97% of VLBW infants and 99% of ELBW infants had weights less than the 10th percentile at the postmenstrual age of 36 weeks.[67] ELBW infants may never reach the height of their full-term peers.[68]

Growth failure begins during the NICU hospitalization in this group. It is the focus of many providers who are concerned about the late consequences of this poor growth that occurs during a critical period of brain development. A prospective study by the NICHD of infants who weighed 500-1000 g at birth showed that their growth in the NICU influenced subsequent neurodevelopmental and growth outcomes in positive or negative ways.[69] The PCP should be aware of their patient’s growth characteristics in the NICU. Growth failure may have many origins in NICU graduates.[70, 71, 72]

As noted above, infants who weigh less than 1500 g at birth must undergo frequent assessments of growth. The PCP should know whether preterm infants or those who are SGA are gaining at least 20 g/day before discharge. If growth is less than 20 g/day, a plan should be in place before the patient is discharged from the NICU and communicated to the PCP, who should carefully follow up the patient's growth.

Infants may also be at risk for nutritional deprivation, depending on their disease states, and the type of nutritional support may also help in identifying infants at risk for growth failure, such as those who are breastfed, infants given special formulas, and infants who are receiving total parenteral nutrition (TPN) for longer than 4 weeks or who are still receiving TPN at discharge.[73]

Despite some increased risks associated with breast milk–related nutrition in ELBW infants (eg, osteopenia of prematurity), neurodevelopmental outcomes at age 18 months are more favorable in breastfed infants than in others.[74] Infants requiring nasogastric tube or gastrostomy feedings after discharge are at significant risk for impaired growth.

Common neonatal conditions for which an evaluation for growth failure is required include the following:

  • Chronic lung disease of prematurity (ie, bronchopulmonary dysplasia)

  • Severe central nervous system injuries or birth defects

  • Congenital heart disease

  • Short bowel syndrome

  • Esophageal and intestinal anomalies

  • Chronic renal disease

  • Inborn errors of metabolism

  • Chromosomal and/or major malformation syndromes

To rectify growth failure, the PCP must understand its origins, especially in the very preterm infant.[75] For example, an infant with congenital heart disease may have growth failure because of feeding difficulties associated with congestive heart failure and an increased work of breathing. Corrective surgery may be the only solution for this condition.

An infant with severe perinatal asphyxia may be unable to suck and swallow because of brain injury. Such an infant may require a permanent gastrostomy (and gastric fundoplication) to ensure adequate nutrition. Even when this is accomplished, the brain insult may still result in poor growth secondary to hypothalamic and pituitary effects or other yet-undefined consequences of severe cerebral damage.

A premature infant recovering from severe bronchopulmonary dysplasia may have reduced growth because of pulmonary disease, which increases the respiratory effort, and inadequate protein intake. Severe chronic lung disease in the NICU graduate is commonly associated with gastroesophageal reflux (GER).[76] In infants with GER, alleviating esophageal pain with H2 receptor antagonists or proton-pump inhibitors in conjunction with prokinetic agents may mitigate the problem and promote increased feeding volumes and weight gain. However, use of these agents in infants has been associated with necrotizing enterocolitis.[77, 78, 79, 80]

Convalescent infants who had severe necrotizing enterocolitis may have an insufficient epithelial surface or a damaged mucosa that does not allow adequate absorption of nutrients from the gut. Persistent poor growth in these infants may require a return to partial parenteral nutrition.

Completion of catch-up growth

Controversy surrounds the age at which catch-up growth is complete for infants who were born prematurely; many clinicians believe that catch-up growth is not complete until age 2.5-3 years. In some SGA infants, body mass may rapidly increase, but a substantial number have little catch-up growth.[81] Referral to a pediatric endocrinologist is important, because therapy with recombinant human growth hormone may be useful in some cases.

Early growth and adult disease

Another concern involves the rate of catch-up growth and its association with an increased risk of obesity and heart disease in later life.[82] In part, the pathophysiology of low birth weight and later adult disease is derived from the Barker hypothesis, which posits that early adverse nutrition, including prenatally, affects intrauterine growth, premature birth, and birth weight, as well as raises a predisposition toward metabolic syndrome, hypertension, coronary heart disease, and other conditions.[83] Emerging data are causing a reexamination of the best rate for catch-up growth and of the strategy to avoid the consequences low birth weight.[82, 84, 85]

Greer has presented a critical review of this topic and recommends postdischarge nutrition.[86] The benefits of breastfeeding appear to substantially affect adult diseases associated with the Barker hypothesis.[87] Continued and prolonged use of breast milk for nutrition after discharge is associated with higher Bayley Mental Development Index scores in ELBW infants assessed at 30 months.[88]

Evaluation of nutrition

Nutritional assessment begins with a complete history and physical examination, including evaluation of the patient's general health status, heart rate, breathing rate, temperature control, and fluid balance.[89] Include anthropometric measurements, such as weight, length, head circumference, and sometimes skin-fold thickness, which are plotted over time. The PCP should also study the patient's fluid and mineral intake and appraise caloric and substrate consumption.

Increases in weight versus length may differ in NICU graduates who are having problems with adequate nutritional intake. A comparison of the two measurements (eg, length increasing faster than weight) can provide evidence of nutritional sufficiency.

The PCP must also monitor the route by which nutrition is provided. Parenteral nutrition, enteral nutrition, or both may be used to attain adequate nutrition. Recognize inadequacies in delivering nutrients by either the parenteral or enteral route.

The PCP may be untrained or inexperienced in this type of nutritional evaluation; consequently, the role of follow-up care of the NICU graduate must often include a pediatric dietitian, and a specialized follow-up clinic may be needed for certain infants. When access to a follow-up clinic and a pediatric dietitian is limited, the PCP may need to use a home feeding diary and/or a nutritional assessment sheet to gather additional information on exact caloric intake and the composition of substrate that the infant is consuming.[61]

Prolonged intubation and repeated insertion of gavage tubes can result in an aversion to oral feeding.[90] Deviations from a normal suck-and-swallow response may include a tonic bite reflex, an abnormal tongue thrust, or a hyperactive gag. More important than these findings, and too often observed, is the presence of a dysfunctional suck, swallow, and breathing pattern that results in hypoxemia, apnea, or both during oral feeding. This problem is often observed in ELBW infants.

Parental anxiety adds to the problem. In this setting, observation of infants by an occupational therapist or nurse specially trained to recognize feeding problems is an excellent method to make the diagnosis and treat these infants properly. Cineradiography of the suck-and-swallow mechanism often helps in this process. Diagnostic tests to exclude GER as a contributor to abnormal feeding behavior are also frequently necessary.

The NICU team is responsible for making these assessments and for developing a treatment plan before discharge. The PCP must be thoroughly aware of this assessment to understand the pathophysiology of the disorder and must comprehend the likelihood of success with the therapy applied.

Finally, stool passage and the composition of the stools may be useful in assessing the adequacy of nutrition. Abdominal distention and oily, mucoid, explosive, or watery stools should heighten the clinical suspicion of epithelial absorptive problems in the intestine. Given the gene frequency in the White population, these signs and symptoms should always alert the PCP to the potential for cystic fibrosis. Most state governments in the United States have neonatal screening programs that now recognize the majority, but not all, of these afflicted children.

Carbohydrate and protein intolerance (an inability to digest food or a true allergy) must be considered in infants with abnormal patterns of stool passage, and diagnostic tests are indicated. Referral to a pediatric gastroenterologist may be appropriate if test results do not indicate a diagnosis or if interventions do not alleviate the problem.

Most infants gain weight and grow with an intake of 108 kcal/kg/day. Infants born prematurely usually require 110-130 kcal/kg/day for sustained weight gain and growth. Protein requirements may also be increased. On average, these infants require approximately 4 g/kg of protein and 3.5 g/kg of fat daily.[62, 85] For these preterm infants, the following simple equation may be used to calculate their increased needs:

Daily intake = 120 kcal/kg × (ideal weight for actual height/actual weight), where both weights are in kilograms.

In extraordinary circumstances, indirect calorimetry may be required to ascertain an infant's energy needs. These measurements include oxygen consumption, production of carbon dioxide, and elimination of urinary nitrogen. These techniques require the assistance of a tertiary care center.

Specific evaluations

Specific assessments of the NICU graduate include the following:

  • Fluid and acid-base balance

  • Mineral content of the blood and bone

  • Energy intake

  • Dietary nutrient composition

Fluid balance

Fluid balance is important in NICU graduates with serious pulmonary, cardiac, gastroenterologic, and/or renal problems. Fluid restriction may result in poor growth unless the patient is fed high-caloric formula, fortified breast milk, or breast milk supplemented with formula intake. Conversely, excessive fluid may cause edema. The disease itself or diuretic therapy may affect the mineral content of the blood.

Acid-base balance

Assessment of the NICU graduate includes not only a determination of blood electrolyte concentrations but also a measurement of acid-base balance. Pulmonary or cardiac disease can be associated with clinically significant respiratory acidosis and renal compensation. Diuretic therapy may accentuate this problem. This is particularly true for low concentrations of potassium and chloride in the blood and a contraction alkalosis in association with severe chronic lung disease of prematurity (ie, bronchopulmonary dysplasia).

Blood and bone mineral content

Diuretic therapy may also cause further disturbances in calcium and phosphorus homeostasis (eg, low concentrations of total or ionized calcium), diminish plasma phosphorus content, and elevate alkaline phosphatase activity in the blood. These chemical findings in the blood frequently reflect osteopenia in preterm infants.

Osteopenia of prematurity is a defined disorder of diminished bone mineralization that is often observed in VLBW infants. A study in the United Kingdom revealed no consistent practices related to osteopenia in preterm infants.[91] The disease can result in rickets or fractures of the ribs and long bones.

