Abstract
Surgical site infection (SSI) is one of the common postoperative complications after caesarean section for pregnant women. Previous studies have investigated the risk factors for SSI in pregnant women undergoing caesarean delivery. Whereas big differences in research results exist, and the correlation coefficients of different research results are quite different. A meta‐analysis was conducted to examine the risk factors related to SSI in pregnant women undergoing caesarean delivery. We searched English databases to collect case–control studies or cohort studies published between 1 January 2015 and 15 November 2023, including PubMed, Web of Science and ScienceDirect. The risk of bias of the included studies was assessed via Newcastle‐Ottawa Scale. The analysis was performed using RevMan 5.4.1 tool. A total of 24 articles (n = 581, 895) were selected in this meta‐analysis. The following risk factors were presented to be significantly correlated with SSI in pregnant women following caesarean delivery: smoking (odds ratio [OR] = 1.64, 95% confidence interval [CI] [1.31, 2.04]), previous caesarean section (OR = 1.46, 95% CI [1.18, 1.82]), multiple vaginal examinations (OR = 2.92, 95% CI [1.91, 4.46]), membrane rupture (OR = 1.68, 95% CI [1.19, 2.38]), hypertensive disorders (OR = 1.85, 95% CI [1.33, 2.57]), diabetes mellitus (OR = 1.36, 95% CI [1.18, 1.57]), high body mass index (OR = 1.57, 95% CI [1.35, 1.84]). Occurrence of SSI is influenced by a variety of factors. Thus, we should pay close attention to high‐risk subjects and take crucial targeted interventions to lower the SSI risk after caesarean section. Owing to the limited quality and quantity of the included studies, more rigorous studies with adequate sample sizes are needed to verify the conclusion.
Keywords: caesarean section, meta‐analysis, pregnant women, risk factor, wound infection
1. INTRODUCTION
The most common consequence that arises following a caesarean section for a birthing mother is surgical site infection (SSI). It affects either deep, superficial, or organ/space tissues and happens within 30 days following surgery. 1 SSI is a common complication in surgical fields, and they account for increasing postoperative morbidity and deaths, causing significant cost burdens in both low‐income and high‐income countries. 2 SSI is also the major contributor to readmissions after caesarean section. 2 , 3 , 4
Predicted factors related to SSI after caesarean delivery in pregnant women explored by previous studies include obesity, 5 , 6 , 7 gestational diabetes mellitus, 8 hypertension, 9 premature membrane rupture (PROM), 10 chorioamnionitis, 11 emergency procedure, 12 previous caesarean section 13 preterm labour, 14 blood transfusion 15 general anaesthesia 16 , 17 and so on. Whereas big differences in research results exist, and the correlation coefficients of different research results are quite different. Currently, there is no meta‐analysis on the risk factors for SSI in pregnant women. Therefore, this analysis was conducted with the aim to examine significant risk factors as strong evidence support for clinical prevention and intervention in pregnancy following caesarean delivery.
2. METHODS
The present meta‐analysis was performed in accordance with the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses (PRISMA) statement.
2.1. Literature research
A meta‐analysis search of PubMed, Web of Science and Embase was carried out for articles published between 01 January 2014, and 15 November 2023. The keywords included caesarean section [all fields], pregnant women [all fields], SSI [all fields], surgical wound infection [all fields], factor [all fields], risk factor [all fields], predicted factor [all fields].
2.2. Inclusion and exclusion criteria
The inclusion criteria for the study, were as follows: (1) all observational studies (including case–control, cross‐sectional, prospective and retrospective cohort studies); (2) pregnant women undergoing caesarean delivery.
Records were excluded if (1) they did not report risk factors related to surgical site or wound infection after caesarean delivery for pregnancy (2), were duplicates (3), were not published in English or Chinese (4) were review articles or conference abstracts.
2.3. Data extraction and quality evaluation
Two researchers independently screened the literature, performed the quality assessment on the included studies. Also, they extracted data and cross‐checked. We contacted the authors about unclear or missing information when necessary. When screening the literature, the two researchers firstly read the title and abstract and then read the full text to determine whether to include or not. Study characteristics and risk factors correlated to SSI were extracted from the included references. Study characteristics include the following details: publication information, study type, subject size (SSI/non‐SSI) and clinical features.
The Newcastle‐Ottawa Scale (NOS) approach was used to evaluate the quality of the selected literatures during the initial literature screening according to the recommendations by the Cochrane non‐randomized studies methods working group and selection. Details of the NOS are available at https://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. This scale is designed specifically for assessing non‐randomized studies on the basis of: (1) selection of study groups, (2) comparability of study groups and (3) assessment of exposures and outcomes. Two investigators independently assessed the quality of the studies according to the NOS criteria and any differences were resolved by discussion, with arbitration by a third author if differences remained.
