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Previous Volume 356:2165-2175 May 24, 2007 Number 21 Next

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ABSTRACT

Background There has been a large increase in both the number of neonatal intensive care units (NICUs) in community hospitals and the complexity of the cases treated in these units. We examined differences in neonatal mortality among infants with very low birth weight (below 1500 g) among NICUs with various levels of care and different volumes of very-low-birth-weight infants.

Methods We linked birth certificates, hospital discharge abstracts (including interhospital transfers), and fetal and infant death certificates to assess neonatal mortality rates among 48,237 very-low-birth-weight infants who were born in California hospitals between 1991 and 2000.

Results Mortality rates among very-low-birth-weight infants varied according to both the volume of patients and the level of care at the delivery hospital. The effect of volume also varied according to the level of care. As compared with a high level of care and a high volume of very-low-birth-weight infants (more than 100 per year), lower levels of care and lower volumes (except for those of two small groups of hospitals) were associated with significantly higher odds ratios for death, ranging from 1.19 (95% confidence interval [CI], 1.04 to 1.37) to 2.72 (95% CI, 2.37 to 3.12). Less than one quarter of very-low-birth-weight deliveries occurred in facilities with NICUs that offered a high level of care and had a high volume, but 92% of very-low-birth-weight deliveries occurred in urban areas with more than 100 such deliveries.

Conclusions Mortality among very-low-birth-weight infants was lowest for deliveries that occurred in hospitals with NICUs that had both a high level of care and a high volume of such patients. Our results suggest that increased use of such facilities might reduce mortality among very-low-birth-weight infants.

Growth in the number of NICUs in community hospitals throughout the United States over the past two decades (i.e., deregionalization) has resulted in increasing numbers of high-risk newborns receiving care in low-volume units offering midlevel care.^{6,11,18,19,20,21} It is uncertain whether lower-volume, lower-level NICUs are associated with worse outcomes. One of the complexities in addressing this question is that the units with the highest level of care are also typically those with the highest volume, making it difficult to ascertain whether both volume and level are independent predictors of neonatal outcome.

We,^4,6 as well as other investigators,^{5,9,10,11,12,13,14,15,16,17,22,23,24,25} have previously demonstrated a relationship between the level of NICU care and neonatal outcome. However, most previous studies, including our own, involved relatively small samples or narrowly defined networks and thus could not adequately assess interaction between volume and level of care. In addition, most studies were based on data collected before the routine use of surfactant-replacement therapy, which has substantially improved mortality rates among very-low-birth-weight infants.

These infants are a vulnerable group and thus particularly likely to be affected by hospital services; in 2000, they accounted for only 1.4% of births but 51% of infant deaths.²⁶ In the current study, we used data collected from all hospitals in California from 1991 to 2000 to examine the effects of NICU level of care and patient volume on mortality among very-low-birth-weight infants. These data reflect outcomes reported after the reduction in mortality associated with the introduction of surfactant-replacement therapy in 1990 and, for the most part, after the increased use of antenatal corticosteroid therapy that occurred after the publication of the results of the National Institute of Child Health and Human Development consensus conference in 1994.^27,28,29,30

Methods

Study Design

We obtained data on very-low-birth-weight infants born in California hospitals and on in-hospital infant and fetal deaths for the period from January 1, 1991, to December 31, 2000 (66,838 infants). California birth and death certificates were linked to hospital-discharge abstracts for both mothers and infants. The death certificates included both infant and fetal death certificates. More than 99% of the maternal and infant discharge abstracts were successfully linked with infant birth certificates.^31,32 The birth-certificate data were also successfully linked to infant discharge abstracts from the receiving hospital for 99% of the infants who were transferred to another hospital. The study was approved by the human subjects committees at Stanford University and the California Office of Statewide Health Planning and Development, and the requirement for obtaining informed consent was waived.

