Introduction
Preterm babies typically need neonatal intensive care unit (NICU) care for extended periods and are at risk for a range of neurodevelopmental, sensory, and musculoskeletal impairments due to prematurity and other significant associated medical conditions.[ 1–3 ] Preterm infants are at great risk for significant short- and long-term neurodevelopmental impairments, as their brains go through a critical period of development and maturation between 24 and 40 weeks of gestation, which occurs mainly during their NICU admission.[ 4 ] Recent studies indicate that extreme, early, and late preterm infants have high mortality and morbidity compared to term infants.[ 5 , 6 ] In recent years, though the rates of severe cerebral palsy (CP) have decreased, mild CP and developmental coordination disorders have increased in preterm infants.[ 7 , 8 ] The stressful sensory environment and exposures in the NICU are prone to alter the developmental trajectories and neurobehavior of preterm neonates.[ 9 , 10 ] Importantly, higher quality of developmental care promotes better neurobehavioral stability.[ 11 ]
Neonates born extremely preterm show cognitive problems, executive dysfunction, depression, and anxiety, which has adverse implications on academic achievement and socioemotional well-being.[ 12–14 ] They also report having a poor health-related quality of life into adulthood.[ 15 ] Infants born very preterm and with very low birth weight are also at higher risk of neurodevelopmental disability, face challenges in behavior and socioemotional development, and have cognitive and motor delays.[ 8 , 16 , 17 ] Neonates born moderate and late preterm who constitute a significant number of preterm births are also at risk of developmental disability, school failure, speech, cognitive and developmental delay, and social and behavior problems.[ 17–19 ]
Even into adolescence and adult life, babies born preterm and with low birth weight are at a higher risk of disability, social and behavior problems, mental health and poor academic performance, and other chronic conditions in adults and adolescents.[ 20–22 ] There is a stronger association between decreasing gestational age and greater challenges in educational levels, employment, and income levels in adulthood.[ 23 , 24 ]
These challenges faced by preterm infants in early childhood, adolescence, and throughout adulthood warrant early screening programs and preventive strategies to be introduced early. There are many challenges faced by a preterm neonate, and a multidisciplinary team comprising neonatal therapists (physiotherapists [PT] and occupational therapists [OT]) is recommended to optimize the neurodevelopmental outcomes and mitigate the adverse effects of the NICU stay, and also during the neurodevelopmental follow-ups post-NICU discharge.[ 25–27 ] Neonatal therapy is an art and science of integrating the typical development of the infant and family into the environment of the NICU.[ 28 ]
Women’s Wellness and Research Center (WWRC) has a level 4 NICU and a nursery, where physiotherapy (PT) and occupational therapy (OT) services are available to the neonates. There are referral criteria [Appendix 1 ] as per which physicians should refer the eligible neonates for inpatient PT and OT consultations and to separate two neurodevelopmental follow-up clinics (baby therapy clinic and neonatal neurodevelopmental clinic) divided based on the gestational ages and severity of conditions. Despite having referral criteria, many neonates are not referred to PT and OT consultations and to neurodevelopmental follow-up clinics. Baseline analysis of 1-month data (318 babies) reveals that 25%, 36%, 62%, and 10% of eligible neonates were not referred to (1) inpatient OT, (2) inpatient PT, (3) baby therapy, and (4) neonatal neurodevelopmental clinic, respectively [Table 1 ].
Appendix 1: Old physiotherapy and occupational therapy referral criteria
Table 1: Baseline and postimplementation data of number of eligible babies not referred to the given services
Not referring the babies to the needed PT and OT services leads to manpower underutilization, delay in diagnosis and intervention in the NICU, lack of neurodevelopmental follow-up appointments, and potentially impaired patient outcomes.
