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DOI: 10.1055/a-2413-5449
Retrospective Evaluation of C-reactive Protein for Ruling Out Infection After Cesarean Section
Eine retrospektive Evaluierung von CRP-Werten zum Ausschluss von Infektionen nach der Kaiserschnittentbindung
- Abstract
- Zusammenfassung
- Abbreviations
- Introduction
- Materials and Methods
- Results
- Discussion
- Conclusion
- Statements and Declarations
- References
Abstract
Introduction
Infection after cesarean section is a major contributor to maternal morbidity. Measurement of C-reactive protein (CRP) is a laboratory test frequently conducted to rule out or confirm postoperative infection. The present study aimed to evaluate whether CRP is a suitable tool for ruling out infection after cesarean section and whether there are any reliable cut-off values.
Materials and Methods
2056 patients with cesarean section (CS) over a 3-year period were included in a retrospective analysis. Outcome parameters and risk factors for postoperative infection were collected. CRP values from preoperative and postoperative tests were compared. Cut-offs for ruling out infection were assessed.
Results
Among 2056 CSs, postoperative infection occurred in 78 cases (3.8%). The prevalence of infection in emergency CS was lowest, at four out of 134 (2.9%), and the highest prevalence was seen in secondary CS, at 42 of 903 (4.6%; p = 0.35). CRP values in the infection group were significantly higher (preoperative, 1.01 mg/dl vs. 0.62 mg/dl; day 1 postoperative, 7.91 mg/dl vs. 6.44 mg/dl; day 4 postoperative, 8.44 mg/dl vs. 4.09 mg/dl; p = 0.01). A suitable cut-off value for ruling out infection was not identified.
Conclusions
Although CRP values were significantly higher in the infection group, the clinical relevance of this appears to be negligible. CRP testing does not appear to be a reliable tool for diagnosing or ruling out postoperative infection.
Zusammenfassung
Einleitung
Infektionen nach einer Kaiserschnittentbindung tragen wesentlich zur mütterlichen Morbidität bei. Die Messung von C-reaktivem Protein (CRP) ist ein häufig durchgeführter Labortest, um postoperative Infektionen auszuschließen oder zu bestätigen. Ziel dieser Studie war es, herauszufinden, ob CRP ein geeignetes Instrument zum Ausschließen von Infektionen nach einer Kaiserschnittentbindung sein könnte, und ob es verlässliche Cut-off-Werte dafür gibt.
Material und Methoden
Es wurden 2056 mit Kaiserschnitt entbundene Patientinnen über einen Zeitraum von 3 Jahren in die retrospektive Analyse aufgenommen. Outcome-Parameter und Risikofaktoren für eine postoperative Infektion wurden gesammelt. Die CRP-Werte der prä- und postoperativen Tests wurden verglichen. Es wurden Cut-off-Werte für den Ausschluss einer Infektion bewertet.
Ergebnisse
Bei 2056 mit Kaiserschnitt entbundenen Frauen gab es in 78 Fällen (3,8%) eine postoperative Infektion. Die Infektionsprävalenz war beim Notfallkaiserschnitt am niedrigsten mit insgesamt 4 Fällen von 134 Patientinnen (2,9%). Die höchste Prävalenz fand sich bei sekundären Kaiserschnittentbindungen mit 42 aus 903 Fällen (4,6%; p = 0,35). Die CRP-Werte der Infektionsgruppe waren signifikant höher (präoperative Werte: 1,01 mg/dl vs. 0,62 mg/dl; 1. postoperativer Tag: 7,91 mg/dl vs. 6,44 mg/dl; 4. postoperativer Tag: 8,44 mg/dl vs. 4,09 mg/dl; p = 0,01). Es ließ sich aber kein geeigneter Wert identifizieren, der verlässlich Infektionen ausschloss.
Schlussfolgerungen
Obwohl die CRP-Werte in der Infektionsgruppe signifikant höher waren, scheint dessen klinische Relevanz vernachlässigbar. CRP-Tests stellen kein verlässliches Instrument für die Diagnose oder den Ausschluss von postoperativen Infektionen dar.