Levels of Care

We defined levels of care as follows: level 1, no NICU; level 2, a NICU that provides care for mildly ill infants but does not provide mechanical ventilation; level 3A, a NICU that provides mechanical ventilation with restrictions (e.g., only for infants with a birth weight above 1000 g); level 3B, a NICU that provides mechanical ventilation without restrictions but does not provide major surgery; level 3C, a NICU that provides major neonatal surgery but neither open-heart surgery nor extracorporeal membrane oxygenation (ECMO); and level 3D, a NICU that provides cardiac surgery requiring cardiopulmonary bypass or ECMO. These definitions are based on the draft version of the American Academy of Pediatrics report on NICU levels of care^8,33 to differentiate NICUs in community hospitals from true tertiary or regional perinatal centers (level 3C or 3D). We used the draft rather than the final version because the draft was a more accurate reflection of how hospitals in California were actually operating. The final version does not allow for NICUs that provide mechanical ventilation without restrictions but that do not provide major surgery (level 3B in the draft version); many California NICUs were actually providing this level of care during the study period.

We assigned levels of NICU care to each hospital, for each year, empirically from our data (see Section A-1 of the Supplementary Appendix, available with the full text of this article at www.nejm.org). For each year, we also counted the number of very-low-birth-weight infants who received care at each hospital (both those born in the hospital and those born elsewhere).

Neonatal and Fetal Deaths

Because of improvements in neonatal care, the standard definition of a "neonatal death" — death within 28 days after birth — may be biased by the exclusion of continuously hospitalized infants who die after 28 days. Thus, we use the term "neonatal-related deaths" to refer to all neonatal deaths plus any deaths that occurred between 29 days and 1 year after delivery if the infant was continuously hospitalized. In 2000, deaths after 28 days accounted for 7.5% of all neonatal deaths.

Differences among hospitals in the level of obstetrical care, especially the ability to perform very rapid cesarean deliveries, can result in the live birth of infants who would otherwise die in utero. Thus, the exclusion of in-hospital fetal deaths would introduce a systematic bias against hospitals with large or high-risk obstetrical services. To arrive at a conservative estimate of the number of fetal deaths that occurred after the mother was admitted to the hospital, we identified in-hospital fetal deaths using the International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) codes (see Table A-2 of the Supplementary Appendix) from the mother's discharge abstract for procedures that are performed only if the fetus is still alive. When added to the neonatal deaths, in-hospital fetal deaths accounted for 22.8% of total deaths.

Data on infants with a birth weight below 500 g (5157 infants) were excluded to be consistent with previous studies and because of the variability in decisions about whether to treat such infants. Because some congenital anomalies can increase the risk of death among infants with very low birth weight, we used ICD-9-CM codes to identify and exclude infants with such anomalies (7667 infants) (see Table A-3 of the Supplementary Appendix). We also excluded fetal deaths that we could not confirm had occurred after hospital admission (5777 fetal deaths), resulting in a final sample of 48,237 infants. A total of 6892 infants were transferred between hospitals; these infants remained in the sample, and deaths among them were attributed to the birth hospital.

Statistical Analysis

We used logistic regression to estimate odds ratios for mortality associated with the NICU level of care and annual volume of very-low-birth-weight infants. The dependent variable was in-hospital neonatal-related or fetal death. The standard errors for the hospital-level independent variables were corrected for within-hospital clustering with the use of the "cluster" option in Stata software, version 9.³⁴ We controlled for the year to offset the decline in neonatal mortality over the course of the study period.^27,28

Regressions run separately for each level of care showed that the effects of the volume of very-low-birth-weight infants varied according to the NICU level. For ease of presentation, we created categorical variables for the volume for each level of care.

We tested several different nonlinear functional forms using birth weight and gestational age but used categorical variables for the final model because they produced a better fit. We used separate birth-weight functions for male singletons, female singletons, and multiple births with 100-g intervals up to 1000 g and 250-g intervals from 1000 to 1500 g. For gestational age, we used 2-week intervals through 33 weeks.

