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Abstract
A random-effects meta-analysis was performed in English and Chinese databases since its inception to August 2020 to assess the incidence, causes and severity of acute pancreatitis (AP) at various stages of pregnancy, maternal and foetal mortality. A total of 154 articles representing 4034 patients with AP during pregnancy in China were included for the analysis. The incidence of AP during pregnancy was 0.0469 (95% confidence interval [CI], 0.0349; 0.0627) in the first trimester, whereas it was 0.2518 (95% CI, 0.2210; 0.2854) and 0.6323 (95% CI, 0.5870; 0.6753) in the second and third trimester, respectively. The major causes of AP were hypertriglyceridaemia (0.351 [95% CI, 0.3202; 0.3834]) and biliary pancreatitis (0.424 [95% CI, 0.4094; 0.5002]). The severity of AP was mild in majority of the patients. The incidence of AP at maternal mortality was 0.0184 (95% CI, 0.0126; 0.0269) and foetal mortality was 0.1018 (95% CI, 0.0867; 0.1192). Our meta-analysis revealed that hypertriglyceridaemia and biliary pancreatitis remain the major causes of AP during pregnancy. Foetal mortality requires further investigation.
What is already known on this subject? Acute pancreatitis (AP) in pregnant women is characterised by acute onset and delay in understanding the interaction of the metabolic changes with pancreatic pathophysiology, and thus becomes difficult to diagnose the disease and provide timely treatment to the patients. This poses a greater health risk among women and their foetus by increasing their chances of mortality.
What the results of this study add? We performed an exhaustive, random-effects meta-analysis involving 154 articles representing 4034 patients to assess the incidence of AP at various stages of pregnancy, the causes of AP and the severity of AP during pregnancy, maternal and foetal mortality.
What are the implications of these findings for clinical practice and/or further research? Our meta-analysis revealed that hypertriglyceridaemia and biliary pancreatitis remain the major causes of AP during pregnancy. Although the rates of maternal mortality have decreased in the recent years, foetal mortality still remains high and requires further investigation.
IMPACT STATEMENT
Introduction
Pregnancy is associated with physiological changes that alter the presenting symptoms and signs of many disease processes (Hernandez et al. Citation2007). Acute pancreatitis (AP) during pregnancy though rare is associated with incidence rate of 1 per 1000–10,000 pregnancies (Eddy et al. Citation2008; Pitchumoni and Yegneswaran Citation2009; Igbinosa et al. Citation2013). AP during pregnancy is more frequent in multiparous women (Ramin et al. Citation19952011; Igbinosa et al. Citation2013). Also, it is more common in East Asian countries, with an incidence rate of 0.227–4.25% (Sun et al. Citation2011; Zhang et al. Citation2013). In Asian countries, cholelithiasis is more common than in the Western world, which may explain the differences in morbidity to AP (Tazuma Citation2006). A study reported that AP was more common in Asian women, and they are more likely to die of AP than their Caucasian counterparts (McNabb-Baltar et al. Citation2014).
Nevertheless, AP in pregnant women is characterised by acute onset and delay in understanding the interaction of the metabolic changes with pancreatic pathophysiology, and thus becomes difficult to diagnose the disease and provide timely treatment to the patients (Pitchumoni and Yegneswaran Citation2009). This poses a greater health risk among women and their foetus by increasing their chances of mortality (Pitchumoni and Yegneswaran Citation2009). Earlier, the maternal-foetal mortality rate was high (37% and 60%, respectively), which has decreased in the recent years to 1% and 0–18%, respectively (Papadakis et al. Citation2011). This can be attributed to earlier diagnosis and dynamic improvement in maternal and neonatal intensive care (Ducarme et al. Citation2014). Besides, the causes of AP during pregnancy can be different similar to the causes that are in non-pregnant women (Ducarme et al. Citation2014). The common identified causes of AP during pregnancy include gallstones (66%), alcohol abuse (12%), hyperlipidaemia (4%), idiopathic (17%), obesity and occasionally trauma, hyperparathyroidism, medication and fatty liver of pregnancy (Eddy et al. Citation2008; Pitchumoni and Yegneswaran Citation2009; Papadakis et al. Citation2011; Igbinosa et al. Citation2013).