2.4. Statistical analysis
The Review Manager software was used for all statistical analyses (RevMan5.4.1). The combined odds ratio (OR) estimates with matching 95% confidence intervals (CIs) were evaluated if the same risk factor was reported in two or more studies. For discontinuous outcomes, the OR was calculated using the original data if it was not stated. In the event where risk factors were found in only one study or that data could not be combined, a descriptive presentation of the findings was used. Heterogeneity among studies was calculated by χ 2 and I 2 tests. The I 2 statistics were used to quantify heterogeneity across trials and the Q‐test (test level α = 0.1) was employed for testing. According to the I 2 value, there was minimal, moderate and high heterogeneity at 25%–50%, 50%–75% and ≥75% respectively. When there was no statistically significant heterogeneity between the studies (p > 0.10 and I 2 < 50%), a fixed‐effects model was run; if not, the source of the heterogeneity was investigated further, and a random‐effects model was run.
3. RESULTS
3.1. Search results
A total of 733 relevant records were obtained in the initial electronic search, including 166 from PubMed, 151 from Web of Science and 416 from Embase. Twenty‐seven studies were imported after removing duplicates and screening the titles and/or abstracts. Of those, studies were excluded due to incomplete data (n = 3). Ultimately, 24 studies were selected for the final analysis. A flowchart of this process is shown in Figure 1.
FIGURE 1.
PRISMA flow diagram of the study selection process for inclusion.
3.2. Characteristics of the included studies
The 24 studies published online between 2015 and 2023 were all case–control studies. Seven studies were conducted in Asia (China, Turkey, India, Egypt, Pero, Thailand), others were performed in Western countries (USA, UK, Australia, Norway, Ireland, Ethiopia, Kosovo, Israel, Brazil). A total of 581, 895 pregnant women were involved, including 9871 patients with SSI and 572 024 without SSI. Additionally, 18 SSI risk factors were reported, including smoking, previous caesarean section, multiple vaginal examinations, membrane rupture, hypertensive disorders, diabetes mellitus, high body mass index (BMI), age ≥30 years, duration of caesarean section ≥1 h, estimated blood loss ≥400/1000 mL, any other chronic illness, general anaesthesia, blood transfusion, chorioamnionitis, emergency procedure, preterm labour, two to three antenatal care visits and delayed antenatal booking. The detailed information is provided in Table 1. The scale of NOS results ranged from 7 and 9 points, and the results of the literature quality evaluation are shown in Table 2.
TABLE 1.
Characteristics of the included studies.
| First author | Year | Country | Study type | Total (n) | SSI (n) | Significantly risk factors |
|---|---|---|---|---|---|---|
| Mezemir 18 | 2023 | Ethiopia | Observational | 741 | 86 | Multiple vaginal examinations, membrane rupture, two to three antenatal care visits, delayed antenatal booking |
| Erritty 5 | 2023 | UK | Case–control | 1682 | 116 | Smoking, high BMI |
| Karaca 6 | 2022 | Turkey | Case–control | 2105 | 62 | High BMI |
| Chaboyer 7 | 2022 | Australia | Case–control | 1459 | 122 | Previous C‐section, high BMI |
| Li 23 | 2021 | China | Case–control | 206 | 48 | High BMI, age ≥30 years, duration of caesarean section ≥1 h, estimated blood loss ≥400/1000 mL |
| Kvalvik 15 | 2021 | Norway | Case–control | 223 | 13 | High BMI, blood transfusion |
| Gupta 24 | 2021 | India | Case–control | 1018 | 679 | Any other chronic illness |
| Alemye 17 | 2021 | Ethiopia | Case–control | 1069 | 156 | General anaesthesia, blood transfusion |
| Scholz 25 | 2021 | Illinois | Case–control | 3637 | 484 | High BMI |
| Gomaa 8 | 2021 | Egypt | Case–control | 15 502 | 828 | Membrane rupture, hypertensive disorders, diabetes mellitus, high BMI duration of caesarean section ≥1 h, estimated blood loss ≥400/1000 mL, chorioamnionitis |
| Ayala 16 | 2021 | Ethiopia | Case–control | 382 | 34 | Hypertensive disorders, general anaesthesia |
| Yerba 19 | 2020 | Pero | Case–control | 4346 | 104 | Multiple vaginal examinations |