We tested a wide range of clinical and demographic variables from the birth certificate and discharge data to control for risk factors, and we considered only those variables that were present at birth (see Table A-4 of the Supplementary Appendix). We developed the model using a random 50% sample and then validated it by applying the estimated coefficients to the remaining data. A Hosmer–Lemeshow test revealed an acceptable fit (P=0.13).³⁵ When applied to the entire data set, the model again fit well (P=0.34 by the Hosmer–Lemeshow test; area under the receiver-operating-characteristic curve=0.86).

Results

The number of NICUs increased slightly between 1991 and 2000, and there was a noticeable shift upward in the levels of care provided (Figure 1). Most of the new NICUs in California in the 1990s were low- or moderate-volume units, as were most of the NICUs that upgraded their level of service (Table A-1 of the Supplementary Appendix).

View larger version (22K): [in this window] [in a new window]   Figure 1. Number of NICUs, According to Level of Care, in California, 1991–2000. Levels of care were empirically determined by the authors on the basis of a modified version of American Academy of Pediatrics definitions.8 Level 2 denotes an intermediate-care NICU, with no mechanical ventilation; level 3A denotes mechanical ventilation with restrictions (e.g., only for infants whose birth weight is greater than 1000 g); level 3B denotes no restrictions on mechanical ventilation but no major surgery; level 3C denotes major neonatal surgery but no cardiac surgery and no extracorporeal membrane oxygenation (ECMO); and level 3D denotes cardiac surgery, ECMO, or both.

 
The percentage of very-low-birth-weight deliveries in hospitals with level 3B, 3C, and 3D NICUs that treated more than 100 such infants decreased from 35.6% in 1991 to 21.5% in 2000 (Table 1), with most of this decline offset by the increase in deliveries at hospitals with level 3B or 3C NICUs that treated 26 to 50 very-low-birth-weight infants annually. The percentage of very-low-birth-weight deliveries in NICUs that treated 51 to 100 of these infants was constant over this time, and there were only minor changes at NICUs with other levels of care.

View this table: [in this window] [in a new window]   Table 1. Distribution of Very-Low-Birth-Weight Deliveries According to Annual Patient Volume and Level of NICU Care Available at the Delivery Hospital in California, 1991 and 2000.

 
There was a wide range in the unadjusted mortality rates among NICU level-of-care and volume groups (Table 2). Mortality decreased as patient volume increased within each level of care and with higher levels of care within each volume group. Table 2 also shows the distribution of several risk factors for death according to the level of care.

View this table: [in this window] [in a new window]   Table 2. Characteristics of Very-Low-Birth-Weight Infants According to NICU Annual Volume and Level of Care, 1991–2000.

 
As compared with deliveries at hospitals with a level 3B, 3C, or 3D NICU that treated at least 100 very-low-birth-weight infants per year, deliveries at hospitals with lower-level and lower-volume NICUs were associated with an increased risk of death (Table 3), adjusted for the risk factors shown in Table 2. (Table A-5 of the Supplementary Appendix, which shows odds ratios for death associated with the other covariates in the model.) The odds ratios decreased as volume increased within each level of care and as the NICU level of care increased within each volume group. The risk of death was significantly higher in level 3B and 3C NICUs that treated 50 or fewer very-low-birth-weight infants per year than in units with larger volumes. The risk of death for NICUs with various combinations of lower levels of care and patient volumes were significantly increased, with the exception of two very small groups of hospitals: those with level 2 NICUs that treated more than 25 very-low-birth-weight infants (four hospitals in 2000) and level 3A NICUs that treated more than 50 such infants (three hospitals in 2000). Although the number of NICUs in these two groups was smaller than normal for categorical variables, model specification tests showed that they should not be combined with smaller NICUs with the same level of care. A NICU that treats 50 very-low-birth-weight infants per year corresponds to an average NICU census of about 15 patients. Thus, most of the increase in the risk of death was accounted for by hospitals with small to moderate-size NICUs.

