PEDIATRICS Vol. 114 No. 6 December 2004, pp. 1584-1590 (doi:10.1542/peds.2004-0708)
Declining Diagnosis of Birth Asphyxia in California: 1991–2000
* Department of Neurology, University of California, San Francisco, California
Department of Pediatrics, University of California, San Francisco, California
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ABSTRACT |
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Objective. Birth asphyxia is recognized as an important cause of neonatal morbidity and mortality. Whether advances in perinatal care have altered the incidence of birth asphyxia is unknown. We determined the incidence of birth asphyxia diagnoses made over a 10-year period in California.
Methods. In a population-based retrospective cohort study of 5 364 663 live births, we determined the incidence and case fatality of birth asphyxia between 1991 and 2000. Using a statewide administrative hospital discharge database, we identified all newborn admissions that generated a diagnosis of birth asphyxia (International Classification of Diseases, Ninth Revision, Clinical Modification codes 768.5, 768.6, or 768.9) or a diagnosis that overlaps with birth asphyxia, such as congenital encephalopathy or fetal distress. We determined incidence and in-hospital case fatality rates adjusted for birth weight and demographic characteristics and stratified by associated perinatal complications.
Results. The 24 330 newborns who received a diagnosis of birth asphyxia yielded a population incidence of 4.5 per 1000 live births. Black ethnicity (relative risk [RR]: 1.3; 95% confidence interval [CI]: 1.2–1.3), male gender (RR: 1.2; 95% CI: 1.1–1.2), and low socioeconomic status (RR: 1.2; 95% CI: 1.1–1.2) all were associated with increased risk. The diagnosis of birth asphyxia decreased by 91% from 14.8 to 1.3 per 1000 live births during the study years. This decrease could not be explained by an increased diagnosis of overlapping conditions. Overall case fatality was 4%, and the majority of deaths in infants >2000 g occurred in the presence of congenital anomalies, cord abnormalities, or maternal hemorrhage. In newborns <2000 g, case fatality was highest in the presence of chorioamnionitis (48%).
Conclusion. The diagnosis of birth asphyxia has decreased dramatically in recent years. The factors that are responsible for this decline are unclear and deserve additional investigation.
Key Words: asphyxia • epidemiology • neonatal
Abbreviations: OSHPD, Office of Statewide Health Planning and Development • ICD-9-CM, Classification of Diseases, Ninth Revision, Clinical Modification • SES, socioeconomic status • LBW, low birth weight • VLBW, very low birth weight • IUGR, intrauterine growth restriction • RR, relative risk • CI, confidence interval
The clinical diagnosis of birth asphyxia, along with the closely related conditions of hypoxic-ischemic encephalopathy and newborn encephalopathy, is recognized as an important cause of morbidity and mortality in newborn infants.1–5 Whether advances in perinatal care have altered the incidence of birth asphyxia is not known.
Birth asphyxia is diagnosed in 2 to 9 per 1000 term births, depending on how the clinical syndrome is defined.5–13 Previous incidence studies were conducted before 1990 with few exceptions,1,10,14 and longitudinal studies are rare.5,10 In the United States, infant mortality as a result of birth asphyxia fell 72% in the years 1979–1996.3 It is unclear how much of this improvement can be attributed to decreased incidence of birth asphyxia, as opposed to improved survival given advances in neonatal care. Although the incidence of newborn hypoxic-ischemic encephalopathy in a British hospital decreased dramatically from 7.7 per 1000 live births in the late 1970s to 1.9 per 1000 in the mid-1990s,8,10 investigators in Sweden found that the incidence of birth asphyxia and neonatal hypoxic-ischemic encephalopathy increased slightly between the years 1985 and 1991.5
We conducted a retrospective evaluation of all newborn hospital admissions that generated a discharge diagnosis of birth asphyxia in California from 1991 through 2000. We determined gender- and ethnicity-specific incidence rates of birth asphyxia, as well as change in incidence of birth asphyxia over a 10-year period.
