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Obstetrics & Gynecology 2001;97:961-964
© 2001 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Obstetric Antecedents to Apparent Stillbirth (Apgar Score Zero at 1 Minute Only)

BASSAM HADDAD, MD, BRIAN M. MERCER, MD, JEFFREY C. LIVINGSTON, MD and BAHA M. SIBAI, MD

From the Department of Obstetrics and Gynecology, University of Tennessee, Memphis, Tennessee; and the Department of Obstetrics and Gynecology, University of Cincinnati, Cincinnati, Ohio.

Address reprint requests to: Baha M. Sibai, MD Department of Obstetrics and Gynecology University of Cincinnati Medical Center 231 Albert Sabin Way Cincinnati, OH 45267-0526


   Abstract
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Abstract
Materials and Methods
 Results
 Discussion
 References
 
Objective: To identify antecedent risk factors for the delivery of an infant with an Apgar score of 0 at 1 minute who is subsequently successfully resuscitated.

Methods: Infants born between January 1986 and February 1999 with 1-minute Apgar score of 0 followed by 5-minute Apgar score above 0 were studied. Each eligible infant was randomly matched with two control infants, born in the same year, with 1-minute Apgar score greater than 0. Hospital records of their mothers were reviewed. The variables were compared between the groups by univariate analysis. Those factors demonstrating significant differences were then analyzed by logistic regression. P < .05 was considered statistically significant.

Results: Seventy-four of 81,603 infants (0.9:1000 births) born with an Apgar score of 0 at 1 minute only were compared with 148 control babies. Univariate analysis revealed significant differences between study and control group regarding: gestational age, abruptio placentae, preterm premature rupture of membranes, chorioamnionitis, preeclampsia, small-for-gestational age, male gender, bradycardia, and abnormal fetal heart rate (FHR) other than bradycardia, respectively. Logistic regression of these factors found gestational age, bradycardia, and abnormal FHR to be independent risk factors for the delivery of an apparent stillborn infant. After exclusion of FHR criteria, logistic regression found gestational age (odds ratio [OR] 0.8 per week), male gender (OR 2.5), preeclampsia (OR 3.9), and abruptio placentae (OR 13.6) to be independent risk factors for the delivery of an apparent stillborn infant.

Conclusion: Preterm birth, male gender, preeclampsia, and abruptio placentae are independently associated with an increased risk of apparent stillbirth.

Despite advances in neonatal management, apparently stillborn infants (ie, born with an Apgar score of 0 at 1 minute) are at high risk for significant morbidity and subsequent mortality.1–7 The frequency of apparent stillbirth ranges from 0.4 per 1000 to 0.8 per 1000 births.4,5,7 In recent studies, subsequent neonatal mortality rates ranged from 28% to 57%, with 14% to 60% of survivors having neurologic disabilities.1,2,4–7 Antecedent obstetric factors leading to the delivery of an apparently stillborn infant have been, however, poorly evaluated.

In view of the poor neonatal outcome associated with apparent stillbirth, we performed a case-control study to evaluate antecedent obstetric risk factors for this morbid condition.


   Materials and Methods
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Abstract
 Materials and Methods
Results
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We identified from our computerized perinatal database all infants with Apgar score of 0 at 1 minute only, who were subsequently successfully resuscitated at the Regional Medical Center of the University of Tennessee, Memphis, and who delivered between January 1986 to February 1999. Two matching control infants, born during the same year, and with a 1-minute Apgar score greater than 0 were identified using random number tables. Review of their maternal medical records was performed. It should be noted that the hospital provides care for primarily indigent, high- and low-risk patients. Moreover, we do not perform termination for fetal anomalies after 20 weeks’ gestation in our institution, and therefore these patients were not excluded from analysis. Fetal heart rate (FHR) monitoring was read and classified by the obstetric attending physician. Finally, the decision of resuscitation and the determination of Apgar score were done by the attending pediatrician.

For each woman, data were collected concerning age, race, parity, illicit drug use, weight, medical complications (including a history of chronic hypertension, diabetes, or severe asthma), obstetric and labor complications, and estimated gestational age at delivery. Gestational age was determined by best obstetric estimate using the last menstrual period and sonographic findings, where available. For each infant, the following data were collected: birth weight, Apgar score at 1 and 5 minutes, gender, umbilical artery acid-base status at delivery (pH, pCO2, pO2, and base deficit) where available, and malformations. Small-for-gestational age was defined as birth weight below the 10th percentile for gestational age.8

Results are presented as mean ± standard deviation (SD) or frequency (%). Categorical variables were analyzed by the {chi}2 test, with Yates correction when appropriate. Continuous variables were compared with Student t test. Subsequent to the univariate analysis, multiple logistic regression analysis was performed to identify relationships between one or more independent variables and 1-minute Apgar score. All statistical analyses were performed with Statview 4.5 (SAS Institute Inc., Cary, NC). A P value <.05 was considered to be statistically significant. The study was approved by the Institutional Review Board of the University of Tennessee, Memphis.


