septic abortion case study

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• Published: 13 March 2024

Obstetric infections and clinical characteristics of maternal sepsis: a hospital-based retrospective cohort study

• Sedina Atic Kvalvik   ORCID: orcid.org/0000-0001-9364-1816 1 , 2 ,
• Sofie Branæs Zakariassen 2   na1 ,
• Sofie Overrein 2   na1 ,
• Svein Rasmussen   ORCID: orcid.org/0000-0003-1313-713X 2 ,
• Steinar Skrede   ORCID: orcid.org/0000-0003-1615-4453 2 , 3 &
• Elham Baghestan   ORCID: orcid.org/0000-0003-0933-6988 1 , 2  

Scientific Reports volume  14 , Article number:  6067 ( 2024 ) Cite this article

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• Epidemiology
• Health care
• Infectious diseases
• Reproductive signs and symptoms

Sepsis is responsible for 50% of intrahospital maternal deaths worldwide. Incidence is increasing in both low and middle-, and high-income countries. There is little data on incidence and clinical outcomes of obstetric infections including maternal sepsis in the Nordic countries. The aims of this study are to give estimates of the occurrence of obstetric infections and maternal sepsis in a Norwegian hospital cohort, assess the quality of management of maternal sepsis cases, and evaluate the usefulness of diagnostic codes to identify maternal sepsis retrospectively. We conducted a retrospective cohort study of pregnant, labouring, post-abortion, and postpartum women. We assessed the accuracy of the diagnostic code most frequently applied for maternal sepsis, O85. We found 7.8% (95% confidence interval 7.1–8.5) infection amongst pregnant, labouring, and postpartum women. The incidence of maternal sepsis was 0.3% (95% confidence interval 0.2–0.5), and the majority of sepsis cases were recorded in the postpartum period. Two thirds of women were given broad-spectrum antibiotics at the time sepsis was diagnosed, but only 15.4% of women with puerperal sepsis were given antimicrobials in accordance with national guidelines. When used retrospectively, obstetric infection codes are insufficient in identifying both maternal and puerperal sepsis, with only 20.3% positive predictive value for both conditions. In conclusion, obstetric infections contribute significantly to maternal morbidity in Norway’s second largest maternity hospital. This study provides incidences of maternal infections for hospitalised patients in temporal relation to pregnancy, labour, abortion and the postpartum period, knowledge which is valuable for planning of health care services and allocation of resources. In addition, the study highlights areas where improvement is needed in clinical handling of maternal sepsis. There is need for studies on the management quality and use of correct diagnostic codes in this patient category.

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Introduction.

Maternal sepsis is considered the most severe infection related to childbirth and is globally ranged as one of the five leading causes of maternal mortality 1 . In 2020 the World Health Organization (WHO) stated that almost half of intrahospital maternal deaths worldwide are caused by infection and sepsis, suggesting that the impact and burden of obstetric infections previously have been underestimated 2 . The last two decades increasing trends in maternal infectious morbidity and mortality, predominantly in low- and middle-income countries, have been reported 3 . Similar trends are seen in high-income countries 4 , 5 .

Obstetric infections constitute both incidental and pregnancy specific infections which can occur during pregnancy, in labour, post labour or after abortion 6 . The association of infection in temporal relation to pregnancy, labour and postpartum period is incompletely known, but reportedly more than two thirds of the infections occur postpartum 7 .

Partly due to their unique physiology requiring different reference values to describe normality, obstetric patients are, however, excluded from the sepsis definitions for the general population 8 , 9 , 10 . WHO stated in 2017 that there is an urgent need for a generally accepted definition of maternal sepsis 11 , and recently consensus has been achieved defining the condition 12 .

Despite the serious potential outcome of obstetric infectious morbidity, there is neither a surveillance program nor a registry of maternal sepsis in Norway. Furthermore, there is no specific diagnostic code for maternal sepsis, and the relevant diagnostic codes in the International Statistical Classification of Disease and Health Related Problems, Tenth Edition (ICD-10) are not evaluated in their precision to encode the condition.

Consequently, our knowledge on the women who survive obstetric infection is limited 13 , 14 . A report from 2014 based on an audit on maternal deaths in Norway in the years 1996–2011 concluded that substandard care was given in two thirds of cases and that earlier recognition and more appropriate management of sepsis could have prevented the maternal deaths 15 . There are 70 survivors per maternal death caused by sepsis, and studies show that also in maternal near-miss sepsis cases, clinical handling needs improvement 16 . There is need for data on incidence and outcomes of obstetric infections, and maternal sepsis in particular, in accordance with WHO’s focus on obstetric infections in the twenty-first century 11 .

The present study aimed to examine the occurrence of obstetric infections in a Norwegian hospital cohort and offer an estimate of the contemporary incidence of maternal sepsis. We also wanted to evaluate the accuracy in the use of obstetric diagnostic codes for infection, as well as the codes’ ability to identify cases with maternal sepsis when used retrospectively. Finally, we wished to evaluate whether the clinical management was in accordance with the established sepsis guidelines for the general population 17 , 18 , 19 .

We conducted a retrospective cohort study of three subgroups of women; the first and second categories being women undergoing either legal or spontaneous abortion, and the third represented by women ≥ 16 weeks pregnant, labouring women, and postpartum women at the women’s clinic, Haukeland University Hospital (HUH) between 1 January and 31 December 2016. This particular year was chosen to create sufficient time distance to the implementation of an obstetrically modified early warning score system in 2018, and thus ensure that the results were unaffected by this. HUH is a tertiary care referral centre and university hospital with a catchment area of 380,000 individuals, and with approximately 5000 births annually it is the second largest maternity hospital in Norway. Both inpatient and outpatient women registered with obstetric infection after legal and spontaneous abortion, during pregnancy, in labour or up to 42 days postpartum, i.e., the puerperium, were included. Pregnant and postpartum women seeking primary or private care due to obstetric infections were not included in our study unless they were referred to our hospital.

Cases with infection were identified by a search for obstetric infection codes (O-codes) after legal and spontaneous abortion and during pregnancy, labour and postpartum according to the International Statistical Classification of Disease and Health Related Problems, Tenth Edition (ICD-10) 20 . Selected diagnostic codes and instruction for obstetric sepsis registration are presented in Table S1 (Supplementary information). Data were obtained from the electronic patient medical record systems. Clinical infections as recorded in the medical records were considered to represent the “gold standard” in quality assessment of the diagnoses. Additionally, we included patients admitted to the maternity department or readmitted after labour for seven days or more to detect infections that possibly were not encoded with any of the codes listed in Table S1 (Supplementary information). Women who had given birth outside the study period or were transferred from other hospitals after giving birth, or who developed infection more than 42 days postpartum as well as women without infection, were excluded. Flow chart of the search strategy is presented in Fig.  1 . One diagnostic code of infection represented one case of infection, and one woman could have had more than one infectious episode.

Flow chart of search strategy for obstetric infection codes and hospital stays 7 days or longer in the pregnant, labouring, post-abortion, and postpartum population at Haukeland University Hospital January to December 2016. Green represents infections following legal abortion, red represents infections following spontaneous abortion and blue represents infections following infections in pregnancy ≥ 16 weeks, in labour or up to 6 weeks postpartum. Abbreviation: pp; postpartum. Figure created with software from Miro© (2024), version 2.0, Miro.com.

Clinical data included respiration rate, peripheral oxygen saturation, body temperature, blood pressure, heart rate, and mental state. Fever was defined as body temperature 38 °C or higher. Clinical and laboratory findings (leukocytes and microbiological findings in cultures where available) were registered for each patient. We did not register whether patients were given antibiotic prophylaxis during labour. However, antibiotic prophylaxis is routinely given in emergency caesarean section cases in accordance with the Norwegian national guideline for intrahospital antibiotic treatment and the WHO 21 , 22 . Medical records were reviewed by three experienced doctors, and for each patient it was concluded whether there was compliance between the diagnostic codes used and clinical infection category. Where both symptoms and clinical infection signs were present, for instance fever in combination with abdominal pain, uterine tenderness on palpation, foul smelling lochia, swelling and/or redness of breasts, surgical sites or perineal or vaginal tears, in addition to findings in laboratory tests (elevated inflammation markers as mentioned above and/or positive bacterial cultures), we concluded that there was an infection. Where infection was confirmed, we concluded its focus based on the description in the medical journals. To define the presence of chorioamnionitis, we applied the clinical criteria suggested by the National Institute of Child Health and Human Development (NICHD) Workshop expert panel 23 . Our primary treatment method of legal abortion consists of a combination of orally administered mifepristone followed by orally, then transvaginally administered misoprostol. We treat post-abortion infections surgically with evacuation of the uterus, in combination with antimicrobial therapy.

Assessment of maternal sepsis

Maternal sepsis was categorized according to the WHO criteria and defined as a life-threatening condition with organ dysfunction resulting from infection during pregnancy, childbirth, post-abortion, or postpartum period 12 . The definition is based upon vital parameters as described in the SEPSIS-3 for the adult population while taking into consideration pregnant physiology by applying obstetrically modified score systems, as well as clinical and laboratory findings 8 , 12 . In cases with ambiguity whether sepsis was present or not, a specialist in infectious diseases reviewed and categorized these. For women fulfilling the sepsis definition, maternal age, pre-gestational body mass index (BMI), parity, tobacco use in the first trimester, mode of delivery, duration of labour, number of vaginal examinations during labour, induction of labour, estimated blood loss, and length of hospital stay were recorded. Timing of sepsis in relation to pregnancy, labour, post-abortion, or postpartum period, presence of pathogens in cultures, and values for physiological parameters at the time of sepsis diagnosis were determined. We further recorded whether sepsis treatment was initiated at the time of diagnosis, and if selection of empiric antibiotic treatment adhered to the national guideline. For puerperal sepsis a combination of penicillin, gentamicin and clindamycin is recommended 21 . We further registered whether source control with drainage of potential infected foci was undertaken, i.e., evacuation of retained products from the uterus in case of endometritis, and drainage of abscesses in case of mastitis, intraabdominal-, perineal- or vaginal infection.

Statistical analyses

We assessed the quality of the relevant diagnostic codes (predominantly O85) by calculating the sensitivity, specificity, positive and negative predictive values. Statistical analyses were performed with SPSS (IBM Corp. Released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp). To calculate confidence intervals for proportions we used the continuity corrected score method 24 .

Ethical approval

The study was approved by the head of the Women’s clinic at HUH. The requirement for informed consent from the study subjects was waived by the Regional Ethics Committee Health Region West (REC-West number 2019/32278), as the ethical committee classified the study as a quality improvement project. All methods were performed in accordance with the ethical standards of the institutional and national research committee as well as with the Helsinki declaration and its later amendments or comparable ethical standards.

In this study, we present three different cohorts with separate denominators, and occurrence of infection are therefore given separately after legal—and spontaneous abortion, and in pregnancy, labour, and postpartum period. Altogether, 27 cases fulfilled the search criteria for post-abortion infection, of which 12 were excluded as they did not represent infection (Fig.  1 ). There were 969 legal abortions registered in the study period, and nine infectious episodes were identified, equalling an occurrence of 0.9% (9/969) (Table 1 ). There were six infections following spontaneous abortion, however the occurrence of infection after spontaneous abortion remains unknown as the denominator of spontaneous abortions is unexplored in the current study (Table 1 ).