In the NICU of WWRC, using developmental care principles,[ 29 ] for the referred neonates, Physiotherapists and Occupational therapists help to/in: 1) prevent osteopenia of prematurity by providing range of motion exercises. Apart from nutritional supplementation, evidence suggests that 4-8 weeks of brief, passive range of motion with gentle joint compression administered 5–15 minutes daily for infants between 26-35 weeks of gestational age improves the bone area, bone mineral content, and bone mineral density,[ 30–32 ] 2) facilitate weight gain, better neurodevelopment, decreased infection rate and length of hospital stay in an infant by massage,[ 33–35 ] 3) engage parents with their baby using Newborn Behavioral Observation (NBO) which is an evidence-based relationship-building tool.[ 36–39 ] Parent engagement in the NICU helps to decrease emotional and behavioral problems in a child’s later life, promotes weight gain and decreases infection, helps in mother-child bonding and increased parental confidence, increases breast milk supply and weight gain, promotes better tone and neurodevelopment, decreases pain, hypoglycemia hypothermia, and readmissions,[ 40–44 ] 4) improve alertness in medically stable preterm infants from 33 weeks onwards, which further enhances sucking organization, tonal maturation, feeding progression and facilitates early discharge by using Auditory, Tactile, Visual and Vestibular (ATVV) stimulation,[ 45–48 ] 5) assist musculoskeletal maturation process and prevent musculoskeletal complications by providing appropriate positioning and discharge teachings,[ 3 ] 6) successfully and safely feed the baby orally by enhancing oromotor skills using oral stimulation program, pacing, and non-nutritive sucking, and reading feeding readiness cues.[ 49–51 ] Incorporating these techniques ensures gradual feeding progression for neonates, easy transition to oral feeds, shortens hospital stay and the duration of parenteral nutrition in the NICU,[ 50 , 52 , 53 ] 7) early detection of cerebral palsy using Prechtl’s assessment of general movements, and initiate early intervention if needed (by mimicking the normal pattern of movements),[ 54 , 55 ] 8) providing developmentally appropriate and supportive positioning which enhances sleep, promotes early midline, decreases fuzziness and motor asymmetry.[ 56–58 ]
In addition, for neonates referred to therapy services, PT and OT educate and inform parents on the range of functional exercises and techniques to achieve independent safe oral feeding, massage, swaddling, positioning, plagiocephaly prevention, and tummy time for their babies upon discharge. These efforts help foster family-centered care, which benefits parents and their babies in the NICU.[ 59 ] Recent research indicates that intervention provided to the babies in the NICU via therapists and parents improved motor, cognitive, and developmental outcomes.[ 26 ]
Currently, there is no standard practice for follow-up of preterm neonates and practices vary among countries and centers.[ 60 ] However, standardized, early assessment and intervention and longer, comprehensive follow-ups by a multidisciplinary allied health-care team are recommended to improve neurodevelopmental outcomes.[ 25 , 27 , 61 , 62 ] Most studies follow up preterm neonates till 3 years of age with the focus to identify neurodevelopmental impairment in the early years of life. These early assessments do not always correlate with long-term outcomes and may not correctly estimate functional concerns in later life.[ 62 ] Thus, standardized, longer, and comprehensive follow-ups are recommended, given the complexity of premature birth.[ 5 , 62 ]
Upon discharge, in the WWRC, according to a set of criteria [Appendix 1 ], physicians need to refer preterm babies to two distinct neurodevelopmental follow-up clinics with separate criteria (neonatal neurodevelopmental clinic and baby therapy clinic). In these clinics, PT and OT assess these babies at different time points and early intervention services are provided if needed. Early developmental interventions postdischarge prevent motor and cognitive impairment in preterm babies.[ 61 ]
This quality improvement study aims to ensure that all babies who fit within the referral criteria are referred to PT and OT inpatient services and to neurodevelopmental follow-up clinics at appropriate times. We aim to reduce the number of babies not referred to inpatient OT and PT services in the NICU and to two neurodevelopmental clinics (neonatal neurodevelopmental clinic and baby therapy clinic) to 50% of the baseline data within 1 month. Literature suggests that educational, technological, and communication strategies help in achieving QI goals, and we aim to implement a combination of similar strategies in this project.[ 63–68 ]
Methods
Context
This quality improvement study was conducted in the level 4 NICU of WWRC, which is a hospital under Hamad Medical Corporation, Qatar. With 112 NICU beds, it is one of the largest NICUs in the world and approximately 2000 babies are admitted yearly. This was a prospective, pre–post intervention study to improve and optimize the referral rates to PT and OT services in NICU and to neurodevelopmental clinics upon discharge. One-month data (January–February 2020) were analyzed to get the baseline values. A data extraction sheet was designed and pilot tested to extract baseline and postintervention data from patients’ electronic records. The study was approved by the NICU quality improvement team and WWRC administration. The paper follows SQUIRE2 guidelines.[ 69 ]
Intervention
The Institute for Healthcare Improvement Collaborative Quality Improvement Model was used to guide the program.[ 70 ] A team meeting was conducted with all the therapists in the NICU and their lead physician to identify the bottlenecks and to find ways for improving the referrals to PT and OT services within the NICU and to neurodevelopmental clinics. Three sequential steps for improvements were identified:
Enquire with stakeholders about the reasons for not referring the babies to appropriate services and address them
To revise the existing referral criteria [Appendix 1 ], to make them clear and comprehensive
Implement the revised criteria.
