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Preterm Premature Rupture of Membranes, Intrauterine Infection, and Oligohydramnios

Risk Factors for Placental Abruption

Cande V. Ananth, PhD, MPH^*, Yinka Oyelese, MD, Neela Srinivas, MBBS, MPH^*, Lami Yeo, MD and Anthony M. Vintzileos, MD

From the *Section of Epidemiology and Biostatistics and Division of Maternal-Fetal Medicine, Department of Obstetrics, Gynecology, and Reproductive Sciences, Robert Wood Johnson Medical School/Robert Wood Johnson University Hospital, University of Medicine and Dentistry of New Jersey, New Brunswick, New Jersey.

	ABSTRACT

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OBJECTIVE: To examine whether preterm premature rupture of membranes (PROM), intrauterine infection, and oligohydramnios are risk factors for placental abruption.

METHODS: Data for this retrospective cohort study were derived from the 1988 National Maternal and Infant Health Survey (N = 11,777). Association between abruption and these clinical risk factors was expressed as relative risk (RR) and 95% confidence interval (CI), with multivariate adjustment for potential confounders.

RESULTS: The overall incidence of abruption was 0.87%. The risk of abruption was 3.58-fold higher (95% CI 1.74–7.39) among women with preterm PROM (2.29%) compared with women with intact membranes (0.86%). The rates of abruption among women with and without intrauterine infection were 4.81% and 0.83%, respectively (RR 9.71, 95% CI 3.23–29.17). However, oligohydramnios was not associated with abruption (1.46% compared with 0.87%; RR 2.09, 95% CI 0.92–5.31). Compared with women with intact membranes, the RR for abruption among preterm PROM and whose membranes were ruptured for 24–47 hours and 48 hours or more before delivery, respectively, were 2.37 (95% CI 0.99–9.09), and 9.87 (95% CI 3.57–27.82). When preterm PROM was accompanied by intrauterine infections, the RR for abruption was 9.03 (95% CI 2.80–29.15) compared with women with intact membranes and no infections. Similarly, preterm PROM accompanied by oligohydramnios conferred over a 7.17-fold risk (95% CI 1.35–38.10) for abruption compared with women with neither of these 2 conditions.

CONCLUSION: Women presenting with preterm PROM are at increased risk of developing abruption, with the risk being higher either in the presence of intrauterine infections or oligohydramnios. Physicians managing patients with preterm PROM should be aware that these patients are at increased risk of developing abruption after 24 hours following preterm PROM.

LEVEL OF EVIDENCE: II-2

The role of bacterial colonization and amniotic fluid infection in the pathophysiology of placental abruption is also poorly understood. Most notably, acute chorioamnionitis, an infection caused when pathogens from the vagina and cervix gain access to the placental-fetal membranes, is suspected of preceding membrane rupture.¹³ Some earlier studies have suggested that intrauterine infection, especially chorioamnionitis, weakens the membranes, leading to premature rupture,^2,14 whereas others believe that the ascending infection is the consequence of preterm PROM.⁶ In addition, there is evidence that oligohydramnios in preterm PROM increases the risk of abruption.⁵ Although the sequence of events linking preterm PROM, intrauterine infections, and oligohydramnios to the risk of abruption is, at best, speculative, we hypothesized that women with both preterm PROM and with a diagnosis of intrauterine infections or oligohydramnios would be at greater risk of developing abruption when compared with women with any 1 of these complications alone.

The objectives of our study, therefore, were to assess whether preterm PROM, intrauterine infections, and oligohydramnios are risk factors for placental abruption. Additionally we evaluated the risk of abruption in relation to the latency between membrane rupture and delivery among women with preterm PROM.

