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Neurodevelopmental and Growth Outcomes of Extremely Low Birth Weight Infants Who Are Transferred From Neonatal Intensive Care Units to Level I or II Nurseries

^a Department of Pediatrics, Women and Infants Hospital, Providence, Rhode Island
^b Statistical and Epidemiology Unit, RTI International, Research Triangle Park, North Carolina

	ABSTRACT

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OBJECTIVE. Transfer of clinically stable infants to level I and II nurseries alleviates demands on NICUs and allows better use of beds and resources. This study compared growth, neurodevelopmental impairments, postdischarge rehospitalization and deaths, and compliance for follow-up assessment at 18 to 22 months' corrected age of extremely low birth weight infants who transferred to level I and II nurseries with those who continued to receive care to discharge in a NICU.

METHODS. A retrospective analysis of prospectively collected data from the National Institute of Child Health and Human Development Neonatal Research Network was performed. Between January 1998 and June 2002, 4896 infants born with birth weights of 401 to 1000 g and cared for in 19 National Institute of Child Health and Human Development Neonatal Research Network centers were included. The sample consisted of 4392 survivors who received continuing care in the NICU to discharge home and 504 infants who were transferred to level I and II nurseries before discharge home. Demographics, perinatal characteristics, growth, and neurodevelopmental impairments were compared. Bivariate and logistic regression analyses were performed.

RESULTS. Transfer of infants to level I and II nurseries was associated significantly with white race, private insurance, outborn status, and lower neonatal morbidities and compliance for follow-up compared with the NICU group. After adjusting for known covariates, transfer to level I and II nurseries was not associated with neurodevelopmental impairments or death; however, it was associated with increased postdischarge rehospitalization.

CONCLUSIONS. Extremely low birth weight infants who are transferred to level I and II nurseries have similar growth and neurodevelopmental outcomes to infants who are discharged from a NICU. They are, however, more likely to be readmitted to the hospital and are less compliant for follow-up. Establishment of consistent guidelines for comprehensive discharge planning for level I and II nurseries may improve follow-up compliance and reduce rehospitalization rates among these infants who are transferred.

Key Words: neurodevelopmental outcomes • ELBW infants • level I and II nurseries • transfer • NICU

Abbreviations: CA—corrected age • ELBW—extremely low birth weight • NICHD—National Institute of Child Health and Human Development • RDS—respiratory distress syndrome • IVH—intraventricular hemorrhage • PVL—periventricular leukomalacia • NEC—necrotizing enterocolitis • ROP—retinopathy of prematurity • BPD—bronchopulmonary dysplasia • NDI—neurodevelopmental impairment • MDI—mental developmental index • PDI—psychomotor developmental index • SIDS—sudden infant death syndrome • OR—odds ratio • CI—confidence interval

The driving forces for the emergence of perinatal regionalization in the 1970s were shortage of trained personnel who are required for the care of low birth weight infants and the financial costs of maintaining these skills.^1,2 This change in the pattern of services provided has improved the morbidity and the mortality of low birth weight, high-risk infants who are born at level I and II nurseries in community hospitals and transferred to a level III tertiary medical center NICU for additional care.³ Transfer of high-risk mothers from community hospital obstetric units to tertiary perinatal centers before delivery has further improved the morbidity and the mortality in this group of infants.⁴

In the past 3 decades, advancing perinatal and neonatal technology, changing socioeconomic conditions, and health behavior patterns have resulted in an increase in the preterm birth rate, as well as survival, of these high-risk infants who require NICU care.⁵ Regional studies of the transport system have shown a 40% increase in transfer of high-risk infants to NICUs from community hospital level I and II nurseries.⁶ This has introduced new demands on the resources of tertiary centers, such as increased need for beds, equipment, skilled staff, and finances. Transfer of clinically stable infants to level I and II nurseries alleviates some of these demands on tertiary NICUs as well as allows for better use of level I and II nursery beds and resources.^7,8

Although a limited number of studies reported better short-term clinical outcomes of infants who were transferred from a NICU to level I and II nurseries, an extensive literature review did not identify reports on the neurodevelopmental outcomes of these infants.^8,9 The objective of our study was to compare neonatal and perinatal characteristics and growth and neurodevelopmental outcomes at a follow-up visit at 18 to 22 months' corrected age (CA) of extremely low birth weight (ELBW) infants who received total care in the tertiary center NICU with infants who were transferred to a community level I or II nursery before discharge home. It was hypothesized that infants who were transferred to level I and II nurseries and infants who continued to receive care in the tertiary center NICU until discharge would have similar neurodevelopmental and growth outcomes at follow-up.

