any clear benefits of NIDCAP neither for long-term neurodevelopmental nor for short term medical outcomes, we cannot recommend the implementa-tion of NIDCAP in its present form as standard care in preterm infants.” These methodological problems alone require the scientific community to dis-regard this report and bring into question its publication in a journal of this stature. NIDCAP requires readiness to embrace each infant as a person who commu-nicates what stresses the infant and what makes the infant comfortable. NIDCAP also requires readiness to embrace the parents as the infant’s key providers and advocates. Families and NICU professionals in many countries feel that NIDCAP is the most humane and comprehensive model of care available and is the infants’ and the families’right. And Ohlsson and Jacobs prove NIDCAP’s scientific validity.
Heidelise Als, PhD, Psychologist
Boston Children’s Hospital and Harvard Medical School, Boston, Massachusetts
Conflict of Interest:
I am the originator of the NIDCAP ap-proach to newborn care and the founder and former president of the NIDCAP Fed-eration International, a nonprofit organi-zation that ensures the quality and is the certifying agency of international train-ing in the NIDCAP approach for advanced professionals in the field of newborn care in hospital settings.
REFERENCES
1. Als H. Program Guide—Newborn Indivi-dualized Developmental Care and Assess-ment Program (NIDCAP): An Education and Training Program for Health Care Pro-fessionals. Boston, MA: NIDCAP Federation International; 2011
2. Als H et al. Manual for the Assessment of Preterm Infants’Behavior (APIB). In: Fitzgerald HE, Lester BM, Yogman MW, eds.Theory and Research in Behavioral Pediatrics. New York, NY: Plenum; 1982:65–132
3. Als H et al. Toward a research instrument for the assessment of preterm infants’
behavior. In: Fitzgerald HE, Lester BM, Yogman MW, eds.Theory and Research in Behavioral Pediatrics. New York, NY: Plenum; 1982:35–63 4. Prechtl HFR.The Neurologic Examination of the Full-Term Infant: A Manual for Clinical Use. 2nd ed . Clinics in Developmental Medi-cine, No. 631977. Philadelphia, PA: Lippincott
5. Einspieler C, Prechtl HF. Prechtl’s assess-ment of general moveassess-ments: a diagnostic tool for the functional assessment of the young nervous system. Ment Retard Dev Disabil Res Rev. 2005;11:61–67
doi:10.1542/peds.2013-1447D
Authors
’
Response:
NIDCAP: A Systematic
Review and
Meta-analyses of Randomized
Controlled Trials
We appreciate the interest in our sys-tematic review on NIDCAP,1much from readers involved with NIDCAP who de-clare their conflict of interest.2–5 We provide a single response to the 4 separate but overlapping e-Letters.2–5 We are neonatologists with expertise in creating and evaluating evidence, and although one of us (AO) has un-dergone basic NIDCAP training by Dr Als at Women’s College Hospital in Toronto, Ontario, Canada, we are not NIDCAP experts and have no conflict of interest to declare. As stated in 20026and again in our recent review,
“Modification of the extrauterine NICU environment and care giving accord-ing to each infant’s current physio-logic and neurobehavioral functioning is a rational and intuitive approach to caring for preterm infants and their families and to supporting infant de-velopment.”1 Like our readers, we strongly endorse and practice hu-mane, developmentally supportive, gentle care2–5 that recognizes and engages the family as their infant’s primary caregiver. We disagree about the lack of evidence from this system-atic review of 11 randomized con-trolled trials involving 627 neonates for
NIDCAP to be the only framework on which to provide care for these vul-nerable infants and families.