The study was divided into three phases:
In the first phase, a questionnaire was created to explore nurses’ and physicians’ awareness of the existing referral criteria, reasons for not referring the babies to appropriate PT and OT services within the NICU and to neurodevelopmental clinics, and suggestions to improve the referral rates (Appendix 2 ). All case managers, nurse educators, 46 nurses, and, 17 physicians completed the survey within one-week time.[ 17 , 46 ]
Appendix 2: 1st Survey Questions
Most nurses and physicians were aware of the criteria and the purpose of the follow-up clinics [Figure 1 ].
Figure 1: Nurses and Physicians responses to survey questions
Nurses and physicians cited the need for reminders as the most common reason for not referring the baby to appropriate therapy services [Figure 2 ].
Figure 2: Reasons for not referring the babies to appropriate services
The most common suggestions to increase the referral rates were a) to place the criteria in patient rooms and nursing stations, and , b) therapists should put the needed orders themselves with doctors co-signing it [Figure 3 ].
Figure 3: Suggestions to increase the consult and referral rates to appropriate therapy services
In the 2nd phase, based on the feedback, the existing criteria [Appendix 1 ] were comprehensively revised to make them evidence based as per the neonatal conditions seen in the NICU of WWRC. The revised criteria were evaluated for clarity using a survey [Appendix 3 ]. The major revisions made were (a) to include all possible diagnoses which could affect the neurodevelopment of preterm neonates, (b) to include late preterm babies for neurodevelopmental follow-ups, (c) to set timelines for consult orders to initiate early referral and intervention, and (d) to clarify pathways for neurodevelopmental and outpatient clinics. A total of 25 nurses and physicians answered the survey and slight clarifications were made based on the feedback. The new criteria were named revised consult and referral criteria for physiotherapy and/or occupational therapy and therapy services within WWRC NICU and Transitional care Neonatal Unit (TCNU) and upon discharge [Figure 4 ].
Appendix 3: 2nd Survey Questions
Figure 4: Revised consult and referral criteria for physiotherapy and/or occupational therapy and therapy services within WWRC NICU and TCNU and upon discharge. WWRC: Women’s wellness and research center, NICU: Neonatal intensive care unit, TCNU: Transitional care Neonatal Unit
Plan-Do-Study-Act (PDSA) cycles are an effective way to implement change.[ 71 ] The 3rd phase focused on implementing the revised criteria using a PDSA cycle. Initially, other than the physician, no other stakeholders were actively involved in the process of getting consults and referral orders. Furthermore, the consult and referral criteria were not accessible and visible to all the stakeholders. Incorporating the feedback from the previous surveys, all the key stakeholders were identified and were given important tasks and a process map was created [Figure 5 ].
Figure 5: Process map to implement the revised consult and referral criteria
Measures and analysis
The aim of the study was to reduce the number of neonates not referred to inpatient OT and PT services and to neurodevelopmental clinics to 50% of the baseline data within 1 month. Quantitative analysis and monthly audit of the patient electronic records admitted from December 6, 2020, to January 2, 2021 (1 month), were done to see if the needed orders were given as per the revised criteria.
Within the 1st month of implementation, the focus was to get the needed consult order before discharge (as opposed to within 48 h of admission/1st week of life/hemodynamic stable as per the revised criteria). Referral orders if given after the discharge were counted as not given.
Results
From December 6, 2020, to January 2, 2021, a total of 239 neonates were admitted to the NICU. Out of 239 neonates, 64, 55, 100, and 20 were eligible for physiotherapy consults, occupational therapy consults, referral to baby therapy, and neonatal neurodevelopmental clinic, respectively.
For referral orders, exceeding our target, no eligible neonates missed the order for the neonatal neurodevelopmental clinic, and 75% of the eligible neonates (target 50%) for the baby therapy clinic were referred appropriately. For inpatient OT and PT services, the percentage of neonates not given consult orders decreased substantially; however, we did not achieve the set target. Twenty-two percent (targeted 12.5%) and 20% (targeted 18%) of the eligible neonates missed OT and PT consult orders, respectively. A comparison of pre–post intervention results is outlined in Table 1 .
Discussion
Following the implementation of the revised referral criteria, for referral orders, exceeding the target, all the neonates eligible for neonatal neurodevelopmental, and 75% of the eligible neonates for baby therapy clinic were referred appropriately. For inpatient OT and PT services, the percentage of neonates missing the needed consult orders decreased substantially; however, we did not achieve the set target. Twenty-two percent (targeted 12.5%) and 20% (targeted 18%) of the eligible neonates missed OT and PT consult orders, respectively. Neonates who got timely orders benefitted from early assessment and interventions within the NICU and neurodevelopmental follow-up clinics. Research indicates that interventions provided to the babies in the NICU and early developmental interventions postdischarge improve motor, cognitive, and developmental outcomes in preterm babies.[ 26 , 61 ] Importantly, an increased number of consults and referrals led to adequate utilization of manpower resources and cost-efficiency in addition to boosting the therapist’s morale.