	METHODS

TOP ABSTRACT METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
This retrospective study was conducted on prospectively collected data on all ELBW infants who were admitted within 14 days of birth between January 1998 and June 2002 with birth weights of 401 to 1000 g at 1 of the 19 level III neonatal centers of the National Institute of Child Health and Human Development (NICHD) Neonatal Network and who survived to discharge home from the NICU or were transferred to level I and II nurseries. Data were obtained from the NICHD Neonatal Network database. Each center's participation was approved by its respective institutional review board. Research coordinators collected demographic, perinatal, and infant data at each participating center using definitions that were developed by the investigators and described in previous publications.^10,11 Neonatal outcome data were assessed at 120 days after birth, at discharge, or at the time of death. Hospital data on infants who were transferred to level I and II nurseries were collected until they were discharged from the hospital. Data including network NICU transfer rates and level of care provided at their affiliate level I and II nurseries.

Length of hospitalization of infants in the NICU included the number of days in the tertiary center NICU until discharge to home, whereas length of hospitalization of the level I and II nurseries group included the number of days in the NICU as well as level I and II nurseries until discharge to home. Demographics including maternal age, race, education, insurance type, gravidity, singleton or multiple birth, and infant birth weight and estimated gestational age were obtained. Neonatal morbidities including the incidence of respiratory distress syndrome (RDS), intraventricular hemorrhage (IVH), periventricular leukomalacia (PVL), necrotizing enterocolitis (NEC), retinopathy of prematurity (ROP), early- and/or late-onset sepsis, bronchopulmonary dysplasia (BPD), and need for home oxygen therapy were collected.

IVH was reported according to the classification of Papile et al.¹² PVL was diagnosed by cranial ultrasonography performed at >2 weeks of age. Cranial ultrasonographs were read by individual radiologists at each center and not by a central reader. Early sepsis was defined as sepsis with a positive blood culture drawn at <72 hours of age, and late-onset sepsis was defined as a positive blood culture drawn 72 hours of age. NEC stage II or higher was recorded using a modified Bells classification.¹³ BPD was defined as a supplemental oxygen requirement at 28 days of age.¹⁴

Follow-up neurologic, developmental, and growth assessments were performed at 18 to 22 months' CA. The neurodevelopmental tests are valid to 36 months' CA. These neurodevelopmental tests were age-adjusted for infants who were seen beyond the 18- to 22-months' CA window. The neurologic examination based on the Amiel-Tison neurologic assessment was conducted by certified examiners.¹⁵ Cerebral palsy was defined as a nonprogressive central nervous system disorder characterized by abnormal muscle tone in at least 1 extremity and abnormal control of movement and posture. The Bayley Scales of Infant Development II mental and motor scales were administered by certified testers. A Bayley score of 100 ± 15 represents the mean ± 1 SD. A score of <70 is 2 SD below the mean.¹⁶ Hearing status information was obtained from parents and follow-up audiologic test results. Hearing impairment was defined as using hearing aids in both ears. An examination of the eyes was completed, and eye examination history was obtained from parents and from physician reports, when available. Blind was defined as no useful vision (>20:200) in both eyes, when corrected. Neurodevelopmental impairment (NDI) was defined as presence of 1 or more of the following: mental developmental index (MDI) <70, psychomotor developmental index (PDI) <70, cerebral palsy, hearing impairment, or blindness. Growth parameters including weight, length, and head circumference measurements were assessed using standardized techniques. Percentiles were determined using growth charts developed by the National Center for Health Statistics (published May 30, 2000). Immunization information, including respiratory syncytial virus prophylaxis, was obtained from parents.

The 2 study groups included infants who received total care in the tertiary center NICU until discharge home and infants who were transferred from a NICU to level I and II nurseries for continuing care before discharge home. Bivariate analyses of demographic characteristics, neonatal morbidities, growth parameters, neurodevelopmental outcomes at the follow-up at 18 to 22 months' CA, compliance for follow-up at 18 to 22 months CA, and rehospitalizations and deaths after discharge were performed. Also, infants who were lost to follow-up were compared with those who were followed for neurodevelopmental and growth assessment using bivariate analysis. Numbers and percentages are shown for categorical covariates. Means and SDs are shown for continuous covariates. For comparison of NICU and level I and II nurseries groups, ² tests were performed for categorical covariates, and Kruskal-Wallis nonparametric tests were performed for continuous covariates. Logistic regression analyses was performed to evaluate the effects of transfer to level I and II nurseries and outborn status on NDI, MDI and PDI <70, postdischarge rehospitalization in the first year of life and before the follow-up visit at 18 to 22 months' CA, postdischarge deaths in the first 6 months after discharge and before the follow-up visit at 18 to 22 months' CA, and loss to follow-up at 18 to 22 months' CA. Factors that were included in the model were neonatal centers, outborn (infant transferred to NICU from level I and II nurseries after birth), infant transfer to level I and II nurseries from NICU, multiple births, maternal education, insurance type, male gender, birth weight, gestational age, IVH (grades 3 and 4 or PVL), ROP, NEC (stage II or higher), RDS, early- and late-onset sepsis, and BPD.