| Wang 26 | 2020 | Taiwan | Case–control | 261489 | 3081 | Multiple vaginal examinations |
| Ketema 12 | 2020 | Ethiopia | Case–control | 520 | 61 | Previous C‐section, multiple vaginal examinations, membrane rupture, emergency procedure |
| Saeed 9 | 2019 | Ireland | Case–control | 219859 | 1396 | Membrane rupture, diabetes mellitus |
| MRCPI 27 | 2019 | Ireland | Case–control | 3948 | 81 | Multiple vaginal examinations, hypertensive disorders, high BMI, emergency procedure |
| Molla 11 | 2019 | Ethiopia | Case–control | 334 | 27 | Hypertensive disorders, chorioamnionitis |
| Zejnullahu 13 | 2019 | Kosovo | Case–control | 325 | 32 | Previous C‐section, Any other chronic illness |
| DO 14 | 2018 | USA | Case–control | 2419 | 133 | Smoking, high BMI, general anaesthesia, emergency procedure |
| Krieger 10 | 2017 | Israel | Case–control | 41 375 | 1521 | Previous C‐section, membrane rupture hypertensive disorders diabetes mellitus high BMI |
| Vallejo 28 | 2017 | USA | Case–control | 3349 | 218 | Smoking, hypertensive disorders diabetes mellitus, emergency procedure |
| SHREE 29 | 2016 | USA | Case–control | 2739 | 178 | Chorioamnionitis, smoking |
| MNS 30 | 2016 | Thailand | Case–control | 4988 | 293 | Multiple vaginal examinations, preterm labour |
| Farret 31 | 2015 | Brazil | Case–control | 8180 | 118 | Membrane rupture |
Abbreviations: BMI, body mass index; SSI, surgical site infection.
TABLE 2.
Quality assessment results of Newcastle‐Ottawa scale (NOS) in the included studies.
| Study design | Author | Year | Selection of population | Comparability | Evaluation of exposure or outcome | Total | |||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Case–control | Mezemir | 2023 | * | * | * | * | * | * | * | * | 8* |
| Case–control | Erritty | 2023 | * | * | * | * | * | * | * | * | 8* |
| Case–control | Karaca | 2022 | * | * | * | * | * | No | * | * | 7* |
| Case–control | Chaboyer | 2022 | * | * | * | * | * | ** | * | * | 9* |
| Case–control | Li | 2021 | * | * | * | * | * | No | * | * | 7* |
| Case–control | Kvalvik | 2021 | * | * | * | * | * | ** | * | * | 9* |
| Case–control | Gupta | 2021 | * | * | * | * | * | * | * | * | 8* |
| Case–control | Alemye | 2021 | * | * | * | * | * | ** | * | * | 9* |
| Case–control | Scholz | 2021 | * | * | * | * | * | No | * | * | 7* |
| Case–control | Gomaa | 2021 | * | * | * | * | * | ** | * | * | 9* |
| Case–control | Ayala | 2021 | * | * | * | * | * | No | * | * | 7* |
| Case–control | Yerba | 2020 | * | * | * | * | * | ** | * | * | 9* |
| Case–control | Wang | 2020 | * | * | * | * | * | * | * | * | 8* |
| Case–control | Ketema | 2020 | * | * | * | * | * | * | * | * | 8* |
| Case–control | Saeed | 2019 | * | * | * | * | * | No | * | * | 7* |
| Case–control | MRCPI | 2019 | * | * | * | * | * | ** | * | * | 9* |
| Case–control | Molla | 2019 | * | * | * | * | * | ** | * | * | 9* |
| Case–control | Zejnullahu | 2019 | * | * | * | * | * | ** | * | * | 9* |
| Case–control | DO | 2018 | * | * | * | * | * | * | * | * | 8* |
| Case–control | Krieger | 2017 | * | * | * | * | * | * | * | * | 8* |
| Case–control | Vallejo | 2017 | * | * | * | * | * | No | * | * | 7* |
| Case–control | SHREE | 2016 | * | * | * | * | * | * | * | * | 8* |
| Case–control | MNS | 2016 | * | * | * | * | * | No | * | * | 7* |
| Case–control | Farret | 2015 | * | * | * | * | * | ** | * | * | 9* |
3.3. Synthesis of the results
A total of 18 factors were reported in the 24 studies included in the meta‐analysis. Among them, we performed the meta‐analysis on seven risk factors (smoking, previous caesarean section, multiple vaginal examinations, membrane rupture, hypertensive disorders, diabetes mellitus, high BMI), all of them were statistically significant. The others were only mentioned in less than three studies (age ≥30 years, duration of caesarean section ≥1 h, estimated blood loss ≥400/1000 mL, any other chronic illness, general anaesthesia, blood transfusion, chorioamnionitis, emergency procedure, preterm labour, two to three antenatal care visits, delayed antenatal booking), thus were not synthesized in the meta‐analysis. The results are exhibited in Table 3 and Figures 2, 3, 4, 5, 6, 7, 8.