View this table: [in this window] [in a new window]   Table 3. Odds Ratios for Mortality among Very-Low-Birth-Weight Infants, According to NICU Level of Care and Annual Patient Volume.

 
Results were materially unchanged when we included infants with congenital anomalies and when we excluded in-hospital fetal deaths. We also performed an analysis stratified according to birth weight. Although the associations between mortality and NICU level and volume were greater for the smallest infants (below 1000 g), they were still significant for the larger infants (see Table A-6 of the Supplementary Appendix). The results of a model limited to infants born after 1995 were consistent with the overall results (data not shown). The very strong correlation between NICU volume and number of deliveries, as well as the lack of other data about obstetrical services, limited our ability to investigate the role of obstetrical factors. However, to address the possibility that obstetrical volume accounted for our results, we created a model based on estimates that included obstetrical volume; the effects on our results were minimal (see Table A-6 of the Supplementary Appendix).

We estimated the number of potentially preventable deaths on the basis of the odds ratios from Table 3 and the distribution of very-low-birth-weight deliveries across NICUs in 2000 from Table 1. Because the distance from the mother's home to a hospital determines the feasibility of delivery at that hospital, this analysis was restricted to geographic areas with at least 100 very-low-birth-weight deliveries in 2000. Since most births occurred in the large urban areas of California, this restriction excluded only 8% of such deliveries. Assuming that only 90% of the deliveries of very-low-birth-weight infants in the large urban areas could be shifted to hospitals with tertiary-level NICUs that care for at least 100 such infants annually, we estimated that 21% of the deaths of very-low-birth-weight infants in the year 2000 were potentially preventable (see Table A-7 of the Supplementary Appendix).

Discussion

Our study shows strong associations between both NICU level and volume at the delivery hospital and mortality. Our analysis of data from a 10-year period strengthens the evidence from previous studies that used data from a period of 1 or 2 years. Mortality was lowest when very-low-birth-weight deliveries occurred in hospitals with tertiary-level NICUs that treat more than 100 of these infants annually.

High-volume, high-level NICUs represent the minority of NICUs in California. Fewer than 25% of very-low-birth-weight infants were delivered in such hospitals in 2000, and the proportion of such deliveries occurring in these hospitals has declined over time.

Some limitations of our study should be noted. Because of the observational design, it was not possible to assess whether there was a causal relationship between NICU features and neonatal mortality. Factors other than NICU level and volume may explain the observed associations. For example, hospitals with large, high-level NICUs may also have better obstetrical care. The ability to provide rapid emergency cesarean sections not only prevents some fetal deaths but also results in the delivery of many infants in healthier condition, with associated improvement in survival. Our results were robust when obstetrical volume was added to the model, but the role of obstetrical volume merits further investigation.

Although our model controlled for many potential confounders, we could address only those variables available from birth certificates and discharge abstracts. These data are of high quality,³⁶ but they do not include information on all the potential differences in mortality. The risk factors we assessed did not differ significantly among the level-of-care and volume groups, but it is possible that unmeasured differences among the groups affected the results. Given that some high-risk cases are selectively referred to large tertiary-care centers, we would expect such factors to introduce a bias against the highest-level NICUs; consequently, they should not explain our findings. Our exclusion of infants with life-threatening congenital anomalies eliminated any bias due to referrals that were restricted to infants with treatable anomalies.

The only outcome we assessed was mortality; other outcomes, such as intraventricular hemorrhage and chronic lung disease, are also important. A recent study showed that a higher NICU volume was associated with a lower risk of intraventricular hemorrhage.³⁷ However, the relationship between volume and outcomes other than mortality requires additional study.