   Results
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Abstract
 Materials and Methods
 Results
Discussion
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A total of 74 of 81,603 infants (over 22 weeks and/or weighing over 500 g) met our inclusion criteria (0.9 per 1000 births). These infants were compared with 148 control infants. Maternal characteristics of cases and controls are shown in Table 1Go. Except for maternal age, no statistical differences were found between the two groups. Although statistically significant, the 2-year difference in maternal ages is not clinically meaningful. Four of the 74 babies born with 1-minute Apgar score of 0 (5%) were delivered from twin pregnancies. One of their siblings was stillborn. Twin pregnancy was not more frequent in the apparent stillbirth group (5% compared with 3%, P = .55). The findings in the control group are similar to those of our general population identified in previous studies.9


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  		Table 1. Maternal Demographic Findings and Clinical Characteristics
 
Newborn characteristics are shown in Table 2Go. Four infants born with 1-minute Apgar score of 0 had malformations (5%) including gastroschisis (one), nonimmune hydrops (one), immune hydrops (one), and omphalocele associated to polydactily (one). Of the four, three had an associated obstetric complication before delivery: bradycardia (two) and abruptio placentae (one). Two infants in the control group (1%) had isolated malformations (hydrocephalus and encephalocele). Birth weight was statistically lower in the apparent stillbirth group (P < .001). Only one of the babies born with 1-minute Apgar score of 0 was not admitted to a neonatal intensive care unit because he quickly recovered and had a 5-minute Apgar score of 7.


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  		Table 2. Neonatal Findings in Infants With Apparent Stillbirth and Controls
 
Obstetric course is evaluated in Table 3Go. In no case was apparent stillbirth preceded by asystole on antecedent FHR testing. Univariate analysis revealed a significant association between the delivery of an apparently stillborn infant and decreasing gestational age at delivery, abruptio placentae, bradycardia (FHR baseline below 110 bpm for at least 10 minutes), abnormal FHR other than bradycardia, chorioamnionitis, preterm premature rupture of membranes (PROM), vaginal bleeding, preeclampsia, and nonvertex presentation at delivery. To evaluate independent associations, significant variables from the univariate analysis were entered in multiple logistic regression analysis. Tables 4Go and 5Go demonstrate the final logistic regression analysis, including only variables found significant on logistic regression. These final analyses revealed gestational age, bradycardia, and abnormal FHR patterns other than bradycardia to be independently associated with increased risk for apparent stillbirth (Table 4Go). After exclusion of FHR patterns from the logistic regression model, the analysis showed that gestational age, male gender, preeclampsia, and abruptio placentae were independent risk factors associated with increased risk for apparent stillbirth (Table 5Go).


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  		Table 3. Obstetric Course Leading to Apparent Stillbirth
 

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  		Table 4. Adjusted Odds Ratios of Variables Significantly Associated With Apparent Stillbirth by Multiple Logistic Regression (n = 210)
 

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  		Table 5. Adjusted Odds Ratios of Variables Significantly Associated With Apparent Stillbirth by Multiple Logistic Regression After Exclusion of Fetal Heart Rate Patterns (n = 15)
 

   Discussion
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Abstract
 Materials and Methods
 Results
 Discussion
References
 
Over the last two decades, few studies have been published regarding the characteristics of apparently stillborn infants. Published studies have focused primarily on the survival and long-term outcome of these infants.1–7 Reported survival without neurologic disabilities ranged from 27% to 40%.1,2,4–7 Antecedent obstetric factors leading to the delivery of an apparently stillborn infant have been either not specified or poorly evaluated in these studies. We therefore designed this case-control study to evaluate antecedent obstetric risk factors for the delivery of an infant with an Apgar score of 0 at 1 minute only and who was subsequently successfully resuscitated. The controls were selected by random process. We purposely did not match for gestational age to evaluate this factor. Moreover, we could have compared the risk factors involved in the cases with those of stillbirths who were not able to be resuscitated. In this way, the study would have led to a conclusion emphasizing the differences, if any, in the risk factors of stillbirths and infants who were successfully resuscitated. This is certainly of interest; however, it does not clarify risk factors of apparent stillbirths.

Univariate analysis revealed an increased risk of apparent stillbirth in pregnancies complicated by at least one of the following: prematurity (less than 32 weeks), abruptio placentae, bradycardia, abnormal FHR other than bradycardia, chorioamnionitis, preterm PROM, vaginal bleeding, preeclampsia, and nonvertex presentation at delivery. In addition, the rates of abruptio placentae, vaginal bleeding, abnormal FHR, and preeclampsia are in agreement with those reported by two descriptive studies.5,7 Our finding, that male infants were more commonly affected (70%), is also in agreement with that of Yeo and Tudehope (69%),5 and in disagreement with that of Casalaz et al (34%).7 We found a trend towards more frequent placenta previa and cord prolapse in the apparent stillbirth group compared with the controls. We did not find apparent stillbirth to be preceded by asystole, suggesting that this diagnosis precludes adequate time for subsequent delivery and successful resuscitation if initial attempts fail.