Recommendations have been established for the intake of calcium salts, phosphorus, and vitamin D that can diminish the risk of fracture.[92] If fractures do occur after discharge, this cause must be distinguished from physical abuse.

Osteopenia of prematurity has a complex etiology that includes rapid bone growth with inadequate intake or metabolism of calcium, phosphorus, vitamin D, and protein. Correction involves treating the specific deficiencies. Renal disease with sodium wasting, excess bicarbonate losses, and poor retention of calcium and/or phosphorus can additionally complicate the clinical picture. On infrequent occasions, genetic disorders may manifest rickets.

The optimal method of monitoring bone mineralization in preterm infants with birth weights less than 1500 g is unsettled and may involve biochemical analyses, dual X-ray absorptiometry (DEXA), and/or ultrasonography.[92, 93] The PCP should be aware of the methods of assessment.

Dietary deficiencies

Other deficiency states observed in NICU graduates may involve the following:

  • Specific vitamins

  • Iron and trace minerals

  • Carnitine

  • Essential fatty acids

  • Protein

Although these deficiencies are not discussed in detail in this article, specific deficiencies are covered briefly below. Most deficiencies are avoided with the use of preterm formulas and/or fortified breast milk. Improved fortifiers, if available and if used before and after hospital discharge, enhance biochemical components associated with growth and affect postnatal growth itself.[94, 95, 96]

Vitamin K deficiency can result in a bleeding disorder from reduced synthesis of liver-related coagulation factors.[97] Folate deficiency can be associated with a megaloblastic anemia, dermatitis, and diarrhea.

Iron deficiency is the most important cause of anemia in NICU graduates. Therefore, infants with iron deficiency are often receiving iron and vitamin supplementation at the time of discharge. Ziegler et al concluded that iron supplementation in breastfed infants is feasible and increases plasma ferritin without increasing hemoglobin.[98]

Although infrequent, zinc deficiency is associated with growth failure, defective host defenses, slow wound healing, and acrodermatitis enteropathica. Exclusive breastfeeding of ELBW infants is the scenario that most often results in zinc deficiency.

Carnitine deficiency can cause failure to thrive, cardiomyopathy, encephalopathy, and recurrent infections. This deficiency is most often recognized in infants who are receiving only parenteral nutrition. For this reason, in infants receiving long-term TPN, the solution should be supplemented with carnitine.

Protein-related malnutrition is among the most serious nutritional problems encountered in patients in the NICU before and after discharge.[99] Protein deficiency is associated with slow growth, hypoproteinemia, edema, lethargy, impaired wound healing, and an increased incidence of infection.

Measuring plasma prealbumin and albumin levels is useful in severe protein-deficiency states, but a strategy for early detection of the deficiency state is problematic. French pediatricians have long used a blood urea nitrogen (BUN) value of more than 5 mg/dL as an indication of adequate protein anabolism, but simple measurements of adequate protein intake and metabolic use are lacking for the most part.

Exclusive breastfeeding of ELBW and VLBW preterm infants creates a likelihood of protein-energy malnutrition, but concerns about this risk should be allayed by the use of fortifiers and a study showing an improved neurodevelopmental outcome in ELBW infants who received human milk.[88] In addition, a prospective trial showed that a human milk fortifier enhanced the growth of preterm infants.[94] Thus, use of human milk fortifier may be incorporated into the postdischarge care of preterm infants. Hay and associates wrote a comprehensive overview of the nutritional needs of ELBW infants.[100] Moreover, early use of intravenous solutions containing amino acids has been shown to prevent the negative protein balance that can begin shortly after birth in the VLBW and ELBW population.[75]

Delivery of preventive care

Healthcare maintenance is the essential function of the PCP, of which assessment of growth and nutrition is an integral part. Other functions include education of parents/caregivers regarding safety concerns; prevention of infectious diseases by means of immunization; and evaluations of vision, hearing, and other aspects of neurologic development. Problems with infant-parent bonding are also the PCP's concern. The neurologic and emotional aspects manifest in NICU graduates are reviewed in subsequent sections of this article.

Two important preventive measures may begin in the NICU. The first preventive therapy is immunization. To obtain current information about the immunization schedule for infants, see the AAP Red Book[32] as well as Recommended Vaccines by Disease and Immunization Schedules from the CDC.[33]

The second measure is education regarding car seat safety and the proper use of car seats. Because some preterm infants have episodes of cardiorespiratory instability when secured in a standard car seat, preterm infants should be tested before they leave the hospital for the absence of airway obstruction or apnea when they are in the seat.[26, 27, 28] However, data are insufficient to confirm the value of this "car seat challenge test."[101]

There is variability in the use of the “car seat challenge test” before discharge of infants born at less than 37 weeks in the United States. Controversy abounds regarding this test in the United Kingdom; nevertheless, use of the car seat challenge test is increasing in that country. Studies have recommended standardizing the test to all infants born at less than 37 weeks' gestation to a duration of at least 90 minutes, along with a failure threshold for bradycardia of less than 80 bpm for longer than 10 seconds, and for saturation of less than 90% for more than 10 seconds.[102]

Car seats do prevent fatal vehicular injuries, so they are strongly recommended; their use is controlled by law in many US states. Before infants are discharged from the NICU, their parents or guardians should be instructed about appropriate use of a car seat. The PCP should also review car seat safety during the initial office visit.

The PCP also has a responsibility to aid in home safety and to prevent crib death. In its Safe to Sleep campaign (formerly the Back to Sleep campaign), the AAP recommends supine sleeping for term infants; this positioning has significantly reduced rates of sudden infant death syndrome (SIDS).[103] The risk of SIDS is increased in preterm infants (birth weight < 2500 g) and SGA infants who sleep in a prone or lateral recumbent position versus the supine position.[104] Therefore, for preterm as well as term infants, "back is best."[105, 106]

However, parents and PCPs must be aware that "back is best" is associated with an increased risk of plagiocephaly and torticollis. Interventions (ie, tummy time with parental observation) are mandatory to prevent or treat of these conditions when they occur.[107]

If indicated, initiate immunizations prior to hospital discharge[108] with the PCP continuing or starting immunizations during follow-up care. Keep in mind that the practice of professionals who deliver in-hospital care of VLBW may lag behind current recommendations for immunizations[109] ; one reason for this lag may be the concern that apnea may increase within 72 hours after immunizations[110, 111] or that febrile responses may occur.[112]

The postimmunization cardiorespiratory status of infants with chronic lung disease may worsen for approximately 48 hours.[113] It remains controversial whether ELBW infants can respond to immunizations within 2 months of birth (eg, 2 months after birth for an infant born at 23 weeks' gestation [ie, postconceptual age 31 wk]). Some investigators believe that immunizations should be given at or after 35 weeks’ postconceptual age, and that this timing enhances the immune response. PCPs must be aware of problems associated with the administration and effectiveness of immunizations given to ELBW infants.

Preterm and other high-risk infants may meet guidelines for the administration of palivizumab. This monoclonal immunoglobulin G (IgG) is given intramuscularly to reduce the severity of respiratory syncytial virus (RSV) infections.[114] In most communities, RSV season usually begins in late October or November and ends in March to May.

In 2014, the AAP published revised guidelines for prophylactic injections of palivizumab.[31] The use of palivizumab has been cost-effective in preterm infants born at less than 30 weeks' gestation.[115]

Health supervision and anticipatory guidance

Review of the patient's neurodevelopment is one of the PCP's primary tasks, and the provider must understand how the patient's physical and mental disabilities affect the parents and the family as a whole. The emotional well-being of the child and the family is critical to a successful life.

The PCP should not only coordinate care for patients leaving the NICU[116] but also pursue follow-up care of any infant who has a hospital predischarge abnormal result on a hearing screen or ophthalmologic examination. Moreover, the PCP has a vital role in assessment of anemia of prematurity. Periodic measurements of hemoglobin levels, hematocrit levels, and reticulocyte counts is important. The PCP also has the responsibility of keeping track of referrals to subspecialists for the numerous problems that an individual NICU graduate may have.

During the NICU stay, social work and care managers should establish, if possible, healthcare insurance coverage of the infant. The PCP should continue to ensure that healthcare insurance, whether funded privately or publicly, is available to the infant. The physician and the family must work together to obtain supplemental Social Security benefits based on the infant’s disabilities, if it has not been previously established. In addition, the PCP must refer the infant to the proper community- and education-based services appropriate to the patient's disabilities. Finally, the PCP must ensure that supplies and services are continuously available to technology-dependent infants.

Personal communication between the PCP and parents about their NICU graduate is essential to the physical and emotional well-being of the infant and family. Many questions are likely to arise before discharge, during the first office visit, and over the next months and years. Issues may include keeping the home warm, dressing the infant, allowing visitors, taking the infant outside, avoiding direct sun exposure, and flying to visit friends or family. Other issues may be more specific than these and related to infant's behavior or health. Sample questions include the following:

  • Why does my baby make grunting sounds ("preemie" noises)? Are these sounds abnormal?

  • Why does my baby's nose seem stuffier now than during my baby’s stay in the hospital?

  • My baby seems to sneeze and cough a lot. Is this a sign of illness?

  • When do I take my baby's temperature?

  • Is it bad that my baby has not had a bowel movement for 2 days?

A predischarge meeting of the NICU staff and the family can help ease the transition home. That said, the PCP must realize that questions such as those listed above are common and may seem numerous. Many answers simply involve common sense. To the authors' knowledge, no complete collection of the typical questions parents asked has been published. Therefore, few or no reference sources are available for PCPs. Practical experience is perhaps the only way to become comfortable in addressing many of these questions.

Many concerns may emanate from the parents' perception that their child is vulnerable to a number of physical and intellectual challenges. This view may be obvious to both the PCP and the parents at the time of discharge. The PCP must recognize patients at risk of becoming vulnerable children because the parents feel guilt or are overprotective. This topic is important enough that it is covered specifically in "The Vulnerable Child" section under Counseling Caregivers During and After the NICU Stay.