Given the low incidence rate and limited clinical data in China regarding the disease, there remains an uncertainty regarding diagnosis and treatment of AP during pregnancy. A study from 36 cases of AP during pregnancy reported that hypertriglyceridaemia was associated with poor outcomes of the disease (Xu et al. Citation2015). The most recent study identified an association between foetal distress and foetal loss with severity of AP during pregnancy (Tang et al. Citation2018). These findings reiterate the significance of precise diagnosis and care for AP during pregnancy in reducing maternal and foetal mortality. Furthermore, in China, there are no standardised guidelines for the management of AP during pregnancy, probably due to low incidence rate. To date, there are no meta-analysis evaluating the incidence and mortality rate of AP during pregnancy in China to the best of our knowledge. We therefore aimed at evaluating the incidence of AP during pregnancy at various stages and identifying the potential risk factors for AP during pregnancy along with their implications on maternal mortality and foetal loss in Chinese women.
Methods
Protocol and registration
This meta-analysis was registered in the International Prospective Register of Systematic Reviews (PROSPERO) under the number CRD42020220316.
Data search strategy and selection
A systematic literature search was performed in EMBASE and PubMed databases since inception to August 2020. Relevant Chinese articles were searched in CNKI and Wanfang literature databases. The following search string was used with minor variations to suit the database ‘acute pancreatitis’ AND ‘pregnancy’. The corresponding Chinese search string was used for screening articles from respective databases.
Study eligibility criteria
The studies were selected for review based on the following criteria: (1) pregnant women with AP (2) patients belonging to geographical region of China (3) studies reporting outcomes such as incidence of maternal mortality, incidence of foetal loss or infant mortality, causes of AP during pregnancy and incidence of AP at any stage of pregnancy (4) prospective and retrospective observational study (5) eligible studies limited to those published in English and Chinese. The studies were excluded if they are in the following criteria (1) case reports, reviews, meta-analysis, randomised controlled trial (RCTs) or other than observational studies (2) duplicate publications from the same patient population (3) studies reporting outcomes other than stated above (4) studies published in language other than Chinese and English.
Data and quality assessment
Two independent investigators initially reviewed articles through the titles and abstracts to assess whether they met the inclusion criteria. Studies satisfying the inclusion criteria and those with abstracts were retrieved for full-text evaluations. Data from included studies regarding author, year of publication, title, study design, demographics of the study population and outcomes of interest were extracted into standardised MS Office Excel. In addition, the data extraction sheet included the number of patients, percentages and p-value reported for each outcome. The Newcastle-Ottawa scale was used to assess the methodological quality of observational studies. A higher score represented better methodological quality. The quality assessment of each article is available as supplements (Supplementary Table 1).
One of the constraints of a meta-analysis of observational studies is that there are no appropriate tools available for assessing publication bias. We therefore performed a thorough research of the available literature to assess publication bias in observational studies.
Data synthesis and statistical analysis
Heterogeneity (I2) is expected among studies with different populations. To incorporate part of the heterogeneity, a random-effects meta-analysis was used, and a series of subgroup analysis was performed concerning publication year, severity of the disease and aetiology of the disease. Heterogeneity among the results of different studies was examined using Cochran’s Q and I2 statistics. A fixed effects model was used to calculate the pooled effect if I2 was <50% (insignificant heterogeneity), whereas the random effects model was used if I2 was >50% (significant heterogeneity). Baseline characteristics were presented using descriptive statistics. A p value of ≤ .05 was considered statistically significant, wherever applicable. All the inferences at each level of analysis were validated, and the limitations were identified. On the basis of the limitations, the generalised inferences are presented in this study.
Results
Study selection and population characteristics
A total of 3643 articles were retrieved from literature search. After removing duplicates and screening for inclusion/exclusion criteria, a total of 155 articles were identified and included in the analysis. represents the PRISMA flowchart for the studies evaluation. The summary characteristics of included studies are presented in Supplementary Table 1.
Figure 1. PRISMA flowchart for selection of studies.