In total there were 5182 deliveries in the study period. Altogether 668 cases fulfilling search criteria were identified, of which 45 cases were excluded because they either delivered outside the inclusion period or at another hospital, or they were registered with infection exceeding 42 days of puerperium, and 221 cases were excluded due to no infection. Most of these were women with hospital stays seven days or longer for other reasons than obstetric infection (Fig.  1 ). We identified 402 infections in the pregnant, labouring, and postpartum cohort, giving a total frequency of obstetric infection of 7.8% (402/5182, 95% CI 7.1–8.5) (Table 2 ).

The distribution of categories is shown for the entire cohort consisting of 417 infections in Table 3 and Fig.  2 a.

( a ) Clinical categories in declining order among women with infection at Haukeland University Hospital, January to December 2016 (n = 417). ( b ) Infection and temporal relation to pregnancy, labour, post-abortion, and postpartum period, Haukeland University Hospital, January to December 2016 (n = 417). ( c ) Maternal sepsis and temporal relation to pregnancy, labour, post-abortion, and postpartum period, Haukeland University Hospital, January to December 2016 (n = 18).

Most pregnancy related infections were recorded in the postpartum period and included mastitis, endometritis, perineal and abdominal wound infections, in addition to postpartum urinary tract infection, constituting 56% (234/417) (Table 3 and Fig.  2 b).

In Table 4 , the eighteen cases of maternal sepsis that were identified, are presented. Seventeen cases resulted from pregnancy, labour and the postpartum period, equivalent to an occurrence in that population of 0.3% (17/5182, 95% CI 0.2–0.5). A single case resulted from spontaneous abortion. Thirteen cases were puerperal, accounting for 72.2% of sepsis cases (Fig.  2 c). In the postpartum period endometritis was most frequent and recorded in seven sepsis cases, accounting for 38.9%. At the time of sepsis diagnosis, most women had an aberration in vital parameters. There were no women with affection of the central nervous system i.e., reduced consciousness at the time sepsis was diagnosed.

A microbial aetiology by culture was identified in 44.4% (of sepsis cases, gram-negative rods (predominantly Enterobactereales) in 33.3% and beta-haemolytic streptococci in 11.1%. In total 72.2% of women were given broad-spectrum antibiotics intravenously at the time of sepsis diagnosis. In only 15.4% of the postpartum cases the antibiotic of choice adhered with the puerperal sepsis guideline. Half of the women were subject to source control with evacuation of an infected focus.

We found that O-codes were most frequently used during the study period and that sepsis patients were recorded among these; unaccompanied by R-codes. The code R65.1 (infection with organ dysfunction) was used in a single case only of postpartum sepsis. An A-code was only applied in a single case, whereas B-codes were applied ten times. Table 5 shows that O85 defined as “Puerperal fever” was the diagnostic code most frequently applied to encode puerperal infection and involves three conditions: postpartum endometritis, peritonitis, and puerperal sepsis 20 . The code O85 was correctly applied in the coding of postpartum endometritis with 91% sensitivity and 81% positive predictive value. In the case of puerperal sepsis and maternal sepsis the positive predictive value was 20.3% for both conditions.

In a hospital cohort we found 0.9% infection following legal abortion and 7.8% obstetric infection during pregnancy, in labour and the postpartum period. The incidence of maternal sepsis was 0.3% during the study period. Most cases of maternal sepsis were recorded in the postpartum period. Evaluation of clinical handling in cases of maternal sepsis showed that two thirds of patients were given broad-spectrum antibiotics at the time sepsis was suspected, but only 15.4% of women with puerperal sepsis were given antimicrobials in accordance with national antibiotic guidelines. Assessment of the relevant diagnostic code (O85) for maternal sepsis showed low positive predictive value.

Until recently there were no epidemiological studies on sepsis in Norway. Knoop et al. showed in 2017 that in hospitalised patients, sepsis incidence for the entire Norwegian population was 140 per 100,000, equivalent to 0.14% 25 . Maternal sepsis studies from other parts of the world show an incidence of 0.03% in the USA with a case fatality rate of 4.4 per 100 cases 26 . In Scotland the incidence of maternal sepsis during the years 1987–2008 was found to vary between 0.31 and 2.11%, whilst for septic shock it varied between 0.00 and 0.24% 27 . The Scottish findings were based upon separate ICD-9 codes for septicaemia, sepsis following abortion, puerperal sepsis, and septic shock, respectively. Together these studies illustrate that maternal sepsis is rare, but also that comparison of sepsis incidence between different regions and countries, in addition to different time periods, is challenging. In contrast to Scotland, we have no unique diagnostic code for maternal sepsis in Norway. Our finding of 0.3% is however higher than in the USA but is consistent with that from Scotland.

We identified a single case of maternal sepsis following spontaneous abortion after a pregnancy with cervical cerclage and none following legal abortion in the study period. Our finding of 0.9% occurrence of infection following legal abortion is consistent with the findings in a prospective study from Haukeland University hospital during 2006–2009 28 . All but one of the nine women with post-abortion endometritis following legal abortion, had surgical evacuation within the same day they presented with infection to our hospital, resulting in fast recovery. A Finnish study from 2009 investigated immediate complications after legal abortions (both medical and surgical) and found 0.8% and 0.6% infection with evacuation in the group of medical and surgical abortion groups, respectively 29 . Arguably, it may be that in countries where abortion is legalised, both near-miss cases and fatalities due to septic abortion are rare, as is the case for Norway where infections following legal abortions are treated promptly.

Concurrently, to the best of our knowledge, there are no epidemiological studies on the incidence of maternal sepsis in the Nordic countries. A Swedish study from 2014 used self-reported patient data to give incidence of puerperal infection both with and without prescription of antibiotics. A total occurrence of postpartum infection of 11.5% was found consisting of 4.7% mastitis (2.9% treated with antibiotics), 3.0% urinary tract infection (2.4% treated with antibiotics), 2.0% endometritis (1.7% treated with antibiotics), and 1.8% perineal wound infection (1.2% treated with antibiotics) 30 . However, the cases with infection were not confirmed either through medical records or prescription registries. The occurrence of infection found in that study cannot be applied to estimate the number of patients requiring hospital admission and is therefore not comparable to results from this study. The incidence of antepartum or intrapartum infections was not examined in the Swedish study, neither was maternal sepsis. The same authors examined the incidence of postpartum sepsis by a search for diagnostic codes in the Swedish ICD-10 and based upon this, the prevalence of postpartum sepsis was 2.4/10,000 women. The weakness in that study is that the code O85 is not equivalent to postpartum sepsis as it can be utilized in cases of infection without the presence of organ dysfunction, as we have demonstrated in our study as well 31 . However, sepsis after abortion, in pregnancy and labour were not examined in that study.

Our study indicates that approximately two thirds of patients were given broad spectrum antibiotics at the time sepsis was diagnosed. Concerningly, only two of the thirteen women with puerperal sepsis were given antibiotics in accordance with the Norwegian national guidelines for intrahospital antibiotic treatment, and eight different antibiotic regimens were used. A possible explanation for the apparent low adherence to guidelines could be that sepsis went unrecognized due to a lack of sepsis definition but also insufficient awareness of the condition. This illustrates the need to both examine the compliance of guidelines in cases of maternal sepsis as well as raise awareness of the condition.

Obstetric infections and maternal sepsis have suffered neglect to be recognized as important areas of maternal health. There are several explanations for this; firstly, all normal physiologic parameters of pregnancy overlap with those of the former Systemic Inflammatory Response Syndrome (SIRS) criteria 10 , which provide low specificity for the identification of sepsis in all patient categories 32 . Secondly, the contemporary sepsis definition for the general population excludes the obstetric population 8 . Finally, no definition of obstetric sepsis has so far been applicable to all stages of pregnancy, i.e., ante-, intra- and postpartum periods.

Delimiting maternal sepsis is difficult. As this study illustrates most obstetric infections are associated with the postpartum period. Postpartum endometritis is indeed the commonest focus of infection leading to maternal sepsis. Only the cases with organ dysfunction are however classified as maternal sepsis. This distinction is crucial, and the recently established maternal sepsis definition by the WHO may lead to more precise recording. Additionally, the new definition may spur further studies that will lead to better understanding of the condition across institutions and countries.

Audits on maternal deaths in the United Kingdom (UK), the MBRRACE reports, demonstrating that maternal sepsis arising from the genital tract was the leading cause of maternal morbidity during the years 2006–2008, have led to increased focus on maternal infection in the recent years 4 . Also, it was concluded that more than half of the sepsis related maternal deaths were preventable, which has given rise to several quality improvement efforts in maternal health care in the UK. One of the major efforts is the development of modified early warning score systems for the obstetric population to detect clinical deterioration in cases of infectious morbidity.

There was no practice of systematic or periodic scoring of physiologic parameters (e.g., “early warning score systems” ) for admitted nor outpatient obstetric patients in the study period at our hospital. Almost all the 18 women with maternal sepsis had an aberration in one or several physiologic parameters: tachycardia, pyrexia, and tachypnoea occurring most frequently. The use of vital parameters shows favourable in detecting deterioration from infection in the obstetric patient. Such systems are established for 30 years in the general adult population 33 , 34 . However, the use of scoring systems is not yet evaluated for the obstetric population and needs further investigation 35 . We implemented a scoring system for obstetric patients in 2018 in obstetric departments in Norway, to standardize the use of vital parameters for uncovering of clinical deterioration 36 . During the covid-19 pandemic we learned that obstetric patients proved to be an extra vulnerable population for serious morbidity and mortality 37 . Proper use of scoring systems makes us better prepared to meet future challenges.

The diagnostic code most frequently applied to encode puerperal sepsis in the study period, was O85, puerperal fever or “child bed fever” . However, this diagnostic code also comprises postpartum endometritis and peritonitis. Its positive predictive value for puerperal and maternal sepsis makes it less useful for the exploration of the true incidence of maternal sepsis in a retrospective manner. Considering that this code was accompanied by an R-code only once during the study period, the indication of organ dysfunction was lacking in most cases. Consequently, it cannot be applied for surveillance purposes of maternal sepsis in Norway. For sepsis occurring antepartum, there exists no specific code. Only intrapartum sepsis has its own diagnostic code, O75.3, “sepsis in labour”. However, this code was only applied once during the year 2016 at HUH. Hence, there is no specific sepsis code for the obstetric population which encompasses the entire pregnancy in the Norwegian ICD-10, but neither exists a unique diagnostic code for antepartum or postpartum sepsis 20 .

The present study had several limitations. The retrospective design provided limited information to the administration of prophylactic antibiotics during labour or caesarean delivery. According to our hospital guideline, all women undergoing emergency caesarean section are given prophylactic antibiotics, while normal weight, healthy nulliparous women are not given antibiotics. However, we have in a previous study showed that elective caesarean sections do not contribute to maternal infectious morbidity, and that prophylactic antibiotics should be restrictedly given, upon indication only, to women undergoing elective caesarean section 38 . Six of the patients with maternal sepsis in our study were delivered by emergency caesarean section, accounting for 33.3% of the sepsis cohort. Some of the sepsis cases were not scored according to respiration rate, indicating that this parameter was not systematically measured in 2016. Additionally, the retrospective design limited information to the timing of antibiotic treatment.