Parents may wish to learn more about their baby's potential problems or disease than time allows in the NICU or in the physician's office. The parents may seek information about community, state, or national resources to help their infant or child. Tertiary-sponsored follow-up clinics can also be resources, as can governmental or private agencies involved in specialized care or rehabilitation. Helping parents to gain access to reliable information or resources is an important function of the PCP.

 

Assessing/Managing Medical Disorders

Medical disorders in neonatal intensive care unit (NICU) graduates cover a wide range of disease states.[57, 58] The conditions covered in this article include disorders uniquely encountered in premature infants.

Anemia of prematurity

Anemia of prematurity is one of the most common and important problems that the primary care physician (PCP) must address in the NICU graduate. After birth, hemoglobin concentrations decrease more rapidly and more severely in premature infants than in term neonates, with the lowest hemoglobin levels observed in extremely low-birth-weight infants (ELBW) infants.[117]

The PCP absolutely must know the patient's hemoglobin and hematocrit values, reticulocyte count, and transfusion history at the time of discharge. The PCP should obtain postdischarge hemoglobin levels, hematocrit measurements, and reticulocyte counts until the results suggest that the patient's anemia is resolving. In ELBW infants, hematocrits usually stabilize and begin to rise by age 3-6 months.

The PCP must be aware of the signs and symptoms of anemia and know how to manage it appropriately. In a hospital-based study, liberal use of blood may have improved neurologic outcome compared with restricted transfusion,[118] and it is associated with a short-term decrease in apnea of prematurity.[119] For information on the treatment of severe anemia after hospital discharge, see the Medscape Drugs & Diseases article Anemia of Prematurity.

Apnea and bradycardia of prematurity

The American Academy of Pediatrics (AAP) has published a policy review of issues related to apnea of prematurity.[30] The severity of apnea and bradycardia in prematurely born infants is inversely proportional to their gestational age. Causes of apnea include immature central regulation of breathing; obstruction due to immature airway reflexes; and/or delayed coordination of sucking, swallowing, and breathing responses. Infants should not be discharged from the NCIU until they are physiologically stable, with mature respiratory control.

The PCP must consider other diagnoses when apnea and/or bradycardia are the presenting signs or symptoms after discharge. Such conditions include, but are not limited to, the following:

  • Profound anemia

  • Severe gastroesophageal reflux (GER)

  • Hypoxia or bronchospasm related to chronic lung disease (CLD)

  • Infection (especially respiratory syncytial virus [RSV] infection)

  • Malfunctioning or infection of a ventriculoperitoneal shunt

  • Seizures

Apnea can recur in preterm infants after they are hospitalized or after they receive general anesthesia for a surgical procedure (eg, inguinal hernia repair). Apnea and bradycardia of prematurity may occur at home, even in an infant who was free of apneic episodes for more than a week before discharge.[30, 120] In this situation, the PCP may have to consider rehospitalization if an acute life-threatening event has occurred.

If no cause for the apnea is found and if the infant is not receiving a methylxanthine, use of caffeine may be considered in conjunction with cardiorespiratory monitoring.[121, 122] Some premature infants may be discharged with cardiorespiratory monitoring and one of these medications.

Home monitoring

Much discussion has focused on whether home monitoring helps prevent death in preterm infants.[29, 30, 105] Because of advertising in the lay media, parents may request or demand home monitoring. Clinicians must explain to such parents that home monitoring does not prevent sudden infant death syndrome (SIDS).[29, 105]

Exclude late causes of apnea, as described above, before an infant is discharged home. Most infants remain in the NICU until they have outgrown their need for caffeine or home monitoring. An occasional infant may be discharged home with monitoring.

One criterion for stopping home monitoring is a 4- to 8-week period with no clinical apnea, no cyanotic episodes, and no history of monitor alarms. Some PCPs may wish to download and review event recordings before stopping monitoring. Spitzer and Gibson published a scheme for judging the cessation of home monitoring.[123]

Chronic lung disease of prematurity

Initially called bronchopulmonary dysplasia (BPD), CLD of prematurity and its manifestations have changed in the last 2 decades or so.[124]  The incidence of CLD of prematurity, or the "new" BPD, increases with decreasing gestational age.[125, 126]  (See the Medscape Drugs & Diseases article Bronchopulmonary Dysplasia.)

Factors that define CLD include a typical radiographic appearance of cystic emphysema and fibrosis or subtle changes of diffuse interstitial edema and a requirement for inspired oxygen at the 28th day of life or the 36th week of postconceptual age.

The infant presenting in the PCP’s office while receiving home oxygen therapy and multiple medications is at risk for developing cardiopulmonary complications after discharge. To prevent cor pulmonale, forestall intermittent or persistent hypoxemia and clinically significant hypercarbia after discharge, a pediatric pulmonologist, in addition to the PCP, should monitor infants discharged home with severe BPD and considerable need for oxygen and respiratory support.

Home oxygen therapy is a safe and cost-effective treatment and may reduce complications (eg, cor pulmonale) in infants with CLD.[127, 128] Oxygen therapy also appears to facilitate growth in infants with BPD.[129] In the PCP’s office, monitor oxygen saturation rates with pulse oximetry. The level of inspired oxygen required to prevent hypoxemia indicates the severity of disease and whether the patient's condition is improving.

Adjunctive therapy for BPD may include inhaled bronchodilators and/or steroids, oral corticosteroids, and diuretics.[130, 131] Management of CLD may involve oxygen, medications, complex technologies, and superb nutrition.[132, 133, 134]

Issues have arisen regarding whether corticosteroids inhibit normal growth of the lung and brain and whether it causes future pulmonary or neurodevelopmental disabilities. Grier and Halliday proposed an appropriate use of corticosteroids in severe BPD that may be lifesaving and that may also minimize adverse responses in the developing brain.[135]

Infants receiving diuretics to treat CLD require periodic evaluation of their electrolyte status. Bumetanide may be associated with fewer electrolyte abnormalities, especially if dosing occurs on alternate days.[130] Note that furosemide therapy for CLD predisposes these infants to nephrocalcinosis; PCPs may need to screen for nephrocalcinosis by performing serial renal ultrasonography, by assessing urinary calcium-to-creatinine ratios, or by examining the urine for erythrocytes (microscopic hematuria).

No current therapy effectively resolves nephrocalcinosis in preterm infants. However, nephrocalcinosis spontaneously resolves in many, but not all, infants in the first year of life. Prevention may be the key. Use furosemide only when this diuretic is proven effective. When nephrocalcinosis is present, every attempt should be made to stop furosemide or other drugs that cause excessive urinary excretion of calcium. Other diuretics such as spironolactone and chlorothiazide may be used as they are effective in controlling pulmonary edema secondary to BPD and they conserve or prevent loss of calcium in the urine.

Infants who have CLD may require more than 120-150 kcal/kg/day for weight gain because of their increased work of breathing.[133] Therefore, either breast milk with added fortifier or a formula with high energy density may be needed for nutritional support. These infants may also need restrictions in fluid intake, a therapeutic strategy that may further impair their growth.

On occasion, infants with CLD may be discharged with home monitoring. For infants who have the most severe illness, this may include pulse oximetry. These infants are candidates for immunoglobulin therapy to prevent or ameliorate RSV infection. Other pulmonary infections should also be managed with attentiveness and concern.

Gastrointestinal (GI) diseases

Two prominent intestinal problems encountered in premature infants discharged from the NICU are GER and complications arising from necrotizing enterocolitis (NEC). Reviews of GER[136, 137] and NEC have been published.[138, 139, 140, 141]

Gastroesophageal reflux

Suspect GER in premature and term infants who have any of the following manifestations:

  • Repeated regurgitation or emesis after feedings

  • Apnea after feedings

  • Fussiness or painful crying during or after feedings

  • Arching of the head and neck during or after feedings

  • Presence of a nasogastric or orogastric feeding tube

  • Rumination syndrome

Each of these signs or symptoms or conditions takes on additional importance if the child's growth is poor.

GER has been associated with esophageal or duodenal atresia, diaphragmatic hernia, brain injury due to hypoxic-ischemic encephalopathy, prematurity whether CLD is present or absent, and many other neonatal conditions. Although data have suggested that GER may have no role in apnea of prematurity,[30, 136] studies have indicated that GER may be responsible for laryngeal edema, microaspiration, worsening of BPD and apnea, and bradycardia.[30, 136, 142]

Testing to confirm GER has been the subject of contentious debate.[76] Diagnostic tests for GER include contrast-enhanced studies of the esophagus and upper GI tract, radiolabeled scanning after feedings, monitoring of esophageal pH (optimally done with dual high and low probes), and esophagoscopy with or without biopsy. Before a reliable pH probe test can be performed, medications that raise gastric pH must be withdrawn for several days (eg, 2-4 days).

The success rate of medical therapy for GER is less than ideal. Treatments that have been tried for GER include the following:

  • Prokinetic agents (eg, metoclopramide, erythromycin)

  • H2-receptor blockers or proton-pump inhibitors

  • Thickened feedings

  • Positioning to facilitate gastric emptying

Prokinetic agents have proved problematic in the treatment of GER in this infant population, including a heightened risk of infantile pyloric stenosis and cardiac arrhythmia with erythromycin and neurologic side effects with domperidone and metoclopramide.[136] In addition, long-term use of metoclopramide has been associated with tardive dyskinesia.[143]

Erythromycin 1.5-2.5 mg/kg given every 6 hours may effectively treat GER in some preterm infants.[143, 144] However, as noted above, erythromycin therapy may raise the risk of hypertrophic pyloric stenosis, although this complication may occur more frequently when erythromycin is given intravenously at therapeutic doses than with the low oral doses used to treat GER. Nevertheless, if erythromycin is used to treat GER, the PCP should watch for symptoms associated with hypertrophic pyloric stenosis.