A major strength of this project was the involvement of multiple stakeholders. Research suggests active involvement of multiple stakeholders and their education is an essential element in QI that leads to success.[ 67 , 68 ] Involving multiple stakeholders allowed us to assign the task to a key stakeholder group and make them responsible for the needed orders. The process map helped in making stakeholders aware of their role, and within a short period, we could achieve the targets for inpatient consults and referral clinics.
Multiple factors led to not achieving the inpatient consult target. As per the process map, the therapists daily conducted the huddle at a dedicated time and informed the charge nurses and the case managers of the needed consult and referral orders, respectively. Charge nurses, primary nurses, and case managers then remind the physician to place the needed orders. Many times, due to the busy schedules of the doctors and the nurses, and due to the dynamic nature of the NICU, communication did not happen efficiently. The nurses work in rotatory shifts and use a patient handover tool to pass the needed information to the incoming colleague at the shift change. If a morning nurse could not contact the physician to get the needed order, she should endorse it to the incoming nurse to contact the physician. At times, if the nurse forgets to endorse the needed orders, the neonate missed the order. Furthermore, as NICU is a dynamic area, emergencies can emerge at any time and doctors need to attend to the emergency. In these cases, even after reminders, at times, doctors forgot to place the needed orders. Making one physician per team responsible and as a point of contact for giving the needed orders might help decrease the communication gap and will ease the burden on the nurses. In addition, reminder pop-ups based on the referral criteria can be enabled in the electronic patient record system which will prompt physicians to place the needed orders, thus closing the communication gap.
Importantly, during their shift, a nurse might have 1–3 babies to take care of. All nurses have a phone via which they can call landline numbers but calls to the mobile number are restricted. Most physicians carry mobile phones, and to call a mobile number, the nurse needs to go to the nursing station leaving her babies and have to ask a colleague or floater nurse to cover her babies while she calls the doctor. At times, due to the busy nature of the NICU and staff shortages, it is difficult to leave the babies and go to the nursing station for calling a physician. Providing nurses with phones having the facility to call mobile numbers will ease the burden on the nurses and will make the care more effective.
In the NICU, the focus is to save life and the neurodevelopment aspect in later life is not often thought of. However, the stressful sensory environment and exposures in the NICU are prone to alter the developmental trajectories and neurobehavior of preterm neonates.[ 9 , 10 ] Few physicians were reluctant to put the needed orders as they didn’t see the value of it. This was more prevalent with the orders for babies with Intra Uterine Growth Retardation (IUGR) and, follow-up orders for the late preterm babies post NICU discharge. Studies show that neonates born moderate and late preterm are at risk of developmental disability, school failure, speech, cognitive and developmental delay, and social and behavior problems.[ 17–19 ] Studies also highlight that neonates born with IUGR are at risk of poor neurodevelopmental and childhood cognitive outcomes.[ 72–75 ] Importantly, the early developmental intervention provided to the babies in the NICU via therapists and parents improves motor, cognitive and developmental outcomes in preterm babies.[ 26 , 61 ] Therapy services are not lifesaving but augment the quality of life of a neonate and parents within the NICU and in later life
Nurses were hesitant to call a few physicians to ask for the needed therapy order, as they anticipated that physicians will not like it. Nurses designed innovative ways and waited to convey something meaningful that physicians value, for e.g., blood test results, and asked for the therapy order when they conveyed the test results to the physicians. Power struggles exist in the NICU and organizational, managerial, and operational changes are needed to optimize the care of babies.[ 76 ] On weekends, therapists work on-call and were not available to do the huddle. This also led to missing some cases, mostly late preterm and babies with IUGR. On weekends, physicians placed the necessary orders for oxygen and medicines, but, were reluctant to put the needed therapy orders (citing its non-urgent and not lifesaving) and waited for the primary physician to place the order on the weekday. This further impacted late-preterm babies, and babies with IUGR as they get discharged quickly and might not be in the NICU when the primary physician comes for weekday duty. Many physicians might not see the need for therapy services for the neonates in the NICU, and thus don’t place the needed order, even after reminders. More education sessions on the implications of prematurity in the later part of life and the role of a therapist in the NICU could help physicians understand the value of therapy services in the NICU, thus making them more likely to give the needed order. More administrative controls and consistent reminders from the leadership management are needed to make physicians comply with the criteria. Additionally, if on-call therapists could do huddles on the weekends, it will further avoid missing the cases.