Another limitation is that we could have missed several cases of less severe infections with for instance endometritis and mastitis diagnosed and handled in the primary health care, which is highly available in Norway. Also, patients admitted to other departments outside the maternity department, were not included. Incidental infections other than urinary tract infections, for instance respiratory tract infections, were hence not recorded as they are not registered with O-codes. Furthermore, we could have missed some patients with severe infection if other diagnostic codes were used, regardless of searching for hospital stays lasting seven days or longer. In 2016 the coding practice shows that O-codes were applied unaccompanied by R-codes and A-codes, resulting in lacking sepsis indication. B-codes which specify bacterial aetiologies but without sepsis indication, were however applied ten times during 2016, further indicating that the coding practice for obstetric sepsis was not in accordance with the national coding instructions. Our incidence data might therefore be lower than the actual incidence.

This study does not provide the incidence of infections after spontaneous abortion as the denominator of spontaneous abortion is unexplored.

The strength of this study was the inclusion of a great number of obstetric infections according to the ICD-10 and a review of the medical records by an expert council to ensure that the cases with infection were correctly coded. All sepsis cases met the diagnostic criteria according to the WHO. Our findings on the occurrence of obstetric infections other than sepsis are most probably applicable to other Norwegian and Nordic maternity departments.

Conclusions

In conclusion, in a Norwegian hospital cohort of pregnant, labouring, and postpartum women obstetric infections were frequent. Most obstetric infections occurred in the postpartum period, as did maternal sepsis. Evaluation of the management in sepsis cases showed that there was low adherence to national antibiotic guidelines in cases of puerperal sepsis. The study concludes that coding of maternal sepsis is poor, as there exists no separate code for this condition. We suggest that a specific diagnostic code for maternal sepsis is constructed to offer more accurate diagnosis, increasing coding compliance and improving surveillance at regional and national level. We plan to do a follow-up study to investigate how implementation of an obstetrically modified early warning score system in our hospital has affected the diagnostics and handling of maternal sepsis.

Data availability

The datasets used and analysed during the current study are available from the corresponding author on reasonable request.

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Sedina Atic Kvalvik, Sofie Branæs Zakariassen, Sofie Overrein, Svein Rasmussen, Steinar Skrede & Elham Baghestan

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Kvalvik, S.A., Zakariassen, S.B., Overrein, S. et al. Obstetric infections and clinical characteristics of maternal sepsis: a hospital-based retrospective cohort study. Sci Rep 14 , 6067 (2024). https://doi.org/10.1038/s41598-024-56486-4

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Infection during Early Pregnancy and Septic Abortions

• First Online: 26 November 2020

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• Orsolya Miskolci 4 ,
• Deirdre Morley 5 &
• Ignacio Martin-Loeches 6  

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Non-obstetric causes of early pregnancy sepsis include pneumonia (especially influenza pneumonia) and urinary tract infections. Obstetric causes include vaginal tract infection, uterine infection, chorioamnionitis, endomyometritis, and septic abortion. Infection may occur after invasive procedures, e.g. amniocentesis, chorionic villus sampling, cervical cerclage, and percutaneous umbilical blood sampling. The incidence of sexually transmitted diseases (STDs) has been increasing in the last decade, being responsible for significant maternal and fetal morbidity. Septic abortion remains an important healthcare problem and ascending infections after abortion can spread rapidly, potentially leading to critical illness, multi-organ failure, or even death.

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Orsolya Miskolci

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Miskolci, O., Morley, D., Martin-Loeches, I. (2020). Infection during Early Pregnancy and Septic Abortions. In: Einav, S., Weiniger, C.F., Landau, R. (eds) Principles and Practice of Maternal Critical Care. Springer, Cham. https://doi.org/10.1007/978-3-030-43477-9_18

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The outcome of septic abortion: a tertiary care hospital experience

Affiliations.

• 1 Vydehi Institute of Medical Sciences and Research Centre, No. 82, EPIP Area, Whitefield, Bangalore, 560066 India.
• 2 Department of OBG, S. V. Medical College, Tirupathi, 571507 A.P. India.
• PMID: 25136172
• PMCID: PMC4126947
• DOI: 10.1007/s13224-014-0509-4

Objective: To study the incidence of septic abortion, reasons for that, sociodemographic profile, abortion providers, complications faced, and treatment given and its outcome.

Methods: All the women with septic abortion admitted at Government Maternity Hospital, Tirupathi, over a period of 2 years 4 months duration from July 2007 to October 2009 were studied prospectively.

Observations and results: Incidence of septic abortion in our study was 6.78 %. 72 % of cases were performed by qualified medical personnel. Fourteen patients had complications, among them peritonitis, pelvic abscess, renal failure, and septic shock were common. Twenty-six patients had Grade-I sepsis, Grade-II: 8, Grade-III: 4, and Grade-IV: 4. Laparotomy was done in six cases. There was no mortality in our study.

Conclusion: The tragedy of septic-induced abortion is totally preventable. It only needs definitive commitment to women's health by providing effective contraception, strengthening the family welfare services, and discouraging repeated terminations of pregnancy as contraceptive method.

Keywords: Complication; Incidence; Septic abortion.

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Infectious Complications of Abortion

Potential conflicts of interest. All authors: no reported conflicts of interest. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

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L Lewis Wall, Awol Yemane, Infectious Complications of Abortion, Open Forum Infectious Diseases , Volume 9, Issue 11, November 2022, ofac553, https://doi.org/10.1093/ofid/ofac553

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This article reviews the infectious complications of abortion (both spontaneous and induced) and the management of this condition. The key points are: (1) Making abortion illegal does not reduce its incidence or prevalence; rather, it only makes abortions unsafe, increasing the likelihood of infectious complications. (2) Timely recognition of developing sepsis in the pregnant patient is critical. This requires constant vigilance and a high index of suspicion. (3) Rapid intravenous administration of broad-spectrum antibiotics targeted to the likely intrauterine source of infection as soon as sepsis is diagnosed is critical to prevent severe sepsis, septic shock, and multisystem organ failure. (4) The mainstay of treatment is prompt evacuation of any residual products of conception from within the uterine cavity under broad-spectrum antibiotic cover targeting the likely intrauterine source of infection. (5) Prompt engagement of specialists in both critical care and obstetrics-gynecology is necessary to optimize outcomes in patients with septic abortion.

The recent Supreme Court ruling in the case of Dobbs v. Jackson Women's Health Organization held that there is no constitutionally protected right to abortion throughout the United States as a whole [ 1 ]. In overturning the constitutional precedent set by Roe v. Wade establishing that right nearly 50 years ago, the court referred such matters back to the individual states, many of which have already established Draconian anti-abortion laws that effectively outlaw most, if not all, abortions within their jurisdictions [ 2–4 ]. Some states are attempting to prevent women from traveling to other states to seek abortion services, to prohibit counseling women on why and how to seek abortion, and to outlaw websites that provide information on self-managed abortions. Some states are even establishing legal frameworks to promote citizen vigilantism against women who seek abortion and those who provide abortion services. Some states are going as far as establishing mechanisms that would allow individual citizens to sue clinicians who provide abortion care to residents in other states. Many states are attempting to restrict the delivery of Food and Drug Administration–approved medications that may be used to produce medical abortions in early pregnancy, and pharmacists—some fearful of incurring legal liability and others who wish to impose their own moral views on pregnant women—are refusing to fill prescriptions for drugs that might be used to produce an abortion, even when those drugs have other, well-established, legitimate medical uses. A patchwork of state abortion laws is developing in the United States that will mean that while elective abortion is freely available in some states, it is beyond the reach of most women in many others.

Without question, these actions will increase abortion-related morbidity and mortality as desperate women confront the prospect of forced birth under the diktats of right-wing legislatures in the states in which they happen to live [ 5–8 ]. Increasingly harsh and intrusive legal environments will hinder the provision of appropriate care to women requiring pregnancy terminations due to medical complications of pregnancy. At the same time, some women in desperate personal circumstances will attempt to terminate their unwanted pregnancies using unsafe methods. The World Health Organization defines an unsafe abortion as “a procedure for terminating an unwanted pregnancy either by persons lacking the necessary skill or in an environment lacking the minimum medical standards or both” [ 9 ]. Such abortions are certain to increase in the now-punitive environment that is developing. Obstetricians, gynecologists, and other clinicians who provide reproductive health care are aghast at the prospect of the nation returning to the status quo ante of the early 20th century before Roe v. Wade, in which the wards of public hospitals were full of young women suffering from the serious, life-threatening complications that resulted from illegal, unsafe abortions [ 5–8 ]. Those days are now quite likely to return [ 8 , 10–13 ]. Richard Schwarz's classic book, Septic Abortion , long out of print, is now sadly relevant again [ 14 ].

This is not alarmist hysteria-mongering. There is abundant evidence that making abortions illegal does little to reduce their incidence and prevalence; rather, when abortion becomes illegal, abortion services are driven underground, abortion practices become unsafe, and there is a dramatic increase in unnecessary injury and death to women of reproductive age, many of whom will live with lingering health consequences into their postreproductive years. When abortion is legalized and becomes safe, maternal mortality drops [ 15 ]. A vivid 20th century historical example of the effects that harsh, restrictive anti-abortion policies have on women's health must be heeded.

Abortion in Romania: A Cautionary Tale

Nicolae Ceausescu became the dictator of Communist Romania in 1965. At the time of his ascension to power, Romania had a maternal mortality rate comparable to other East European countries [ 16 ]. In 1966, however, without advance warning, Ceausescu outlawed abortion in Romania except under extraordinarily strict conditions. He also banned the importation of contraceptives in order to increase the country's population as part of his master economic development program, and for the next 23 years he pursued “the world's most rigidly enforced pronatalist population policy,” while also establishing the most repressive totalitarian government in Eastern Europe [ 16 ].

The Romanian government's intrusion into reproductive life was ubiquitous and breathtaking. Employed women had to undergo monthly gynecological examinations, and those who refused lost their access to medical and dental care as well as their pensions and social security. Factories had a required monthly birth quota, and the supervising factory physicians had their salaries reduced if these quotas were not met. Unmarried individuals over age 25 were subjected to a special 10% surtax. Taxes were also increased for childless couples who had been married for over 2 years unless they could document a medical reason for their lack of fertility. A special police unit was established to investigate alleged illegal abortions, and agents were placed in every maternity ward and obstetrical and gynecological clinic. Self-induced abortion became punishable by a prison term of up to 2 years. Physicians convicted of performing illegal abortions could be imprisoned for up to 12 years, with loss of their medical licenses [ 16 ].