Recent independent critical appraisals published in Evidence Updates (from the BMJ Evidence Centre and McMaster University)7contradict these e-Letters to support our systematic reviewfindings. The clinical rater for Pediatric Hospital Medicine writes, “This is an important article which poses 2 clear questions and answers them emphatically.”7 For Pediatric Neonatologythe rater writes,
“Good article summarizing the key evi-dence well. I previously thought that NIDCAP had been associated with im-proved short term outcomes. The data is well presented and easy to as-similate. This is useful as training staff to use NIDCAP is expensive and I would need to see evidence of ben-efit before committing to this.”7 The reviewer for Pediatrics (General) writes, “Interesting. Clear evidence of no benefit. It is rare that we get such conclusive results from a meta analysis. Very important to know because NIDCAP is a very labour and resource intensive intervention.”7 We apologize for our error and un-fortunate choice of wording when we stated that the NIDCAP assessment
“requires trained and certified care-givers to use the Assessment of Pre-mature Infant Behavior (APIB) tool to observe 91 neonatal behaviors every 2 minutes for 1 hour before, during, and after a care giving intervention.”1 As detailed in our previous reviews,6,8,9we are well aware that although they are related the APIB and NIDCAP assessments differ. The term NIDCAP was not used in the first phase-lag study of the intervention published in 1986.10Dr Als wrote, “The behavioral observation sheet (Figure. Behav-ioral observation sheet) is based on the conceptualization of the Assess-ment of Preterm Infant’s Behavior (APIB).”10 We apologize for using the
troduction, instead of “The Prechtl Neurologic Assessment of the Fullterm Newborn Infant,” which is what was reported in the included studies11–14 and which we correctly referenced15 in our systematic review.1 We thank the readers for drawing our attention to these oversights, and we have rectified them in a separate erratum that was submitted to the editors of Pediatrics on April 9, 2013. These two errors in terminology do not affect the validity of the methods or the results of our sys-tematic review. Importantly, “To be in-cluded in the review, the intervention had to be NIDCAP as described by Dr Als and applied to low-birth-weight or preterm infants while in the hospi-tal.” “The intervention had to be tested in a randomized controlled trial (RCT) design and compared with standard care.”1
Randomized controlled trials and sys-tematic reviews provide the most valid results on which to build an evidence-based perinatal practice.16 We ac-knowledge the work by Dr Als and all the authors of the studies included in this systematic review, who recognized the importance of using RCT method-ology to evaluate the effectiveness of NIDCAP in improving outcomes. This has enabled us to summarize the evi-dence from a larger sample of preterm infants than in previous reviews and provide more precise estimates of ef-fect sizes. We too have been and are involved in the design, conduct, analy-sis, and interpretation of many neo-natal RCTs17–19and systematic reviews undertaken to identify effective inter-ventions20,21 and to inform practice guidelines including management of stress and pain in newborns.22,23 Sev-eral of these trials have provided evi-dence of beneficial outcomes, and in contrast to Dr Lawhon’s assertions, translation of this knowledge has
We used standard Cochrane methods for conducting this and previous sys-tematic reviews on NIDCAP.24Cochrane states, “Main outcomes should gen-erally not include surrogate or in-terim outcomes. They should not be chosen on the basis of any anticipated or observed magnitude of effect, or because they are likely to have been addressed in the studies to be re-viewed.”24 “In addition, indirect or sur-rogate outcome measures, such as laboratory results or radiologic results (e.g. loss of bone mineral content as a surrogate for fractures in hormone replacement therapy), are potentially misleading and should be avoided or interpreted with caution because they may not predict clinically important outcomes accurately.”24 Therefore, in accordance with Cochrane methodology, transverse relaxation time and diffusion tensor MRI and sleep cortical spectral coherence electroencephalography were not reported in our systematic review. The primary outcome for this sys-tematic review was selected on the basis of our review questions, which support Dr Als’stated NIDCAP goal“to improve neurodevelopmental func-tioning.”2“The composite of death or major sensorineural disability at 18 months corrected age (CA) or later in childhood” is considered an impor-tant primary outcome in neonatal RCTs and systematic reviews.17–21,25 This is consistent with the 1993 care-giving review by Lacy (an occupational therapist) and Ohlsson, published be-fore any NIDCAP RCTs had been con-ducted, stating that “follow-up should be extended to school age,”26 and is recognized by NIDCAP researchers with the results included in our sys-tematic review27,28 and even reported since publication of our review.29 Death should be reported in all neo-natal trials after randomization, with