TABLE 3.
Synthesis results of the risk factors for endometrial cancer patients.
| Risk factor | Number | Heterogeneity test (I 2, p) | Model | Combined OR (95% CI) | p |
|---|---|---|---|---|---|
| Smoking | 4 | I 2 = 0%, p = 0.89 | Fixed | 1.64 [1.31, 2.04] | <0.001 |
| Previous caesarean section | 5 | I 2 = 88%, p < 0.001 | Random | 1.46 [1.18, 1.82] | <0.001 |
| Multiple vaginal examinations | 5 | I 2 = 83%, p < 0.001 | Random | 2.92 [1.91, 4.46] | <0.001 |
| Membrane rupture | 6 | I 2 = 97%, p < 0.001 | Random | 1.68 [1.19, 2.38] | 0.003 |
| Hypertensive disorders | 6 | I 2 = 74%, p < 0.001 | Random | 1.85 [1.33, 2.57] | <0.001 |
| Diabetes mellitus | 4 | I 2 = 58%, p = 0.07 | Random | 1.36 [1.18, 1.57] | <0.001 |
Abbreviations: CI, confidence interval; OR, odds ratio.
FIGURE 2.
Forest plot: Effect of smoking on surgical site infection risk in pregnant women.
FIGURE 3.
Forest plot: Effect of previous caesarean section on surgical site infection risk in pregnant women.
FIGURE 4.
Forest plot: Effect of multiple vaginal examinations on surgical site infection risk in pregnant women.
FIGURE 5.
Forest plot: Effect of membrane rupture on surgical site infection risk in pregnant women.
FIGURE 6.
Forest plot: Effect of hypertensive disorders on surgical site infection risk in pregnant women.
FIGURE 7.
Forest plot: Effect of diabetes mellitus on surgical site infection risk in pregnant women.
FIGURE 8.
Forest plot: Effect of high body mass index on surgical site infection risk in pregnant women.
3.4. Results of meta‐analysis
Four studies reported the relationship between smoking and the SSI risk. There was no heterogeneity in the four studies (I 2 = 0%, p = 0.89). A significant relation between smoking and the SSI risk was observed (OR = 1.64, 95% CI [1.31, 2.04]), p < 0.001; Figure 2).
Five studies discussed the correlation between previous caesarean section and the risk of SSI in pregnancy. A high heterogeneity was observed in the four studies (I 2 = 88%, p < 0.001). There was a significant difference in the estimate of the study effect size (OR = 1.46, 95% CI [1.18, 1.82], p < 0.001; Figure 3).
There were five studies presented the association between multiple vaginal examinations and the SSI risk. A significant heterogeneity was observed between the five studies (I 2 = 83%, p < 0.001). The results showed a statistically association between multiple vaginal examinations and the SSI risk (OR = 2.92, 95% CI [1.91, 4.46], p < 0.001; Figure 4).
Six studies reported the relationship between premature rupture of membrane and the SSI risk. There was a high heterogeneity in the six studies (I 2 = 97%, p < 0.001). Whereas a significant relation between this factor and the SSI risk was observed (OR = 1.68, 95% CI [1.19, 2.38], p = 0.003; Figure 5).
Six studies reported the relationship between hypertensive disorders and the SSI risk. There was a high heterogeneity in the six studies (I 2 = 74%, p < 0.001). Whereas a significant relation between this factor and the SSI risk was observed (OR = 1.85, 95% CI [1.33, 2.57], p < 0.001; Figure 6).
Four studies showed the correlation between diabetes mellitus and the SSI risk. The results presented a moderate heterogeneity in the four studies (I 2 = 58%, p = 0.07). Whereas a significant relation between this factor and the SSI risk was observed (OR = 1.36, 95% CI [1.18, 1.57], p < 0.001; Figure 7).
A total of 10 studies exhibited a significant difference in BMI between patients with SSI and those without SSI. A significant heterogeneity was observed between the 10 studies (I 2 = 92%, p < 0.001). The results showed a statistical association between 1.35, 1.84 and the SSI risk (OR = 1.57, 95% CI [1.35, 1.84], p < 0.001; Figure 8).