Initially, these policies led to a brief upturn in births, but the birth rate soon fell to previous levels. At the same time, maternal mortality skyrocketed as women sought to terminate unwanted pregnancies by any means possible. Surveys confirmed that three-quarters of Romanians wanted families with only 1 or 2 children. Between 1981 and 1989, maternal mortality doubled, and Romania had the highest maternal mortality ratio in Europe at 159 maternal deaths per 100 000 live births, roughly 20 times higher than the US maternal mortality ratio during the same time period [ 17 ]. It was estimated that 87% of these maternal deaths were due to unsafe, illegal abortions. During Ceausescu's rule, at least 10 000 women died from abortion complications [ 15 ]. It was also estimated that 20% of Romania's women had been rendered infertile from infectious and other complications of these unsafe practices [ 15 , 16 ].

In addition to the toll on female reproductive health, staggering damage was inflicted upon the nation's children. The infant mortality rate in 1989 was 26.9 deaths per 1000 live births and 25.3 deaths per 1000 infants within the first 6 months of life. Thousands of children were abandoned by mothers who could not care for them, leaving them living in truly appalling conditions as wards of the state. It was estimated that only 2% of children in Romanian orphanages were truly “orphans”: The vast majority had been abandoned at birth by families who either did not want them or who could not afford to care for them. As many as 200 000 “orphans” were living in horribly substandard institutions when the regime finally fell [ 18 ].

In December 1989, increasing popular discontent led to a revolution that overthrew the Ceausescu government. Ceausescu and his wife, Elena, attempted to flee, but were captured and executed on Christmas Day, 1989. The next day, the new provisional government overturned the prohibitions on the importation of contraceptives and made abortion legal again as of January 1, 1990. Almost immediately clinical facilities were overrun with women seeking contraception and abortion services. Over 1 million safe abortions were performed in Romania in 1990, triple the number of live births. At the same time, maternal mortality dropped by 50%, decreasing to 83 deaths per 100 000 live births in 1990 [ 16 , 18 ]. By 2017, maternal mortality in Romania was 19 deaths per 100 000 live births—the same as in the United States [ 19 ]. (Both countries, however, continue to have maternal mortality 5 times higher than Sweden, at 4 maternal deaths per 100 000 live births [ 19 ].) Almost every country that has legalized abortions has seen similar trends in falling maternal mortality, as also happened in the United States after the initial Roe decision [ 15 , 16 , 18 , 20 ]. As Stubblefield and Grimes wrote nearly 30 years ago, “The most important effect of the legalization of abortion on public health in the United States was the near elimination of deaths from illegal abortion” [ 20 ]. The United States now seems likely to reverse this trend.

Complications of Unsafe Abortion

Worldwide, ∼6 out of 10 unintended pregnancies are terminated by induced abortion, 45% of which are unsafe and 97% of which take place in low-resource, developing nations [ 9 , 21–24 ]. Estimates suggest that nearly 50 000 women die each year from complications of unsafe abortion, primarily as the result of hemorrhage, infection, or both, and this accounts for 8%–13% of total world maternal deaths [ 23 , 24 ]. Treating complications of unsafe abortions also imposes huge social and economic burdens on the health care systems of countries where abortions are illegal and generally unsafe [ 24–27 ].

When performed in safe, medically supervised environments, first trimester abortion is extremely safe compared with the risks of delivering a pregnancy at term. In the United States between 1998 and 2005, the pregnancy-associated mortality rate for women who delivered live neonates was 8.8 per 100 000 live births, but the mortality rate for induced abortions was only 0.6 deaths per 100 000 abortions. The risk of death from childbirth is 14 times higher than that associated with safe abortion, and the rates of morbidity are similarly greatly increased after childbirth at term [ 28 ]. The number of unsafe abortions in the United States will certainly increase as a result of the changes currently taking place in state abortion laws [ 2–8 ].

This means that practitioners of internal medicine and specialists in infectious diseases increasingly will be consulted to help manage the infectious complications of abortion, both spontaneous and induced. Because the most important management of septic abortion is surgical—prompt evacuation of the infected products of conception under broad-spectrum antibiotic coverage—infectious disease specialists will not be the primary clinicians managing such cases, but they will be called upon increasingly to help manage the most difficult cases of severe sepsis and septic shock. This review provides background information needed for such care.

The relevant obstetrical terminology is given in Table 1 .

Terminology Related to Abortion

Although sepsis can complicate pregnancy at any point in gestation, the developing medico-legal environment in the United States suggests that there will be an uptick in 2 particular types of cases.

The first group of cases will likely be those in which women who are desperate to end an unwanted pregnancy and who are denied access to safe, legal abortion procedures as the result of restrictive abortion laws will resort to unsafe abortions on their own or at the hands of unqualified practitioners. The more invasive the abortion technique used, the more likely it is to disrupt the pregnancy, but also the more likely it is to cause dangerous complications, such as perforation of adjacent organs, hemorrhage, and sepsis—sometimes all together. The greater the gestational age of the pregnancy when such procedures are performed, the greater the likelihood of serious complications.

A wide variety of unsafe methods have been used in attempts to procure abortions [ 29 ]. These include the insertion of unclean objects such as coat hangers or knitting needles into the cervix and uterus; ingestion of toxic substances such as bleach, turpentine, or quinine or injecting such substances into the uterine cavity; physical violence to the abdomen with the intention of disrupting the placenta; and the placement of caustic chemicals such as potassium permanganate into the vagina, which, although ineffective in producing abortion, nonetheless can cause severe chemical burns that may erode through the vagina into the rectum [ 29 ]. Injection of substances such as liquid soap or disinfectant into the uterine cavity are particularly dangerous and may lead to extensive uterine necrosis [ 30 ]. Infectious complications may occur with any and all such unsafe techniques and will vary according to the characteristics of particular cases.

The second group of cases involves women with previable or periviable fetuses who develop preterm, prelabor rupture of the amniotic membranes. Many of these cases will occur as tragic complications of planned, wanted pregnancies, but the women involved may be denied termination of their nonviable pregnancies because of anti-abortion laws that prohibit any intervention in the presence of a fetal heartbeat. This has been the practice in Catholic hospitals in the United States for many years (largely unknown to the general public), but with the increasing instantiation of Roman Catholic theology into the legal system by aggressive conservative legislatures, this will be an increasing problem for clinicians working in non-Catholic hospitals who are now subject to these new legal restrictions [ 31–33 ].

Incomplete abortion is a powerful risk factor for death from infection. The death-to-case ratio for women with incomplete abortion is over 50 times higher than that for those who have adequate evacuation of the products of conception; the comparative mortality ratio is approximately 18 times higher. Retained tissue provides a nidus for the development of local infection, which then leads to generalized sepsis. [ 43 ]

Pathophysiological Considerations in Septic Abortion

It is important to understand the underlying physiology that makes septic abortion such a dangerous complication of pregnancy.

Pregnancy begins with the implantation of the blastocyst into the endometrial lining of the uterus. The placenta develops at the point of implantation, becoming the primary interface with the woman's body and the seat of the fetal-maternal communication system that regulates pregnancy. The embryo/fetus develops inside a membranous sac within the uterine cavity. This membranous sac is full of amniotic fluid, which provides the liquid environment necessary for fetal development but which is also a potentially nutritious culture medium for bacterial growth. At term, the amniotic fluid volume around the fetus is ∼800 mL [ 44 , 45 ].

The fetal and maternal circulatory systems are separate and normally do not intermix. The transfer of nutrients from the maternal to the fetal side and the transfer of waste matter from the fetal to the maternal side take place across the placenta. There are roughly 15 square meters of surface area through which these interchanges take place [ 46 ]. Effective gas exchange and the transfer of nutrient and waste matter across the placenta are dependent upon the enormous volume of blood flow going to the uterus and placenta. The nonpregnant uterus receives roughly 2% of cardiac output, but in pregnancy uterine blood flow increases almost 10-fold, with nearly 20% of the cardiac output flowing through the uterus and placenta at term [ 46 ]. This blood flows from uterine spiral arterioles into lacunar spaces beneath the placenta that bathe the placental villi across which nutrient/waste exchanges take place before the blood drains away through the engorged uterine venous system [ 47 ].

The infectious agents that produce septic abortion arise from the polymicrobial environment of the vagina and lower genital tract, reaching the uterine cavity through ascending infection [ 16 , 29 , 41 , 42 ]. Devitalized tissue is often present in the uterine cavity in septic abortions, allowing anaerobic bacteria to flourish. Because of the extreme vascularity of the uterus and the placental circulation, septic abortion results in very high rates of bacteremia (up to 60% of cases). When bacteria gain access to the maternal bloodstream, they can spread rapidly to every organ system in the body [ 10 ]. The confluence of these physiological and microbiological factors explains why infection of the amniotic fluid and membranes (chorioamnionitis) can explode in such a fulminant way, progressing from chorioamnionitis to sepsis, to severe sepsis, and to potentially fatal toxic shock in only a few hours.

Many of the bacteria found in septic abortions produce potent endotoxins that can result in damage to distant organ systems, affecting the pulmonary, renal, cardiac, and coagulation systems [ 40 ]. One study of 63 patients admitted to an intensive care unit with septic abortions found that 73% developed acute renal failure, 31% developed disseminated intravascular coagulopathy, 13% developed acute lung injury or acute respiratory distress syndrome, 32% developed septic shock, and 48% developed multiple organ failure [ 48 ].

This is why every modern review emphasizes 4 key actions in the diagnosis and management of septic abortion: (1) timely recognition of developing sepsis (which requires constant vigilance and a high index of suspicion); (2) rapid intravenous administration of broad-spectrum antibiotics targeted to the potential/likely intrauterine source of infection as soon as sepsis is diagnosed; (3) prompt evacuation of any residual products of conception from within the uterine cavity under antibiotic cover; and (4) prompt involvement of clinicians experienced in critical care in the management of patients with septic abortion [ 7–43 ]. An overview of the steps that should be taken in a case of septic abortion is given in Table 2 .

Steps in Clinical Management of Septic Abortion (Based on [ 10 , 20 , 25–32 ])

Abbreviation: CT, computed tomography.

Prompt diagnosis, speedy intervention, and rapid escalation of care are of critical importance. One cohort study of admissions of pregnant women with sepsis to an obstetric critical care unit found that in nearly 60% of those who died, there had been a delay of more than an hour in initiating antibiotic therapy after the diagnosis of sepsis had been made. The need for vasopressors to combat septic shock carried with it an odds ratio of 26.4 for dying [ 49 ]. In another study of 63 women with septic abortions admitted to an intensive care unit, 92% of those who died had developed septic shock [ 48 ].

Among women who died from sepsis, the majority had a delay in care and a delay in escalation of care. Most were afebrile, possibly delaying the recognition of the presence of sepsis. Even after the diagnosis, 73% of women were started on antibiotics that provided inadequate coverage…. The early involvement of consultant with expertise in infectious disease may expedite treatment of sepsis and help improve outcomes. [ 41 ]

Large-scale maternal mortality reviews from the United Kingdom have reached similar conclusions [ 36–38 ].