	MATERIALS AND METHODS

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The U.S. 1988 National Maternal and Infant Health Survey (NMIHS) data¹⁵ were used to examine the risk of placental abruption in relation to preterm PROM. The NMIHS study was conducted by the National Center for Health Statistics of the Centers for Disease Control and Prevention to examine factors related to pregnancy outcomes in the United States. The study involved a survey component of a nationally representative sample of women who delivered a live birth (N = 13,417), late (28 weeks or more) fetal death (n = 4,472), and women whose liveborn died within the first year (n = 8,166). The NMIHS intentionally over-sampled very low (less than 1,500 g) and moderately low (1,500–2,499 g) birth weight infants, as well as black women with fetal or infant death, to increase reliability and obtain sufficient number of births resulting from high-risk pregnancies. The final data from the NMIHS survey contained information from vital records, a maternal and hospital provider interview, as well as a prenatal care provider questionnaire.

Detailed description of the NMIHS study has been previously published.¹⁵ Briefly, survey respondents included 9,953 women who had a live birth (74%), 3,309 women who had a fetal death (69%), and 5,322 women who had an infant death (65%). It was later determined by the National Center for Health Statistics that women who were white, married, and had at least a high school education were more likely to have responded to the questionnaire. Accordingly, a sample-weighting adjustment was added to the data files as part of the final sampling weight to correct for nonresponders. The survey also contained extensive information from the prenatal care provider(s) as well as hospital delivery questionnaires that were then linked to the index pregnancy of the women in the NMIHS sample.

We restricted our study to women who delivered between 20 weeks and 42 weeks gestation, and for whom prenatal and medical care provider information was available in the survey. Placental abruption was defined as the complete or partial separation of a normally implanted placenta before delivery, usually accompanied by abdominal pain and vaginal bleeding. Preterm PROM cases were defined as those pregnancies with a diagnosis of spontaneous rupture of the chorioamniotic membranes before labor and delivery before 37 completed weeks of gestation. This diagnosis was considered regardless of the presence or absence of chorioamnionitis. Calculation of gestational age was based on menstrual dating for most pregnancies. A clinical diagnosis of intrauterine infection was considered in the presence of fever (100.8°C) in labor accompanied by signs or symptoms of uterine tenderness, foul smelling discharge or positive amniotic fluid cultures from an amniocentesis by the attending physician, or when available, based on histopathologic examination of the placenta, cord, or membranes. However, the exact type of the intrauterine infection was not recorded, nor was an indication of whether the diagnosis was clinical or a histologic diagnosis. Oligohydramnios was considered if there was evidence of reduced amniotic fluid based on an ultrasound assessment, or a vertical deep pocket less than 2 cm. Latency between membrane rupture and delivery was calculated by subtracting the time of membrane rupture from the time of delivery. The latency was categorized as less than 12 hours, 12–23 hours, 24–47 hours, and 48 hours or more. The times of membrane rupture and delivery were abstracted from the medical charts. All conditions (abruption, intrauterine infections, and oligohydramnios) were based on physician diagnosis and were abstracted from medical care provider records. These conditions were recorded in the final NMIHS database based on International Classification of Diseases, 9th Revision, Clinical Modification coding.

The incidence of placental abruption was compared between pregnancies with and without preterm PROM. Estimates of crude relative risk (RR) with 95% confidence intervals were computed as the measure of effect. Adjusted odds ratios were derived through the fit of logistic regression models as estimates of adjusted RR. Effect modification of the association between abruption and preterm PROM was assessed by comparing the association among subgroups defined by the presence or absence of intrauterine infections and oligohydramnios. The presence of statistically significant effect modification was evaluated by the Breslow–Day test of homogeneity of effect measure.¹⁶

Potential confounders considered for adjustment included maternal age, parity (nulliparous, primiparous, and multiparous), cigarette smoking, alcohol, cocaine, and marijuana use (yes or no), marital status (single or married), chronic hypertension, mild and severe preeclampsia, and urinary tract infection. Covariates were included in the final model for adjustment if their presence in the logistic regression model altered the unadjusted RR by at least 10%. Because maternal age demonstrated a nonlinear pattern with the risk of abruption (results not shown), we spline transformed¹⁷ maternal age. This approach allows for the flexible examination of the relationship between a continuous predictor and the outcome, and does not impose any restriction on the shape of the distribution. However, preliminary analysis did not reveal any dose-response trend between the number of cigarettes smoked and the risk of abruption (results not shown). Hence, we analyzed the cigarette smoking as an indicator variable (smoker or nonsmoker).