4. DISCUSSION
This meta‐analysis evaluated the risk factors for SSI after caesarean section in pregnant women. A total of 24 studies with 581, 895 samples were selected in the analysis. Our findings showed that smoking, previous caesarean section, multiple vaginal examinations, membrane rupture, hypertensive disorders, diabetes mellitus, high BMI were identified as correlated risk factors for SSI after caesarean section in pregnant women with low or moderate heterogeneity between results. Among all the variables analysed, multiple vaginal examinations presented the highest OR for SSI. The present analysis provided evidence support for the targeted prevention and intervention of SSI in pregnancy, thus providing valuable insights into the management of pregnant women.
Our results showed that the emergence of postoperative infection was substantially correlated with the number of vaginal exams performed during labour. This result is in line with research conducted in other countries, such as in Ethiopia, Pero, Ireland and Israel. 9 , 10 , 18 , 19 This may be explained by the fact that the endogenous vaginal microbiota that causes SSI might spread to the upper genital tract through frequent vaginal exams. The risk of SSI was almost twice as high for women with a history of PROM as it was for those without one. The results were confirmed by numerous findings, which also showed a substantial correlation between SSI and PROM. One explanation would be that the amniotic fluid, amniotic membrane and cervical mucus plug act as natural barriers to infection throughout pregnancy. However, when these barriers are compromised due to amniotic fluid losing its sterility, the protective role is compromised. It is also thought that contaminated amniotic fluid can act as a point of entry for bacteria into the skin incision and uterus, thus contributing to the development of chorioamnionitis and related inflammation. 18
Other pregnancy‐related chronic comorbidities, such as hypertensive disorders, diabetes mellitus and high BMI are also significantly linked to the risk of SSI. Molla et al. 11 showed that individuals with pregnancy‐induced hypertension (PIH) had a five‐fold increased risk of developing SSI in comparison to those without PIH. The same results were validated by other investigations. Pregnancy‐induced hypertension has a peripheral vasoconstrictive impact that results in wound hypoperfusion. In situations of PIH that are severe, odema may be present, which could be the source of further organism entry and SSI development. The increased vascular resistance in women with hypertensive disorders may affect peripheral blood supply, which reduces blood supply to skin and subcutaneous tissue, making it more susceptible to infection. This could account for the higher risk of infection in these women. The best management of hypertension during pregnancy may have an impact on peripheral arterial blood flow and microcirculation, which could reduce skin and subcutaneous tissue perfusion and delay wound healing, raising the risk of SSI. 20 , 21
Numerous results have demonstrated a correlation between high BMI and SSI. This may occur from the preventive dose of antibiotics in obese women reaching insufficient quantities in their tissues. 5 , 22 Furthermore, inadequate adipose tissue perfusion may hinder the healing of wounds and lower local immunity, which will promote the growth of infection. Another plausible explanation could be the requirement for extended incisions in patients with obesity, leading to increased tissue contamination. It is important to consider the connection between gestational diabetes mellitus and BMI. Nonetheless, a number of studies have shown that gestational diabetes mellitus is directly connected with an increase in BMI and that women with higher BMIs are at a higher risk of developing GDM than women in the normal range. 22
To our knowledge, this is the first meta‐analysis analysing the risk factors for SSI in pregnant women, providing evidence support for the targeted prevention and intervention of SSI in pregnancy, thus providing valuable insights into the management of pregnant. However, the present review has some limitations. First, a limited quality set of records was gathered for the research due to the dearth of online literature, which partially contributed to publication bias. Second, the majority of studies used sample sizes that were either small or moderate, which suggests that our findings might still be underpowered. Furthermore, four or five research reported on the majority of the synthesized risk factors. This imbalance could have an impact on data synthesis and cause our analysis to be highly heterogeneous. Furthermore, we did not conduct subgroup analysis or funnel plot analysis because of the inadequate source data. Future research on the SSI risk factors in pregnancy should be conducted using large sample sizes of high‐quality longitudinal and multi‐central investigations. This would allow for strong evidence in patient‐related, preoperative and postoperative preventive and care.
5. CONCLUSION
Occurrence of SSI is affected by a variety of factors. Clinical healthcare providers should give high‐risk patients careful consideration and implement effective preventative strategies to reduce the risk of SSI following caesarean delivery. The finding needs to be verified by more rigorous investigations with sufficient sample sizes because of the inadequate quality and quantity of the included studies. Predicted factors supported by evidence should be found in order to prevent SSI.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
Zhu D, Wu Y, Fan L, Liu X. Risk factors related to surgical wound infection after caesarean section: A systematic review and meta‐analysis. Int Wound J. 2024;21(2):e14580. doi: 10.1111/iwj.14580
Dawei Zhu and Yujie Wu contributed equally to this work as co‐first authors equally to this work.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.