Note that H-2 receptor blockers (specifically, ranitidine [Zantac]) have been associated with a potentially increased risk for cancer and were thus removed from the market in 2020 by the US Food and Drug Administration (FDA).[145]

Thickened feedings and positioning effectively decrease GER,[136, 146, 147] but they have had mixed success in treating GER in neonatal clinical trials. Although GER may be a lifelong problem in some infants (eg, term infants with profound brain injury due to hypoxic-ischemic encephalopathy), premature infants generally have self-limited disease that improves as the gastroesophageal sphincter and gastroduodenal motility matures.

Infants with severe GER associated with hypoxic-ischemic encephalopathy may be candidates for treatment with gastric fundoplication. A pediatric gastroenterologist should collaborate with the PCP in caring for infants with severe GER.

Necrotizing enterocolitis (NEC)

For graduates of the NICU who have had NEC, the PCP must be able to care for late complications and problems. Complications of NEC include the following:

  • Need for ostomy care

  • Malabsorption

  • Intestinal dysmotility

  • Need for parenteral nutrition despite enteral feedings

  • Cholestasis

  • Infections of the ascending biliary tract

  • Biliary calculi

  • Late partial or complete bowel obstruction

  • Short bowel syndrome

The prognosis of patients with short bowel syndrome is guarded[148, 149] ; the PCP must follow up with these infants, as should a pediatric gastroenterologist and surgeon. Some of these complications may be present at discharge from the NICU, and some require continued surveillance. Poor growth is a frequent outcome.

Dumping syndrome occurs in infants with ostomies or severe diarrhea during GI infections (eg, those due to rotavirus). This condition may cause rapid dehydration and electrolyte imbalance. Strong evidence suggests that NEC is associated with increased occurrence of adverse neurologic outcomes.[150, 151]

The PCP must be diligent in recognizing growth failure, fluid imbalance, and electrolyte abnormalities in infants with GI disease. Scarring after neonatal GI surgery can cause partial or complete bowel obstruction after discharge. Always investigate repeated emesis, particularly if it is bilious, and/or a sudden onset of abdominal distention. Polymicrobial sepsis may be another indicator of partial or complete bowel obstruction after NEC or GI malformations.

When short bowel syndrome necessitates parenteral nutrition at home, catheter or gut-related bacteremia is a major risk factor. The possibility of bacteremia must be suspected even if the patient has only subtle signs of infection (eg, irritability, low-grade fever, apnea).

A pediatric gastroenterologist should monitor infants who have clinically significant complications secondary to NEC and other GI diseases. In particular, short bowel syndrome occurs in ELBW infants as a complication of NEC and has a high mortality.[149] These infants have complex conditions and require management at a major pediatric gastroenterology or transplant center.

Central nervous system (CNS) disorders

The most common and serious CNS disorders that may be present in premature infants at the time of discharge are posthemorrhagic hydrocephalus, postmeningitic hydrocephalus, periventricular leukomalacia (PVL), and seizures. Term infants may have suffered from hypoxic-ischemic encephalopathy. These disorders place the NICU graduate at high risk for poor long-term neurologic outcomes; thus, affected infants with these problems should be monitored in the NICU follow-up clinic.

The discussion below is mostly limited to CNS complications that affect infants born prematurely. Complications of term infants including hypoxic-ischemic encephalopathy are only briefly addressed in this review. Other common conditions affecting the CNS of NICU graduates include developmental defects in the brain and/or spinal cord that may affect either premature or term infants.

Posthemorrhagic complications

Despite past beliefs, ELBW preterm infants with grade I subependymal or II intraventricular hemorrhage may have poor neurodevelopmental outcomes.[152, 153] Grade III intraventricular or grade IV intracortical hemorrhage is associated with the least favorable neurodevelopmental results, but the degree of prematurity and the presence of chorioamnionitis may also be major contributors to severe long-term disabilities.

Intraventricular hemorrhage may lead to posthemorrhagic hydrocephalus. In turn, intracortical hemorrhage causes cerebral infarction and may culminate in cerebral or cerebellar porencephaly. Porencephaly and posthemorrhagic hydrocephalus are among the most devastating CNS events in premature infants.[154]

The risk of these conditions is inversely proportional to gestational age. If posthemorrhagic ventricular dilatation occurs after intraventricular hemorrhage, it is usually apparent on cranial ultrasonography within 2-3 weeks.

Hemorrhagic cerebral events are occasionally observed in term neonates. Such hemorrhage in term infants carries an ominous prognosis. Infants who have had intracranial hemorrhage must always be monitored in neurodevelopmental follow-up clinics, and they should also be referred to community services because rehabilitation is frequently necessary.

Although ventricular dilatation may be reversible, infants with severe intraventricular hemorrhage with posthemorrhagic ventricular enlargement are at high risk for neurodevelopmental handicap.[155] The PCP must be informed of this clinical scenario.

Rapidly progressive posthemorrhagic hydrocephalus may require permanent placement of a cerebrospinal fluid (CSF) shunt.[155] The long-term neurodevelopment of ELBW infants who require shunt insertion is very unfavorable compared with ELBW infants with intraventricular hemorrhage who do not have ventricular enlargement.[156]

If a ventriculoperitoneal shunt is needed, the PCP must monitor the infant for shunt infections or malfunctions. Malfunctions are typically due to an occlusion of the proximal or distal cannula, with a subsequent increase in intracranial pressure. Poor feeding, vomiting, irritability, lethargy, sleepiness, apnea, and seizures may be signs and symptoms of shunt blockage. If fever or a septic appearance is present, the PCP should suspect shunt infection and meningitis. The patient's head circumference should be monitored for rapid or slow growth.

Periventricular leukomalacia

PVL results from an ischemic infarction of the white matter, most commonly adjacent to the lateral ventricles. It can be observed in either preterm or term infants. The pathogenesis of cerebral white matter injury in preterm infants has been associated with antenatal or intrapartum hemorrhage and severe placental disease (eg, chorioamnionitis).[157, 158] It is widely accepted that both hypoxic-ischemic events and inflammatory processes produce PVL; diffuse PVL is caused by less severe ischemia and resultant free radicals.[159] Postnatal sepsis and NEC are also associated with white matter abnormalities on magnetic resonance imaging (MRI) at term gestation, with adverse neurodevelopmental outcomes.[160, 161]

Other postnatal events leading to PVL include CSF infections or intraventricular hemorrhage, life-threatening apnea and bradycardia, and cardiorespiratory arrest. The quality of general movements of preterm infants at age 3 months can often identify white matter pathology.[162] The condition is otherwise identified on cranial sonograms as echogenic areas in the periventricular white matter or as diffuse damage to the white matter on MRI. Injuries in these areas may evolve into cysts.[161, 163]

PVL is highly associated with subsequent neurodevelopmental disabilities, particularly cerebral palsy (motor dysfunction of infancy or spastic paresis). Persistence of cysts is known to increase the risk of severe neuromotor abnormalities. PVL is always a reason to schedule appointments in a neurodevelopmental follow-up clinic. Affected infants should also be referred to community services that provide early intervention and rehabilitation.

Cranial imaging

Preterm infants whose cranial sonograms show reduced growth of the corpus callosum during the patient's NICU stay are at increased risk for psychomotor delays and cerebral palsy.[164] Moreover, abnormal findings on MRIs obtained at term in very preterm infants at term corrected age are predictive of adverse neurologic outcomes.[164, 165, 166, 167]

Some investigators believe that identification of neuroanatomic abnormalities on MRI scans can predict the need for early interventions.[168] The PCP should be advised about any imaging findings that suggest the possibility of an unfavorable neurodevelopmental outcome before the patient is discharged home, and the parents should be fully counseled about the findings. Whether this knowledge, when conferred to parents, enhances or diminishes parental involvement in their infant's rehabilitation is controversial.

Seizures

A history of neonatal seizures is associated with long-term psychomotor or neuromotor handicaps.[169, 170, 171] Reasons for neonatal seizures include hypoxic-ischemic injury, direct cerebral trauma, intracranial hemorrhage, metabolic abnormalities, malformations, and infections. Neurodevelopmental outcomes after neonatal seizures are clearly related to the etiology of the seizures. However, in some patients, a specific cause is never determined.

When known, the cause may be predictive of the ease or difficulty with which the seizures can be controlled with anticonvulsants. Phenobarbital has been the mainstay of anticonvulsant therapy for neonatal seizures[172, 173, 174] ; however, levetiracetam, lorazepam, and fosphenytoin have also been safely used to control seizures.[175]

The duration of treatment for neonatal seizures is controversial, partly because of concerns that anticonvulsants may hinder brain development; therefore, the use and duration of these agents should be done in conjunction with a pediatric neurologist. Among infants without signs and symptoms of seizures, and in the absence of electroencephalographically recorded seizures, pediatric neurologists may recommend discontinuing anticonvulsants before the patient's discharge or shortly thereafter. Before anticonvulsants are withdrawn, electroencephalography must be performed to exclude subclinical seizures.

A neurologist should evaluate any NICU graduate who has persistent or difficult-to-control seizures. These infants should also be monitored in neurodevelopmental follow-up clinics and referred to appropriate community services.

A common neurologic condition associated with neonatal seizures is hypoxic-ischemic encephalopathy. Maternal intrapartum conditions that commonly result in profound hypoxic-ischemic encephalopathy include placental abruption, uterine rupture, and prolonged cord compression. Hypoxic-ischemic encephalopathy is a devastating event that most often affects term neonates. Survivors of hypoxic-ischemic encephalopathy have long-term sequelae more commonly than survivors of extreme prematurity. All neonates with Sarnat stages 2 (moderate) and 3 (severe) hypoxic-ischemic encephalopathy should be enrolled in follow-up programs.[176] The PCP should be aware of whether the hypoxic-ischemic encephalopathy was treated with therapeutic hypothermia.[177]

If infants have profound damage (often in association with a burst-suppression pattern on initial electroencephalography and an abnormal MRI finding), extensive home care and community services may be required. The PCP must monitor the patient for recurrence of seizures many months after anticonvulsants are discontinued. The PCP has the responsibility for coordinating the complex care required by infants with hypoxic-ischemic encephalopathy.