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METHODS |
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The Office of Statewide Health Planning and Development (OSHPD) of California maintains a database of discharge abstracts for all admissions to nonfederal hospitals. Hospitals began contributing cases in January 1990 with complete participation after June 1990. All birth hospitalizations for a newborn infant are identified in the OSHPD database with a newborn code. We searched the OSHPD hospital discharge database from January 1991 through December 2000 for newborns with a discharge diagnosis of birth asphyxia as follows: mild or moderate birth asphyxia, International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) code 768.6; severe birth asphyxia, ICD-9-CM code 768.5; or unspecified birth asphyxia, ICD-9-CM 768.9.15 Newborns whose zip code did not indicate residence in California were excluded.
Annual incidence of birth asphyxia was calculated as the number of newborns discharged with a diagnosis of birth asphyxia each year, divided by the total number of live births recorded in the OSHPD hospital discharge data set for that same year. According to the California natality figures available from the Centers for Disease Control and Prevention for the years 1991–1998,16 the 4 355 047 live births recorded in the OSHPD hospital discharge data set from 1991 to 1998 represent 96.7% of all live births in California. Because uncomplicated home births are not counted in our denominator, our calculations slightly overestimate the incidence of birth asphyxia diagnosed in California. However, we chose to use the live births in the OSHPD data set as the denominator so that our incidence rates could be stratified by ethnicity, birth weight and other demographic variables available in the OSHPD data set. As an indicator of socioeconomic status (SES), we analyzed the source of payment for the admission. "High SES" included individuals with private insurance or health maintenance organization coverage, whereas "low SES" consisted of those who are indigent, are self-pay, or have Medicaid or Medicare.
To evaluate the possibility that variation in hospital discharge coding practices over time may have affected our incidence calculations, we analyzed a variety of other discharge diagnoses that are related to birth asphyxia and that could have been chosen instead of birth asphyxia in the coding process. These diagnoses included (1) fetal distress in a liveborn infant, associated with newborn morbidity (ICD-9-CM codes 768.2, 768.3, and 768.4); (2) birth trauma, unspecified (ICD-9-CM code 767.9); (3) subdural and cerebral hemorrhage as a result of birth trauma or of intrapartum anoxia or hypoxia (ICD-9-CM code 767.0); (4) other specified birth trauma, such as encephalopathy as a result of birth injury (ICD-9-CM code 767.8); (5) cerebral irritability, depression, coma, and other abnormal cerebral signs, including central nervous system dysfunction in newborn not otherwise specified (ICD-9-CM codes 779.1 and 779.2); (6) convulsions in newborn (ICD-9-CM code 779.0); (7) unspecified anomaly of nervous system, including congenital encephalopathy (ICD-9-CM code 742.9); and (8) other specified and unspecified conditions originating in the perinatal period, including hypotonia (ICD-9-CM code 779.8 and 779.9). We calculated annual incidence rates for each of these diagnoses in the same manner as described above.
Newborns were placed in 1 of 3 birth weight strata (normal birth weight, low birth weight [LBW], or very low birth weight [VLBW]) on the basis of hospital discharge diagnoses. All infants who receive a diagnosis of prematurity, small for gestational age, or intrauterine growth restriction (IUGR) are assigned an ICD-9-CM code that denotes the infant's birth weight. Using these codes, VLBW infants (<1500 g) were identified as those with 1 of the following discharge ICD-9-CM codes: 764.01 to 764.05, 764.11 to 764.15, 764.21 to 764.25, 764.91 to 764.95, 765.01 to 765.05, and 765.11 to 765.15. LBW infants (1500-1999 g) were identified as those with 1 of the following discharge ICD-9-CM codes: 764.06 to 764.07, 764.16 to 764.17, 764.26 to 764.27, 764.96 to 764.97, 765.06 to 765.07, and 765.16 to 765.17. Infants with normal birth weight were those who did not carry a diagnosis of prematurity, small for gestational age, or IUGR, as well as infants who did carry 1 of these diagnoses but were found to have a birth weight >2000 g on the basis of the following ICD-9-CM discharge codes: 764.08 to 764.09, 764.18 to 764.19, 764.28 to 764.29, 764.98 to 764.99, 765.08 to 765.09, and 765.18 to 765.19.