	RESULTS

TOP ABSTRACT METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
A total of 4896 infants with birth weight between 401 and 1000 g were born at the 19 network centers or transferred in within 14 days of birth between January 1998 and June 2002 and survived to be transferred to level I and II nurseries or discharge home; 4392 (89.7%) infants received complete care in the NICU, and 504 (10.3%) infants were transferred to level I and II nurseries before discharge home. Twenty-three infants who were transferred from a network NICU to another level III NICU and 41 infants who were transferred to long-term care facilities were excluded from the study. As expected, there was a significantly high risk for NDI (75%) and death (11%) in the group of infants who were transferred to long-term care facilities.

All network NICUs transferred infants to level II nurseries, and 50% of NICUs transferred infants to level I nurseries. During the study period, the network NICU transfer rates to level I and II nurseries ranged from 1% to 44%. Among the units that received transfers, 80% of level II nurseries were staffed by a neonatologist and 53% of these level II nurseries provided conventional ventilatory care to the infants, whereas only 20% of level I nurseries were staffed by a neonatologist and none provided ventilatory care. None of the level I or level II nurseries had admission criteria for infant gestational age or weight.

The maternal demographic and socioeconomic characteristics of the NICU and level I and II nurseries groups are presented in Table 1. There were no significant differences in maternal age, education, gravidity, and multiple gestation between NICU and level I and II nurseries groups. Infants who were white compared with other ethnic groups (P < .0001) and infants with private health insurance (P = .002) were more likely to be transferred to level I and II nurseries.

Neurodevelopmental and growth outcomes at the follow-up visit 18 to 22 months' CA are shown in Table 6. The mean Bayley MDI score in the level I and II nurseries group was 2.3 points higher than in the NICU group (P = .01). NDI was identified in 38% of infants who were cared for in the NICU and 32% of those who were transferred to level I and II nurseries (P = .03). Growth parameters were similar among NICU and level I and II nurseries groups at follow-up.

	DISCUSSION

TOP ABSTRACT METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
ELBW infants who were transferred to level I and II nurseries from tertiary care NICUs had similar neurodevelopmental outcomes and growth compared with infants who received continuing care in the NICU until discharge home. Unique demographic characteristics of infants who were cared for in level I and II nurseries were identified. Their mothers are more likely to be white and have private health insurance. The infants who were cared for in level I and II nurseries were more likely to be outborn, spent >1 month in the level I and II nurseries, and were discharged earlier than the NICU infants.

Transfer of clinically stable ELBW infants to level I and II nurseries has potential advantages. In our cohort, infants who were transferred to a level I and II nurseries had a 21-g higher birth weight, 0.4-week higher gestational age, and lower rates of late-onset sepsis and ROP than the NICU group. This suggests that infants who were transferred to level I and II nurseries had a more benign neonatal course, making them candidates for both transfer and earlier discharge to home. In fact, the infants in level I and II nurseries group were discharged 5 days earlier and 160 g lighter in weight than infants in the NICU group. These findings were similar to those that were observed by Pittard et al,⁸ who reported that outborn infants who were back-transferred were discharged from the hospital 42 days earlier and with a 353-g lower discharge weight than those who were discharged from a tertiary center.