Eye problems

Retinopathy of prematurity (ROP) has a complex pathophysiology and is an important problem that the PCP must monitor because blindness from this condition is one of the most devastating complications of preterm birth. Certain clinical conditions, such as infections, increase the risk of ROP, and its association with oxygen therapy is long known, but this causal relationship is complex. One firmly established etiologic factor is the degree of prematurity. Therefore, the infants at highest risk are those who were born prematurely with an ELBW.

The American Academy of Pediatrics (AAP) published guidelines for ROP screening in 2013,[35] with the most recent update in 2018.[36] A subspecialist trained to recognize neonatal retinal diseases not only must perform the screening for ROP but also must continue to examine the patient and make recommendations for follow-up examination of the neonatal retina until it is fully vascularized.

Complete vascularization usually occurs by 44-48 weeks after conception but occasionally takes longer. Screening examinations are important, because if retinal detachment (ie, threshold disease) is a risk, the infant may be referred for laser therapy of the retina to prevent it. Studies from the United Kingdom have proposed more aggressive criteria for intervention when preterm infants have ROP.

Retinal detachment can also occur relatively late in life. Again, this is particularly common in premature ELBW infants. Preterm infants who have had evidence of ROP must also be screened for refractive disorders and for amblyopia at 6 months after discharge, at age 2-3 years, before they begin school, during grade school, and during adolescence when rapid growth of the ocular globe is occurring.

Infants with a history of ROP are also at greater risk for myopia and amblyopia. In later life, glaucoma may also be more common in preterm infants than in their term counterparts. When a PCP examines premature infants younger than 1 year, the PCP must assess the baby for strabismus.

Hearing problems

The incidence of hearing loss is higher in NICU graduates than in the general population of well neonates. Many factors can contribute to such hearing loss, including hypoxia, certain drugs used alone or in combination, and infections.

Silent or symptomatic congenital or postnatally acquired cytomegaloviral (CMV) infection is highly associated with hearing loss in later life, and this hearing loss may progress over time. Most NICUs in the United States use only CMV-seronegative blood for red blood cell transfusions, which has lowered the incidence of acquired postnatal CMV infection among hospitalized neonates, but infants might still become infected with CMV from platelet or plasma-derived blood products.

All NICU graduates must undergo a hearing evaluation before leaving the hospital. A number of devices are available for this purpose. The PCP should be informed at discharge whether the patient passed the hearing screen. If the infant did not, they must be referred to an audiologist who practices with a pediatric otolaryngology specialist.

 

Developmental Follow-up

Advances in neonatal intensive care have improved the survival and lowered the morbidity of high-risk neonates[178, 179] ; however, this improvement has not been accompanied by a proportional decrease in certain morbidities. As a result, reduction in mortality does not necessarily equal a reduction in rates of certain disabilities. Cognitive deficits without major motor deficits are now the dominant neurodevelopmental sequelae.

As the total number of neonatal intensive care unit (NICU) survivors at potential risk for neurodevelopmental morbidity increases, many clinical research questions with major ramifications on medical care have evolved. These questions can be answered only by performing long-term follow-up studies, because many of the neurocognitive deficits are not identified early on.[180]

Although neurodevelopmental outcomes can be used to determine the efficacy of medical interventions in infants born preterm, long-term follow-up studies are infrequently performed because of cost and subject dropout. The bias of neurodevelopmental data is that they are not as precise as radiographic or biologic measurements. There is also concern that it is the pattern of change over time versus a one-time assessment that is most predictive of outcome.

In addition, confusion occurs because of the following factors[181, 182] :

  • The frequent disconnect between adverse perinatal experiences and later outcomes

  • The moderating and mediating effects of socioeconomic status and other environmental influences

  • The long time lag necessary to complete longitudinal assessments

Besides initial biologic risks, perinatal interventions designed to address these risks may substantially affect later development. Therefore, extended follow-up is critical to identify possible negative effects that a medical intervention or the standard of care might have on the child’s brain that might not be obvious in the first years of life. This point was clearly demonstrated in the use of postnatal steroids to treat chronic lung disease[183] and with the use of oxygen in causing late visual impairment and developmental delays.[184, 185]

Of interest, standardized guidelines about follow-up services for high-risk infants in tertiary care centers are lacking despite the requirement for approved neonatal fellowship training programs to include experience in follow-up clinics and the increasing number of centers involved in networks.[186]

A National Institute of Child and Human Development (NICHD)–National Institute of Neurological Disorders and Stroke (NINDS) workshop on follow-up care of high-risk infants identified surveillance and research as the two primary areas of responsibility for neonatal follow-up programs.[186] Surveillance involves monitoring medical care during hospitalization and serial evaluation of health and neurodevelopmental outcomes after discharge. This process is necessary for the following reasons:

  • Auditing of NICU interventions

  • Monitoring of important quality indicators for the individual NICU

  • Summarizing center-specific outcomes for selected conditions (eg, intraventricular hemorrhage, retinopathy of prematurity [ROP])

  • Summarizing annual outcome data to be combined and used in policy decisions

Provision of feedback to the family and the primary care physician (PCP) at each serial evaluation and appropriate referrals are in line with the medical home concept. Follow-up research data are necessary to evaluate the long-term effect of medical interventions and to identify previously unidentified adverse risks. Areas of concern include social issues; neurologic, cognitive, behavioral, and physical issues; health-related quality-of-life; and functional outcomes.

Outcome studies have primarily emphasized the incidence of major disabilities such as moderate-to-severe intellectual disabilities, sensorineural deficits (eg, hearing loss, blindness), cerebral palsy, and epilepsy. Disabilities increase as birth weights decrease.[187, 188] Cognitive and motor scores below 70 are the major neurodevelopmental disabilities. The same inverse relationship is found with gestational age and the prevalence of disabilities.

The nature of impairment in premature infants is changing, with notable problems found in survivors without the major disabilities just described.[181] For example, many children now show developmental coordination disorders (DCDs), which some consider to be on a continuum with cerebral palsy.[189] Recognition of this change may be related to changes in medical management, longer follow-up, refined assessment techniques, and improved survival rates.[181]

High-prevalence, low-severity dysfunctions[181, 190] appear to be increasing, particularly in premature infants of lower birth weight and gestational ages.[191, 192, 193] These abnormalities include the following:

  • Learning disabilities

  • Borderline to low-average intelligence quotients (IQs)

  • Attention-deficit hyperactivity disorder (ADHD)

  • Specific neuropsychological deficits (eg, visual motor integration, executive dysfunction)

  • Behavior problems (internalizing problems, social difficulties)

High-prevalence, low-severity dysfunctions may occur in as many as 50-70% of very low birth weight/very preterm (VLBW/VPT) infants, with an inverse relationship to birth weight/gestational age. Thus, VLBW/VPT and extremely low birth weight/extremely preterm (ELBW/EPT) infants have the highest risk. An estimated 25-40% of VLBW/VPT children require special education services, 20% or more need a self-contained learning disabilities placement, and 16-20% repeat a grade in school.[194] As many as 60-70% of ELBW/EPT children require special assistance in school. Conversely, 17% of late-preterm (34-36 weeks’ gestational age) require such services—this in comparison to a 2.3-8% rate in children born full term. Moreover, these dysfunctions do not occur in isolation. Affected infants more often than not have several concomitant problems that synergistically produce academic difficulties.

The situation is complex because the parents' social, ethnic, and educational backgrounds may also influence the prevalence of these disabilities. In addition, although major disabilities are often identified during infancy, high-prevalence, low-severity dysfunctions become more obvious as the child reaches school age and performance demands increase. Further compounding the issue is that predictors of these subtle problems are difficult to identify during infancy or preschool age.

It is extremely difficult to determine in early infancy whether problems are transient and result from continuing recovery or are catch-up from the negative effects of preterm birth or whether they reflect the emergence of a permanent handicap. Stated differently, below-average functioning could be indicative of a delay or a deficit. Many functional outcomes cannot be adequately gauged until the child encounters broad, complex demands and situations that require developmentally complex functions. Preexisting deficits in these functions become apparent only when they are challenged directly.[181]

This situation again substantiates the necessity of longitudinal follow-up. Follow-up protocols vary in terms of patients who should be followed, levels and frequencies of follow-up, and testing and outcomes of interest.

Patients who require follow-up

As mentioned previously, clinicians should consider birth weight and gestational age when determining who should be monitored following hospital discharge. Neonates are categorized into one of the three following gestational groups:

  • Extremely premature (EPT): Less than 28 weeks' gestation

  • Very premature (VPT): 28-32 weeks' gestation

  • Premature: 33-36 weeks' gestation (late preterm is 34-36 weeks)

Categorization on the basis of birth weight alone may result in the inclusion of infants who are relatively mature but whose growth was restricted because of an adverse intrauterine environment. In addition, use of birth weight alone may bias evaluations or biomedical findings, because conditions such as periventricular leukomalacia (PVL) are relatively infrequent in growth-restricted fetuses. ELBW infants need follow-up assessments because they are subject to “2-hit” CNS involvement. The CNS of the at-risk infant is potentially subject to developmental disruption, insult, or both (eg, first hit: growth restriction; second hit: sustained systemic inflammation[195] ). Premature birth changes the spatial and temporal progression of brain structures (eg, migration, organization and differentiation, myelination) and alters brain architecture and connectivity. Also compounding the disrupted brain development are altered postnatal visual, auditory, tactile, and vestibular-proprioceptive experiences.