Birth asphyxia incidence rates stratified by gender, ethnicity, birth weight, and insurance status were compared in univariate analyses by calculating relative risks (RR) and 95% confidence intervals (CIs) using the Cornfield method.17 Multivariate RRs and 95% CIs were calculated by including these variables in a logistic regression model. Case fatality rates, defined as the percentage of infants who had birth asphyxia and died before hospital discharge, were similarly compared in univariate and multivariate analyses. The change in incidence rates and case fatality rates over the 10 years of the study was analyzed using the Cochran-Armitage trend test.18
An analysis of the underlying causes and risk factors for birth asphyxia was beyond the scope of this study. However, in an attempt to characterize the major medical conditions that were associated with the diagnosis of birth asphyxia, we evaluated the presence of congenital anomalies and other perinatal conditions by searching accompanying discharge diagnoses. The OSHPD database lists up to 25 diagnoses for each admission, and we performed additional ICD-9 code searches within our cohort to identify coexisting conditions (see Appendix for list of diagnoses). All statistical analyses were performed with SAS 8.2.18
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Incidence
Of 5 364 663 newborns identified between the years 1991 and 2000 in California, 24 330 received a diagnosis of birth asphyxia, providing an incidence of 4.5 per 1000 live births. Birth asphyxia severity was coded as "mild or moderate" in 65% of affected newborns, whereas 23% were considered "severe" and 12% had an unspecified severity. Compared with whites, blacks were 28% more likely to receive a diagnosis of birth asphyxia after adjusting for the effects of gender, SES, and birth weight stratum (Table 1). Male gender and low SES were also associated with elevated risk for receiving a diagnosis of birth asphyxia.
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Most (89.3%) infants with birth asphyxia were in the normal birth weight stratum (Table 1). However, after adjusting for other factors, LBW and VLBW infants were at significantly higher risk for receiving a diagnosis of birth asphyxia compared with infants who weighed >2000 g (RR: 4.1 and 7.8, respectively). In addition, infants in the VLBW stratum were more likely to receive a diagnosis of severe birth asphyxia than were infants in the normal birth weight stratum (55% vs 21%; P < .0001).
The annual incidence of birth asphyxia diagnosed in the newborn period decreased dramatically by 91% between the years 1991 and 2000, from 14.8 to 1.3 per 1000 live births (P < .0001). Changes in the demographics of the state population could not explain the change in birth asphyxia incidence, as a similar decline was present among infants of all birth weight strata (Fig 1), ethnic groups, and socioeconomic strata (data not shown). The fall in the incidence of mild birth asphyxia (10.6-0.7 per 1000) was similar in magnitude to that observed for severe birth asphyxia (3.7-0.2 per 1000).
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Diagnoses related to birth asphyxia also declined consistently during the study period. For instance, fetal distress decreased exponentially from 38 to 7 per 1000 between the years 1991 and 2000, and hospital diagnoses of birth trauma (0.3-0.1 per 1000), perinatal subdural and cerebral hemorrhage (0.8-0.5 per 1000), cerebral irritability (0.5-0.1 per 1000), and convulsions (1.2-1.1 per 1000) all declined as well. A code for "unspecified conditions originating in the perinatal period" that includes hypotonia (ICD-9-CM codes 779.8 and 779.9) increased slightly from 3.3 to 4.2 per 1000 live births. The diagnosis of "unspecified anomaly of nervous system" (ICD-9-CM code 742.9) that includes congenital encephalopathy fluctuated between 4.8 and 8.8 per 1000 live births and did not show a significant trend across the study years.
