Human infants are bom biologically prepared to form attachments to their caregivers. Bowlby suggested that the attachment system evolved to enhance the chances of survival.1'2 By the time infants are capable of moving away from attachment figures, they typically prefer to remain close under conditions of threat. Therefore, they do not wander away and become vulnerable to accidents or predators, but rather maintain close proximity to attachment figures. Given that human infants are "designed" to maintain contact with attachment figures, there is perhaps no greater threat than the disruption in the "parent-child" relationship. When young children experience disruptions in their relationships with their caregivers, such as when entering foster care, the disruptions have consequences for their behavior and their physiology.
EFFECTS OF DISRUPTIONS IN CARE ON BIOLOGICAL SYSTEMS
Seymour Levine and colleagues conducted a study with non-human primates that illustrates the importance of attending to the effects of disruptions in care, even when the effects may be hard to see.3 In the study, monkey infants were separated from their mothers for a 24-hour period. In one condition, the separated monkeys were placed in cages adjacent to their mothers where they could hear their mothers. In another condition, the separated monkeys were placed in isolated cages where they could not hear their mothers. At the end of the 24-hour separation, the monkeys that could hear their mothers cried significantly more than monkeys that could not hear their mothers. However, those monkeys who could not hear their mothers showed levels of cortisol (a stress hormone) that were as high as monkeys who could hear their mothers. If one focuses only on the overt behavioral evidence of distress, one may come to the conclusion that the monkeys that could not hear their mothers were not distressed; physiological data, however, showed these monkeys were at least as distressed as the monkeys that could hear their mothers. Similarly, when relationships with caregivers are disrupted, children are likely to experience distress, whether or not it is seen at the behavioral level.
Figure. Percentage of foster children, with typical, low and high cortisol patterns. From: Dozier M, Mannim M, Gordon MK, et al. In: CWW Maltreatment Washington, DC: American Psychological Association; 2006:197. Copyright 2006 by the American Psychological Association. Reprinted with permission of the author.
We have studied children's behavioral and biological reactions to disruptions in care. Most children who have never experienced a disruption in care from a biological parent show high morning levels of cortisol production followed by decreases across the day to near zero levels at night (see Figure). This diurnal pattern is part of what helps humans be diurnal creatures that are awake during the day and asleep at night. But young children who have been placed into foster care show atypical patterns of cortisol production across the day. Some children show very low patterns of cortisol production with low morning values. Others show extremely high patterns of cortisol production throughout the day.
Low levels of cortisol production are associated with conduct disorder, substance abuse, and other problems. High levels are associated with internalizing disorders, such as depression and anxiety. Until longitudinal studies have been conducted with children who have experienced early adversity, such as a disruption in care, it is not known whether children's high or low cortisol levels put them at risk for later disorders. However, it seems plausible that these early experiences may create conditions at the neurobiological level that confer risk for such disorders. Whatever outcome disruption of care portends, it is clear that disruption in basic biological systems occurs.
EFFECTS OF DISRUPTIONS IN CARE ON BEHAVIOR
When children experience disruptions in care, their reactions and behaviors vary depending on their age. When younger than 12 months old, infants tend to be able to trust new caregivers relatively quickly.4 Within a week or so after placement in new foster homes, infants are able to seek out new caregivers directly when they are distressed. For infants and toddlers who enter foster care later than a year of age, the process takes much longer. Even as much as two months after placement, toddlers continue to turn away from new caregivers or are inconsolable when distressed.4 These behaviors tend to push caregivers away, suggesting to them that children do not need their nurturance. Whether the behavioral adjustments in learning to turn to their caregiver when distressed takes a week or two (in the case of young infants), or a month or two (in the case of toddlers), the transition into foster care can have ongoing effects on a bio-behavioral level.
When children behave as if they do not need caregivers or as if caregivers cannot soothe them, caregivers typically respond in kind; that is, caregivers respond as if children do not need nurturance.5 Therefore, even otherwise nurturing parents may not nurture children who are placed in their care. In intervention programs, such as the one we conduct at the University of Delaware, we help caregivers see that children's behaviors are not "personal" - that children have developed these strategies in response to a history of caregiving failures.