Logistic regression models were fit to generate adjusted odds ratios as estimates of RR, with appropriate 95% confidence intervals (CI). We also calculated etiologic fractions using the relation p(RR – 1)/(1 + p[RR – 1]), where "p" denotes the proportion of women with abruption without the risk factor (ie, intact membranes). The etiologic fraction is interpreted as the proportion of women who developed abruption as a result of the risk factor. Because patients in the NMIHS study were recruited based on a complex sampling strategy, all statistical analyses were performed using the SAS-callable (8.2; SAS Institute, Inc., Cary, NC) SUDAAN software (8.0; Research Triangle Institute, Cary, NC). The study received ethics approval of the Institutional Review Board of UMDNJ-Robert Wood Johnson Medical School, New Brunswick, New Jersey.

	RESULTS

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The weighted incidence of placental abruption in this sample was 0.87% (n = 441). Distribution of maternal characteristics of women with abruption is shown in Table 1. Women with abruption tended to be between 20 years and 34 years of age, although increasing parity was associated with an increasing risk (Table 1). The risk of abruption was higher among smokers (1.19%), women with chronic hypertension (2.67%), preeclampsia (1.03%), and gestational diabetes (2.70%), although none of these differences reached statistical significance.

The rate of placental abruption among women with preterm PROM was 2.29%, compared with a rate of 0.86% among women with intact membranes (Table 2). After adjustment for confounders, the RR of abruption in relation to preterm PROM was 3.58 (95% CI 1.74–7.39). Placental abruption was also significantly increased among women with a diagnosis of intrauterine infection (4.81%), compared with women without a diagnosis of infection (0.83%), resulting in an adjusted RR of 9.71 (95% CI 3.23–29.17). Further, an analysis of etiologic fractions shows that 6.7% of all abruptions are associated with intrauterine infections. Although the incidence of abruption was greater among women with oligohydramnios (1.46%) compared with those without this condition (0.87%), the association did not reach statistical significance (RR 2.09, 95% CI 0.92–5.31).

We examined the risk of abruption in relation to increasing latency between membrane rupture and delivery among women with preterm PROM (Fig. 1). Among women with a latency of less than 12 hours, the RR for abruption was 0.10 (95% CI 0.02–0.57), with a progressively increasing risk with increasing latency. The RR for abruption among women with preterm PROM and who delivered between 24 hours and 47 hours after membrane rupture was 2.37 (95% CI 0.99–9.09). This risk increased steadily with increasing latency between rupture of membranes and delivery, reaching almost 10 (RR 9.87, 95% CI 3.57–27.82) for women who delivered at or beyond 48 hours.

View larger version (14K): [in this window] [in a new window]   Fig. 1. Risk of placental abruption in relation to latency between the time of membrane rupture and delivery among women with preterm premature rupture of membranes. Data from U.S. National Maternal and Infant Health Survey, 1988. Ananth. Clinical Risk Factors for Placental Abruption. Obstet Gynecol 2004.