For both normal birth weight infants and infants who were born at <2000 g, the risk of birth asphyxia was highest in those with multiple congenital anomalies (Table 2). Other complications associated with an increased risk for birth asphyxia in both birth weight groups include central nervous system anomaly, chromosomal anomaly, breech vaginal delivery, and congenital heart disease. Although the diagnoses of IUGR and small for gestational age both were associated with an increased risk for birth asphyxia in normal birth weight infants, these diagnoses were protective against birth asphyxia in infants who weighed <2000 g.
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The total incidence of these risk factors also declined in our birth cohort. For example, the diagnosis of congenital anomalies declined from 68.0 to 59.7 per 1000 live births between the study years 1991 and 2000. Breech vaginal deliveries also became less common across all birth weight groups during this period. In contrast, IUGR has become increasingly common in all birth weight groups. The diagnosis of IUGR rose slightly from 2.1 to 2.7 per 1000 live births during the study period.
The cesarean section rate in infants who weighed >2000 g followed a U-shaped curve, dipping slightly from 21.7% to 19.8% during the years 1991-1996 but then increasing to 22.5% by 2000. This is consistent with reported national trends in cesarean delivery rate.19 The cesarean section rate for infants who weighed <2000 g climbed consistently throughout the study period from 45% to 55%.
Case Fatality
The case fatality rate in infants who received a diagnosis of birth asphyxia was 4.0% and increased from 2.8% to 4.7% between the years 1991 and 2000. Because 2.5% of newborns with the diagnosis of birth asphyxia were transferred to another hospital for additional care, the case fatality rate may in fact be higher, as those who are transferred are more likely to be severely affected. Infants with severe birth asphyxia had a 24-fold increased risk for dying before discharge compared with infants with mild birth asphyxia. Other univariate predictors of in-hospital death included black ethnicity, low SES, and low birth weight (Table 3). However, after adjusting for these factors in a multivariate model, the only significant predictors of in-hospital death after birth asphyxia were LBW (RR: 4.9; 95% CI: 3.8–6.4) and VLBW (RR: 27.9; 95% CI: 24.1–32.4), when compared with newborns who were born at >2000 g.
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For newborns with birth weight >2000 g, the highest case fatality was seen in conjunction with congenital anomalies, prolapsed cord, other cord abnormalities (excluding nuchal cord), and maternal hemorrhage (Table 4). More than half of all birth asphyxia deaths in infants who weighed >2000 g were associated with 1 of these 4 conditions.
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Cord abnormalities and maternal hemorrhage similarly conferred a high case fatality in infants who weighed <2000 g. In contrast, chorioamnionitis and other maternal infections were associated with a high case fatality only in the lower birth weight group. For infants who weighed <2000 g, the case fatality of birth asphyxia was as high as 48% in the presence of chorioamnionitis. Among infants who died with birth asphyxia, the presence of chorioamnionitis or other maternal infection was noted more frequently in those with birth weight <2000 g than among larger infants (11% vs 3%; P < .0001).
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Although estimates of birth asphyxia incidence vary depending on how the syndrome is diagnosed and how the study population is selected, our incidence of 4.5 per 1000 live births falls within the previously reported range of 2 to 9 per 1000 live births.5–13 We found that birth asphyxia has been diagnosed with decreasing frequency over the past decade in California. Similarly, the incidence of hypoxic-ischemic encephalopathy also declined by 75% between the late 1970s and mid-1990s in Great Britain.10,20
Our understanding of birth asphyxia is hampered by vague terminology. The term "birth asphyxia" is imprecise and potentially misleading, as it implies the lack of oxygen and blood supply to the brain and other organs, yet the clinical signs and symptoms used to define birth asphyxia, such as low Apgar scores, encephalopathy, and low cord pH,4,10,11,21,22 may result from a variety of underlying causes, including infectious and metabolic disorders.13,22–25 Therefore, "neonatal encephalopathy" has emerged as the preferred terminology in the research literature, as it does not imply a specific underlying pathophysiology.13,26,27
Because the clinical syndrome of birth asphyxia is not specific for hypoxic-ischemic brain injury or any other single cause, some have recommended that the term be dropped altogether.22,23 However, birth asphyxia is still commonly diagnosed in clinical practice, and medical malpractice lawsuits brought against obstetricians often center around this diagnosis. In addition, birth asphyxia continues to be assigned its own code in the ICD-9 and ICD-10 manuals, whereas neonatal encephalopathy does not exist as a distinct diagnostic category in the ICD.15
It is possible that a decreased use of the term "birth asphyxia," driven in part by the medicolegal crisis in the United States, is responsible for the apparent decline in incidence within our population. The dramatic decline in "fetal distress" diagnoses during the study period may also reflect changing diagnostic practices in an increasingly litigious environment. However, when we investigated other diagnoses that might be preferentially chosen instead of birth asphyxia to describe a neurologically impaired newborn, we found that these, too, have decreased dramatically over the same period. Although a single diagnostic category (ICD-9 779.8 and 779.9) representing nonspecific complications in the perinatal period exhibited an increased incidence during the study period, the small magnitude of this increase could not account for the marked decline in incidence of birth asphyxia.