ity was reported in 4 RCTs enrolling 354 infants in this review (Table 3). We could not include the 18 deaths that occurred in the 3-center study by Dr Als and colleagues because deaths were not reported by NIDCAP and control groups.30The authors reported outcomes only for the 92 surviving infants among the 110 infants en-rolled.30 Any RCT evaluating an inter-vention in newborn infants, particularly a developmentally sensitive interven-tion in preterm infants, should report on neurodevelopmental outcomes at 18 months or later. Our review included short-term medical and developmental outcomes previously evaluated and reported by Drs Als and Lawhon and colleagues,10 with similar outcomes reported in all RCTs to date. We are a little confused that Dr Lawhon and colleagues disagree with our inclusion of short-term medical outcomes such as “in hospital deaths, chronic lung disease, necrotizing enterocolitis, in-traventricular hemorrhage and like. In, contrast, NIDCAP is aimed at a different array of important targets.”4
we interpret and use judgment to assess the clinical relevance of this information (knowledge translation).32 The readers of our review have focused on the few statistically significant results and ignored the statistically nonsignificant findings in Tables 2 and 3, our interpretation of these findings in the Discussion sec-tion, and the supplemental information about the baseline characteristics and the numerous serious issues related to bias (Supplemental Appendix 2, “Risk of Bias in Included Studies”).1 These include the exceedingly long time lapses between recruitment and publica-tion of the results,14trial registration in all included studies only after the last patient was recruited, and in Dr Als and co-workers’ 2 latest studies an unexplained imbalance between the numbers of infants randomized to the NIDCAP and the control groups.33,34 In the 2011 report there were 12 infants in the NIDCAP group and 18 in the control group.33 In the 2012 report there were 13 infants in the NIDCAP group and 17 in the control group.34 Did the difference of 10 more infants enrolled in the control groups than in the NIDCAP groups in these very small trials happen by chance? Although the 2 studies have the same NCT registra-tion number (NCT00914108), we as-sumed they were different studies because different recruitment periods were reported. As researchers con-ducting meta-analyses, we have to be careful not to include outcome data from the same infant twice, but this has been difficult. More recently, the 9-year outcomes were published for 23 infants from the 2011 report33(9 chil-dren in the NIDCAP group and 14 in the control group; 23% lost to follow-up).29 The study has the same NCT number (NCT00914108) as the 2 previous stud-ies from 201133and 2012.34
In Supplemental Appendix 3 we report on the weighted mean difference for
each of the 6 system scores for the APIB on 281 enrolled infants at 2 weeks’CA. The weighted mean difference in the APIB scores range from 20.53 for
“Attention system” to 20.88 for “ Exam-iner facilitation.” Although statistically significant, these differences between the groups of ,1 point on a 9-point scale35 cannot be considered clinically important.
None of the e-Letter writers acknowl-edge the statistically significant but clinically unimportant differences be-tween the groups. The standardized mean differences in Bayley Mental Developmental Index and Psychomotor Development Index at 9 months of 1 point or less, although statistically significant, cannot be considered clini-cally important, especially because sig-nificant differences were not found at earlier or later ages (Table 2). Similarly, the 1.5 g/day (0.05 oz/day) difference in in-hospital weight gain between the groups, though statistically significant, is not clinically meaningful, especially with no difference in weights noted at term or 2 weeks or at 9, 12, or 24 months of age corrected for preterm birth (Table 4). The e-Letter writers disregard the important outcomes that were not statistically significantly dif-ferent between groups (Table 3 and Supplemental Appendix 4, “Sleep Out-comes”). These include chronic lung disease at 36 weeks’postmenstrual age (PMA), intraventricular hemorrhage, sepsis, retinopathy of prematurity, nec-rotizing enterocolitis, days on supple-mental oxygen, days on assisted ventilation, and sleep outcomes at 36 weeks’ PMA and 3 months’CA, which have often been claimed to be favorably affected by NIDCAP. With the increased sample size in this review (n 5 627) compared with our 2002 review (n 5 136), the outcomes of duration of ven-tilation and supplemental oxygen were no longer statistically significant, and
weight gain was reduced from 3.2 to 1.5 g/d.1,6
We report a 6-day reduction in length of hospitalization, with a related 0.5-week reduction in PMA at discharge (thePvalue is .04, but the upper 95% confidence interval includes 0 weeks, suggesting borderline statistical sig-nificance). At study entry, the PMA fa-vored the NIDCAP group by 0.18 weeks, offsetting the findings in PMA at dis-charge. There was moderate hetero-geneity for both of these outcomes, with the same 2 clear outliers