Our data suggest that there is a potential for adverse outcomes that are associated with transfer of ELBW infants to level I and II nurseries. In general, ELBW infants remain at risk for late-onset sepsis, respiratory compromise, and failure to thrive during the convalescent period whether it is in the NICU or level I or II nursery. Four infants died after transfer to a level I or II nursery. Although in this study the NICU group rehospitalization rate (49%) and death rate (2%) were similar to those that were reported in previous NICHD network publications,^17–19 a higher rate of rehospitalization (56%) was reported in infants who were discharged from level I and II nurseries. After adjustment for standard covariates, transfer to level I and II nurseries was associated with an increased risk of rehospitalization between discharge and the follow-up visit at 18 to 22 months' CA but not in the first year of life. A higher percentage of infants in the level I and II nurseries group were rehospitalized for surgical issues, and a significantly higher number of infants who were discharged from level I and II nurseries received hernia surgery after discharge. We speculate that community hospitals where these level I or level II nurseries are located may lack pediatric subspecialties, including pediatric surgery, requiring that infants be rehospitalized for surgical procedures after discharge home, whereas, NICU infants at tertiary care centers are more likely to have surgical procedures before discharge. Rehospitalization rate was significantly higher for infants who were discharged from the hospital on oxygen from level I and II nurseries compared with those who were discharged from the hospital on oxygen from the NICU. Rehospitalization rates were similar for infants who were discharged from the hospital on room air in the 2 groups. We speculate that infants who were discharged from level I and II nurseries may have decreased access to subspecialty and neonatal follow-up care after discharge. This lack of access would have greater implications for infants with complex medical problems or those who require additional surgery.

After adjustment for standard covariates, the postdischarge death rate was not associated with transfer to level I and II nurseries. The causes of death were similar in the 2 groups, except for the trend for higher incidence of SIDS (40%) in the level I and II nurseries group. Lower birth weight is known to be associated with SIDS.^20,21

Although a general framework for different levels of neonatal care exists,²² there are no standard definitions or classifications for the complexity of care provided at different levels of neonatal units. Some states have policies that designate different levels of care that can be provided by a nursery. However, the interpretation of these designations and the applications of these NICU-related regulations vary considerably.²³ The level of care that is provided by a level I nursery and level III NICUs is fairly consistent. Greater diversity in the level of care is seen in level II nurseries.²⁴ In our study, 80% of level II nurseries and only 20% of level I nurseries that received transfers from the network NICU centers were staffed by a neonatologist, and 50% of level II nurseries provided ventilatory care in the unit. Also, none of the level I or level II nurseries had a lower limit for infant weight or gestational age for admission. In this cohort, at least 1 infant had a transfer weight of 600 g and another was transferred at a CA of 25 weeks (confirmed by centers). This suggests that there is a degree of variability in the level of intensive care that is provided at different community hospital nurseries that are affiliated with the network centers. We speculate that there may be differences in the medical management and comprehensive discharge planning that are provided to infants who are discharged from different level I and level II nurseries that may affect hospital readmission rates. The characteristics of the level of care that is provided to ELBW infants as well as the discharge planning and postdischarge management at community hospitals requires additional evaluation.

Infants in level I and II nurseries had higher birth weight and gestational age and lower neonatal morbidities. NDI is known to be associated with lower birth weight and neonatal morbidities.^19,25,26 In our study, after adjustment for demographic and neonatal characteristics, NDI was not affected by transfer to level I and II nurseries; delivery outside the tertiary center was associated with increased risk for NDI and for MDI <70. Higher mortality and morbidity in infants who were born outside a tertiary center have been reported³; however, an association with worse NDI and MDI was not reported previously.

Transfer of infants to levels I and II hospitals within the community may decrease parental stress by facilitating better parental and sibling bonding and allowing the continuing care physician to be involved in the medical issues that are specific to the infant.²⁷ However, transfer also may lead to increased stress on the parent. Family reaction to transfer may be either positive or negative. This depends on many factors, including the transfer experience of staff, the quality of communication between the staff at the 2 hospitals, and the availability of support services for the parents.^28,29 Lack of communication between the 2 hospitals may result in inadequate referrals and follow-up for needed services such as early intervention, developmental assessment, and subspecialty clinics. In this study, 78% of infants who were cared for in level I and II nurseries compared with 89% of NICU infants were assessed at follow-up at 18 to 22 months' CA. Similar to other studies,³⁰ in this cohort, outborn infants who were born to younger mothers with public insurance, had higher gestational age, and had shorter hospitalization were more likely to be noncompliant for follow-up. Infants in the level I and II nurseries group also were more likely to receive follow-up assessment beyond the 18- to 22-months CA window than those in the NICU group. Increased geographic distance and limited access to specialty and support services may be some of the additional factors that are difficult to measure but may have contributed toward the loss to follow-up.