Studies using data from the Vermont Oxford Network showed weaker relationships between NICU volume and mortality^38,39 than we observed.^4,6 Further, in these analyses, volume explained less of the variance in mortality than it did in our study. One potential explanation for these differences is that our data included a broader sampling of hospitals, particularly community hospitals. Data from the Vermont Oxford Network also demonstrated considerable variation in outcomes across hospitals after taking the effects of NICU level and volume into account.^38,39

On the basis of our model, we estimated that increased regionalization of NICU care may have the potential to prevent 21% of deaths among very-low-birth-weight infants. This estimate relies on several assumptions, including a causal relationship between large, high-level NICUs and reduced mortality, and a very high level of regionalization. Our observation that 92% of the very-low-birth-rate deliveries in our study occurred in urban areas with more than 100 such deliveries suggests that it would be geographically feasible to regionalize the vast majority of these deliveries in California. To do so would probably require the addition of some large perinatal centers, which, ideally, would be strategically located to maximize geographic access and could be created through the mergers of existing smaller NICUs. There could be some disadvantages to closing facilities that are not included in our estimates, and efforts to increase regionalization are likely to draw some opposition. Although it would be more difficult to regionalize very-low-birth-weight deliveries in more sparsely populated areas of the United States, our results suggest that reductions in mortality could be achieved by moving from low to moderate volumes, which may be a more feasible goal in these areas.

In conclusion, our study showed that the NICU volume and level in the hospitals where very-low-birth-weight infants are born is strongly associated with mortality; the mortality was lowest for deliveries that occurred in hospitals with high-level and high-volume NICUs. Less than a quarter of very-low-birth-weight infants are born in hospitals with such NICUs, and this percentage has been declining over time. Our results suggest that increased regionalization of perinatal care might reduce mortality among very-low-birth-weight infants.

Supported by a grant (HD-36914) from the National Institute of Child Health and Human Development and the Agency for Healthcare Research and Quality.

Dr. Baker reports receiving consulting fees from a consortium of hospitals in the state of Georgia, from Blue Cross of California (Wellpoint), and from Catholic Healthcare West and serving as an expert witness in legal matters related to certificate-of-need legislation. Dr. Phibbs reports serving as a scientific adviser for the Leapfrog Group's evidence-based hospital referral program and as chairman of the neonatal subcommittee. No other potential conflict of interest relevant to this article was reported.

Source Information

From the Health Economics Resource Center and the Center for Health Care Evaluation, Veterans Affairs Palo Alto Health Care System, Menlo Park, CA (C.S.P., S.K.S.); the Department of Pediatrics (C.S.P.) and the Department of Health Research and Policy and the Center for Primary Care Outcomes Research (C.S.P., L.C.B.), Stanford University School of Medicine, Stanford, CA; the National Bureau for Economic Research, Cambridge, MA (L.C.B.); the Department of Obstetrics and Gynecology (A.B.C.) and the Department of Pediatrics and the Cardiovascular Research Institute (R.H.P.), University of California, San Francisco; and Health Information Solutions, Rocklin, CA (B.D.).

Address reprint requests to Dr. C. Phibbs at the Health Economics Resource Center (152), VA Palo Alto Health Care System, 795 Willow Rd., Menlo Park, CA 94025, or at cphibbs{at}stanford.edu.

