Variance in proportion of KC initiation across units was statistically significant (model 1; unit-level variance, var(1) = 1.07; p < 0.001). Differences in infants’ characteristics across units could not explain unit-level variations in KC initiation that remained significant and slightly increased after adjustment for patient-level variables (model 2). GA was the main factor associated with KC initiation (odds ratio [OR], 5.8; 95% CI, 4.5–7.5 for neonates born at 27–31 weeks of GA compared with neonates born at 23–26 weeks of GA) and, to a lesser extent, type of pregnancy, intrauterine growth, and maternal employment. The inclusion of unit variables (model 3) reduced the variance (var(3) = 0.64; p < 0.001). Unit-level variables explained 40% of unit-level variation in KC initiation across units. After adjustment for infant-level factors, unit policies and training were significantly associated with KC initiation (OR, 3.3; 95% CI, 1.5–7.4 for KC group 3 compared with group 1 and OR, 3.5; 95% CI, 1.8–7.0 for NIDCAP training compared with no training).
The proportion of neonates whose mothers started to express milk was higher in the group of units with higher level of BF policies (group 3) (p < 0.001) (Fig. 1).
The multilevel regression analysis (2,635 completed cases) is reported in Table 5. No difference between neonates included and excluded from the analysis was observed. As the rate of BF initiation was similar in BF group 1 and 2 units, data for these 2 groups were aggregated and compared with group 3 data.
Variation in proportion of BF initiation across units was statistically significant. Adjustment for patient-level variables (model 2) slightly increased this variance. Maternal employment before pregnancy was the main factor associated with BF initiation (OR, 1.3; 95% CI,1.1–1.6). Inclusion of unit-level variables (model 3) slightly reduced the variance in BF initiation across units. After adjustment for infant-level factors, group 3 units were significantly associated with BF initiation (OR, 1.8; 95% CI, 1.0–3.2).
For both models, results using multiple imputations were consistent with those from complete case analyses (data not shown).
This study is the first to investigate dissemination of neurodevelopmental care at country level and the impact of structured programs on this dissemination. In this large population-based French sample, we found that almost 90% of NICUs allowed unlimited parental presence and over half routinely offered KC to both parents. Policies that support parents increased significantly between 2004 and 2011, and importantly, units with more evidence-based KC or BF policies were significantly more likely to apply these interventions. In addition, structured programs, such as NIDCAP, seemed to enhance KC and, to a lesser extent, BF initiation.
Areas explored have ethical and legal support or have received a high level of evidence. Not separating neonates and parents has been advocated internationally (28–30) and in several national recommendations, including France (31). KC is highly recommended even in high-income environments (25). Breast milk has many proven benefits for preterm newborns (2324). However, difficulties in translating research findings and recommendations into clinical practice are well known (32), and many studies point out the underutilization of appropriate research-based knowledge in clinical practice (33). In our study, large variabilities between units were observed with gaps between policies and opportunities for implementation. Open access visiting policies were nearly universal, but facilities for parents were lacking. KC was widespread but with frequent restrictions. Professional support for BF was available in most units, but one third of these professionals did not receive any formal training in human lactation. Although policies had positively evolved since 2004, they were still less developed than those described in countries with the highest uptake in 2004, such as Denmark, Sweden, and the United Kingdom for parental access or Denmark, Sweden, and the Netherlands for KC (1819). It is generally stated that it takes an average of 17 years for research evidence to reach widespread clinical practice (34), and the evolution described in our study can be considered as positive. On the other hand, a better understanding of factors that facilitate the translation of research into practice is necessary. Public policies and funding, together with stakeholder groups, have effectively promoted family-centered and neurodevelopmental care program at national levels (3536), and countries that showed greater implementation of neurodevelopmental care in 2004, compared with France, are also described as having strong national policies or adequate governmental funding (11). In comparing the 2004 and 2011 French data, areas of improvement were mainly those that require strong supportive leadership in the NICUs rather than additional resources and clinical-administrative partnerships. However, all aspects of neurodevelopmental care are embedded in complex healthcare systems (16) where change is dependent on macro- and microlevel organization. For example, multifaceted interventions are needed to implement KC, even in countries with many facilitators, such as Sweden (1438). In our cohort, initiation of KC was associated with maternal and neonatal characteristics, but a substantial part of the variance among units was explained by unit policies and training. Higher levels of supportive policies were associated with greater KC initiation, but specific neurodevelopmental care training aiming to support KC (15) strengthened the implementation. Guidelines do not implement themselves (39), and our results support this assumption; policies increased KC uptake, but structured training based on NIDCAP theory strengthened the impact of policies. However, we do not know if the “dose” of KC received by the infants in those units was influenced by training. Units with training in the sensory-motor development program (27) were less likely to initiate KC during the first week of life. The two programs have different theoretical frameworks with the NIDCAP, emphasizing relationship-based care with guidance for system change (915), whereas the sensory-motor program is more task focused.