AP during pregnancy in each trimester
The overall incidence of AP in this population was reported in very few studies (19 studies), and it was found to be 0.0009 (95% confidence interval [CI], 0.0001; 0.0145). Of 154 studies, 94 studies (9 English and 85 Chinese) were included for the analysis of the incidence of AP during pregnancy for each trimester. Among these studies, the incidence of AP during pregnancy was found to be 0.0469 (95% CI, 0.0349; 0.0627) in the first trimester, whereas the incidence of AP during pregnancy in the second trimester was 0.2518 (95% CI, 0.2210; 0.2854) and the third trimester was 0.6323 (95% CI, 0.5870; 0.6753; ).
Table 1. Incidences of acute pancreatitis in pregnancy in different subgroups.
AP during pregnancy based on publication year
We divided the included articles based on the publication year as follows: before 2010 and after 2010. Thirty-five articles were found before 2010, whereas 60 articles were included after 2010 for each trimester. The incidence rate of AP during pregnancy before 2010 was 0.0459 (95% CI, 0.0256; 0.0810) in the first trimester, whereas after 2010, it was 0.0469 (95% CI, 0.0334; 0.0655). Similar results were obtained for AP during pregnancy in the second and third trimester ().
Causes of AP during pregnancy
One hundred seventeen articles were included for the analysis of hypertriglyceridaemia as a risk factor. The number of articles analysing biliary pancreatitis, idiopathic and other causes were 115, 15 and 15, respectively. The rate of hypertriglyceridaemia was found to be 0.351 (95% CI, 0.3202; 0.3834), whereas the cause of AP during pregnancy was idiopathic in 0.168 of patients (95% CI, 0.1014; 0.2654) and biliary in 0.424 (95% CI, 0.4094; 0.5002) of patients ().
Severity of AP during pregnancy
Mild and severe forms of AP during pregnancy were reported in 117 articles. For the number of years, the incidence rate of mild AP among women was 0.6494 (95% CI, 0.6124; 0.6848) and severe AP was 0.2988 (95% CI, 0.2678; 0.3317) ().
Mortality outcomes
Maternal mortality was reported in 144 studies, whereas foetal loss was reported in 120 studies. The incidence of maternal mortality was found to be 0.0184 (95% CI, 0.0126; 0.0269), whereas foetal loss was found to be 0.1018 (95% CI, 0.0867; 0.1192; ).
Discussion
To our knowledge, this is the first meta-analysis reporting the incidence of AP in terms of severity, aetiology as well as maternal and foetal mortality outcomes in Chinese pregnant women. Our analysis included articles reporting AP during pregnancy for a period of 40 years. The incidence of AP during pregnancy was found to be the highest (63.23%) in the third trimester. This proportion was similar to the previous studies reporting that most AP during pregnancy occurred in the third trimester (Ducarme et al. Citation2014; Vilallonga et al. Citation2014; Luo et al. Citation2018; Yang et al. Citation2020). This might be attributed to the increased compression to the pancreas and gallbladder by the enlarging uterus as the trimester advances, as well as change in steroids that directly affects gallbladder function (Braverman et al. Citation1980). In later stages of pregnancy, incomplete emptying of the gallbladder may lead to the retention of cholesterol crystals, a precursor of cholesterol-gallstone formation (Braverman et al. Citation1980). Increase in serum triglyceride levels due to oestrogen produces hyper viscosity, which leads to ischaemia and acidosis in pancreatic capillaries (Swisher et al. Citation1994). This results in change in bile composition, which may induce the formation of gallstones and sludge (Ducarme et al. Citation2014).
Hypertriglyceridaemia (35%) and biliary pancreatitis (45%) remain the leading causes of AP during pregnancy among women to date. Similar findings were reported by Luo et al. stating that gallstone and hypertriglyceridaemia were the common causes of AP among pregnant Chinese women (Luo et al. Citation2018). One probable reasons for this consistent rise may include a 2-fold to 4-fold increase in plasma triglycerides, particularly in the third trimester of pregnancy (Takaishi et al. Citation2009). A blood triglyceride level >1000 mg/dL is considered as a high risk factor for AP during pregnancy (Athyros et al. Citation2002; Okura et al. Citation2004), although they never reach levels above 300 mg/dL (3.42 mmol/L) (Saharia et al. Citation1977). Nevertheless, patients with abnormal lipid metabolism may experience severe elevations in circulating triglycerides and chylomicrons, which may cause pancreatic circulation-related ischaemic lesions (Saharia et al. Citation1977). A literature reports that lipoprotein lipase mutation is associated with extreme hypertriglyceridaemia during pregnancy (McGladdery and Frohlich Citation2001). Besides, abnormal lipid and glucose metabolism due to high-fat diet is reported to be an important inducer of AP during pregnancy (Gürsoy et al. Citation2006). Contrary to these findings, various studies from the United States indicate that gallstones is the most common cause of AP during pregnancy (>50%) (Pitchumoni and Yegneswaran Citation2009; Tang et al. Citation2010; Mali Citation2016). This may reflect regional differences between Chinese and other populations, and more studies are needed to clarify these findings.