The CNS of high-risk fetuses and neonates is also frequently subject to insults, such as maternal infections, exposure to proinflammatory cytokines, hypoxic-ischemic encephalopathy, intraventricular hemorrhage, or PVL. Extreme prematurity (weight < 1000 g or age ≤ 28 wk), regardless of other factors, increases the risk of CNS insults, including grade III or IV intraventricular hemorrhage, PVL, and seizures. Many infants have both developmental disruption and insult, with the brain areas having the greatest rapidity and complexity of developmental events being most vulnerable to negative exogenous and endogenous influences. This is analogous to so-called encephalopathy of prematurity.

CNS risk criteria differ depending on whether the infant was born preterm or at full term. Moreover, medical conditions can exacerbate the risk; examples of such conditions are the following:

  • Extracranial or intracranial trauma

  • Respiratory disorders

  • Infections

  • Hyperbilirubinemia that requires exchange transfusion

  • Encephalopathy

  • Fetal growth restriction

Likewise, interventions to deal with specific disease states (eg, resuscitation, prolonged ventilation, postnatal steroids, total parenteral nutrition) can also raise the risk. Also contributory are social and/or environmental risks; these often occur in conjunction with biologic risks and place infants at double jeopardy of adverse behavioral and developmental outcomes.[196]

Levels of follow-up

As indicated in the NICHD/NINDS workshop, levels of follow-up can differ.[186] The workshop monograph identified four levels of follow-up intensity, as summarized below.

Level I follow-up could consist of a telephone interview from a designated NICU staff member or use of a screening instrument, such as the Cognitive Adaptive Test and Clinical Linguistic and Auditory Milestone Scale (CAT/CLAMS),[197] the Ages and Stages Questionnaire-3,[198] or the Bayley-4 Adaptive and Social-Emotional Scales.[199] Subsequent referrals could be made as needed.

Level II follow-up could involve a clinic visit with the use of one of the aforementioned screening instruments or a hands-on test, such as the Bayley Infant Neurodevelopmental Screener (BINS),[200] or the Bayley-4 Screening Test.[199] Additional allied professionals, such as a dietitian and physical, occupational, and speech therapists, may or may not also evaluate the child.

Level III follow-up can entail comprehensive assessment at a single visit (eg, Bayley-4), and level IV follow-up involves serial assessments by a multidisciplinary team.

Frequency of follow-up

The frequency of follow-up contact is superimposed on the level. Patients at high risk or those in whom neurodevelopmental problems have already been identified should be evaluated soon after discharge from the NICU and frequently thereafter. In general, serial contact is recommended whether follow-up is for surveillance (eg, quality assurance) or for research purposes, and regardless of the level of follow-up.

The frequency of follow-up involves two issues: the optimal ages for assessment and the intensity or level of follow-up, which also depends on constraints such as cost, personnel, and/or unique characteristics of the center. Some have found that beginning follow-up visits shortly after discharge enhances the likelihood the family will continue with subsequent visits.

Evaluation at corrected age 6 months

Evaluation at corrected age 6 months (chronologic age minus weeks born prematurely) offers a window during which indicators of severe handicaps can be identified. An evaluation at this time also provides early contact with the family, enhances continuity of contact, and helps to ensure that children are receiving early intervention services.

By this age, the influence of many medical and/or biologic issues is decreasing. However, recovery from medical procedures, feeding difficulties, and subsequent hospitalizations may still affect neurodevelopmental assessments. Tone, neurosensory (eg, auditory, visual) functions, gross and fine motor coordination, early verbal skills, interactive capacities, early indicators of attention, and some cognitive processes can be evaluated.

Use of assessment before this age is questionable. Screening with tests such as the BINS or Bayley-4 Screening Test may be sufficient, but this approach again underscores the interplay between the frequency and level of follow-up.

Evaluation at corrected age 12 months

Environmental factors do not exert a major influence at this age, and biomedical issues, such as oxygen supplementation for chronic lung disease, tend to improve and have a lesser effect on testing. By 12 months’ corrected age, a varied behavioral repertoire is emerging, motor skills are developing, and cognitive processes and early language skills can be assessed.

However, at corrected age 12 months, cognitive and motor functions are still highly intertwined, and this period of developmental acquisition is a time of variability as well. Some neurologic abnormalities identified in the first year of life are now transient or improving (eg, transient dystonia of prematurity). Conversely, findings in some infants worsen over time.

Evaluation at corrected age 18-24 months

By corrected age 18-24 months, environmental factors exert increasing influences on evaluation results. Cognitive and motor abilities diverge, language and reasoning skills develop, and the ability to predict early school performance improves. However, many intelligence tests have weak floors at this age, restricting assessment to only developmental tests. As a result, more subtle impairments may be underestimated. Test refusals may invalidate results or produce false-positive results. Some developmental assessments such as the Bayley-4 (see above) now allow for limited caregiver report.

Judging performance at age 2 years on the basis of corrected age (chronologic age minus weeks born prematurely) rather than actual age is controversial but generally accepted. There are some professionals who report that the duration of age adjustment should be extended to 3 years or later in infants born in the lower range of viability.[201] Standard follow-up protocols in many multicenter networks specify how the age at evaluation is calculated.

Evaluation at age 3-4 years

Intelligence can first be assessed at age 3-4 years. Intelligence includes concept development, pre-academic readiness skills, early indicators of executive function and attention, and abilities in visual-motor integration. Verbal and nonverbal skills can be differentiated. Moreover, the predictability of later IQ on the basis of scores at this age is acceptable. Environment and social support, as well as other factors, broadly influence test results most strongly from this age onward.

Evaluations at age 6 years and age 8 years

By age 6 years, additional tests and procedures can be used to access attention problems, academic skills (at approximately the first-grade level), socialization, and neuropsychological functions, particularly executive function. The selection of possible tests that can be used is more limited at age 5 years than at age 6 years.

By age 8 years (approximately the third grade), intelligence, neuropsychological functions, learning disabilities, school performance, and social and behavioral adjustment can be adequately assessed. The predictive validity of IQ scores is highest now compared to earlier ages.

Summary of the frequency of evaluation

Evaluation after age 3-4 years is often not feasible in many follow-up programs whose main focus is surveillance. This is when the PCP should monitor the child's school performance and periodically review developmental, cognitive, academic, and behavioral concerns.

 

Testing and Outcomes of NICU Graduates

In addition to obvious moderate-to-severe disabilities, other suboptimal neurodevelopmental outcomes can occur in high-risk infants, such as the following:

  • Motor and neurologic deficits (including developmental coordination disorder)

  • Reduced intelligence (usually in low average to borderline range)

  • Learning disorders (math, spelling, reading)

  • Language difficulties (processing)

  • Visuomotor problems

  • Impaired executive function (attention, inhibition, working memory)

  • Attention-deficit/hyperactivity disorder (ADHD)

Motor and neurologic deficits

Motor and neurologic outcomes are major concerns when they arise as a high-risk infant matures. Different risk factors may affect these outcomes,[180, 202] with the link between perinatal problems and deficits in these areas appearing to be relatively direct. The incidence of transient dystonia in preterm infants peaks at 7 months’ corrected age, with a prevalence of 21-36%.[203]

It is noteworthy that children with dystonia have an increased risk of later cognitive and motor problems. Neurologic soft signs (eg, motor, sensory, or integrative functions but not localized brain dysfunctions) are often recognized. These deficits increase the risk of subnormal IQ or learning disabilities (particularly math and reading) in children with normal IQs.

Upper extremity motor tasks involving visually guided ballistic arm movements (eg, bouncing, catching, throwing) are particularly affected.[204] The proposed underlying mechanism is that parallel mental dysfunction involves circuits in the neighborhood of motor tracts that also sustain damage, but these abnormalities are not apparent until later in life. Motor injury is more self-correcting, whereas cognitive abnormalities are not.

Reduced intelligence

In a 1989 meta-analysis, low birth weight (LBW) infants had a mean IQ score that was 5-7 points below that of control children.[205] More recent studies continue to confirm that preterm infants have a lower mean IQ scores compared to their term peers.[181, 190, 206]

Studies have shown that children with birth weights below 1500 g and without major disabilities had mean group IQ scores ranging from borderline to average, with most of the data suggesting that a low-average score was the mode.[181, 190, 207] These children's scores are generally 8-11 points lower than those of their full-term counterparts or even siblings.

A meta-analysis of 16 studies indicated that VLBW/VPT infants had IQ scores that were 10.9 points below their full-term peers (0.66 standard deviation [SD]).[207] There was a gestational age gradient: the smaller or younger the infant, the lower the mean group IQ. Based on meta-analyses, the EPICURE study[191, 193] and the Bavarian Longitudinal Follow-up Study,[208] for each week of gestational age younger than 33 weeks, there is an average mean decline of 1.7-2.5 IQ points. Correlations between gestational age and cognitive scores, as well as between birth weight and cognitive scores, generally are r = 0.50 (thus accounting for 25% of the variance).

Such changes in intelligence place affected children at a distinct disadvantage when they have to compete with peers whose IQ scores are average or above. Moreover, the lowered IQ scores typically do not occur in isolation.

Learning disorders

More than half of all former VLBW/VPT infants and 60-70% of ELBW/EPT infants require special assistance in school. By middle school, ELBW/EPT infants are 3-5 times more likely than those born at term to have a learning problem in reading, spelling, writing, or mathematics, with mathematics and written language being most disrupted.[194, 209]  Overall, it appears that in descending order, disabilities are found in math, written expression, spelling, and reading.

Approximately 16-20% of children born VLWB/VPT repeat a grade, and 20% are taught in self-contained classrooms for students with learning disabilities. Almost one third are in mainstream classrooms, but these children are functioning more than one grade below their placement.[194] Once again, there is a gestational age gradient: 25-40% of those born at younger than 32 weeks are retained, 20-30% of those at 32-33 weeks, and 17% of those at 34-36 weeks (vs 2.3-8% of infants born at ≥37 wk).