	CONCLUSIONS

TOP ABSTRACT METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
In this ELBW cohort, infants who were transferred to level I and II nurseries had fewer neonatal morbidities, were discharged earlier, and had similar NDI and growth compared with the NICU only infants. However, infants who were cared for in level I and II nurseries were more likely to be rehospitalized and were at an increased risk for loss to follow-up. Establishment of consistent guidelines for neonatal management and comprehensive discharge planning by community hospital nurseries in partnership with the tertiary center NICUs may improve follow-up compliance and reduce rehospitalizations.

	ACKNOWLEDGMENTS

 
Members of the NICHD Neonatal Research Network were as follows: follow-up center, principal investigator, follow-up principal investigator, network coordinator, follow-up coordinator (grants): Brown University, William Oh, MD, Betty Vohr, MD, Angelita Hensman, RNC, Lucy Noel, RNC (U10 HD27904); Case Western Reserve University, Avroy A. Fanaroff, MB, BCh, Dee Wilson, MD, Nancy Newman, RN, Bonnie Singer, RN (U10 HD21364); Duke University, Ron Goldberg, MD, Ricki Goldstein, MD, Melody Lohmeyer, Melody Lohmeyer (U10 HD40492); Emory University, Barbara J. Stoll, MD, Barbara J. Stoll, MD, Ellen Hale, RNC, BS, Ellen Hale, RNC, BS (U10 HD27851, M01 RR00039); Harvard University, Ann R. Stark, MD, Ann R. Stark, MD, Kerri Fournier, RN (U10 HD34167, M01 RR02635, M01 RR02172, M01 RR01032); Indiana University, James A. Lemons, MD, Anna Dusick, MD, DeeDee Appel, RN, Leslie Richards, RN (U10 HD27856, M01 RR00750); Stanford University, David K. Stevenson, MD, Susan Hintz, MD, Bethany Ball, RN, Bethany Ball, RN (U10 HD27880, M01 RR00070); University of Alabama, Waldemar A. Carlo, MD, Myriam Peralta, MD, Monica Collins, RN, Vivien Phillips (U10 HD34216); University of Cincinnati, Edward F. Donovan, MD, Jean Steichen, MD, Cathy Grisby, RN, Teresa Gratton, PA (U10 HD27853, M01 RR08084); University of Miami, Shahnaz Duara, MD, Charles Bauer, MD, Ruth Everett, RN, Mary Allison, RN (U10 HD21397); University of New Mexico, Lu-Ann Papile, MD, Lu-Ann Papile, MD, Conra Backstrom, RN (U10 HD27881, M01 RR00997); University of Tennessee, Sheldon B. Korones, MD, Kimberly Yolton, PhD, Tina Hudson, RN (U10 HD21415); University of Texas–Dallas, Abbot R. Laptook, MD, Roy Heyne, MD, Susie Madison, RN, Jackie Hickman, RN (U10 HD40689); University of Texas–Houston, John E. Tyson, Brenda Morris, Georgia McDavid, Georgia McDavid (U10 HD21373); University of California–San Diego, Neil Fiener, MD, Yvonne Vaucher, MD, Wade Rich, Martha Fuller (U10 HD40461); Wayne State University, Seetha Shankaran, MD, Yvette Johnson, MD, Gerry Muran, BSN, Debbie Kennedy, RN (U10 HD21385); Wake Forest University, Michael O'Shea, MD, Robert Dillard, MD, Nancy Peters, Barbara Jackson (U10 HD40498); Yale University, Richard A. Ehrenkranz, MD, Richard A. Ehrenkranz, MD, Pat Gettner, RN, Elaine Romano, MSN (U10 HD27871, M01 RR06022); Rochester University, Dale L. Phelps, MD, Gary Myers, MD, Linda Reubens, RN, Diane Hust, PNP (U10 HD40521, M01 RR00044); NICHD, Linda L. Wright, MD, Rose Higgins, MD, Scott McDonald, BS, Beth B. McClure, MEd, Carolyn Petrie, MS; RTI International (Steering Committee Chairman: Alan H. Jobe, MD, PhD), W. Kenneth Poole, PhD, W. Kenneth Poole, PhD, Betty Hastings, Beth B. McClure, MEd (U10 HD36790); George Washington University, Biostatical Coordinating Center, Joel Verter, PhD (U10 HD 19897).

	FOOTNOTES

 
Accepted Nov 7, 2006.

Address correspondence to Shabnam Lainwala, PhD, MBBS, Department of Pediatrics, Women and Infants Hospital, 101 Dudley St, Providence, RI 02905. E-mail: slainwala{at}wihri.org

The authors have indicated they have no financial relationships relevant to this article to disclose.

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