We assessed the combined effect of preterm PROM with intrauterine infections or oligohydramnios on the risk of placental abruption (Table 3). The excess risk of abruption associated with a combined influence of preterm PROM and oligohydramnios was greater than the sum of the excess risk for preterm PROM and oligohydramnios considered independently. This implies that preterm PROM and oligohydramnios have a strong interaction upon the occurrence of abruption. The excess risk of abruption for women with preterm PROM alone was 2.24 (ie, 3.24 – 1.00) and for women with oligohydramnios alone was 1.00 (ie, 2.00 – 1.00); for women with both preterm PROM and the presence of oligohydramnios, the excess risk was 6.17 (ie, 7.17 – 1.00), compared with an expected excess risk of 3.24 (ie, 2.24 + 1.00), had the effects of preterm PROM and oligohydramnios been completely independent (P < .01). Furthermore, the etiologic fraction for abruption based on the combined effects of preterm PROM and intrauterine infections was 6.2%, indicating that up to 6.2% of abruptions are potentially preventable if both preterm PROM and intrauterine infections are prevented. Similarly, the excess risk for the combined influence of preterm PROM and intrauterine infections was 8.03 (ie, 9.03 – 1.00) compared with an expected excess risk of 7.48 (ie, 2.17 + 5.31). However, the interaction between preterm PROM and intrauterine infections on the risk of abruption was not statistically significant (P = .754).

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Although placental abruption has been studied extensively,^18–25 its cause remains largely speculative. Few studies have attempted to evaluate the effect of clinical risk factors, especially preterm PROM, intrauterine infection, and oligohydramnios, on the risk of abruption.^4,5,10,11,26 This large, retrospective cohort study corroborates the earlier findings of a strong association between preterm PROM and abruption and adds additional insight into the role of intrauterine infection and oligohydramnios in the pathogenesis of abruption. Notable findings from our study include 1) preterm PROM and intrauterine infection are strong risk factors for abruption; 2) oligohydramnios in the presence of preterm PROM increases the risk of placental abruption; and 3) women with preterm PROM managed expectantly are at increased risk of developing abruption if the latency between the time of membrane rupture and delivery exceeds 24 hours.

Several plausible biologic mechanisms have been suggested regarding the relationship between preterm PROM and abruption. Vintzileos et al⁵ speculated that maternal or fetal infection did not seem to be implicated in the mechanism by which preterm PROM predisposes to the development of abruption. This finding was supported by our data, because we observed preterm PROM and intrauterine infections to be independent risk factors for abruption (Table 2). On the other hand, Nelson et al¹¹ speculated that an acute reduction in the uterine volume and intrauterine surface area as a consequence of (preterm) PROM could ultimately lead to a disruption of the site of placental attachment in the decidual spongiosa layer, thereby predisposing to abruption.

Prior studies on preterm PROM and placental abruption excluded those with preterm PROM and patients who went into labor or delivered within 24 hours after membrane rupture.^4,5,11 It was concluded, after this exclusion, that abruptions that developed after 24 hours of ruptured membranes could be directly attributable to preterm PROM. In our study, we did not restrict our analysis only to cases delivered with preterm PROM and delivered at least 24 hours later for of the following reasons: First, regardless of any latency time between membrane rupture and delivery, preterm PROM has been established as a strong risk factor for abruption.^4,5,9,11 Hence, with expectant management of patients presenting with preterm PROM,^6–8 the decision of allowing the pregnancy to continue or to undergo induction should depend on the gestational age at which the patient ruptured membranes. Second, it is often very difficult to assess the timing of spontaneous onset of labor accurately, thereby introducing bias in the analysis from previous studies involving varying latency periods. Third, we reanalyzed the data with preterm PROM defined with a minimum latency of 24 hours. The results indicated stronger patterns of association between preterm PROM and abruption with increasing latency between preterm PROM and delivery (Fig. 1). In fact, our results clearly indicate that in the presence of preterm PROM, waiting more than 24 hours to deliver confers a substantially increased risk of abruption.

Although previous studies have observed an association between intrauterine infection, especially chorioamnionitis, and abruption,^26,27 the influence of chorioamnionitis and preterm PROM together on the risk of abruption has not been properly examined. Using data from the National Hospital Discharge Survey, Saftlas et al⁹ observed that chorioamnionitis increased a woman's risk of abruption 2.5-fold (95% CI 1.6–3.9). Similarly, a recent case-control study²⁶ concluded that chorioamnionitis was more than 7.1 (95% CI 1.8–28.7) times more likely to occur in patients with abruption than among women without abruption. However, neither of these 2 studies^6,26 differentiated between chorioamnionitis with or without intact membranes. Furthermore, the latter study was restricted to all pregnancies resulting in preterm deliveries. Our analysis indicates that women with both intrauterine infection and preterm PROM were almost 10 times more likely to develop abruption compared with women without these complications.