Not surprisingly, BF policies were more strongly associated with BF initiation than neurodevelopmental care training, which uses newborn neurobehavioral observation to facilitate transition from tube to oral feeds (39). BF initiation requires knowledge of the physiology of human lactation, and units with trained professionals in lactation may have higher competencies to support early breast milk expression.
The lack of shared knowledge on newborn neurobehavioral observation might hold back the dissemination of beneficial practices. A U.K. survey indicated that having staff trained in newborn observation positively affected developmental care uptake in units (40). In our cohort, less than 30% of units used a scale to assess newborn neurobehavior. Surprisingly, this number decreased between 2004 and 2011, possibly because the practice is time consuming and neuroimaging has increased (4142).
The French situation is not unique in Europe. A gap between North and South has been described for neurodevelopmental care implementation and more generally for parental role in NICUs, suggesting social and cultural differences (1819). However, a study in Spain highlighted how structured programs based on the NIDCAP framework can bridge this gap, with staff perceptions after training becoming similar to those described in Northern Europe (43). Several models designed to improve neonatal neurodevelopmental care have been published, all of which incorporate neurobehavioral observations of neonates are shared with parents (1544–46), and some of them have investigated the impact on outcome (4748). However, they were evaluated in a research context, and no data are available on their dissemination at national level. The number of neurodevelopmental care programs available in France was limited, but we were able to investigate modes of training, based on different strategies for implementation.
This study has limitations. Although KC and BF initiation are two core neurodevelopmental measures, they do not cover a full range of neurodevelopmental care practices. However, both have large developmentally supportive effects, promoting parental participation and attachment, as well as physiologic stability, preservation of sleep, and analgesia (212226). It might have been interesting to study the “dose” of KC received by each infant, as well as BF at discharge, but practices during the first week of life were more easily explored at population level, and dose is usually related to early initiation (49). The observational design of the study allowed us to establish potential associations rather than causal factors. NIDCAP seemed to enhance early KC initiation and, to a lesser extent, BF initiation, but we were not able to describe the level of implementation in each unit, and variability among units could also be explained by patient or unit characteristics, such as nurse-to-patient ratio, that we did not control for. Finally, data for 12% of the neonates were missing and excluded from final analysis. Their exclusion might have altered the strength of associations, but this was not observed after multiple imputations.
The strengths of the study are substantial. Data were recorded at population level, with a high rate of completeness for NICU questionnaires. The large sample size assures representativeness and power of the study. Questions in the ESFs and the French survey were worded exactly the same, facilitating the comparison between the two studies. Availability of unit policies and parallel data at the level of individual babies allowed us to investigate the impact of policies on clinical care, taking into account maternal and infant characteristics. The significant associations that were found between policies and practices suggest that these data could help to define national guidelines and realistic goals to improve neonatal services.
In Europe, neurodevelopmental care implementation is advocated by parent associations. It has been increasingly recognized that context is a critical element in the successful implementation of evidence into practice. Unit policies seem essential for neurodevelopmental care implementation, but conceptual models to guide clinical care seem to affect practices and strengthen policies. This study contributes to a better understanding of factors that effectively spread the implementation of neurodevelopmental care measures and factors that need to be explored for a wider range of strategies and in different cultural backgrounds.