In China, reports from 1980 to 1990 revealed that the incidence of AP during pregnancy was 12.5% (Xiuhai and Yushan Citation1993). Gradually, in recent years, the incidence of AP during pregnancy has improved with articles reporting the incidence rate around 0.1% (Xu et al. Citation2015; Ding and Chou Citation2017; He Fang et al. Citation2017; Tang et al. Citation2018; Wang Xiaowei et al. Citation2018). Similarly, the rate of maternal mortality was very low among this population of patients, indicating an improvement in laboratory tests and imaging techniques leading to early diagnosis (Ramin et al. Citation1995). However, the foetal mortality rate was quite high (10%). A study predicted that gestational trimesters, delayed diagnosis, hypertriglyceridaemia, multiple organ failure, gestational diabetes mellitus and pre-eclampsia are significant predictors of foetal loss (Yang et al. Citation2020). Sun et al. predicted that miscarriages and pre-term infants contributed to foetal loss in the mild group, whereas foetal death and stillbirth contributed to foetal loss in the severe group (Sun et al. Citation2011). The deficit in foetal state monitoring, lack of assessment and management of pregnant women might be the main cause of increased foetal loss of AP during pregnancy (Tang et al. Citation2018). Owing to lack of studies reporting data between severity of AP during pregnancy and maternal and foetal outcomes, a relationship could not be established. However, a study reported that severe AP (44%) was associated with a higher risk of foetal death (Luo et al. Citation2018). Systematic inflammation cytokine explosion is a characteristic of tissue damage in severe AP (Luo et al. Citation2018). A previous study by Sun et al. also indicated that the increased intra-abdominal pressure during severe AP was also associated with a higher risk of foetal death (Sun et al. Citation2015). Furthermore, severe AP during early pregnancy is particularly threatening to foetal life due to the severe onset of the disease (Abdullah et al. Citation2015). Thus, the severity of AP during pregnancy ascertains the risk for neonatal health and maternal and foetal death.
One of the major strengths of this meta-analysis is the inclusion of English and Chinese articles, which gave us an insight to a wider range of studies reporting AP during pregnancy in Chinese population. Secondly, a random effects model was used to pool the data to provide a more conservative estimate. However, there are certain limitations that warranted mention. Owing to the inclusion of limited number of articles that are published in English, a possible bias cannot be eliminated. Also, a limited number of studies assessed the incidences of AP during pregnancy, which could create bias in the analysis and interpretation of results. Occurrence of publication bias cannot be eliminated despite thorough literature search. The pharmacological management of AP during pregnancy could not be assessed because of heterogeneity of treatment reported in various studies. Lastly, limited number of studies reported severity of AP at various trimesters, and thus this parameter could not be assessed.
Conclusion
In conclusion, our study results indicate the lower incidence of AP among Chinese women in the recent years. Analysis reported that hypertriglyceridaemia and biliary pancreatitis still remain the major causes of AP during pregnancy. Moreover, although the rates of maternal mortality have improved with increasing years, AP during pregnancy poses serious threats to the safety of foetus compared with the mother.
Author contributions
Study conception and design: Zhao Haiyan, Peng Na, Gao Yong, Bai Xiumei and Bai Jianying. Acquisition of data: Zhao Haiyan and Peng Na. Analysis and interpretation of data: Zhao Haiyan, Peng Na, Bai Xiumei and Bai Jianying. Drafting of manuscript: Zhao Haiyan and Peng Na. Critical revision: Zhao Haiyan, Peng Na, Gao Yong, Bai Xiumei and Bai Jianying
Supplemental Material
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The authors declare that they have no competing interests.
Data availability statement
Data are available from the author upon request.
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