Although we have limited data of 1 month, we were able to involve all the stakeholders and decreased the number of nonreferrals to all 4 therapy services. In this project, we focused on getting the needed consult order before discharge and did not follow timelines as proposed in the revised criteria. In the future, to further decrease the number of nonreferrals to the needed services, and to get the needed orders within the stipulated time, a quality control team with dedicated time and staff is needed: (a) to conduct ongoing data analysis and audit, (b) to monitor the compliance of the project, and (c) to address the issues emerging from the iterative data analysis. A vested team of neonatal therapists is imperative for the long-term sustenance of this project and will help modulate the long- and short-term neurodevelopment of these babies.
Conclusion
Within 1 month, we decreased the number of nonreferrals to all 4 therapy services. Inpatient PT and OT referrals need more focus to achieve the target. The major reason for not referring the neonates to the therapy services was the lack of reminders, and suggestions to increase the referrals were to keep the criteria in various locations where it is available and visible. We kept the revised criteria in every baby file and also made it available to all the stakeholders. The following strategies are further needed to achieve the targets in entirety. Education of physicians and nurses on the implications of prematurity, neurodevelopmental implications of late preterm births and IUGR, and the role of a therapist in the NICU can help get the needed orders. Administrative controls such as (a) making one physician per team responsible for getting the needed orders and (b) consistent reminders from the leadership management to make physicians comply with the criteria are needed to achieve the targets. Using technology, reminder pop-ups based on the referral criteria can be enabled in the electronic patient record system which will prompt physicians to place the needed orders, thus decreasing the nonreferrals.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
Acknowledgments
We acknowledge Ms. Lizy, Fathen, Sabah (Case managers), Ms. Tiruveni, Rose, Silveria, Amor (Head nurses), Ms. Binsy (Clerk), Ms. Ava (secretary), Ms. Bindu (medical transcriptionist), and all NICU nurses for their cooperation and support.
References
1. Atkinson P, Coffey A, Delamont S, Charmaz K, Eakin JM, Gibaud-Wallston J, et al. Needs of families with children who have a physical disability:A literature review. Dev Med Child Neurol 2012;1:5–21.
2. Doyle LW, Saigal S. Long-term outcomes of very preterm or tiny infants. Neoreviews 2009;10:e130–7.
3. Sweeney JK, Gutierrez T. Musculoskeletal implications of preterm infant positioning in the NICU. J Perinat Neonatal Nurs 2002;16:58–70.
4. Pickier RH, McGrath JM, Reyna BA, McCain N, Lewis M, Cone S, et al. Amodel of neurodevelopmental risk and protection for preterm infants. Adv Neonatal Care 2013;13 Suppl 5:S11–20.
5. Duncan AF, Matthews MA. Neurodevelopmental outcomes in early childhood. Clin Perinatol 2018;45:377–92.
6. Allotey J, Zamora J, Cheong-See F, Kalidindi M, Arroyo-Manzano D, Asztalos E, et al. Cognitive, motor, behavioural and academic performances of children born preterm:A meta-analysis and systematic review involving 64 061 children. BJOG 2018;125:16–25.
7. McGowan EC, Vohr BR. Neurodevelopmental follow-up of preterm infants:What is new?. Pediatr Clin North Am 2019;66:509–23.
8. Pascal A, Govaert P, Oostra A, Naulaers G, Ortibus E, Van den Broeck C. Neurodevelopmental outcome in very preterm and very-low-birthweight infants born over the past decade:A meta-analytic review. Dev Med Child Neurol 2018;60:342–55.
9. Philpott-Robinson K, Lane SJ, Korostenski L, Lane AE. The impact of the neonatal Intensive Care Unit on sensory and developmental outcomes in infants born preterm:A scoping review. Br J Occup Ther 2017;80:459–69.
10. Pineda RG, Tjoeng TH, Vavasseur C, Kidokoro H, Neil JJ, Inder T. Patterns of altered neurobehavior in preterm infants within the neonatal Intensive Care Unit. J Pediatr 2013;162:470–6.e1.
11. Montirosso R, Del Prete A, Bellù R, Tronick E, Borgatti R Neonatal Adequate Care for Quality of Life (NEO-ACQUA) Study Group. Level of NICU quality of developmental care and neurobehavioral performance in very preterm infants. Pediatrics 2012;129:e1129–37.
12. Hirschberger RG, Kuban KC, O'Shea TM, Joseph RM, Heeren T, Douglass LM, et al. Co-occurrence and severity of neurodevelopmental burden (Cognitive Impairment, Cerebral Palsy, Autism Spectrum Disorder, and Epilepsy) at age ten years in children born extremely preterm. Pediatr Neurol 2018;79:45–52.
13. Burnett AC, Anderson PJ, Lee KJ, Roberts G, Doyle LW, Cheong JL, et al. Trends in executive functioning in extremely preterm children across 3 birth eras. Pediatrics 2018;141:e20171958.