APPENDIX 1. The EPIPAGE-2 Neurodevelopmental Care Writing Group Members
A. Burguet, MD, PhD, Department of Neonatal Pediatrics, Dijon University Hospital, Dijon, France; G. Cambonie, MD, PhD, Department of Neonatal Pediatrics and Intensive Care, Arnaud de Villeneuve Hospital, Montpellier, France; L. Caeymaex, MD, PhD, Department of Neonatal Medicine, CHIC de Créteil, Centre de recherche clinique CHIC, CEDITEC Paris Est Créteil University, Paris, France; C. Gire, MD, PhD, Department of Neonatal Pediatrics and Intensive Care, Nord Hospital, Marseille, France; B. Guillois, MD, PhD, Department of Neonatal Pediatrics and Intensive Care, University Hospital, Caen, France; P. Kuhn, MD, PhD, Department of Neonatal Pediatrics and Intensive Care, Strasbourg University Hospital, Strasbourg, France; B. Lecomte, MD, Department of Neonatal Pediatrics, University Hospital Estaing, Clermont-Ferrand, France; A. Mitha, MD, Neonatal Unit, Jeanne de Flandre Hospital, Lille, France; H. Patural, MD, PhD, Department of Neonatal Pediatrics and Intensive Care, Saint Etienne University Hospital, Saint Etienne, France; J. C. Picaud, MD, PhD, Department of Neonatal Pediatrics and Intensive Care, La Croix Rousse Hospital, Lyon, France; J. C. Roze, MD, PhD, Department of Neonatal Medicine, Nantes University Hospital, Nantes, France, Epidémiologie Clinique, Centre d’Investigation Clinique (CIC004), Nantes University Hospital, Nantes, France; J. Sizun, MD, PhD, Department of Neonatal Pediatrics and Intensive Care, Pôle de la Femme, de la Mère et de l’Enfant, Brest University Hospital, Brest, France.
We thank members of the EPIPAGE-2 study group and all the regional teams participating in the study for their substantial contribution to acquisition of data; Diep Tran for administration of the EPIPAGE-2 database and provision of the data; and Delphine Druart, Myrtha Martinet, and Nathalie Ratynski for helpful collaboration to validate data on Developmental Care Program implementation; Inga Warren for fruitful discussions on the final version of the article. We are grateful for the participation of all families of preterm infants in the EPIPAGE-2 cohort study and for the cooperation of all maternity and neonatal units in France.
1. Milligan DW: Outcomes of children born very preterm in Europe. Arch Dis Child Fetal Neonatal Ed 2010; 95:F234F240
2. Wolke D, Baumann N, Strauss V, et al.: Bullying of preterm children and emotional problems at school age: Cross-culturally invariant effects. J Pediatr 2015; 166:14171422
3. Forcada-Guex M, Borghini A, Pierrehumbert B, et al.: Prematurity, maternal posttraumatic stress and consequences on the mother-infant relationship. Early Hum Dev 2011; 87:2126
4. Korja R, Latva R, Lehtonen L: The effects of preterm birth on mother-infant interaction and attachment during the infant’s first two years. Acta Obstet Gynecol Scand 2012; 91:164173
5. Cacciani L, Di Lallo D, Piga S, et al.: Interaction of child disability and stressful life events in predicting maternal psychological health. Results of an area-based study of very preterm infants at two years corrected age. Res Dev Disabil 2013; 34:34333441
6. Als H, Duffy FH, McAnulty GB, et al.: Early experience alters brain function and structure. Pediatrics 2004; 113:846857
7. Melnyk BM, Crean HF, Feinstein NF, et al.: Maternal anxiety and depression after a premature infant’s discharge from the neonatal intensive care
unit: Explanatory effects of the creating opportunities for parent empowerment program. Nurs Res 2008; 57:383394