Several of the variables associated with the delivery of an apparent stillborn infant might be related through their association with other factors. Multivariable analysis showed that increased gestational age is strongly and negatively associated with apparent stillbirth, independent of causes that might lead to premature delivery such as preterm PROM, chorioamnionitis, or preeclampsia. Previous studies have shown that Apgar score less than or equal to 3 is common in preterm infants.10 In addition, Catlin et al found that low Apgar scores may reflect developmental immaturity of muscle tone, respiratory effort, and reflex irritability related to gestational age.11 However, in this latter study, none of the 73 infants studied had an initial Apgar score of 0. Gardner et al reported that nonvertex presentation was a risk factor for having a low Apgar score at 1 minute.12 The number of infants having an Apgar score of 0 is not, however, specified in that study. In our study, nonvertex presentation was associated with a 1-minute Apgar score of 0 on univariate analysis but not in the regression analysis. This finding probably relates to the increased rate of nonvertex presentation in preterm deliveries.

Abnormal FHR pattern was observed in 74% of the apparently stillborn infants. Although this finding is not surprising, none of these fetuses had documented asystole before delivery. Thus, abnormal FHR patterns themselves should be considered risk factors. Multivariable analysis revealed that an abnormal FHR pattern was the most highly correlated independent risk factor for delivery of an infant with an Apgar score of 0. Conversely, it was somewhat surprising that causes of stillbirth such as abruptio placentae, preeclampsia, or fetal growth restriction13 were found not to be independent risk factors for apparent stillbirth in multivariable analysis. This finding likely relates to the association between these factors and preterm birth, with abnormal FHR patterns as a final common pathway. This suggestion was confirmed by our last multivariable analysis where (after exclusion of FHR patterns variables from the logistic regression model [Table 5Go]) preeclampsia and abruptio placentae were independently found to be risk factors for apparent stillbirth.


   Footnotes
 
PII S0029-7844(01)01352-7

Received September 11, 2000. Received in revised form January 4, 2001. Accepted January 31, 2001.


   References
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Abstract
 Materials and Methods
 Results
 Discussion
 References
 
1. Steiner S, Neligan G. Perinatal cardiac arrest. Quality of survivor. Arch Dis Child 1975;50:696–702.[Abstract]

2. Scott H. Outcome of very severe birth asphyxia. Arch Dis Child 1976;51:712–6.[Abstract]

3. Thomson AJ, Searle M, Russell G. Quality of survival after severe birth asphyxia. Arch Dis Child 1977;52:620–6.[Abstract]

4. Jain L, Ferre C, Vidyasagar D, Nath S, Sheftel D. Cardiopulmonary resuscitation of apparently stillborn infants: Survival and long-term outcome. J Pediatr 1991;118:778–82.[Medline]

5. Yeo CL, Tudehope DI. Outcome of resuscitated apparently stillborn infants: A ten year review. J Pediatr Child Health 1994;30: 129–33.

6. Perlman JM, Risser R. Cardiopulmonary resuscitation in the delivery room. Arch Pediatr Adolesc Med 1995;149:20–5.[Abstract]

7. Casalaz DM, Marlow N, Speidel BD. Outcome of resuscitation following unexpected apparent stillbirth. Arch Dis Child Fetal Neonatal Ed 1998;78:F112–5.[Abstract/Free Full Text]

8. Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996;87: 163–8.[Abstract]

9. Mercer BM, McNanley T, O’Brien JM, Randal L, Sibai BM. Early versus late amniotomy for labor induction: A randomized trial. Am J Obstet Gynecol 1995;173:1321–5.[Medline]

10. Goldenberg RL, Huddleston JF, Nelson KG. Apgar scores and umbilical arterial pH in preterm newborn infants. Am J Obstet Gynecol 1984;149:651–4.[Medline]

11. Catlin EA, Carpenter MW, Brann BS, Mayfield SR, Shaul PW, Goldstein M, et al. The Apgar score revisited: Influence of gestational age. J Pediatr 1986;109:865–8.[Medline]

12. Gardner MO, Goldenberg RL, Gaudier FL, Dubard MB, Nelson KG, Hauth JC. Predicting low Apgar scores of infants weighing less than 1000 grams: The effect of corticosteroids. Obstet Gynecol 1995;85:170–4.[Abstract]

13. Incerpi MH, Miller DA, Samadi R, Settlage RH, Goodwin TM. Stillbirth evaluation: What tests are needed? Am J Obstet Gynecol 1998;178:1121–5.[Medline]




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