Many children born prematurely later develop nonverbal learning disabilities (NVLD).[210] Environment, sex, and heredity also have moderating effects, and learning disorders are likely related to both medical-biologic and environmental risks. The prevalence of learning disorders appears to increase 4-fold in children born at risk.[181] Despite broadly normal IQ, one third of these children have more than one learning disability.

Language difficulties

Functional magnetic resonance imaging (MRI) and event-related potential studies indicate differences in the way auditory and language functions are carried out in infants born prematurely.[211, 212] Language is also susceptible to negative environmental influences.

For preterm infants, many language functions are in the average range, particularly vocabulary, receptive language, verbal fluency, and memory for prose. However, relative to term infants, preterm infants demonstrate deficiencies in relatively complex and subtle verbal processes or measures, such as the following[213, 214] :

  • Understanding syntax

  • Abstract verbal skills

  • Verb production

  • Mean length of utterance

  • Auditory discrimination

  • Ability to follow complex instructions

  • Organization

  • Language processing and reasoning

Deficits in verbal working memory may also be present. In a meta-analysis, Barre et al found that, on average, children born VPT had language test scores that ranged from 5.7 to 11.6 points less than that of controls at school age.[215] This has an impact on social and academic functioning.

Visuomotor problems

Most VLBW/VPT and ELBW/EPT babies manifest later visuomotor problems.[216]  The following skills may be affected[217, 218, 219] :

  • Copying

  • Perceptual matching

  • Spatial processing

  • Finger tapping

  • Pegboard performance

  • Visual memory

  • Spatial organization and visual-sequential memory

  • Handwriting speed and legibility

A greater proportion of preterm patients are left-handed than in the general population. In addition, their probability of needing glasses is 3-fold greater than that of healthy full-term infants. These deficits may contribute to problems with written expression.

Impaired executive function

Executive function is a broad term that refers to coordination of many interrelated processes. It involves purposeful, goal-directed behavior that is instrumental to cognitive, behavioral, and social functions. Executive functions are necessary to plan, execute, and update behavior in response to changing environmental demands. Problems in executive function are reported in children born prematurely, especially if they have white-matter pathology.[220, 221, 222]

Children born VLBW/VPT reportedly have 2-3 times greater difficulty initiating activities, displaying flexibility in generating ideas and strategies for problem solving (shift/switching), holding information in short-term or working memory, planning a sequence of actions, verbal fluency, and organizing information. These deficits appear to be in the so-called "cool" metacognitive processes, versus the "hot," behavioral regulation executive functions (ie, inhibition, emotional control). Deficits in executive function have an impact on IQ, academics, fluid intelligence, and social competence.

Attention-deficit hyperactivity/disorder

Symptoms suggestive of ADHD are reported to occur 2.6-4 times more frequently in children born VLBW/VPT and ELBW/EPT than in control subjects, with some estimates indicating a 6-fold increase. The male predominance is not as great as in the general population, and there is no strong association with oppositional defiant disorder or conduct disorder. The modal range of ADHD is 20-33% in this population (vs 8-10% in the general pediatric population). Vigilance/alertness is more of a problem than is impulsivity, with the inattentive presentation being more frequently reported than the combined presentation. The association between prematurity and ADHD is indirect and could be influenced by environmental advantages and disadvantages.[223]

Other behavioral features have been associated with prematurity. Shyness, unassertiveness, withdrawn behavior, anxiety, depression, and social skills deficits occur more frequently in LBW children than in infants born with normal birth weights.[224, 225, 226] Johnson and Marlow reported a “preterm behavioral phenotype” that includes inattention, anxiety, and social difficulties, with a 3- to 4-fold increased risk for disorders in childhood.[227]

Autism spectrum disorders (ASDs)

LBW and prematurity have been cited as risk factors for ASDs. In a study by Limperopoulis et al, 20% of 91 toddlers who were VLBW infants had positive results on the Modified Checklist for Autism in Infants and Toddlers (M-CHAT).[228] Although the M-CHAT does not diagnose an ASD, positive findings raise concerns. More recently the M-CHAT was used in the EPICure2 study and applied to children born at 26 weeks.[193] A positive screening was found for 41% of the children, and 62% had coexisting disabilities; 95.5% of those with severe motor disabilities and 55.9% of infants with cognitive impairment screened positive, suggesting that a positive screen must be viewed in light of other neurodevelopmental sequelae.[229, 230]

Currently, evidence is insufficient to implicate any one perinatal or neonatal factor in ASD etiology. Exposure to a broad range of general, negative influences on prenatal, perinatal, and neonatal health increases the risk, perhaps in an epigenetic fashion. Moreover, differences seem to exist between screening instruments; in the National Institute of Child and Human Development (NICHD) neonatal network, of infants born at less than 27 weeks and screened at 18-22 months, 20% scored positive on one screen, but only 1% scored positive on all three screeners that were used. The items failed were indicative of deficits found in children with language and motor delays, again suggesting confounding comorbidity issues.[231]

Schendel and Bhasin reported data from a longitudinal surveillance study that indicated a 2- to 3-fold increase in ASDs in infants born as either LBW or preterm infants compared with peers.[232] An increased tendency was observed toward ASD and mental retardation, intellectual disability, and/or developmental disability compared with ASD alone.

Moster et al used data from the National Registries of Norway and followed more than 900,000 individuals into adulthood, finding that the prevalence of ASD in those born prematurely was 2-3 times greater than in the general population and perhaps 7-9 times greater in ELBW infants.[233] These investigators reported an odds ratio (OR) of 9.7 for ASD in those born at 23-27 weeks' gestation and an OR of 7.3 for those born at a postconceptual age of 28-30 weeks.

Finally, in a long-term outcome study of adolescents born LBW/PT, 5% were found to have an ASD, a finding 5-times greater than that of the general population.[234]

Although further investigation is needed, this trend underscores the need for ASD screening at the 18-24 month NICU follow-up visit.

Late preterm infants

Another area of increased interest involves infants born in the late preterm range (34-36 wk); this group comprises 75% of preterm births. Normally, in the last 6-8 weeks of gestation, a 35% increase in brain size and a 5-fold increase in white matter volume occurs; neuronal connectivity, dendritic arborization, synaptic junction formation, and maturation of neurochemical and enzymatic processes occur.[235]

Chyi et al reported that late preterm (LPT) infants had lower reading and math scores than their term counterparts in kindergarten and first grade, and they had lower teacher ratings of reading from kindergarten through fifth grade.[236] The likelihood of special education involvement was 1.4 to 2.1 times higher.

Similarly, Huddy et al reported that one third of their sample of children born at 32-35 weeks' gestation had special education needs.[237] Moster et al documented a risk ratio (RR) of 1.6 for mental retardation/intellectual disability and 1.5 for psychological, developmental, or emotional disorders in late preterm infants.[233]

One of the big questions is the reason for late preterm delivery, including the possibility of multiple births. Although, as a general rule, these children do better than their younger preterm counterparts, they do not do as well as their term peers.[238] This was also found with the clinical populations for the Bayley-4 standardization where moderate and LPT scores were only slightly lower than their normal birth weight peers.[199]

These data suggest that late preterm infants have an incidence of sequelae that falls on a continuum between those born at younger gestational ages and those born at term. Given the large number of these infants, many programs do not routinely follow them, despite the increased risk for neurodevelopmental problems. As a result, the primary care physician should monitor the cognitive and academic performance of these children during routine surveillance.

 

Areas of Assessment and Assessment Tools

Proper assessment is critical to evaluate the areas of function that may be impaired in neonatal intensive care unit (NICU) graduates. In both research and clinical surveillance programs, the ideal situation is to extend assessment beyond traditional intelligence quotient (IQ) and achievement testing. Global scores may not help in identifying subtle problems that can interfere with a child’s learning and development.

Tests or rating scales should be directed at measuring the following areas that are likely to be deficient[181, 190] :

  • Intelligence, including verbal and nonverbal function

  • Achievement

  • Attention and executive functions: Planning, organization, monitoring, inhibition, working memory

  • Language: Phonologic awareness, syntax, verbal fluency, comprehension of instructions, high-order abstracting and processing functions

  • Sensorimotor functions: Visual-motor precision, fine motor speed

  • Visual-spatial processes: Design copying, visual closure, visual-spatial planning, handwriting

  • Memory and learning: List learning, delayed recall, narrative memory, assessment of semantic, strategic, rote, and episodic verbal and visual functions

  • Behavioral adjustment: Attention-deficit/hyperactivity disorder predominantly inattentive (ADHD-I), internalizing and socialization problems

Detailed evaluation obviously raises costs, which may be difficult to justify and therefore unfeasible in many clinical or research settings. A compromise is to use representative tests to measure areas of function that are likely to be problematic in children born prematurely or to assess certain functions at different times. Multiple tools are available for assessing the premature infant; they vary based on areas to be tested and ages at which they should be utilized. Some tools require specific training for use and should be performed by a developmental pediatrician, whereas others are easier to conduct in the setting of the primary care physician (PCP) office.

In summary, developmental follow-up is a critical component of the overall care of high-risk infants. Numerous options are available in terms of level, frequency, and patient age at the time of assessment.

Summary

Follow-up of high-risk infants can be undertaken for surveillance, research, or both. However, serial evaluation is necessary because of rapid developmental changes during infancy, silent periods, test behaviors in young children, and increasing environmental and educational demands that may uncover previously unidentified deficits. Medical status and quality of life should also be monitored. The child’s family and the PCP should be active partners in this entire process.

 

Counseling Caregivers During and After the NICU Stay

Whether they are dealing with extreme prematurity or serious malformations, parents of high-risk neonates typically ask two basic questions during counseling: "Will my baby survive?" and "Will my baby be normal?"