A second reason that caregivers sometimes fail to behave in nurturing ways is that nurturance may not come naturally to them. About 35% of parents in the general population are not very nurturing when children are distressed.6 For example, rather than soothe an upset child, many parents may say, "You're not hurt. Hop up." Children whose caregivers have difficulty providing nurturing care often assume that these individuals will not consistently respond to them in a sensitive manner when they are distressed. Therefore, these children turn away from their caregivers when distressed. Although this tendency to turn away may not be optimal, the child's attachment strategy represents an organized strategy for dealing with the caregiver's non-availability.
However, without nurturing care, foster children are at greatly increased risk for developing what are known as "disorganized attachments." Children with disorganized attachments lack strategies for approaching their parents when distressed. Disorganized attachment places children at risk for a number of long-term problematic outcomes, including internalizing disorders, externalizing disorders, and dissociation.7
HELPING CAREGIVERS HELP VULNERABLECHILDREN
Young children in foster care experienee disruptions in care at a developmental point when they are biologically prepared to hold onto and depend on caregivers. The early adversity faced by young children with changing caregivers leaves them very vulnerable and in need of "therapeutic parents" who can respond sensitively to their needs. The Attachment and Biobehavioral Catch-up Intervention Program helps caregivers to become therapeutic in their interactions with their children. Several specific issues are targeted (See Table).
First, the program emphasizes to parents that these children need nurturing caregivers. Even if children push away caregivers and even if nurturance does not come naturally to the caregivers, these children need nurturance. Through the first step of the intervention program, caregivers are provided techniques to appreciate children's needs by "seeing through" behaviors that might otherwise push caregivers away.8
This phase of the intervention also helps caregivers to provide nurturance when it does not come naturally to them. The metaphor of "voices from the past" is used to help parents think of how their own experiences of being parented may be affecting their approach to parenting now. It is suggested that, when parents pick up their crying child, they are likely to hear (in their "mind's ear") the voice of someone from their past who either believed or did not believe in soothing a distressed child. For example, they may feel guilty when picking up their distressed child, "hearing" their mother say, "You'll spoil that child. Let him cry." When they think about these "voices from the past," they can become conscious of the influences. They then become free to choose to behave in the way that is most appropriate for their child, rather than responding automatically to the 'Voices from the past." There is an emphasis on foundational experiences, to help parents "over-ride" maladaptive messages and provide nurturance anyway.
Attachment and Biobehavioral Catch-Up Interventions
In addition to nurturance, the second issue targeted in the intervention program is understanding children's behavioral and biological dysregulation. Observations in parent-child interventions throughout the years revealed a particularly effective strategy where parents provide a very predictable interpersonal world for their children. To do this, counselors help parents in the intervention program to let their children take the lead both in play and in tasks of the day, as much as possible.
Finally, children who have experienced early adversity need a non-threatening world. Given that they are at risk for developing disorganized attachments,5 it is especially important that caregivers learn to behave in ways that are gentle, reassuring, and not frightening.9," Some parents may play games with children that involve threat and reassurance. For example, some parents may tell a story that frightens their children, but then provide reassurance after children are scared. Or perhaps parents threaten to leave children at a park (or tell them they'll give them away) if they misbehave. These frightening behaviors are likely to be difficult for any children to cope with, but especially difficult for children who have experienced early adversity. Therefore, parents are sensitized to the effects of using threat on their children. Whether in play or as a disciplinary strategy, parents are urged to behave in ways that are not frightening or threatening.
THE ROLE OF THE PEDIATRIC VISIT
The pediatrician's office is an ideal place for conveying the importance of nurturing vulnerable children and providing a predictable, non-threatening interpersonal environment. Foster parents may bring up concerns regarding their children's behavioral and emotional development while they address the children's physical health needs. Further, the conditions of the pediatrie visit (eg, concern about vaccines, etc.) provide opportunities to observe how parents and children negotiate dealing with children's distress (see Sidebar, page 208).
It is important that medical professionals support parents' behaving in nurturing ways with all children, but especially those who have had changing caregivers. Even non-nurturing parents can often overcome their usual ways of parenting when they get advice from experts about the importance of nurturing care. Whereas parents may worry about "spoiling" children or making children dependent on them, pediatricians can emphasize that such issues are not relevant for infants and young children. Babies cry because they need support and protection from caregivers. In fact, infants with nurturing parents usually become more independent and confident as they grow older compared with infants who have non-nurturing parents.