References

1. Luft HS, Bunker JP, Enthoven AC. Should operations be regionalized? The empirical relation between surgical volume and mortality. N Engl J Med 1979;301:1364-1369. [Abstract]
2. Halm EA, Lee C, Chassin MR. Is volume related to outcome in health care? A systematic review and methodologic critique of the literature. Ann Intern Med 2002;137:511-520. [Free Full Text]
3. Kahn JM, Goss CH, Heagerty PJ, Kramer AA, O'Brien CR, Rubenfeld GD. Hospital volume and the outcomes of mechanical ventilation. N Engl J Med 2006;355:41-50. [Free Full Text]
4. Cifuentes J, Bronstein J, Phibbs CS, Phibbs RH, Schmitt SK, Carlo WA. Mortality in low birth weight infants according to level of neonatal care at hospital of birth. Pediatrics 2002;109:745-751. [Free Full Text]
5. Mayfield JA, Rosenblatt RA, Baldwin LM, Chu J, Logerfo JP. The relation of obstetrical volume and nursery level to perinatal mortality. Am J Public Health 1990;80:819-823. [Free Full Text]
6. Phibbs CS, Bronstein JM, Buxton E, Phibbs RH. The effect of patient volume and level of care at the hospital of birth on neonatal mortality. JAMA 1996;276:1054-1059. [Abstract]
7. Williams RL. Measuring the effectiveness of perinatal medical care. Med Care 1979;17:95-110. [ISI][Medline]
8. Stark AR. Levels of neonatal care. Pediatrics 2004;114:1341-1347. [Erratum, Pediatrics 2005;115:1118.] [Free Full Text]
9. Yeast JD, Poskin M, Stockbauer JW, Shaffer S. Changing patterns in regionalization of perinatal care and the impact on neonatal mortality. Am J Obstet Gynecol 1998;178:131-135. [CrossRef][ISI][Medline]
10. Verloove-Vanhorick SP, Verwey RA, Ebeling MC, Brand R, Ruys JH. Mortality in very preterm and very low birth weight infants according to place of birth and level of care: results of a national collaborative survey of preterm and very low birth weight infants in the Netherlands. Pediatrics 1988;81:404-411. [Free Full Text]
11. Powell SL, Holt VL, Hickok DE, Easterling T, Connell FA. Recent changes in delivery site of low-birth-weight infants in Washington: impact on birth weight-specific mortality. Am J Obstet Gynecol 1995;173:1585-1592. [CrossRef][ISI][Medline]
12. Paneth N, Kiely JL, Wallenstein S, Marcus M, Pakter J, Susser M. Newborn intensive care and neonatal mortality in low-birth-weight infants: a population study. N Engl J Med 1982;307:149-155. [Abstract]
13. Paneth N, Kiely JL, Wallenstein S, Suser M. The choice of place of delivery: effect of hospital level on mortality in all singleton births in New York City. Am J Dis Child 1987;141:60-64. [Abstract]
14. Chien LY, Whyte R, Aziz K, Thiessen P, Matthew D, Lee SK. Improved outcome of preterm infants when delivered in tertiary care centers. Obstet Gynecol 2001;98:247-252. [Free Full Text]
15. Bode MM, O'Shea TM, Metzguer KR, Stiles AD. Perinatal regionalization and neonatal mortality in North Carolina, 1968-1994. Am J Obstet Gynecol 2001;184:1302-1307. [CrossRef][ISI][Medline]
16. Menard MK, Liu Q, Holgren EA, Sappenfield WM. Neonatal mortality for very low birth weight deliveries in South Carolina by level of hospital perinatal service. Am J Obstet Gynecol 1998;179:374-381. [CrossRef][ISI][Medline]
17. Johansson S, Montgomery SM, Ekbom A, et al. Preterm delivery, level of care, and infant death in Sweden: a population-based study. Pediatrics 2004;113:1230-1235. [Free Full Text]
18. Howell EM, Richardson D, Ginsburg P, Foot B. Deregionalization of neonatal intensive care in urban areas. Am J Public Health 2002;92:119-124. [Free Full Text]
19. Goodman DC, Fisher ES, Little GA, Stukel TA, Chang CH, Schoendorf KS. The relation between the availability of neonatal intensive care and neonatal mortality. N Engl J Med 2002;346:1538-1544. [Free Full Text]