Microbial Pathogens in Septic Abortions

As noted previously, most bacteria involved in septic abortions are found in the normal vaginal flora, which ascend to cause infections of the uterus and upper genital tract, if favorable conditions for growth are present [ 16 , 29 , 36–42 ]. Anaerobic bacteria are commonly present. Cervical and uterine cultures, cultures of the placenta and of any evacuated products of conception, and blood cultures should all be part of the microbiological investigation of such cases. It is also particularly important to obtain urine cultures in these cases, as acute pyelonephritis is the most common serious infectious complication of pregnancy. Acute pyelonephritis may present similarly to septic abortion and may also progress rapidly to urosepsis and multisystem organ involvement [ 50–52 ].

Cultures are especially important in identifying bacteria that may produce endotoxins, such as Clostridum spp., group A Streptococcus (the pathogen of classic puerperal sepsis), Staphylococcus aureus (associated with toxic shock syndrome), and various toxin-producing strains of E. coli , but it is critically important to start patients on broad-spectrum antibiotics that cover these infections as soon as infection is suspected . Delay in starting intravenous antibiotics may be fatal. When culture results become available, the antibiotic focus may be narrowed if indicated [ 41 ].

The initial choice of antibiotics is empirical but must be broad-spectrum [ 49 ]. The 2 most commonly used regimens employ triple antibiotic therapy to attain broad-spectrum microbial coverage: ampicillin 2 g intravenously (IV) every 4 hours, gentamicin 5 mg/kg/d IV, plus clindamycin 900 mg IV every 8 hours. A reasonable alternative to clindamycin is metronidazole 500 mg IV every 8 hours. Specific cases may require case-specific adjustments. Once patients have been afebrile and asymptomatic on intravenous antibiotics, they can be discontinued. Although some authors prefer to place patients on oral antibiotics to complete a 10-day course of treatment, there is evidence that this is not necessary [ 40 , 42 , 53 ].

Role of Surgery in Septic Abortion

As noted previously, prompt evacuation of the infected uterine contents under broad-spectrum antibiotic therapy is the mainstay in the treatment of septic abortion [ 12 , 16 , 29 ]. This can usually be done with suction curettage or a blunt curette; however, if patients do not respond promptly to uterine evacuation and intravenous antibiotics, more aggressive surgical intervention may be required. Exploratory laparotomy is indicated if there is evidence of organ perforation and/or tissue necrosis in a septic abortion. The presence of gas in the myometrium on radiologic studies is strongly suggestive of anaerobic Clostridium infection, which frequently requires hysterectomy to remove the nidus of infected tissue. Prompt surgical intervention, including hysterectomy, may be lifesaving, whereas delay may be fatal [ 14 , 40 , 53–59 ].

Case Study: The Death of Savita Halappanavar From Septic Abortion

The unnecessary death of Savita Halappanavar from a septic abortion in Ireland in 2012 outraged the world and was an important factor in the subsequent amendment of the Irish constitution several years later to permit abortions [ 60–63 ]. The case is instructive because the factors that led to Savita's untimely death are now likely to become increasingly prevalent in the United States as abortion access becomes much more restricted. Because individual states have now outlawed abortions irrespective of the surrounding circumstances, even in pregnancies occurring in girls as young as 10 who have been raped or under circumstances where a pregnancy has occurred as the result of rape or in which the pregnant woman's life is in jeopardy, clinicians are increasingly uncertain as to whether they will face prosecution for intervening, even when it is obvious what “the right thing to do” clinically is in such cases.

In 2012 when Savita Halappanavar's death occurred, Irish law recognized the “equal right to life” of both mother and fetus, except under extraordinary (and previously unspecified) circumstances. The result was that most doctors felt that they could not intervene in a complicated pregnancy if a fetal heartbeat was present, unless there was a clear and immediate danger to the life of the pregnant woman. The criteria to determine whether such a danger was present had never been clarified, leading to much medico-legal confusion.

Savita Halappanavar was a 31-year-old married dentist from India living in Ireland with her husband, when she became pregnant in the summer of 2012 with a much-wanted pregnancy [ 62 ]. She registered for prenatal care and had an unremarkable pregnancy until 17 weeks, when she presented to the gynecology ward at University Hospital Galway on October 21, 2012, with complaints of back pain. Initially she was diagnosed with sciatica (without undergoing a pelvic examination) and sent home with analgesia and an appointment for physical therapy. She returned several hours later, upset and crying, in worsening pain. A pelvic examination revealed ballooning amniotic membranes, bulging almost to the vaginal introitus. She was admitted with a diagnosis of inevitable abortion. A fetal heartbeat was present. She was afebrile at admission but had an elevated white blood count of 16 900 per microliter. The potential significance of this laboratory finding was ignored by the admitting team.

Because intra-amniotic infection is a common cause of premature labor, it is likely that Savita was already infected at this time. She was admitted to the hospital for observation and expectant management. Early the following morning, she had spontaneous rupture of the membranes. In this scenario, with a previable 17-week fetus and ruptured membranes, the risk of maternal infection is high, and the risk accelerates progressively with each hour the patient is not delivered. The inquest into Savita's death confirmed that international best obstetric practice in such cases mandates prompt delivery of the previable fetus to preserve the woman's life, irrespective of the presence of a fetal heartbeat [ 63 , 64 ].

In light of these facts, Savita and her husband both requested that her pregnancy be terminated expeditiously, but this was denied them because a fetal heartbeat was still present. They were told that such a course of action was not possible because “Ireland is a Catholic country,” and “theoretical” risk was not enough to justify the procedure. The attending gynecologist told them that because “we can’t predict who is going to get an infection,” no intervention was possible [ 63 ]. They protested that they were both practicing Hindus from India and that in their circumstances they regarded termination of the pregnancy as standard medical care, especially considering that the fetus was not viable. Their requests were ignored.

Savita's clinical care over the next few days was substandard, marred by poor communication among clinicians, lack of follow-up with appropriate laboratory studies, and inattention to her deteriorating clinical condition. The inquest into her subsequent death noted that there “was an apparent over-emphasis on the need not to intervene until the fetal heart stopped altogether with an under-emphasis on the need to focus appropriate attention on monitoring for and managing the risk of infection and sepsis in the mother” [ 63 ]. Because she was a healthy, 31-year-old woman, the risk of her developing fulminant sepsis, which might speedily turn into fatal septic shock, was discounted, if not ignored, because of the persistent presence of a fetal heartbeat and medico-legal fears about performing an abortion.

Early in the morning of Wednesday, October 24, the patient complained of being cold. When the midwife gave Savita a blanket, she noticed that her teeth were chattering, even though her temperature was normal. A few hours later, she vomited and spiked a fever to 39.6°C (103.3°F). She was now tachycardic with a pulse of 160 beats per minute, a blood pressure of 94/55 mmHg, a foul-smelling vaginal discharge, and diffuse abdominal tenderness. Blood cultures were obtained, a serum lactate was drawn (but subsequently lost), and she was started on intravenous amoxicillin/clavulanate. Somewhat later, metronidazole was added.

A fetal heartbeat was still present at noon, but Savita's condition was deteriorating. Her blood pressure was 76/46 mmHG. She was having trouble breathing, complained of diffuse myalgias, and was noted by the midwives to be “very unwell.” Her antibiotics were changed to piperacillin/tazobactam and gentamicin after consulting with the hospital microbiologist. Metronidazole was continued.

Arrangements were made to move her to the high dependency unit (one tier below intensive care), but a bed was not readily available. She was taken to the gynecology operating room, where a central venous catheter was placed. While in the operating room, she spontaneously delivered a stillborn female fetus along with the placenta, which appeared to be intact.

From this point on, Savita Halappanavar received excellent medical care, but it was too little, too late. She continued to deteriorate and was finally admitted to the intensive care unit with a diagnosis of septic shock. There she was intubated and placed on a ventilator. Vasopressors were needed to maintain her blood pressure. A trans-esophageal echocardiogram showed a dilated right ventricle, severe triscupid regurgitation, a hypokinetic left ventricle, and a possible pulmonary embolism. She developed disseminated intravascular coagulopathy and was heparinized. Her blood cultures, which had earlier shown the presence of a gram-negative bacillus, grew out extended-spectrum beta-lactamase–producing E. coli .

Savita Halappanavar had a cardiac arrest at 12:45 Am on October 28, 2012, and was pronounced dead after failed resuscitation at 1:09 Am that morning.

A postmortem examination on October 30 and the subsequent coroner's inquest concluded that the cause of her death was “fulminant septic shock from E. coli bacteremia, ascending genital tract sepsis, and miscarriage at 17 weeks’ gestation associated with chorioamnionitis” [ 63 ]. There were no comorbidities.

Two extensive investigations into these events by the Irish government determined that there had been gross clinical mismanagement of the case from the beginning, which led to inadequate medical treatment, insufficient monitoring of the patient's clinical status, and inappropriate delays in treatment, all stemming from an excessive concern about the persistent presence of a fetal heartbeat [ 63 , 64 ]. Similar cases are now likely to occur in the United States [ 65 ].

Until a child is born into the world, it is literally part of its mother's body, and belongs to her and her mate. It does not belong to society at all, nor has it been accepted into any faith. Its existence is entirely and exclusively the business and concern of its parents, whether they are married or not. It is men and women who alone must decide whether or not they wish their union to lead to the birth of a child, not the synagogue or chuch, and certainly not the state. [ 66 ]

We must do everything possible to prevent the intrusion of these radical theological beliefs into the practice of medicine. The recent constitutional referendum in Kansas, which resoundingly protected the right to abortion access, demonstrates that the loudest, most radical voices against abortion rights are not representative of the opinions of the majority of the population [ 67 ].

Patient details of the clinical case study are in the public domain due to the Irish Government's investigation of the case and the publication of the inquest documents, cited in the references.

Author contributions. L.L.W. wrote the original draft, and A.Y. reviewed and contributed critical comments and additional references. Both authors approved the final version.

Patient consent. As this is a review article, no patient consent was required. As noted in the article and in the references, all of the information concerning the case of Savita Halappanavar is widely accessible in the public record, and no consent was required to access this information. As a review article, institutional approval from an Institutional Review Board was not required.

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Knight M , Tuffnell D , Kurinczuk JJ; on behalf of the Sepsis Chapter-Writing Group. Message for the prevention and treatment of sepsis. In: Knight M , Tuffnell D , Shakespare J , Kenyon S , Kurinczuk JJ , eds. Saving Lives, Improving Mothers’ Care: Lessons Learned to Inform Maternity Care From the UK and Ireland Confidential Enquiries Into Maternal Deaths and Morbidity 2013 – 2015 . National Perinatal Epidemiology Unit, University of Oxford ; 2017 ; 59 – 66 .

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Plante LA , Pacheco LD , Louis JM . Society for Maternal-Fetal Medicine consult series #47: sepsis during pregnancy and the puerperium . Am J Obstet Gynecol 2019 ; 220 : B2 – 10 .

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Ross MG , Beall MH . Amniotic fluid dynamics. In: Resnick R , Lockwood CJ , Moore TR , Green MF , Copel JA , Silver RM , eds. Creasy and Resnick's Maternal-Fetal Medicine . 8th ed. Elsevier . 2019; 62 – 7 .

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Wang Y , Zhao S . Placental blood circulation. In: Vascular Biology of the Placenta . Morgan & Claypool Life Sciences ; 2010 . ncbi.nlh.gov/books/NBK53254/. Accessed November 1, 2022.