In a hospital-based case-control study, Vintzileos et al¹ reported a high rate of chorioamniotic infection among patients with preterm PROM and that the risk of intrauterine infection was inversely proportional to the amount of amniotic fluid. We observed that more than 17% of pregnancies with abruption had both preterm PROM and oligohydramnios, yielding a RR of 7.17 (95% CI 1.35–38.10) compared with women without these 2 conditions.

Our study demonstrated a strong dose relationship between the time between membrane rupture and delivery among women with preterm PROM and the risk of abruption. However, our data did not allow the examination of temporal sequence of events among patients diagnosed with preterm PROM, intrauterine infections, and placental abruption. It will be interesting to know from future studies whether patients with abruption and intrauterine infections were predominantly those who developed these problems soon after ruptured membranes or whether they occur with similar frequency throughout the latency period.

Our results must, however, be interpreted with caution with respect to the relationship between preterm PROM and abruption. Because not all patients in our study with preterm PROM were screened for asymptomatic bacterial infections, this limitation precluded us from assessing the risk of abruption in women with such a condition. More specifically, our data did not contain information on the specific infections. A further limitation of the study was that the criteria for the definitions of oligohydramnios and intrauterine infection were not specified. The assumption is made that these diagnoses were made using conventionally accepted definitions. Although the NMIHS study involved carefully abstracting and coding medical and obstetric conditions from medical charts of each patient, the possibility of misdiagnosis of some of these conditions remains. The strengths of our study include its population-based nature, with generalizability of findings to the U.S. population in 1988. Although several high-risk groups were oversampled in the original survey (eg, low birth weight babies or stillborn fetuses), proper weighting of the data through appropriate statistical approaches to account for the complex sampling strategy of the NMIHS¹⁵ will not affect the conclusions drawn from this study. Finally, we were careful to adjust for several potential confounders in the analysis through multivariate logistic regression models.

The increased risk of placental abruption with preterm PROM should be considered in any discussion about prompt induction of labor compared with expectant management. Of course, there are other factors to consider in contemplating when to deliver, such as gestational age and maternal and fetal status. In patients with membrane rupture at 32–34 weeks, conservative management of preterm PROM is often the practice in obstetrics, typically waiting until spontaneous onset of labor begins or signs or symptoms of intrauterine infection occur. Our findings suggest that up to 6.2% of cases of abruption can be attributed to the presence of both preterm PROM and intrauterine infections. The clinician should be aware of this risk, and therefore, the option of effecting delivery within the first 24 hours of ruptured membranes should be considered as one of the various options available. Future studies must be designed to assess adverse perinatal and infant outcomes among women with preterm PROM and placental abruption.

	Footnotes

 
Received January 14, 2004. Received in revised form February 24, 2004. Accepted March 3, 2004.

Reprints are not available. Address correspondence to: Cande V. Ananth, PhD, MPH, Department of Obstetrics, Gynecology, and Reproductive Sciences, UMDNJ-Robert Wood Johnson Medical School, 125 Paterson Street, New Brunswick, NJ; e-mail: cande.ananth{at}umdnj.edu.

Drs. Ananth and Srinivas are partially supported through a grant (R01-HD038902) awarded to Dr. Ananth from the National Institutes of Health.

10.1097/01.AOG.0000128172.71408.a0

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ananth, C. V. Articles by Vintzileos, A. M. Search for Related Content PubMed PubMed Citation Articles by Ananth, C. V. Articles by Vintzileos, A. M. Related Collections Obstetric complications of pregnancy