These questions cannot be easily addressed, and the answers depend on circumstances of the individual infant. Therefore, responses may need to be given in general terms, which can be frustrating for parents. These questions may arise again during the infant's hospital stay, although parents may be reluctant to ask them again because of their fears about the potential answers.

When an infant arrives in the neonatal intensive care unit (NICU) or in the office during follow-up visits, another important question is, "Is my baby gaining weight or growing?" Parents often reduce their fear and apprehension to these simple terms. The psychological trauma parents experience when their infant is hospitalized in the NICU cannot be underestimated.[239, 240]

One of the most difficult and perhaps most overlooked aspects of care of the high-risk neonate is effective, timely, and compassionate delivery of information to parents and family members by the medical staff involved. Although most members of the medical team are well prepared to meet the physiologic and medical needs of the infants they care for, the psychological, emotional, and spiritual needs of the family members can be ineffectually met when concern is directed primarily toward the infant.

The goal of communication is to provide information to all who need it in an efficient and compassionate manner. Parents are often the first people to whom a change in the patient's status and in future plans for the infant should be directed, but others may also require this information. Social service agencies, state and federal agencies, and pastoral support staff may also require timely updates according to the desires of the particular parents.

To effectively counsel parents of high-risk neonates, caregivers should identify the specific needs of the family early in the infant’s hospitalization. Also, members of the medical team should be aware of their individual skills and responsibilities in interacting with parents and extended family members.

A helpful approach is to plan a visit occurring immediately before or soon after discharge to ascertain the parental expectations regarding their child's outcome and follow-up care. As risk factors for later problems are identified, these must immediately be explained to parents and other care providers in a manner that is understandable and complete. Healthcare providers must be able to collaborate with parents who may feel isolated and who may be in various stages of grieving.

By suggesting support services or parental support groups, providers may assist parents in coping with the stresses of uncertainty regarding their individual situation and their child's anticipated outcomes.[241] Please see Resources for Parents and Healthcare Professionals.

By the time of discharge, the NICU and hospital staff should have established the parents’ understanding about their infant’s status and potential outcome. Medical conditions that require close follow-up should be identified and communicated, and care plans should be developed. Providers must understand and accept cultural diversity in child care, and skilled medical interpreters should be available when necessary. Each medical provider must listen carefully to the parents’ questions to answer them as well as any implied questions.

The medical team can anticipate that parents will have new questions regarding their child’s potential outcome and abilities at subsequent visits. Goals of medical professionals and other professionals should be to explain previous problems and risks in relation to current physical and developmental findings.

It is important to avoid using medical jargon; instead, use language that is appropriate to each parent’s level of understanding. For example, early use of the term cerebral palsy to explain motor dysfunction of infancy or spastic paresis desensitizes parents to it and may open avenues of explanation regarding neurologic dysfunction and therapeutic intervention.

The phrase "out of the normal range" must often be carefully explained. Although the phrase may be distressing to parents, its use may allow an infant to qualify for interventional services earlier than otherwise possible.

Providers must often explain the difference between medical and parental responsibilities. Initial counseling should be directed at the importance of maintaining the discharge plans, including preventive healthcare. Address routine healthcare at each visit, including immunizations and safety counseling. The need for respiratory syncytial virus (RSV) prophylaxis and influenza vaccination may be important points of discussion for infants with chronic lung disease.

Reinforce regular multidisciplinary neurodevelopmental evaluation, as well as the necessity for preplanned or future referrals to medical specialists. In discussions about outcome, introduce the potential need for periodic or regular evaluations by gastroenterologists, nutritionists, neurologists, rehabilitation specialists, orthopedic surgeons, physical therapists, occupational therapists, and speech therapists.

In the process of discharge planning and follow-up, providers should stress the uncertainty of outcomes for specific neurologic risks in the extremely low-birth-weight (ELBW) infant. The propensity for later dysfunction should be discussed, even if an infant appears to be doing well during early follow-up.[187, 242] Although the relative statistical risks associated with some of the previously described conditions should be covered, clinicians must carefully explain that definitive medical diagnoses can be appreciated only over an extended period.

Physicians must be candid in discussing abnormalities found on examinations in the NICU or during early follow-up visits, especially if they increase the risk of an adverse outcome. Providers may want to avoid sharing this information because it creates sadness and anger in the parents and other caregivers; nevertheless, the provider must undertake this task because the parents may later claim that they were never told that their infant was affected or at risk. Thoroughly document these discussions in the child’s medical record. It may also be helpful to hold these conversations in conjunction with social workers or care managers present, as appropriate.

Avoiding the truth about potential neuromotor and psychomotor disabilities may destroy the relationship and future collaboration between providers and caregivers. Honesty regarding an unfavorable outcome also enables parents and other caregivers to understand what interventions and therapeutic plans are needed.

The counseling process is often complicated because of denial of the apparent facts by the parents and family members. Although honesty regarding anticipated outcomes is always wise, stressing that many high-risk situations change in ways that are not initially evident is prudent. Unrealistic parental hopes can be gently addressed and should not be ridiculed or disparaged.

A stable and consistent home environment almost always improves the infant's outcomes. Parental or familial guilt over a poor neuromotor and/or psychomotor outcome in an ELBW infant or an infant with a malformation syndrome that requires complex medical care can result in serious discord in the family. The provider must always be aware of this potential situation and be ready to intervene with counseling. Disruption of the family unit only potentiates unfavorable outcomes for the infant or child.

It is unwise to ask parents what they want or expect, particularly early in the evaluation. Rather, suggest to parents that, in the opinion of the multidisciplinary team, certain adverse physical or developmental outcomes might be anticipated and that therapies will be recommended if these outcomes occur. In this scenario, asking parents what they feel about such outcomes and plans opens communication and helps them participate, even if they do not completely understand what is being discussed.

Each family unit eventually decides on the degree to which they wish to participate in the health care of their child. As parents learn about their child’s condition and take on advocacy roles, they may become active participants. However, some parents are never able or willing to actively participate in planning. Be cautious to avoid making parents feel guilty about too much, or too little, intervention.

As parents find healthcare providers with whom they can communicate, that individual may assume the role of coordinator of care.[53] Information must flow between this person and other providers. In the ideal situation, this individual is a primary care physician (PCP), but it is often another healthcare professional participating in the child's care. A primary coordinator with whom parents can feel comfortable should be identified as the team leader, because such a person facilitates parent-staff and interdisciplinary communication.

Seamless communication between public and private agencies, as well as parents and physicians, helps prevent duplication of services and provides parents the emotional and medical support that they require for the optimal care of their child. In some cases, the parent may become the best care coordinator for their child. If this situation occurs, the parent must be accepted as an active participant in the healthcare team.

Healthcare providers who are unwilling to allow active participation of informed parents in their child’s care create a difficult environment for continuing and optimizing care. Indeed, providers must always remember that the major goal of parents and providers is to achieve the best outcome for the patients and families. With regard to keeping the family intact, the risk of divorce may increase among parents of NICU graduates, and the PCP should be alert for signs of family stress.[243]

Specific recommendations

In the present day, counseling of parents often begins before birth.[244] The availability of prenatal biochemical screening tests, improved knowledge of genetic diseases and family histories, and the use of fetal ultrasonography have made the recognition and management of maternal and/or fetal disease more commonplace than ever before.

Depending on the specific problems, counseling may entail one or more prenatal conferences with obstetricians, perinatologists, geneticists, surgical subspecialists, neonatologists, and the infant’s and family’s PCPs. The PCP should be kept informed about these consultations, and these conferences should continue throughout the patient's NICU stay and during visits to the PCP’s office.

Parents or caregivers must actively participate in decision making. Many studies indicate that parental contribution to the physical and psychomotor welfare of their NICU graduate is the most important factor for a favorable long-term outcome.[245]

The internet has become an important source of information to find institutions that provide specialized care for NICU graduates. Care facilities are often near the family’s home. To identify local or national support groups, parents of infants with extreme prematurity, unusual or complex malformations, or rare metabolic diseases can consult social workers, PCPs, online resources, and special agencies (eg, the March of Dimes). Please see the section titled “Resources for Parents and Healthcare Professionals." The PCP should take a proactive role in helping parents connect with other parents in similar situations.

The vulnerable child

An interesting and perplexing management problem in the follow-up of high-risk neonates is vulnerable child syndrome. Morris Green, MD, and Albert Solnit, MD, described this syndrome in 1964[246, 247] and Green summarized its nature in 1986.[248] Others have continued to describe this syndrome[249] in NICU graduates, especially those born prematurely, wherein these infants are at risk for developing behavioral problems as a consequence of excessive parental anxiety.

Some investigators have questioned whether this syndrome actually occurs.[250] Others, however, have published strong evidence of its presence in NICU graduates.[251, 252, 253, 254]

Some parents react with an overprotective response after dealing with the emotional stress of multiple medical problems or even simply the admission to the intensive care nursery. Vulnerable child syndrome is occasionally observed when children have a tentative diagnosis of a minor disorder or when physicians suggest that certain neonatal findings be reevaluated in the future.

The vulnerable child response often manifests as limitations in the child's contact with the environment. Parents may limit or prevent exposure with other people or family members. In the most severe form, parents become virtual recluses with their child, refusing to leave the child to care for themself. An exaggerated fear of infection, hypoxia, injury, or ridicule may be the initiating factor for some parents.

Healthcare providers must reinforce the idea of normal interaction with other children, family members, and extended communities that is limited only by the child’s tolerance. A mistake practitioners frequently make is inadvertently reinforcing the parents' overprotective behavior by accentuating the risks of infection or injury in an infant with residual problems of prematurity, congenital heart disease, or neurologic injury.

Involving children with family members and with other infants is an increasingly important part of normal development. If a child is restricted because of technological dependence or a real infectious risk, a reasonable plan of participation should be designed so that they can be involved in as many age-appropriate activities as possible.