Finkielman JD , De Feo FD , Heller PG , Afessa B . The clinical course of patients with septic abortion admitted to an intensive care unit . Intensive Cae Med 2004 ; 30 : 1097 – 102 .

Holanda AMC , Ramos de Amorim MM , Bezerra SMB , Aschoff LMS , Katz L . Risk factors for death in patients with sepsis admitted to an obstetric intensive care unit: a cohort study . Medicine (Baltimore) 2020 ; 99 : e23566 .

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Savaris RF , de Moraes GS , Cristovam RA , Braun RD . Are antibiotics necessary after 48 hours of improvement in infected/septic abortions? A randomized controlled trial followed by a cohort study . Am J Obstet Gynecol 2011 ; 204 : 301.e1 – 5 .

Singhal PC , Kher VK , Dhall GI , et al.  Conservative vs. surgical management of septic abortion with renal failure . Int J Gynaecol Obstet 1982 ; 20 : 189 – 94 .

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Barrett JP , Whiteside JL , Boardman LA . Fatal clostridial sepsis after spontaneous abortion . Obstet Gynecol 2002 ; 99 : 899 – 901 .

Nanda S , Sangwan K , Agarwal U . The ugly face of septic abortion . Eur J Obstet Gynecol Reprod Biol 2002 ; 105 : 71 – 2 .

Eaton CJ , Peterson EP . Diagnosis and acute management of patients with advanced clostridial sepsis complicating abortion . Am J Obstet Gynecol 1971 ; 109 : 1162 – 6 .

O’Connor A . How the death of Savita Halappanavar changed the abortion debate . Irish Examiner. October 28, 2017 .

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Holland K . Savita: The Tragedy That Shook a Nation . Transworld Ireland ; 2013 .

Health Service Executive . Investigation of Incident 50278 From Time of Patients Self-Referral to Hospital on the 21st of October, 2012 to the Patient's Death on the 28th of October, 2012 . Irish Health Services Executive; 2013 . Available at: https://www.lenus.ie/handle/10147/293964 . Accessed September 1, 2022.

Health Information and Quality Authority . Investigation Into the Safety, Quality and Standards of Services Provided by the Health Service Executive to Patients, Including Pregnant Women, at Risk of Clinical Deterioration, Including Those Provided in University Hospital Galway, and as Reflected in the Care and Treatment Provided to Savita Halappanavar . Health Information and Quality Authority; 2013 . Available at: https://www.hiqa.ie/sites/default/files/2017-01/Patient-Safety-Investigation-UHG.pdf . Accessed September 1, 2022.

Wall LL . The ghost of Savita Halappanavar comes to America . Obstet Gynecol 2022 ; 140 ( 5 ): 724 – 8 .

Margolies IR . A reform rabbi's view. In: Hall RE , ed. Abortion in a Changing World . Vol. I . Columbia University Press ; 1970; 30 – 3 .

Doan A . The Kansas abortion vote shows the loudest voices in this debate are not representative ones . BMJ 2022 ; 378 : o2024 .

Author notes

• abortion, induced
• abortion, septic
• abortion, spontaneous
• infection as complication of medical care

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Abortion, not georgia’s abortion ban, killed woman.

The real and documented harms of pregnancy-ending pills

The heartbreaking death of Amber Nicole Thurman raises critical concerns about the risks associated with abortion pills and the broader landscape of abortion. It is essential to examine the facts and address the preventable factors that contributed to this loss, especially regarding the documented risks of medication abortion and the removal of crucial safety measures.

Abortion pills, while marketed as a safe and simple solution, carry real risks. Mifepristone and misoprostol, the drugs involved in medical abortions, are not without complications. A study published in Obstetrics & Gynecology reported that up to 5% of women who take abortion pills incomplete abortions, meaning that fetal remains are left in utero, potentially leading to infection, sepsis and bleeding.

This is exactly what happened in Amber’s case. Had the proper precautions been in place, such as required ultrasounds and follow-up care with a qualified medical provider, the 28-year-old mother’s death likely could have been prevented.

When the Food and Drug Administration first approved the abortion pill regimen, it implemented risk evaluation and mitigation strategies, or REMS, to protect women from these risks. REMS required in-person visits, an ultrasound to confirm gestational age and follow-up appointments to ensure no fetal tissue remained.

In recent years, these safeguards have been stripped away, making it easier to obtain abortion pills via telemedicine or even by mail without the critical involvement of medical professionals. Women not only administer their own abortion pills but also must assess and manage their own symptoms. Because women are promised privacy when they are sold abortion pills, many are hesitant to seek medical care when symptoms indicate the need. In Amber’s case, she did not access emergency care quickly enough when her complications arose — a tragic consequence of these relaxed FDA regulations.

The FDA’s omission of medical oversight and ultrasounds from the abortion pill process is no small matter.

Without an ultrasound, there is no way to confirm whether the pregnancy is ectopic, which can be life-threatening. Abortion pills are far less effective when the pregnancy is growing outside the uterus, and women may not know they are in danger during the abortion. As we saw in Amber’s case, without timely access to proper medical oversight during an abortion, severe complications such as sepsis can quickly escalate. Medical professionals must remain central to the abortion pill process, particularly when it comes to monitoring for retained fetal tissue.

Those selling abortions continue to profit from women such as Amber yet are rarely available to respond to medical complications during or after the abortion. Instead, women are increasingly going to emergency departments with complications during and after their abortions, especially with symptoms of bleeding and infection.

Abortion restrictions, such as those in Georgia, do not prevent doctors from providing lifesaving care when necessary. No law — whether in Georgia or elsewhere — prevents doctors from performing a dilation and curettage to save a woman’s life in cases of septic abortion or miscarriage.

The tragic delay in Amber’s treatment was not because of legal restrictions but rather an abortion process that required her to deliver twins on her own without medical support and then manage her own follow-up care.

Advocates of abortion often argue that restricting access to abortion puts women’s lives in danger. The reality is that unrestricted access to abortion pills without proper oversight is what leads to preventable tragedies like this one.

Incomplete abortions, retained fetal tissue and the failure to follow up with medical care are not rare complications; they are documented risks that can have deadly consequences. It’s vital that we address these risks head-on rather than promote policies that remove critical safeguards for women’s health.

While Amber Nicole Thurman’s death is used by some to further the abortion agenda, it’s important to recognize that seeking more abortion access in response to such stories does little to educate women about the real and documented harms of abortion pills. Instead, it stokes division on a matter where lives are at stake — both the lives of mothers and their unborn children.

The reality is that abortion, regardless of the circumstances, always results in death. In Amber’s case, abortion claimed three lives — her own and those of her unborn twins.

Abortion is not the “safe and easy” solution that it’s often portrayed to be, and Amber’s death proves it. Women deserve to know the truth about the risks of abortion pills, from incomplete abortions to the serious complications that arise when medical oversight is removed.

Exploiting tragic stories like Amber’s to advocate expanding abortion access without addressing these life-threatening risks is not only misleading, it sidelines the essential conversation about real women’s health care. Women deserve comprehensive information about their options, including the dangers associated with abortion pills, so they can make informed decisions.

Advocacy should focus on reducing harm, not increasing access to practices that put more lives in jeopardy.

As we grieve the loss of Amber and her children, let’s not allow her story to become another tool to push an agenda that ultimately causes more harm. Instead, we should work to protect both women and children by ensuring that all women have access to life-affirming care and that no woman or child needlessly loses their life to abortion.

Amber’s death was a tragedy that could have been avoided if the abortion provider had afforded her medical oversight during and after her abortion. Had the REMS protocol remained intact, had an ultrasound been required and had her health and safety been a priority for those who provided her abortion pills, Amber would likely still be alive today.

We must demand better for women — life-affirming care that provides women with the support, safety and real health care they deserve, ensuring that every life is valued and nurtured.

• Andrea Trudden is vice president of communications at Heartbeat International.

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Perinatal Outcomes Among Patients With Sepsis During Pregnancy

Christine a. blauvelt.

1 Department of Obstetrics, Gynecology and Reproductive Sciences, Division of Maternal-Fetal Medicine, University of California, San Francisco

Kiana C. Nguyen

Arianna g. cassidy, stephanie l. gaw.

Accepted for Publication: July 6, 2021.

Published: September 3, 2021. doi:10.1001/jamanetworkopen.2021.24109

Open Access: This is an open access article distributed under the terms of the CC-BY License . © 2021 Blauvelt CA et al. JAMA Network Open .

Author Contributions: Drs Blauvelt and Gaw had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Blauvelt, Cassidy, Gaw.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Blauvelt, Cassidy, Gaw.

Critical revision of the manuscript for important intellectual content: All authors.

Statistical analysis: Blauvelt, Cassidy, Gaw.

Administrative, technical, or material support: Nguyen.

Supervision: Cassidy, Gaw.

Conflict of Interest Disclosures: Dr Gaw reported receiving grants from the National Institutes of Health, Bill and Melinda Gates Foundation, Centers for Disease Control and Prevention Foundation, California Health Care Foundation, and Robert Wood Johnson Foundation outside the submitted work. No other disclosures were reported.

Funding/Support: Dr Gaw was supported by grant NIAID K08AI141728 from the National Institutes of Health.

Role of the Funder/Sponsor: The funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Meeting Presentation: These data were presented at the 41st Annual Pregnancy Meeting of the Society for Maternal-Fetal Medicine; January 30, 2021; virtual conference.

Associated Data

This cohort study compares rates of perinatal complications among pregnant individuals with and without antepartum sepsis hospitalization.

Do patients who remain pregnant after discharge from an antepartum sepsis hospitalization have increased rates of perinatal complications?

In this cohort study of 14 565 patients with nonanomalous, singleton pregnancies, a history of antepartum sepsis hospitalization was associated with higher odds of perinatal complications that are associated with placental dysfunction compared with no history of antepartum sepsis. After adjustment for possible confounders, including maternal age, parity, body mass index, and medical comorbidities, patients with antepartum sepsis had 2-fold higher odds of perinatal complications.

This study found that pregnancies with antepartum sepsis were associated with higher odds of complications that are associated with placental dysfunction, suggesting that increased antenatal surveillance may be warranted for these patients.

Rates of maternal sepsis are increasing, and prior studies of maternal sepsis have focused on immediate maternal morbidity and mortality associated with sepsis during delivery admission. There are no data on pregnancy outcomes among individuals who recover from their infections prior to delivery.

To describe perinatal outcomes among patients with antepartum sepsis who did not deliver during their infection hospitalization.

Design, Setting, and Participants

This retrospective cohort study was conducted using data from August 1, 2012, to August 1, 2018, at an academic referral center in San Francisco, California. Included patients were all individuals with nonanomalous, singleton pregnancies who delivered after 20 weeks’ gestation during the study period. Data were analyzed from March 2020 through March 2021.

Antepartum admission for infection with clinical concern for sepsis and hospital discharge prior to delivery.

Main Outcomes and Measures

The primary outcome was a composite of perinatal outcomes associated with placental dysfunction and consisted of 1 or more of the following: fetal growth restriction, oligohydramnios, hypertensive disease of pregnancy, cesarean delivery for fetal indication, child who is small for gestational age, or stillbirth.