Another possible explanation for the declining incidence is that infants with low Apgar scores may have been previously considered "asphyxiated," even in the setting of a normal neonatal course. That is, if otherwise healthy infants with transient low Apgar scores at birth are no longer labeled as having birth asphyxia, then this would also result in an overall decrease in the diagnostic rate. However, one then would expect the fall in mild birth asphyxia to be more marked than that of severe birth asphyxia. Instead, we found that diagnoses of both mild and severe birth asphyxia decreased by >90% during our study period. Therefore, although a change in practice regarding the use of the term "birth asphyxia" most likely contributed in some degree to the observed decline in incidence, it is unlikely to account entirely for our findings.
Whether improvements in antepartum and intrapartum medical management, demographic changes, or other factors may also have contributed to the decline in birth asphyxia is unclear. Infant mortality declined throughout the 1990s both in California and in the United States.16,19 Factors associated with lower rates of infant mortality and morbidity, such as enhanced prenatal diagnosis and pregnancy termination for congenital anomalies,28–30 increased access to neonatal intensive care,31 and planned cesarean section for breech presentation,32 may also have an impact on the incidence of birth asphyxia. During the study period, there was indeed a decline in the incidence of congenital anomalies and breech vaginal deliveries, although these changes could account for only a small proportion of the decline in birth asphyxia. Whether changes in obstetric practice such as increased antibiotic use for group B streptococcus prophylaxis33 and increased treatment with prenatal steroids34 may also have contributed to the declining incidence of birth asphyxia is unknown.
The overall mortality from birth asphyxia has been regarded as a reflection of the quality of intrapartum care,1,14,35,36 yet we and others have found that antenatal factors, including congenital anomalies and IUGR, contribute to the risk for birth asphyxia.13 IUGR has been linked to a number of perinatal complications, including fetal death, perinatal mortality, neonatal encephalopathy, and low Apgar scores.11,13,37,38 Our finding that IUGR was associated with an increased risk for birth asphyxia only in infants who weighed >2000 g, whereas IUGR had a protective effect in lower birth weight infants, is consistent with previous reports of adverse pregnancy outcomes that are seen only in infants who have IUGR and are born at or near term.39
We found that lower SES is associated with an increased incidence of birth asphyxia. A population-based case-control study of neonatal encephalopathy similarly reported that lack of private health insurance and maternal unemployment are significant risk factors.13 Black ethnicity was associated with a 28% increased risk for birth asphyxia in our population after adjusting for potential confounders such as SES and birth weight stratum. This association between birth asphyxia and black ethnicity has not been previously reported to our knowledge. Whether the ethnic differences are attributable to genetic, environmental, or other factors deserves additional investigation.
