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JH Kennell, MD, Rainbow Babies and Children's Hospital, Division of Developmental and Behavioral Pediatrics, Mail Stop 6038, 11000 Euclid Avenue, Cleveland. OH 44106, USA (Tel. 116 368 0073, Fax. 216 368 0116)
The report about the "Human Neonatal Care Initiative" by Professor Adik Levin from Estonia reminds us that medical care innovation did not disappear during the years of Soviet rule. More importantly, the ideas and programs developed by Professor Levin parallel humanizing efforts by family-focused neonatologists around the world. Hopefully, these ideas will stimulate all neonatologists to review critically their policies for parents and siblings, and consider how to make the 11 step changes Dr Levin recommends to keep all mothers with their newborns and involved in their care.
In 1979 a special facility with 35 beds for preterm infants (<37 wk gestation) and 35 beds for sick and malformed full-term infants was started in Tallinn (1). Because of a shortage of nurses, mothers were called upon to provide all of the care for their infants and to stay in the hospital until the infant's discharge. The nurses gave medications and injections and acted as consultants by assisting mothers with breastfeeding, guiding feeding plans and teaching them to care for the infant. Most of the premature infants coming to this nursery weighed more than 1500g at birth. The dominant features of this special department were the 24-h care by mothers with assistance from the hospital staff, minimizing exposure to infection by restricting contact between the baby and hospital staff members, promoting breastfeeding and using technology as little as possible.
In the new facility Levin and his staff noticed a decrease in the number of infections in infants and in the need for antibiotics and intravenous fluids. Weight gain was faster, breastfeeding increased, and social and psychological development was advanced. The mothers also benefited; recovery from childbirth was faster, confidence about caring for the infant was increased and mother-infant attachment was enhanced.
In the last 100 y, the improvement in survival of preterm infants as a result of advances in medical knowledge and technology has been remarkable. The focus on technology may not be without cost, however. In his book The Nursling in 1907, Dr Budin wrote with great insight that "a certain number of mothers abandon the babies whose needs they have not had to meet, and in whom they have lost all interest. The life of the little one has been saved, it is true, but at the cost of the mother" (2). This cautionary advice was pushed aside by concern about the extremely high death rate in hospitalized infants and parturient mothers due to infection. A disciple of Budin, Martin Cooney, provided a damaging role model, as he exhibited premature infants in fairs and expositions in England and the USA from 1902 to 1940. The mothers of these infants were not permitted to take care of their infants. Pediatricians copied the practice of separating mothers and premature infants as they set the policies for hospital premature nurseries. In the period from 1930 to 1960 parental visiting to hospitalized pediatric patients was strictly limited to 1 or 2 h per week in most pediatric hospitals, and the unit for the care of premature infants was a fortress allowing no entry by family members. When antibiotic therapy became available and research reports showed the benefits of admitting parents into the neonatal intensive care unit (NICU) with no increase in infections, neonatologists responded swiftly, starting in the late 1960s, by opening the NICU doors to parents and providing them with opportunities to touch and hold their infants. This shift contrasted with the much slower process in maternity hospitals of bringing mothers and babies together in the first 2 h after birth and providing rooming-in. Only parental pressure on obstetricians and hospitals brought about this change.
The restrictions that separated mothers and full-term babies arose from the suspicion that parents brought infection into the hospital. Up to the present time in North America, the reflex response of some physicians and nurses has been to separate mothers and babies unless they are sure that the baby is well; most US hospitals still operate a central nursery. In contrast, separation is rarely required in the Tallinn and a number of other hospitals where both the early and long-term benefits of keeping mother and baby together are stressed. Key steps in the WHO-UNICEF Baby Friendly Hospital Initiative (BFHI) in maternity hospitals world-wide include early mother-infant contact, rooming-in, and early and frequent breastfeeding. These steps have not only resulted in more mothers breastfeeding their infants longer, but also significantly decreased the abandonment of infants in the hospital in Thailand, the Philippines, Costa Rica and Russia. Professor Levin argues that the benefits of the BFHI should be extended to sick and premature newborns in pediatric hospitals. Increased breastfeeding success and decreased abandonment could be particularly advantageous for preterm, malformed and sick newborns for whom abandonment and other tragic parenting disorders are more frequent (2).