identi-fied for both outcomes, with mean differences in length of hospitalization of 43 and 44 days in the NIDCAP versus the control group and mean differ-ence of 6 and 5 weeks in PMA14,30(Figs 5 and 6). In sensitivity analyses (post hoc analyses) excluding these 2 studies, statistical significance dis-appeared for both length of hospital-ization and PMA at discharge, and there was less between-study hetero-geneity, making the findings more robust. Maguire and colleagues13,36 commenced NIDCAP within 48 hours of birth and included weekly behavioral interventions and found no significant differences in respiratory support, days of intensive care, or growth or neuromotor development at term PMA nor in growth, cognitive, psychomotor, and neurodevelopment at 1 and 2 years in infants born at ,32 weeks’ PMA. Our findings are in agreement with this well-conducted study. We disagree with Dr Haumont et al, who state, “There is little need of random-ized controlled trials (RCT) to evaluate the importance of: pain and stress management, protection of sleep, ef-fects of bright light and noise, hemo-dynamic changes related to handling, positioning, skin-to-skin, breastfeeding, parental presence and supportive patient–caregiver relationship. All these aspects have been addressed and studied.”3 The Cochrane review on
includes 57 studies enrolling 4730 infants but concludes, “Additional re-search is needed to determine the minimally effective dose of sucrose during a single painful procedure and the effect of repeated sucrose adminis-tration on immediate (pain intensity) and long-term (neurodevelopmental) outcomes.”37 The Cochrane review on the effects of cycled lighting in 469 infants reports that trends for many outcomes favored cycled light compared with near darkness and favored cycled light compared with continuous bright light, but the intervention requires ad-ditional trials.38The upcoming review on
“Noise reduction management in the neonatal intensive care unit for preterm or very low birth weight infants” will probably include only 2 small trials.39So yes, these interventions have been studied, but additional RCTs are needed, the results of which should inform de-velopmental care practices.
We strongly urge health care pro-viders in the European Association of Developmental Care to consider our systematic review and provide inter-pretations of our findings with rep-resentatives of the parent-initiated Association for Developmental Care.3 We advise health care providers and researchers in Europe, Japan, and elsewhere to consider our findings before deciding which developmental care interventions to introduce or to study further. We recommend that providers of any innovative hospital-based developmentally sensitive in-tervention for preterm infants take into account our findings using critical ap-praisal skills. Such interventions should start at birth in the resuscitation area, where the sensory input (stress) to the immature brain is enormous.9
Nursing researchers have identified 5 cat-egories or “core measure sets” to rep-resent the first step in operationalizing
sleep, pain and stress assessment and management, activities of daily living (positioning, feeding, and skin care), family-centered care, and the healing environment. We recommend that large, well-designed, well-conducted, and timely reported RCTs be undertaken in the preterm population of various combinations of these core measures, starting in the resuscitation area and using well-defined long-term clinical and neurodevelopmental outcomes (the composite of death or major sensorineural disability at 18 months’ CA or later in childhood) as the main end points. We encourage consumers of neonatal health care or their om-budsmen to take part in setting the agenda and defining important out-comes for such research.8,16
Systematic reviews of the literature serve as good examples of knowledge management, defined as “making proper use of the sum of what is known.”32We stand by our conclusions that “because we were not able to identify any clear benefits of NIDCAP for long-term neurodevelopmental outcomes, nor for any short-term medical outcomes, we cannot recom-mend the implementation of NIDCAP in its present form as standard care in preterm infants.”1
Arne Ohlsson, MD, MSc, FRCPC, FAAP, Professor Emeritus
Departments of Paediatrics, Obstetrics and Gynaecology, Health Policy, Management and Evaluation, University of Toronto, Ontario, Canada; Honorary Consultant, Department of Paediatrics, Mount Sinai Hospital, Toronto, Ontario, Canada
Susan E. Jacobs, MBBS, MD, FRACP
Neonatal Services, Royal Women’s Hospital, Melbourne, Victoria, Australia; Critical Care and Neurosciences, Murdoch Childrens Research Institute, Melbourne, Victoria, Australia; and Department of Obstetrics and Gynecology, University of Melbourne, Victoria, Australia
Conflict of Interest: None declared
review and meta-analyses of randomized controlled trials. Pediatrics. 2013;131(3). Available at: www.pediatrics.org/cgi/con-tent/full/131/3/e881
2. Als H. Re: Ohlsson and Jacobs, NIDCAP: a systematic review and meta-analyses. [E-Letter to the Editor published online ahead of print March 18, 2013].Pediatrics
3. Haumont D, Amiel-Tison C, Casper C, et al. NIDCAP and developmental care: a Euro-pean perspective. [E-Letter to the editor published online March 14, 2013.]. Pediat-rics
4. Lawhon G, Als H, Alberts JR, et al. NIDCAP Federation International response. [E-Letter to the Editor published online March 12, 2013].Pediatrics
5. Nishida H. From the Japan Association of Research on Developmental Care. [E-Letter to the Editor published online March 5, 2013].Pediatrics
6. Jacobs SE, Sokol J, Ohlsson A. The Newborn Individualized Developmental Care and As-sessment Program is not supported by meta-analyses of the data [published cor-rection appears inJ Pediatr2002;141:451– 452].J Pediatr. 2002;140(6):699–706 7. Evidence updates. Available at: http://plus.