14. Van Lieshout RJ, Ferro MA, Schmidt LA, Boyle MH, Saigal S, Morrison KM, et al. Trajectories of psychopathology in extremely low birth weight survivors from early adolescence to adulthood:A 20-year longitudinal study. J Child Psychol Psychiatry 2018;59:1192–200.
15. Saigal S, Ferro MA, Van Lieshout RJ, Schmidt LA, Morrison KM, Boyle MH. Health-related quality of life trajectories of extremely low birth weight survivors into adulthood. J Pediatr 2016;179:68–73.e1.
16. Peralta-Carcelen M, Schwartz J, Carcelen AC. Behavioral and socioemotional development in preterm children. Clin Perinatol 2018;45:529–46.
17. Synnes A, Hicks M. Neurodevelopmental outcomes of preterm children at school age and beyond. Clin Perinatol 2018;45:393–408.
18. You J, Yang HJ, Hao MC, Zheng JJ. Late preterm infants'social competence, motor development, and cognition. Front Psychiatry 2019;10:69.
19. Woythaler M. Neurodevelopmental outcomes of the late preterm infant. Semin Fetal Neonatal Med 2019;24:54–9.
20. Raju TN, Buist AS, Blaisdell CJ, Moxey-Mims M, Saigal S. Adults born preterm:A review of general health and system-specific outcomes. Acta Paediatr 2017;106:1409–37.
21. Wolke D, Johnson S, Mendonça M. The life course consequences of very preterm birth. Annu Rev Dev Psychol 2019;1:69–92.
22. Pyhälä R, Wolford E, Kautiainen H, Andersson S, Bartmann P, Baumann N, et al. Self-reported mental health problems among adults born preterm:A meta-analysis. Pediatrics 2017;139:e20162690.
23. Saigal S, Day KL, Van Lieshout RJ, Schmidt LA, Morrison KM, Boyle MH. Health, wealth, social integration, and sexuality of extremely low-birth-weight prematurely born adults in the fourth decade of life. JAMA Pediatr 2016;170:678–86.
24. Saigal S, Morrison K, Schmidt LA. “Health, wealth and achievements of former very premature infants in adult life”. Semin Fetal Neonatal Med 2020;25:101107.
25. Orton JL, Olsen JE, Ong K, Lester R, Spittle AJ. NICU graduates:The role of the allied health team in follow-up. Pediatr Ann 2018;47:e165–71.
26. Khurana S, Kane AE, Brown SE, Tarver T, Dusing SC. Effect of neonatal therapy on the motor, cognitive, and behavioral development of infants born preterm:A systematic review. Dev Med Child Neurol 2020;62:684–92.
27. Craig JW, Smith CR. Risk-adjusted/neuroprotective care services in the NICU:The elemental role of the neonatal therapist (OT, PT, SLP). J Perinatol 2020;40:549–59.
28. Sturdivant C. A collaborative approach to defining neonatal therapy. Newborn Infant Nurs Rev 2013;13:23–6.
29. Soleimani F, Azari N, Ghiasvand H, Shahrokhi A, Rahmani N, Fatollahierad S. Do NICU developmental care improve cognitive and motor outcomes for preterm infants?A systematic review and meta-analysis. BMC Pediatr 2020;20:67.
30. Sezer Efe Y, Erdem E, Güneş T. The effect of daily exercise program on bone mineral density and cortisol level in preterm infants with very low birth weight:A randomized controlled trial. J Pediatr Nurs 2020;51:e6–12.
31. El-Farrash RA, Abo-Seif IS, El-Zohiery AK, Hamed GM, Abulfadl RM. Passive range-of-motion exercise and bone mineralization in preterm infants:A randomized controlled trial. Am J Perinatol 2020;37:313–21.
32. Torró-Ferrero G, Fernández-Rego FJ, Gómez-Conesa A. Physical therapy to prevent osteopenia in preterm infants:A systematic review. Children (Basel) 2021;8:664.
33. Lu LC, Lan SH, Hsieh YP, Lin LY, Chen JC, Lan SJ. Massage therapy for weight gain in preterm neonates:A systematic review and meta-analysis of randomized controlled trials. Complement Ther Clin Pract 2020;39:101168.
34. Álvarez MJ, Fernández D, Gómez-Salgado J, Rodríguez-González D, Rosón M, Lapeña S. The effects of massage therapy in hospitalized preterm neonates:A systematic review. Int J Nurs Stud 2017;69:119–36.
35. Pados BF, McGlothen-Bell K. Benefits of infant massage for infants and parents in the NICU. Nurs Womens Health 2019;23:265–71.