8. Montirosso R, Provenzi L, Calciolari G, et al.; NEO-ACQUA Study Group: Measuring maternal stress and perceived support in 25 Italian NICUs. Acta Paediatr 2012; 101:136142
9. Westrup B: Family-centered developmentally supportive care. NeoReviews 2014; 15:e325e35
10. Coughlin M, Gibbins S, Hoath S: Core measures for developmentally supportive care in neonatal intensive care
units: Theory, precedence and practice. J Adv Nurs 2009; 65:22392248
12. Jobe AH: A risk of sensory deprivation in the neonatal intensive care
unit. J Pediatr 2014; 164:12651267
13. Gibbins S, Hoath SB, Coughlin M, et al.: The universe of developmental care: A new conceptual model for application in the neonatal intensive care
unit. Adv Neonatal Care 2008; 8:141147
14. Wallin L, Rudberg A, Gunningberg L: Staff experiences in implementing guidelines for Kangaroo mother care–a qualitative study. Int J Nurs Stud 2005; 42:6173
15. Als H, McAnulty GB: The Newborn Individualized Developmental Care and Assessment Program (NIDCAP) with Kangaroo Mother Care (KMC): Comprehensive care for preterm infants. Curr Womens Health Rev 2011; 7:288301
16. Chandler J, Rycroft-Malone J, Hawkes C, et al.: Application of simplified complexity theory concepts for healthcare social systems to explain the implementation of evidence into practice. J Adv Nurs 2016; 72:461480
17. Franck LS, Oulton K, Bruce E: Parental involvement in neonatal pain management: An empirical and conceptual update. J Nurs Scholarsh 2012; 44:4554
18. Greisen G, Mirante N, Haumont D, et al.; ESF Network: Parents, siblings and grandparents in the neonatal intensive care
unit. A survey of policies in eight European countries. Acta Paediatr 2009; 98:17441750
19. Pallás-Alonso CR, Losacco V, Maraschini A, et al.; European Science Foundation Network: Parental involvement and Kangaroo care
in European neonatal intensive care
units: A policy survey in eight countries. Pediatr Crit Care Med 2012; 13:568577
20. Ancel PY, Goffinet F; EPIPAGE 2 Writing Group: EPIPAGE 2: A preterm birth cohort in France in 2011. BMC Pediatr 2014; 14:97
21. Conde-Agudelo A, Díaz-Rossello JL: Kangaroo mother care to reduce morbidity and mortality in low birthweight infants. Cochrane Database Syst Rev 2014; 4:CD002771
22. Johnston C, Campbell-Yeo M, Fernandes A, et al.: Skin-to-skin care for procedural pain in neonates. Cochrane Database Syst Rev 2014; 1:CD008435
23. Gartner LM, Morton J, Lawrence RA, et al.: Breastfeeding and the use of human milk. Pediatrics 2005; 1152:496506
24. Moro GE, Arslanoglu S, Bertino E, et al.: XII. Human milk in feeding premature infants: Consensus statement. J Pediatr Gastroenterol Nutr 2015; 61(Suppl 1):S16S19
25. Nyqvist KH, Anderson GC, Bergman N, et al.: Towards universal Kangaroo mother care: Recommendations and report from the first European conference and seventh International Workshop on Kangaroo Mother Care. Acta Paediatr 2010; 99:820826
26. Nyqvist KH, Häggkvist AP, Hansen MN, et al.: Expansion of the ten steps to successful breastfeeding into neonatal intensive care
: Expert group recommendations for three guiding principles. J Hum Lact 2012; 28:289296
27. Martinet M, Borradori Tolsa C, Rossi Jelidi M, et al.: [Development and assessment of a sensory-motor scale for the neonate: A clinical tool at the bedside]. Arch Pediatr 2013; 20:137145
28. UNICEF - Convention on the Rights of the Child [Internet]: Convention on the Rights of the Child. Available at: http://www.unicef.org/crc/
. Accessed January 2016
29. Giannini A, Garrouste-Orgeas M, Latour JM: What’s new in ICU visiting policies: Can we continue to keep the doors closed? Intensive Care Med 2014; 40:730733