Our study is based on administrative data and thus is subject to a number of limitations. We were unable to determine the criteria used by treating physicians to make specific diagnoses such as birth asphyxia, and we relied on hospital discharge diagnoses that may not have been recorded accurately. Although we did not find evidence that incidence rates for birth asphyxia declined because of increased use of related codes, it is possible that other systematic changes in coding practice contributed to the apparent decline in birth asphyxia. Given that maternal discharge records were not available to us, our data on maternal complications could not be ascertained in healthy infants without birth asphyxia and were likely to be incomplete in infants with birth asphyxia. Neonatal conditions such as congenital and chromosomal anomalies may also be underascertained in infants without a diagnosis of birth asphyxia. These limitations are offset by several study strengths, including the population-based setting, the large numbers and ethnic diversity, and the ability to analyze temporal trends.
The diagnosis of birth asphyxia, commonly made in the setting of low Apgar scores, is a well-known risk factor for neurodevelopmental disability such as cerebral palsy,25,40,41 yet birth asphyxia is diagnosed in only 8% to 20% of cerebral palsy cases,4,42–44 and a recent review concluded that known causes of cerebral palsy, such as birth asphyxia, account for only a minority of cases.45 Although our study was not designed to track cerebral palsy prevalence, numerous studies suggest that the prevalence of cerebral palsy has remained essentially unchanged for 30 years.46,47 Unless the observed decrease in birth asphyxia diagnoses was accompanied by a dramatic decrease in cerebral palsy over the course of this study, our findings would support the notion that the diagnosis of birth asphyxia, as used in medical practice during the 1990s, did not contribute to the majority of cerebral palsy cases.
Among infants who received a diagnosis of birth asphyxia in our study, a portion will have sustained a true hypoxic-ischemic brain injury. More studies are needed to clarify the exact role of hypoxic-ischemic brain injury in causing cerebral palsy and other long-term neurologic disabilities. However, the concept of birth asphyxia is problematic and subject to conflicting and potentially misleading interpretations that lead only to additional confusion among patients, clinicians, and researchers. Progress in our understanding of birth-related brain injury can be made only if we abandon the term "birth asphyxia."
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APPENDIX |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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The major congenital anomalies in our data set potentially related to the birth asphyxia were grouped into the following categories: neural tube defects (ICD-9 code 740.0–741.9), brain anomalies (742.0742.2–742.4745.9), microcephaly (742.1), major congenital heart disease (745.0–745.3, 745.6, 746.0–746.9, 747.1, 747.3, and 747.41), cerebrovascular anomaly (747.81), respiratory system anomaly (748.3–748.6), gastrointestinal anomaly (750.3, 751.0–751.5, 751.8, and 751.9), renal/bladder anomaly (753.0–753.9), craniosynostosis (756.0), abdominal wall defect (756.7), Down syndrome (758.0), other chromosomal anomaly (758.1–758.9), and multiple congenital anomalies unspecified (759.7). Patients with a discharge diagnosis lying between 740.0 and 759.9 (all congenital anomalies) in any position were identified as having a major or minor congenital anomaly.
Obstetric complications were grouped as follows: maternal hypertensive disorders (760.0); maternal infection (760.2 and 762.7); maternal toxin, including alcohol, cocaine, and narcotics (760.71–760.73, 760.75, and 779.5); premature rupture of membranes (761.1); maternal or fetal hemorrhage (762.1 and 772.0); prolapsed cord (762.4); other cord compression, including nuchal cord (762.5); other cord abnormalities (762.6); and breech vaginal delivery (763.0). Finally, infant characteristics included small for gestational age (764.0 and 764.1), intrauterine growth retardation (764.9), large for gestational age (766.0 and 766.1), and postterm (766.2).
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ACKNOWLEDGMENTS |
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Drs Wu and Fullerton were supported in part by the Neurological Sciences Academic Development Award K12 NSO1692-05.
We thank Karin Nelson, Donna Ferriero, Tom Newman, and Steve Miller for careful reviews of the manuscript.
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FOOTNOTES |
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Accepted May 26, 2004.
Address correspondence to Yvonne W. Wu, MD, MPH, Department of Child Neurology, Box 0136, University of California, San Francisco, 500 Parnassus Ave, Room 411, San Francisco, CA 94143-0136. E-mail: wuy{at}neuropeds.ucsf.edu
No conflict of interest declared.
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