36. Regina C, Alves L, Duarte ED. Contribution of the Newborn Behavioral Observations (NBO) for the maternal care of preterm neonates. J Hum Growth Dev 2017;27:262–71.
37. Guimarães MA, Alves CR, Cardoso AA, Penido MG, Magalhães LC. Clinical application of the Newborn Behavioral Observation (NBO) System to characterize the behavioral pattern of newborns at biological and social risk. J Pediatr (Rio J) 2018;94:300–7.
38. Nugent JK, Bartlett JD, Von Ende A, Valim C. The Effects of the Newborn Behavioral Observations (NBO) system on sensitivity in mother-infant interactions. Infants Young Child 2017;30:257–68.
39. McManus BM, Nugent JK. A neurobehavioral intervention incorporated into a state early intervention program is associated with higher perceived quality of care among parents of high-risk newborns. J Behav Health Serv Res 2014;41:381–9.
40. Vittner D, Butler S, Smith K, Makris N, Brownell E, Samra H, et al. Parent engagement correlates with parent and preterm infant oxytocin release during skin-to-skin contact. Adv Neonatal Care 2019;19:73–9.
41. Boundy EO, Dastjerdi R, Spiegelman D, Fawzi WW, Missmer SA, Lieberman E, et al. Kangaroo mother care and neonatal outcomes:A meta-analysis. Pediatrics 2016;137:e20152238.
42. Evereklian M, Posmontier B. The impact of kangaroo care on premature infant weight gain. J Pediatr Nurs 2017;34:e10–6.
43. Reynolds LC, Duncan MM, Smith GC, Mathur A, Neil J, Inder T, et al. Parental presence and holding in the neonatal Intensive Care Unit and associations with early neurobehavior. J Perinatol 2013;33:636–41.
44. Pineda R, Bender J, Hall B, Shabosky L, Annecca A, Smith J. Parent participation in the neonatal Intensive Care Unit:Predictors and relationships to neurobehavior and developmental outcomes. Early Hum Dev 2018;117:32–8.
45. White-Traut RC, Nelson MN, Silvestri JM, Vasan U, Littau S, Meleedy-Rey P, et al. Effect of auditory, tactile, visual, and vestibular intervention on length of stay, alertness, and feeding progression in preterm infants. Dev Med Child Neurol 2002;44:91–7.
46. White-Traut RC, Nelson MN, Silvestri JM, Cunningham N, Patel M. Responses of preterm infants to unimodal and multimodal sensory intervention. Pediatr Nurs 1997;23:169–75, 193.
47. Kanagasabai PS, Mohan D, Lewis LE, Kamath A, Rao BK. Effect of multisensory stimulation on neuromotor development in preterm infants. Indian J Pediatr 2013;80:460–4.
48. Medoff-Cooper B, Rankin K, Li Z, Liu L, White-Traut R. Multisensory intervention for preterm infants improves sucking organization. Adv Neonatal Care 2015;15:142–9.
49. Fucile S, Gisel EG, Lau C. Effect of an oral stimulation program on sucking skill maturation of preterm infants. Dev Med Child Neurol 2005;47:158–62.
50. Arora K, Goel S, Manerkar S, Konde N, Panchal H, Hegde D, et al. Prefeeding oromotor stimulation program for improving oromotor function in preterm infants –A randomized controlled trial. Indian Pediatr 2018;55:675–8.
51. Ludwig SM, Waitzman KA. Changing feeding documentation to reflect infant-driven feeding practice. Newborn Infant Nurs Rev 2007;7:155–60.
52. Arvedson J, Clark H, Lazarus C, Schooling T, Frymark T. Evidence-based systematic review:Effects of oral motor interventions on feeding and swallowing in preterm infants. Am J Speech Lang Pathol 2010;19:321–40.
53. Greene Z, O'Donnell CP, Walshe M. Oral stimulation for promoting oral feeding in preterm infants. Cochrane Database Syst Rev 2016;9:CD009720.
54. Novak I, Morgan C, Adde L, Blackman J, Boyd RN, Brunstrom-Hernandez J, et al. Early, accurate diagnosis and early intervention in cerebral palsy:Advances in diagnosis and treatment. JAMA Pediatr 2017;171:897–907.
55. Soloveichick M, Marschik PB, Gover A, Molad M, Kessel I, Einspieler C. Movement imitation therapy for preterm babies (MIT-PB):A novel approach to improve the neurodevelopmental outcome of infants at high-risk for cerebral palsy. J Dev Phys Disabil 2020;32:587–98.
56. Visscher MO, Lacina L, Casper T, Dixon M, Harmeyer J, Haberman B, et al. Conformational positioning improves sleep in premature infants with feeding difficulties. J Pediatr 2015;166:44–8.