Among 14 565 patients with nonanomalous singleton pregnancies (mean [SD] age at delivery, 33.1 [5.2] years), 59 individuals (0.4%) were in the sepsis group and 14 506 individuals (99.6%) were in the nonsepsis group; 8533 individuals (59.0%) were nulliparous. Patients with sepsis, compared with patients in the reference group, were younger (mean [SD] age at delivery, 30.6 [5.7] years vs 33.1 [5.2] years; P  < .001), were more likely to have pregestational diabetes (5 individuals [8.5%] vs 233 individuals [1.6%]; P  = .003), and had higher mean (SD) pregestational body mass index scores (26.1 [6.1] vs 24.4 [5.9]; P  = .03). In the sepsis group, the most common infections were urinary tract infections (24 patients [40.7%]) and pulmonary infections (22 patients [37.3%]). Among patients with sepsis, 5 individuals (8.5%) were admitted to the intensive care unit, the mean (SD) gestational age at infection was 24.6 (9.0) weeks, and the median (interquartile range) time from infection to delivery was 82 (42-147) days. Antepartum sepsis was associated with higher odds of placental dysfunction (21 patients [35.6%] vs 3450 patients [23.8%]; odds ratio, 1.77; 95% CI, 1.04-3.02; P  = .04). On multivariable logistic regression analysis, antepartum sepsis was an independent factor associated with placental dysfunction (adjusted odds ratio, 1.88; 95% CI, 1.10-3.23; P  = .02) after adjusting for possible confounders.

Conclusions and Relevance

This study found that pregnancies complicated by antepartum sepsis were associated with higher odds of placental dysfunction. These findings suggest that increased antenatal surveillance should be considered for these patients.

Introduction

Maternal sepsis is the second leading cause of maternal mortality in the United States. 1 Among all maternal deaths in the US, 13% are attributed to infection or sepsis, with case fatality rates as high as 10% to 30% in the obstetric population. 2 , 3 , 4 Pregnant patients may be particularly susceptible to rapid progression to sepsis and septic shock due to pregnancy-specific physiologic, mechanical, and immunological adaptations. 5 Rates of sepsis during pregnancy and the puerperium are also increasing, with 1 population-based study in Texas 6 finding a 2-fold increase in pregnancy-associated sepsis, from 11 incidences per 10 000 deliveries in 2001 to 26 incidences per 10 000 deliveries in 2010. This increase may be associated with evolving characteristics of obstetric patients, including older age, increased body mass index scores (BMI; calculated as weight in kilograms divided by height in meters squared), and increasing prevalence of chronic comorbid conditions.

Pregnancies complicated by sepsis are associated with increased rates of adverse obstetric outcomes, including cesarean delivery, postpartum hemorrhage, and preterm delivery. 7 , 8 , 9 Much of our current understanding of sepsis in pregnancy is based on studies of peripartum infections occurring during labor or the postpartum period, such as septic abortion, intra-amniotic infection, and endometritis. 10 , 11 , 12 , 13 Studies of antepartum infections have primarily focused on immediate maternal outcomes, such as intensive care unit (ICU) admission and death. Little is known about the association of sepsis with long-term pregnancy outcomes, particularly among individuals who recover from their infections prior to delivery.

There is abundant evidence regarding placental dysfunction after maternal infection with pathogens capable of causing placental or fetal infection. 14 , 15 , 16 , 17 , 18 , 19 Some studies have also suggested an association between infection with pathogens that do not cross the utero-placental interface and placental dysfunction. 20 , 21 Antenatal risk stratification for placental disorders is of paramount importance, given that impaired placental development and function are important factors associated with multiple pregnancy complications, including preeclampsia, placental abruption, preterm birth, infants born small for their gestational age, and stillbirth.

The objective of this study was to describe perinatal outcomes among patients with an antepartum sepsis hospitalization who recovered from their infection and did not deliver prior to hospital discharge. We hypothesized that these patients were at an increased risk of pregnancy complications, particularly complications associated with placental dysfunction.

The University of California, San Francisco, institutional review board approved this retrospective cohort study with a waiver of informed consent because of the study’s retrospective design and use of deidentified data. The Strengthening the Reporting of Observational Studies in Epidemiology ( STROBE ) reporting guideline was followed in the writing of this report.

Study Population

We performed a retrospective cohort study of patients with a nonanomalous, singleton pregnancy who delivered at 20 weeks’ gestation or later at an academic referral center from August 1, 2012, to August 1, 2018. Individuals included in the study were identified through the institution’s electronic medical and delivery records. Patients were screened using diagnoses coded with the International Classification of Diseases, Ninth Revision, Clinical Modification ( ICD-9-CM ) and International Statistical Classification of Diseases, Tenth Revision, Clinical Modification ( ICD-10-CM ) for an infection-related hospital admission during the 10 months prior to delivery (see eMethods in the Supplement for list of ICD-9-CM and ICD-10-CM codes used). Exclusion criteria included toxoplasmosis, syphilis, varicella, parvovirus B19, Zika virus, rubella, cytomegalovirus, and herpes simplex virus (TORCH) infections. All patients identified through ICD-9-CM and ICD-10-CM codes were reviewed by 2 authors (C.A.B. and K.C.N.) to confirm the presence of an antepartum infection and to determine whether there was clinical concern for sepsis. We defined sepsis as “life-threatening organ dysfunction caused by a dysregulated host response to infection,” 22 in accordance with The Third International Consensus Definitions for Sepsis and Septic Shock Task Force. We defined the antepartum period as the time from a positive pregnancy test until onset of labor or rupture of membranes. Patients were included in the sepsis group if they had an antepartum infection with clinical concern for sepsis and were subsequently discharged prior to delivery. Patients were included in the reference group if they did not have an infection with concern for sepsis during their pregnancy.

Variables and Outcome Measures

We extracted patient variables from medical records. Collected variables were maternal age, parity, pregestational BMI (patient-reported BMI immediately prior to pregnancy or earliest documented BMI during pregnancy), pregestational diabetes (ie, type 1 or 2 diabetes diagnosed prior to pregnancy or hemoglobin A 1C ≥6.5% prior to 14 weeks’ gestation [to convert to proportion of total hemoglobin, multiply by 0.01]), gestational diabetes (ie, abnormal glucose tolerance testing after 14 weeks’ gestation by 1-step or 2-step approach), chronic hypertension (ie, elevated blood pressure diagnosed prior to pregnancy or before 20 weeks’ gestation), smoking during pregnancy, and admission indication during delivery hospitalization.

We additionally obtained perinatal outcomes. Collected outcomes were fetal growth restriction (ie, sonographic estimation of fetal weight <10th percentile for gestational age), oligohydramnios (ie, amniotic fluid index ≤5 cm or single deepest pocket <2 cm), hypertensive disease of pregnancy (ie, new hypertension after 20 weeks’ gestation, with systolic blood pressure ≥140 mm Hg or diastolic blood pressure ≥90 mm Hg on 2 occasions at least 4 hours apart), cesarean delivery for nonreassuring fetal status or intolerance of labor, infant born small for gestational age (ie, sex-specific birthweight <10th percentile for gestational age), 23 stillbirth, preterm birth, preterm premature rupture of membranes at less than 37 weeks’ gestation, intra-amniotic infection (ie, maternal fever and ≥1 of fetal tachycardia, maternal white blood cell count >15,000/mm 3 , or purulent fluid from the cervical os), retained placenta, cesarean delivery for any indication, postpartum hemorrhage (ie, delivery blood loss ≥1000 mL), blood transfusion during delivery hospitalization, postpartum infection (ie, uterine or surgical site infection diagnosed up until 6 weeks post partum), maternal ICU admission during delivery hospitalization, 5-minute Apgar score less than 7, and term neonatal ICU admission.

Patient characteristics and perinatal outcomes were compared between the sepsis group and reference group. The primary outcome was a composite of perinatal outcomes associated with placental dysfunction and consisted of 1 or more of the following: fetal growth restriction, oligohydramnios, hypertensive disease of pregnancy, cesarean delivery for nonreassuring fetal status or intolerance of labor, infant born small for gestational age, or stillbirth. Secondary outcomes included each component of the composite placental dysfunction outcome, as well as other maternal and neonatal complications.

Statistical Analysis

Descriptive analyses were performed for all patient characteristics and clinical variables. Between-group differences were assessed by χ 2 test or Fisher exact test for binary variables and by t test for continuous variables. Subgroup analyses were performed according to severity of infection, gestational age at time of infection, and organ system involved. Multivariable logistic regression analysis was performed to adjust for potential confounders that could be associated with placental dysfunction. All statistical tests were 2-tailed, with P values less than .05 considered statistically significant. Statistical analyses were performed using Python programming language version 3.8.5 (Python Software Foundation) and the following libraries: SciPy version 1.5.2 (Travis Oliphant, Pearu Peterson, Eric Jones) and Pandas version 1.1.2 (NumFocus). Data were analyzed from March 2020 through March 2021.

Among 14 565 patients (mean [SD] age 33.1 [5.2] years), 59 individuals (0.4%) were in the sepsis group and 14 506 individuals (99.6%) were in the nonsepsis group; 8533 individuals (59.0%) were nulliparous. Figure 1 shows the flow of patients. There were 15 689 patients who delivered at our institution from August 1, 2012, to August 1, 2018. Of these, 1113 patients were excluded: 535 patients excluded for multifetal gestation, 482 excluded for major fetal structural or genetic anomalies, and 96 excluded for missing data. We cross-referenced the remaining 14 576 patients with hospital discharge records to identify patients with an infection in the 10 months prior to delivery, resulting in 700 patients. The medical records for these patients were then reviewed in detail, with 636 patients (4.4%) confirmed to have an antepartum infection and 70 patients (0.5%) with sepsis; 10 of these patients (14.3%) required ICU admission. We excluded 11 patients (15.7%) who delivered during their sepsis hospitalization. Among individuals with antepartum sepsis hospitalizations, 59 patients (84.3%) were discharged prior to delivery and were included in the sepsis group.

ICD-9-CM indicates International Classification of Diseases, Ninth Revision, Clinical Modification ; ICD-10-CM , International Statistical Classification of Diseases, Tenth Revision, Clinical Modification .

Table 1 summarizes the baseline characteristics of patients in the sepsis and reference groups. Patients in the sepsis group were younger (mean [SD] age at delivery, 30.6 [5.7] years vs 33.1 [5.2] years; P  < .001), were more likely to have pregestational diabetes (5 individuals [8.5%] vs 233 individuals [1.6%]; P  = .003), and had higher mean (SD) pregestational BMI scores (26.1 [6.1] vs 24.4 [5.9]; P  = .03) than patients in the reference group. Among patients in the sepsis group, the most common infection types were urinary tract infections (24 patients [40.7%]) and pulmonary infections (22 patients [37.3%]), and 5 individuals (8.5%) were admitted to the ICU. The mean (SD) gestational age at the time of infection was 24.6 (9.0) weeks, and the median (interquartile range) time from infection diagnosis to delivery was 82 (42-147) days. Quick Sequential (Sepsis-Related) Organ Failure Assessment (qSOFA) scores of 2 points or more were found for 16 patients (27.1%), and 5 patients (8.5%) were admitted to the ICU. In the sepsis group, 1 patient died post partum, giving an overall maternal mortality rate within this group of 1.7%. This patient had a history of cystic fibrosis and developed sepsis from pneumonia, recovered, and later died from noninfectious pulmonary complications.