Levin wisely stresses the importance of maintaining the integrity of the biological and psychological umbilical cords between the mother and infant. Whether labeled as umbilical cords or as mother-infant bonding and infant-mother attachment, the pediatric goal should be the enhancement of infant growth, nutrition, development and secure attachment, as well as mother-infant and parent-infant bonding and the prevention of parenting disorders such as abuse, abandonment, failure to thrive and neglect.
In his 1907 text on premature infant care Pierre Budin stated that "the food for infants is human milk" (2). The role of breast milk in the care of premature infants has been studied and debated repeatedly throughout the twentieth century (3-6). The discovery that preterm milk has a different composition to term milk in the first month has provided support for Dr Levin's strong emphasis on mothers breastfeeding their infants in his unit. Preterm milk in general has more protein, nitrogen, chloride, sodium and less lactose than term milk. However, there is considerable variation between mothers and a definite diurnal variability in milk content. The information about preterm milk composition, the evidence that it supports satisfactory growth for infants over 1500g and the recently reported advantages of breastmilk for premature infants has tilted the support in favor of preterm mother's milk for infants between 1500 and 2500 g, the choice at Tallinn Children's Hospital since 1979. For infants weighing less than 1500g, debate continues about the use of modified or unmodified preterm milk. Further research is needed to clarify this issue, but for infants of at least 1500 g, the benefits of breastmilk cannot be overstated. The ever-increasing list of bacteriostatic and bacteriocidal factors in mother's milk, including lactoferrin, lysozyme, complement, lymphocytes producing immunoglobulins A, G and M, and colonization with nonpathogenic flora in the milk, is the basis for fewer infections in breastfed premature infants and probably contributes to the reduced incidence and decreased severity of necrotizing enterocolitis in breastfed premature infants (7). The very long-chain fatty acids present in human milk are suspected to be responsible for the reduced incidence and severity of retinopathy of prematurity. Lucas et al. reported a mean verbal IQ 8 points higher at 8 y in infants fed human milk, whether by gavage or at the breast (6). Preterm infants tend to have a lower oxygen level during feeding but oxygenation is better maintained during breastfeeding than bottle-feeding (8). For infants weighing less than 1500g, there is considerable debate and the need for further study about the use of modified or unmodified preterm milk.
Professor Levin has presented data showing that the preterm infants who received care by their mothers gained significantly more weight in the first 30 d of life compared with the infants whose care was provided by nurses (p < 0.001) (1). This evidence of the effectiveness of care by mothers in this unit extended to full-term sick infants, but the greatest benefit was apparent in the more immature infants. Determining the mechanism by which weight gain was more rapidly increased by maternal care will require further research, but some of the following physiological processes that occur between mothers and infants and with breastfeeding may be involved. If multiple caregivers are responsible for the infant's feeding, these beneficial physiological processes may be interrupted.
Babies respond preferentially to their mother's voice shortly after birth, select the breast for the first suckling that has not been washed and appear to recognize the mother with other sensory systems. When mothers are with their babies in the early period a cascade of interactions takes place between mother and infant, locking them together and ensuring the further development of attachment (2). When the infant suckles from the breast 19 different gastrointestinal hormones are released in both the mother and the infant, including cholecystokinin and gastrin, which stimulate the growth of the baby's and mother's intestinal villi and increase the absorption of calories with each feeding (9). Touch on the mother's nipple and the inside of the infant's mouth are the stimuli that lead to this release.
Oxytocin may have been a factor in the improved weight gain of infants in the Levin study who received care from their mothers (10). Dilatation of the cervix during birth in sheep releases oxytocin within the brain, which attaches to brain oxytocin receptors which initiate maternal behavior and bonding of the mother to her newborn lamb. Although a blood-brain barrier for oxytocin exists in the human, oxytocin produced in the brain attaches to multiple oxytocin receptors within the brain. Elevated levels of brain oxytocin result in feelings of great love for the baby, slight drowsiness, euphoria and a raised pain threshold. During breastfeeding increased maternal blood levels of oxytocin are associated with increased brain levels. The bursts of oxytocin released with breastfeeding may enhance the bonding of the mother to her preterm or sick newborn, just as it does with healthy full-term infants. This experience repeated several times a day could lead to more affectionate and responsive mother-infant interactions. Breastfeeding has a central role in the bonding process, and is even more important when the newborn is sick or premature.