57. Madlinger-Lewis L, Reynolds L, Zarem C, Crapnell T, Inder T, Pineda R. The effects of alternative positioning on preterm infants in the neonatal Intensive Care Unit:A randomized clinical trial. Res Dev Disabil 2014;35:490–7.
58. Liaw JJ, Yang L, Lo C, Yuh YS, Fan HC, Chang YC, et al. Caregiving and positioning effects on preterm infant states over 24 hours in a neonatal unit in Taiwan. Res Nurs Health 2012;35:132–45.
59. Ding X, Zhu L, Zhang R, Wang L, Wang TT, Latour JM. Effects of family-centred care interventions on preterm infants and parents in neonatal Intensive Care Units:A systematic review and meta-analysis of randomised controlled trials. Aust Crit Care 2019;32:63–75.
60. Gong A, Johnson YR, Livingston J, Matula K, Duncan AF. Newborn intensive care survivors:A review and a plan for collaboration in Texas. Matern Health Neonatol Perinatol 2015;1:24.
61. Spittle A, Orton J, Anderson PJ, Boyd R, Doyle LW. Early developmental intervention programmes provided post hospital discharge to prevent motor and cognitive impairment in preterm infants. Cochrane Database Syst Rev 2015;2015:CD005495.
62. Kilbride HW, Aylward GP, Carter B. What are we measuring as outcome?Looking beyond neurodevelopmental impairment. Clin Perinatol 2018;45:467–84.
63. Ozawa M, Yokoo K, Funaba Y, Fukushima S, Fukuhara R, Uchida M, et al. Aquality improvement collaborative program for neonatal pain management in Japan. Adv Neonatal Care 2017;17:184–91.
64. LeBlanc S, Haushalter J, Seashore C, Wood KS, Steiner MJ, Sutton AG. A quality-improvement initiative to reduce NICU transfers for neonates at risk for hypoglycemia. Pediatrics 2018;141:e20171143.
65. Oza-Frank R, Kachoria R, Dail J, Green J, Walls K, McClead RE Jr. A quality improvement project to decrease human milk errors in the NICU. Pediatrics 2017;139:e20154451.
66. Fry TJ, Marfurt S, Wengier S. Systematic review of quality improvement initiatives related to cue-based feeding in preterm infants. Nurs Womens Health 2018;22:401–10.
67. Howe CC, Rose KP, Ferrick J, Pines R, Pardo A. Improving developmental positioning in a level III NICU using evidence-based teaching and a standardized tool:An evidence-based quality improvement project. Neonatal Netw 2022;41:273–80.
68. Knudsen K, Steffen E, Sampson L, Bong K, Morris M. Collaboration to improve neuroprotection and neuropromotion in the NICU:A quality improvement initiative. Neonatal Netw 2021;40:201–9.
69. Ogrinc G, Davies L, Goodman D, Batalden P, Davidoff F, Stevens D. SQUIRE 2.0 (Standards for QUality Improvement Reporting Excellence):Revised publication guidelines from a detailed consensus process. BMJ Qual Saf 2016;25:986–92.
70. . IHI Innovation Series White Paper B. The Breakthrough Series: IHI's Collaborative Model for Achieving Breakthrough Improvement. Boston: Institute for Healthcare Improvement; 2003. 1–20.
71. Horbar JD, Plsek PE, Leahy K. NIC/Q 2000. NIC/Q 2000:Establishing habits for improvement in neonatal Intensive Care Units. Pediatrics 2003;111:e397–410.
72. Sacchi C, Marino C, Nosarti C, Vieno A, Visentin S, Simonelli A. Association of intrauterine growth restriction and small for gestational age status with childhood cognitive outcomes:A systematic review and meta-analysis. JAMA Pediatr 2020;174:772–81.
73. Sacchi C, O'Muircheartaigh J, Batalle D, Counsell SJ, Simonelli A, Cesano M, et al. Neurodevelopmental outcomes following intrauterine growth restriction and very preterm birth. J Pediatr 2021;238:135–44.e10.
74. Levine TA, Grunau RE, McAuliffe FM, Pinnamaneni R, Foran A, Alderdice FA. Early childhood neurodevelopment after intrauterine growth restriction:A systematic review. Pediatrics 2015;135:126–41.
75. Murray E, Fernandes M, Fazel M, Kennedy SH, Villar J, Stein A. Differential effect of intrauterine growth restriction on childhood neurodevelopment:A systematic review. BJOG 2015;122:1062–72.
76. Mirlashari J, Brown H, Fomani FK, de Salaberry J, Zadeh TK, Khoshkhou F. The challenges of implementing family-centered care in NICU from the perspectives of physicians and nurses. J Pediatr Nurs 2020;50:e91–8.