Abbreviations: BMI, body mass index (calculated as weight in kilograms divided by height in meters squared); ICU, intensive care unit; IQR, interquartile range; NA, not applicable.

Perinatal outcomes are presented in Table 2 . Features of placental dysfunction were more commonly seen among patients in the sepsis group than patients in the reference group (21 patients [35.6%] vs 3450 patients [23.8%]; odds ratio [OR], 1.77; 95% CI, 1.04-3.02; P  = .04). Antepartum sepsis was associated with higher odds of hypertensive disease of pregnancy (14 patients [23.7%] vs 1614 patients [11.1%]; OR, 2.49; 95% CI, 1.36-4.54; P  = .006). Among patients with sepsis, 5 individuals (8.5%) developed preeclampsia and 9 individuals (15.3%) developed gestational hypertension (64.3% of those with sepsis who had hypertensive disease of pregnancy). Antepartum sepsis was also associated with higher odds of postpartum hemorrhage (14 patients [23.7%] vs 1871 patients [12.9%]; OR, 2.10; 95% CI, 1.15-3.83; P  = .02) and maternal ICU admission during delivery hospitalization (2 patients [3.4%] vs 10 patients [0.1%]; OR, 39.70; 95% CI, 8.51-185.24; P  = .002). Other perinatal outcomes were similar between the 2 groups. In the multivariable logistic regression analysis ( Figure 2 ), antepartum sepsis was an independent factor associated with placental dysfunction (adjusted OR [aOR], 1.88; 95% CI, 1.10-3.23; P  = .02) after adjustment for possible confounders. Parity, pregestational BMI, smoking during pregnancy, gestational diabetes, age, and chronic hypertension were also factors associated with placental dysfunction in multivariable analysis.

Abbreviation: ICU, intensive care unit; OR, odds ratio.

Data for the univariable analysis indicate odds of having placental dysfunction for each covariate using simple logistic regression; data for the multivariable analysis indicate adjusted odds ratios (ORs). All variables are covariates retained in the final model after adjustment. BMI indicates body mass index.

In subgroup analyses ( Table 3 ), among patients with sepsis vs those without sepsis, earlier gestational age at the time of infection was associated with higher odds of placental dysfunction (12 of 26 patients [46.2%] at <24 weeks; OR, 2.75; 95% CI, 1.27-5.94; P  = .02), but later gestational age at time of infection was not (9 of 33 patients [27.3%] at ≥24 weeks’ gestation; OR, 1.20; 95% CI, 0.56-2.59; P  = .68). Patients with antepartum sepsis prior to 24 weeks were more likely to develop hypertensive disease of pregnancy (8 patients [30.8%] vs 1614 patients [11.1%]; OR, 3.55; 95% CI, 1.54-8.18; P  = .01) and to have newborns who were small for their gestational age (6 patients [23.1%] vs 1438 patients [9.9%]; OR, 2.73; 95% CI, 1.09-6.80; P  = .04) compared with patients in the reference group who did not have antepartum sepsis. Patients with antepartum sepsis prior to 24 weeks also delivered newborns with lower mean (SD) birth weights than patients in the reference group (2967 [537] g vs 3249 [620] g; P  = .02). There were no differences in outcomes when stratified by organ system involved, antepartum ICU admission, or qSOFA score of 2 or greater.

Abbreviations: ICU, intensive care unit; NA, not applicable; OR, odds ratio; qSOFA, quick Sequential (Sepsis-Related) Organ Failure Assessment.

Placental pathology results were available for 20 patients (33.9%) and unavailable for 39 patients (66.1%) in the sepsis group. We were therefore unable to find associations between histopathological findings and clinical outcomes of placental dysfunction. Among individuals in the sepsis group, 41 patients (69.5%) had a third-trimester ultrasonography for fetal growth. Among 7 patients (11.9%) with sepsis who delivered infants who were small for their gestational age, 4 patients (57.1%) had third-trimester ultrasonography screening for fetal growth restriction and 1 patient (14.3%) was diagnosed with fetal growth restriction prenatally.

This cohort study found that patients with a history of antepartum sepsis had statistically significantly higher odds of obstetric complications associated with placental dysfunction. When adjusting for possible confounders, including maternal age, parity, BMI score, and medical comorbidities, patients with antepartum sepsis had nearly 2-fold higher odds of placental dysfunction compared with patients without antepartum sepsis. The timing of infection during pregnancy also had important associations with perinatal outcomes. Early infection (ie, at less than 24 weeks’ gestational age) was associated with the greatest increase in odds of composite placental dysfunction, hypertensive disease of pregnancy, and newborns who were small for gestational age. High rates of obstetric complications were also seen in those who experienced antepartum sepsis, including postpartum hemorrhage, blood transfusion, cesarean delivery, and peripartum ICU admission.

Consistent with previous work, 4 , 8 , 24 our study found that 70 pregnant patients (0.5%) had antepartum sepsis, with 10 of these patients (14.3%) requiring maternal ICU admission and 11 patients (15.7%) having imminent delivery. Much of the previous literature regarding severe antepartum infection has focused on maternal morbidity, and few studies have examined obstetric and neonatal outcomes. A population-based cohort study 25 in Nova Scotia, Canada, compared pregnant patients with and without hospital admission for respiratory illness and reported increased rates of infants who were born small for their gestational age and decreased birth weights among patients with respiratory hospitalization. Our study had similar findings among patients with antepartum sepsis, although our data were statistically significant only among individuals with sepsis whose infections occurred at less than 24 weeks’ gestation vs those without sepsis (infants born small for their gestational age: 6 patients [23.1%] vs 1438 patients [9.9%]; mean [SD] birthweight 2967 [537] g vs 3249 [620] g). In another study, Farkash et al 26 found that antepartum pyelonephritis was associated with multiple perinatal outcomes that are potentially associated with placental dysfunction, including fetal growth restriction, placental abruption, preterm delivery, intrapartum fetal distress, and an Apgar score less than 7 at 1 minute. In contrast to our findings, their study did not find a difference in rates of hypertensive disorders among individuals with and without antepartum pyelonephritis.

Our study differs from previous investigations in several important ways. First, this is the first study, to our knowledge, to examine perinatal outcomes among patients who recovered from antepartum sepsis prior to delivery, given that prior studies of maternal sepsis have focused on sepsis that occurred during delivery admission. This represents a distinct clinical scenario from antepartum sepsis that leads to imminent delivery. Second, we did not restrict our study by organ system involved in the infection and instead included all infection types that led to sepsis. Third, we conducted detailed medical record reviews for patients with antepartum infections, and only individuals with concerning features for sepsis were included. Fourth, our study was unique, to our knowledge, in examining associations of gestational age at the time of infection and of latency between infection and delivery with perinatal outcomes.

We hypothesize that the dysregulated host response to maternal infection that occurs during sepsis may disrupt placental development and function, leading to poor perinatal outcomes among these patients. There is a large body of research finding that placental pathologies, such as maternal spiral artery remodeling, abnormal villous development, maternal vascular malperfusion, and impaired umbilical blood flow, are associated with pregnancy complications. 27 , 28 , 29 , 30 , 31 Moreover, abnormal placental histopathologic findings have been observed among pregnant individuals with bacterial, viral, and parasitic infections. 32 , 33 , 34 , 35 , 36 Maternal infection and systemic inflammation may be associated with impaired vasculogenesis and angiogenesis, with associated placental insufficiency, inadequate oxygen and nutrient transport to the fetus, and adverse birth outcomes. These outcomes may be magnified among pregnant individuals with sepsis at earlier gestational ages. We hypothesize that this association may be explained by the coincident timing of infection with establishment of placental vasculature or by increased duration of exposure to utero-placental dysfunction.

The recognition that antepartum sepsis may be associated with placental dysfunction has important implications for pregnancy management. Ultrasonographic screening for fetal growth restriction may be considered for patients with a history of antepartum sepsis. Of 7 patients in our study who delivered infants who were small for their gestational age, 4 patients (57.1%) had growth ultrasonography screenings in the third trimester and 1 patient (14.3%) was diagnosed with fetal growth restriction prenatally. Fetal growth restriction is known to be associated with increased risk of stillbirth, neonatal morbidity, and mortality, 37 underscoring the potential need for increased antepartum surveillance for pregnancies complicated by antepartum sepsis. We also observed increased rates of hypertensive disease of pregnancy in the sepsis group, occurring in approximately 24% of patients. Of note, most of these individuals (9 patients [64.3%]) exhibited mild hypertensive disease at the time of delivery. These findings suggest that patients with antepartum sepsis should be counseled on signs and symptoms of preeclampsia and receive close monitoring of their blood pressure.

Strengths and Limitations

Strengths of our study included that, to our knowledge, this is the first study to directly assess perinatal outcomes of patients who experienced sepsis in pregnancy and recovered prior to delivery. Additionally, we performed detailed medical record review, allowing us to have complete and accurate data for sepsis admission and ultimate delivery admission.

Several limitations of our work should be recognized, including the retrospective nature of data collection at a single institution. We included only pregnancies that led to delivery at our institution; thus, patients who delivered elsewhere may have been missed. If such patients had a different risk of perinatal outcomes than those who delivered at our institution, this could have biased our findings. Furthermore, our sample size was likely too small to detect differences in rare perinatal complications, such as stillbirth. In addition, we did not use standardized diagnostic criteria for sepsis, given that pregnant patients have been excluded from major trials validating systemic inflammatory response syndrome (SIRS), SOFA, qSOFA, and other sepsis scoring systems. Therefore, these sepsis severity scores have not been well validated in obstetric populations and have not been adjusted for pregnancy physiology. Given the lack of a consensus definition of sepsis in the obstetric population, patients in this study were included in the sepsis group if there was agreement between 2 authors (C.A.B. and K.C.N.) regarding the presence of infection and organ dysfunction. Additionally, placental pathology reports were not available for most patients (39 patients [66.1%]) in the sepsis group. It is likely that many placentas were not sent for histopathologic review because the patients had recovered from sepsis at the time of delivery. Thus, we were not able to associate clinical findings of placental dysfunction with histopathologic findings; however, this should be considered in future work.

Conclusions

This study found that antepartum sepsis was associated with increased odds of placental dysfunction. Earlier gestational age at the time of infection was associated with higher odds of placental dysfunction, including hypertensive disease of pregnancy and lower birth weight. Our study provides new information to inform patient counseling regarding expected perinatal outcomes after antepartum sepsis and the potential need for increased pregnancy surveillance. This study may also open up new avenues for research regarding pathophysiologic mechanisms of placental dysfunction after antepartum sepsis and potential interventions including anti-inflammatory medications to mediate the association of sepsis with adverse pregnancy outcomes.

Supplement.

eMethods. Coded Diagnoses for Infections During Pregnancy