Because a visit to a pediatrie office may be challenging to children, multiple opportunities to observe what children do when distressed will likely arise. For example, if the child becomes frightened during the visit, behavioral cues of turning away from their caregiver, or not crying when he or she is in pain, may be evident, Caregivers are often hurt or frustrated by such behaviors, or at the least, worried about the behaviors. Pediatrie staff can acknowledge the behaviors, and point out how powerful the behaviors are in eliciting non-nurturing behaviors from the caregiver. The pediatrician can discuss trying to soothe an adult who pushes comfort away and how this would have a powerful effect on the person offering care (eg, making the person pull away) and liken that process to the effect that the child is having on the caregiver. Nearly everyone can relate to the feeling of offering someone help and having the person "brush them off." Although many parents are not aware of it, the behaviors of infants can be powerful in these same ways. Helping parents to provide nurturance, even though the child does not appear to need it, is critical. Pediatricians can offer information regarding more subtle cues of distress, such as elevated heart rate, or lack of engagement with the environment, even when the distress may not be apparent to caregivers from the child's overt behavior.
Pediatrie office settings are also excellent opportunities to encourage caregivers to "follow their children's lead" whenever possible in day-to-day life. This becomes especially important when observations or reports of irritability in the child are made, as these are possible signs of biobehavioral dysregulation. Professionals can encourage caregivers to create a predictable, controllable environment, whereby the parent follows the child's lead to allow him or her a sense of mastery and control. For example, during play time, the parent can let the child's behaviors guide the interaction; if the child puts a block on his or her nose, the parent does as well, and shows delight in the child's actions.
Helping caregivers to read their children's cues, respond to their children when it may be difficult, and create a world that promotes adequate behavioral and biological regulation are important aspects that can be addressed in a pediatrician's office. In many ways, a visit to a pediatrician is an ideal setting to create opportunities to address nurturance. Interaction patterns between the child and caregiver can be observed, and the visits provide opportunity for caregivers to disclose concerns parents have about the physical, emotional or behavioral health of the child. Pediatricians can take an important role in help- ^ ing parents recognize and respond to their child's distress on multiple levels. Efforts to do so will enhance the probability that vulnerable infants grow into healthy, welladjusted children.
1. Bowlby J. Attachment and loss: retrospect and prospect. Am J Orthopsychialry. 1982;52(4):664-678.
2. Bowlby J. A secure base: clinical applications of i attachment theory. London: Routledge; 1988.
3. Levine S, Stanton ME. The hormonal consequences of mother-infant contact. In: Barnard K, Brazelton TB, eds. Touch: The Foundation of Experience. Madison, CT: International Universities Press; 1990:165-194.
4. Stovall-McClough KC, Dozier M. Forming attachments in foster care: Infant attachment behaviors in the first two months of placement. Dev Psychopathol. 2004;16(2):253-271.
5. Dozier M, Stovall KC, Albus K, Bates B. Attachment for infants in foster care; The role of caregiver state of mind. Child Dev. 2001 ;72(5): 1467- 1477.
6. van LTzendoom MH. Adult attachment representations, parental responsiveness, and infant attachment: a meta-analysis on the predictive validity of the adult attachment interview. PsycholBull 1995;117(3)387-403.
7. van llzendoorn MH, Schuengel C, Bakermans-Kranenburg MJ. Disorganized attachment in early childhood: meta-analysis of precursors, concomitants, and sequelae. Dev , Psychopathol. 1999;ll(2}:225-249.
8. Dozier M. Infant-Caregiver Lab. The Attachment and Bio-Behavioral Catch-Up Intervention; A Training Manual for Foster Parents. Unpublished manual. University of Delaware, Newark, DE: 2002.
9. Schuengel C. Unresolved loss, disorganized ( attachment, and frightening parental behavior: A pilot-study/Onverwerkt verlies, gedesorganiseerde gehechtheíd en beängstigend opvoedersgedrag: Een vooronderzoek. Pädagogische Stuthen. 1997;74:355-366.
10. Schuengel C, Bakermans-Kranenburg M, Van Uzendoorn M. Frightening maternal behavior linking unresolved loss and disorganized infant attachment. / Consult Clinical Psychol. 1999;67(l):54-63.
11. Lyons-Ruth K, Dutra L, Schuder MR, Bianchi I. From infant attachment disorganization to adult dissociation: Relational adaptations or traumatic experiences? Psychiatr Clin North Am. 2006;29(l):63-86.
Attachment and Biobehavioral Catch-Up Interventions