30. Flacking R, Lehtonen L, Thomson G, et al.; Separation and Closeness Experiences in the Neonatal Environment (SCENE) Group: Closeness and separation in neonatal intensive care
. Acta Paediatr 2012; 101:10321037
32. Rycroft-Malone J: Implementing evidence-based practice in the reality of clinical practice. Worldviews Evid Based Nurs 2012; 9:1
33. Eccles MP, Armstrong D, Baker R, et al.: An implementation research agenda. Implement Sci 2009; 4:18
34. Morris ZS, Wooding S, Grant J: The answer is 17 years, what is the question: Understanding time lags in translational research. J R Soc Med 2011; 104:510520
35. Bedford Russell AR, Passant M, Kitt H: Engaging children and parents in service design and delivery. Arch Dis Child 2014; 99:11581162
36. Staniszewska S, Thomas V, Seers K: Patient and public involvement in the implementation of evidence into practice. Evid Based Nurs 2013; 16:97
37. Vesel L, Bergh AM, Kerber KJ, et al.; KMC Research Acceleration Group: Kangaroo mother care: A multi-country analysis of health system bottlenecks and potential solutions. BMC Pregnancy Childbirth 2015; 15(Suppl 2):S5
38. Boivin A, Currie K, Fervers B, et al.; G-I-N PUBLIC: Patient and public involvement in clinical guidelines: International experiences and future perspectives. Qual Saf Health Care 2010; 19:e22
39. Browne JV, Ross ES: Eating as a neurodevelopmental process for high-risk newborns. Clin Perinatol 2011; 38:731743
40. Hamilton KE, Redshaw ME: Developmental care in the UK: A developing initiative. Acta Paediatr 2009; 98:17381743
41. Brown N, Spittle A: Neurobehavioral evaluation in the preterm and term infant. Curr Pediatr Rev 2014; 10:6572
42. Pierrat V: Computer-based analysis of general movements reveals stereotypies predicting cerebral palsy. Dev Med Child Neurol 2014; 56:922923
43. Mosqueda-Peña R, Lora-Pablos D, Pavón-Muñoz A, et al.: Impact of a developmental care training course on the knowledge and satisfaction of health care professionals in neonatal units: A multicenter study. Pediatr Neonatol 2015; 89:3733
44. Welch MG, Hofer MA, Brunelli SA, et al.; Family Nurture Intervention (FNI) Trial Group: Family nurture intervention (FNI): Methods and treatment protocol of a randomized controlled trial in the NICU. BMC Pediatr 2012; 12:14
45. Milgrom J, Newnham C, Anderson PJ, et al.: Early sensitivity training for parents of preterm infants: Impact on the developing brain. Pediatr Res 2010; 67:330335
46. Melnyk BM, Feinstein NF, Alpert-Gillis L, et al.: Reducing premature infants’ length of stay and improving parents’ mental health outcomes with the Creating Opportunities for Parent Empowerment (COPE) neonatal intensive care
unit program: A randomized, controlled trial. Pediatrics 2006; 118:e1414e1427
47. Als H, Duffy FH, McAnulty G, et al.: NIDCAP improves brain function and structure in preterm infants with severe intrauterine growth restriction. J Perinatol 2012; 32:797803
48. Newnham CA, Inder TE, Milgrom J: Measuring preterm cumulative stressors within the NICU: The Neonatal Infant Stressor Scale. Early Hum Dev 2009; 85:549555
49. Beake S, Pellowe C, Dykes F, et al.: A systematic review of structured compared with non-structured breastfeeding programmes to support the initiation and duration of exclusive and any breastfeeding in acute and primary health care settings. Matern Child Nutr 2012; 8:141161
breast-feeding; cohort study; kangaroo care; neurodevelopmental care; neonatal intensive care; preterm neonate
Supplemental Digital Content
Copyright © 2016 by the Society of Critical Care Medicine and the World Federation of Pediatric Intensive and Critical Care Societies.