20. Goodman DC, Fisher ES, Little GA, Stukel TA, Chang CH. Are neonatal intensive care resources located according to need? Regional variation in neonatologists, beds, and low birth weight newborns. Pediatrics 2001;108:426-431. [Free Full Text]
21. Haberland CA, Phibbs CS, Baker LC. Effect of opening midlevel neonatal intensive care units on the location of low birth weight births in California. Pediatrics 2006;118:e1667-e1679. [Free Full Text]
22. Kirby RS. Perinatal mortality: the role of hospital of birth. J Perinatol 1996;16:43-49. [Medline]
23. Paneth N, Kiely JL, Susser M. Age at death used to assess the effect of interhospital transfer of newborns. Pediatrics 1984;73:854-861. [Free Full Text]
24. Rosenblatt RA, Mayfield JA, Hart LG, Baldwin LM. Outcomes of regionalized perinatal care in Washington State. West J Med 1988;149:98-102. [ISI][Medline]
25. Sanderson M, Sappenfield WM, Jespersen KM, Liu Q, Baker SL. Association between level of delivery hospital and neonatal outcomes among South Carolina Medicaid recipients. Am J Obstet Gynecol 2000;183:1504-1511. [CrossRef][ISI][Medline]
26. Mathews TJ, Maenacker F, MacDorman MF. Infant mortality statistics from the 2000 period linked birth/infant death data set. Natl Vital Stat Rep 2002;50:1-28. [Medline]
27. Horbar JD, Badger GJ, Carpenter JH, et al. Trends in mortality and morbidity for very low birth weight infants, 1991-1999. Pediatrics 2002;110:143-151. [Free Full Text]
28. Fanaroff AA, Wright LL, Stevenson DK, et al. Very-low-birth-weight outcomes of the National Institute of Child Health and Human Development Neonatal Research Network, May 1991 through December 1992. Am J Obstet Gynecol 1995;173:1423-1431. [CrossRef][ISI][Medline]
29. NIH Consensus Development Panel on the Effect of Corticosteroids for Fetal Maturation on Perinatal Outcomes. Effect of corticosteroids for fetal maturation on perinatal outcomes. JAMA 1995;273:413-418. [Abstract]
30. Jobe AH. Pulmonary surfactant therapy. N Engl J Med 1993;328:861-868. [Free Full Text]
31. Herrchen B, Gould JB, Nesbitt T. Vital statistics linked birth/infant death and hospital discharge record linkage for epidemiological studies. Comput Biomed Res 1997;30:290-305. [CrossRef][ISI][Medline]
32. Danielsen B. Probabilistic record linkages for generating a comprehensive epidemiological research file on maternal and infant health. Rocklin, CA: Health Information Solutions, 2000.
33. Bhatt DR, Stillwell J. California directory of NICUs, neonatologists, perinatologists, pediatric surgeons & congenital heart surgeons. Elk Grove Village, IL: American Academy of Pediatrics, 2002.
34. Stata user's guide. 8th ed. College Station, TX: Stata Press, 2003.
35. Hosmer DW, Taber S, Lemeshow S. The importance of assessing the fit of logistic regression models: a case study. Am J Public Health 1991;81:1630-1635. [Free Full Text]
36. Meux EF, Stith SA, Zach A. Report of results from the OSHPD reabstracting project: an evaluation of the reliability of selected patient discharge data, July through December 1988. Sacramento: Office of Statewide Health Planning and Development, California Department of Health Services, 1990.
37. Synnes AR, Macnab YC, Qiu Z, et al. Neonatal intensive care unit characteristics affect the incidence of severe intraventricular hemorrhage. Med Care 2006;44:754-759. [CrossRef][ISI][Medline]
38. Rogowski JA, Staiger DO, Horbar JD. Variations in the quality of care for very-low-birthweight infants: implications for policy. Health Aff (Millwood) 2004;23:88-97. [Free Full Text]
39. Rogowski JA, Horbar JD, Staiger DO, Kenny M, Carpenter J, Geppert J. Indirect vs direct hospital quality indicators for very low-birth-weight infants. JAMA 2004;291:202-209. [Free Full Text]

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