Professor Levin comments about "a growing tendency towards the humanization of high-technology medicine." One exciting example of this is the innovative approach of Dr Heideliese Als. Over many years she and her colleagues have developed and tested a relationship-based, developmentally supportive approach to newborn intensive care for preterm infants to optimize their long-term health and development (11-14). This approach is referred to as the Newborn Individualized Developmental Care and Assessment Program (NIDCAP). The program is guided by a neurodevelopmental framework for understanding preterm infants and involves a professional alliance among the caregivers that supports the parents' affection towards their child and meets the infant's needs. The infant is considered an active collaborator working to continue the developmental trajectory started during intrauterine life. The infant's behavior provides the information from which to design care. Working with the infant involves inferring from the baby's behavior what the baby wishes to accomplish and what strategies he or she is using. This information is used to predict what might be useful to support the infant's overall development and neurobehavioral organization, while at the same time accomplishing the intensive caregiving goals of the physicians and nurses.
The NIDCAP provides the clinical framework to carry out this type of care. The model includes a systematic method for the detailed observation of infant behavior and for using each infant's individual pattern of behaviors as a guide for caregiving. Particular note is made of behaviors that indicate stress and self-regulatory behaviors to reduce stress. A detailed report is prepared with suggestions for ways to support the infant's physiological stability, behavioral organization and developmental progression. This information is shared with the caregiving professionals and the family.
Guidelines for care include pacing of caregiving based on the infant's cues, individually appropriate positioning, individualized feeding support, opportunities for skin-to-skin holding [i.e. kangaroo care (15, 16), which enhances breastmilk production], and collaborative care for all special procedures so that the parent can oversee the infant's comfort and well-being. The emphasis is on a quiet, soothing environment, which supports the family's comfort and provides opportunities to feel close to and affectionate with their infant. Several randomized studies have been conducted to evaluate the impact of the NIDCAP (11). Experimental and control groups of infants were evaluated during hospitalization, at 2 wk corrected age (with the Assessment of Preterm Infant's Behavior) and at 9 mo (with the Bayley Scales of Infant Development). Infants whose hospital course was managed using the individualized care and assessment program had significantly lower rates of morbidity (i.e. lower incidence of intraventricular hemorrhage, reduced severity of chronic lung disease), less need for ventilator support and oxygen, earlier move to oral feedings, better weight gain, significant cost savings due to earlier discharge and improved behavioral outcomes.
The NIDCAP would be a valuable supplement and would also reinforce some of the components of the Humane Neonatal Care Initiative. However, the individualized care program should not replace Levin's key components of keeping mother and baby together, with the mother engaged in caring for and breastfeeding her baby (17). Both programs consider the stress and strain on parents who have an infant that is hospitalized and attempt to ameliorate this by keeping the unit as quiet and peaceful as possible.
Benefits similar to those reported in Tallinn have been reported from other programs that provide facilities for mothers to stay in the hospital and care for their infants: in Baragwaneth, South Africa; Ethiopia; Buenos Aires, Argentina; Santiago, Chile; and High Wycombe, UK (18-20). Results from the Tallinn as well as these other five programs have shown that such an approach to newborn care is feasible and has positive effects for infants and their mothers. Randomized clinical trials and other research data to document the specific effects of such programs, both positive and negative, can be the basis for a re-evaluation of how best to blend and balance high-technology care with humane neonatal care.
Thirty years ago the walls of the premature nursery fortress began to crumble. Mothers, fathers and siblings are now welcomed into most NICUs to observe, touch, hold and feed small and sick infants. Surely it is time for all neonatologists to consider the next step, i.e. mothers staying with their babies for 24 h a day with maximum skin-to-skin contact (kangaroo care) (15, 16), providing breastmilk and much of the direct care for the infant under supervision, and participating in an individualized appraisal and care program for their infant. Dr Pierre Budin, in France at the beginning of the twentieth century, extolled the advantages of premature infant care by the mother, writing, "it is better by far to put the little one in an incubator by its mother's bedside; the supervision which she exercises is not to be lightly estimated." Careful attention to the needs of the mother for rest, support, breaks, encouragement, group meetings with other mothers, attentive listening, and visits from her partner and family will enhance her ability to meet the needs of her infant.
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