mcmaster.ca/EvidenceUpdates/. Accessed April 20, 2013
8. Ohlsson A, Jacobs SE. Meta-regression can indicate if further NIDCAP studies are jus-tified [in Swedish]. Lakartidningen. 2007; 104(3):134–137
9. Ohlsson A. NIDCAP: new controversial evi-dence for its effectiveness. Pediatrics. 2009;124(4):1213–1215
10. Als H, Lawhon G, Brown E, et al. In-dividualized behavioral and environmental care for the very low birth weight preterm infant at high risk for bronchopulmonary dysplasia: neonatal intensive care unit and developmental outcome. Pediatrics. 1986; 78(6):1123–1132
11. Buehler DM, Als H, Duffy FH, McAnulty GB, Liederman J. Effectiveness of individualized developmental care for low-risk preterm infants: behavioral and electrophysiologic evidence.Pediatrics. 1995;96(5 pt 1):923–932 12. Als H, Duffy FH, McAnulty GB, et al. Early experience alters brain function and structure.Pediatrics. 2004;113(4):846–857 13. Maguire CM, Walther FJ, Sprij AJ, Le Cessie
14. McAnulty G, Duffy FH, Butler S, et al. In-dividualized developmental care for a large sample of very preterm infants: health, neurobehaviour and neurophysiology.Acta Paediatr. 2009;98(12):1920–1926
15. Prechtl HFR.The Neurological Examination of the Full-term Infant: a Manual for Clini-cal Use. 2nd ed . Clinics in Developmental Medicine, No 63. Philadelphia, PA: Lippincott; 1977
16. Ohlsson A. Randomized controlled trials and systematic reviews: a foundation for evidence-based perinatal medicine. Acta Paediatr. 1996;85(6):647–655
17. Schmidt B, Roberts RS, Davis P, et al; Caf-feine for Apnea of Prematurity Trial Group. Long-term effects of caffeine therapy for apnea of prematurity.N Engl J Med. 2007; 357(19):1893–1902
18. Jacobs SE, Morley CJ, Inder TE, et al; Infant Cooling Evaluation Collaboration. Whole-body hypothermia for term and near-term newborns with hypoxic-ischemic encepha-lopathy: a randomized controlled trial.Arch Pediatr Adolesc Med. 2011;165(8):692–700 19. Garland SM, Tobin JM, Pirotta M, et al;
ProPrems Study Group. The ProPrems trial: investigating the effects of probiotics on late onset sepsis in very preterm infants.
BMC Infect Dis. 2011;11:210
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21. Ohlsson A, Walia R, Shah SS. Ibuprofen for the treatment of patent ductus arteriosus in preterm and/or low birth weight infants.
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Drugs; Section on Anesthesiology; and Section on Surgery), Canadian Paediatric Society (the Fetus and Newborn Commit-tee). Prevention and management of pain and stress in the newborn infant.Paediatr Child Health (Oxford). 2000;5:31–47 24. Higgins JPT, Green S, eds. Cochrane
Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration; 2011. Available at: www.cochrane-hand-book.org
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27. Westrup B, Böhm B, Lagercrantz H, Stjernqvist K. Preschool outcome in chil-dren born very prematurely and cared for according to the Newborn Individualized Developmental Care and Assessment Pro-gram (NIDCAP). Acta Paediatr. 2004;93(4): 498–507
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DOI: 10.1542/peds.2013-1447E
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