Schlüsselwörter
C-reaktives Protein - CRP - Kaiserschnittentbindung - Infektion - postoperative WundinfektionAbbreviations
Introduction
Cesarean section (CS) is one of the most frequent major operations worldwide, with a rate that is still rising [1]. The results of the nosocomial infection surveillance system in Germany show that there is an infection rate of 1.8% after CS, with endometritis, wound infections, mastitis, and urinary tract infections being most frequent [2]. The rate of surgical site infection (SSI) after CS ranges from 3% to 15%, and SSI is a major contributor to maternal morbidity [3]. SSI can be categorized as superficial incisional SSI, deep incisional SSI, and organ/space SSI, using the criteria recommended by the Centers for Disease Control and Prevention (CDC) [4]. Risk factors that are associated with a higher risk of SSI are a high body mass index, diabetes, high number of previous CSs, emergency CS, and the surgeon’s grade, among others [5] [6]. Several perioperative strategies and infection control policies have been introduced and evaluated in order to reduce the risk of postoperative infections [7] [8]. Many studies have recommended the use of prophylactic antibiotics to reduce the risk of postpartum endometritis, wound complications, and urinary tract infections [9] [10] [11] [12]. The use of extended-spectrum prophylaxis with azithromycin in nonelective CS is also suggested to further reduce the risk of postpartum infections [13]. Although the optimal timing of antibiotic administration requires careful consideration, due to unknown long-term effects for the neonate when it is carried out before cord clamping, most authors suggest that antibiotics should be given within 60 minutes before surgery if possible [14] [15].
C-reactive protein (CRP) levels increase in response to injury, inflammation, and infection [16] [17]. CRP testing is frequently carried out to exclude or confirm infection. Many studies have investigated the value of postoperative CRP testing after major gastrointestinal surgery [18] [19] [20]. Raised CRP levels are expected after surgery, with peaks 48 hours postoperatively [21] [22]. As the CRP response in patients is highly variable, it does not appear to be a good indicator of the presence of early SSI [21] [23]. Attempts have been made to develop reference ranges, but it is not clear whether these are generally applicable [24]. Nevertheless, CRP testing is still an important tool for monitoring the clinical response to treatment when infection is diagnosed [25]. Investigations of CRP in the postpartum period have shown that levels are higher after CS than after spontaneous birth [26] [27]. To the best of our knowledge, no previous studies have focused on the role of CRP solely after CS.
The aim of the present study was to evaluate the potential of CRP for diagnosing early infection after CS and to determine thresholds for the prevalence of infection, so that early administration of antibiotics can be avoided.
Materials and Methods
Study protocol
A retrospective analysis of patients’ records was conducted using data from the hospital information system (i.s.h. med.; SAP Austria Ltd., Vienna, Austria). All patients who had undergone cesarean sections at Kepler University Hospital, Linz, Austria (formerly Landesfrauenklinik) over a 3-year period were included in the study. Primary CS, in contrast to secondary CS, was defined as CS before the onset of labor or rupture of membranes. Emergency CS is an operation conducted within 20 minutes due to fetal or maternal risk, in accordance with the clinical practice guidelines of the Austrian Society for Gynecology and Obstetrics [28].
Analyzed data
Maternal serum levels of CRP (in mg/dl) were measured using immunochemical testing with a cobas 6000 analyzer (cobas e analyzers; Roche Diagnostics, Mannheim, Germany). Patients underwent routine CRP testing preoperatively and on the first and fourth postoperative days. CRP values ranging up to 0.5 mg/dl are classified as normal. Baseline clinical characteristics and laboratory parameters were recorded. Patients with incomplete data records, intraoperative complications (such as intestinal or urinary lesions), pregnancies with abnormally invasive placenta, and patients needing revision surgery were excluded.
The gestational week was calculated on the basis of crown–rump length using ultrasound during the first trimester. Preterm birth was defined as delivery before 37 + 0 weeks of gestation. Premature rupture of membranes (PROM) is defined as rupture of the amniotic membranes at least 6 hours before onset of labor. Preterm premature rupture of membranes (PPROM) refers to PROM before 37 + 0 weeks of gestation. The diagnosis of gestational diabetes mellitus (GDM) was based on a pathological oral glucose tolerance test with oral administration of 75 g glucose.
During the study period, all women undergoing CS were given antibiotic prophylaxis with parenteral ampicillin/sulbactam (Unasyn, 3 g). Patients with a penicillin allergy were given an alternative (cefuroxime, clindamycin). In patients receiving a primary CS, antibiotic prophylaxis was administered after cord clamping. Patients with PROM received antibiotics, with administration starting 12 hours after rupture of the membranes; in patients with a positive test for group B streptococcus (GBS), antibiotics were started at the onset of labor or premature rupture of the membranes. Patients with PPROM received antibiotics immediately after hospitalization. In secondary or emergency CS, antibiotic prophylaxis was also administered after cord clamping if it had not yet been started for the other reasons mentioned above. Postoperative antibiotic therapy was administered as prescribed by the clinician on duty.
CS was conducted following standard surgical procedures and international guidelines. Povidone-iodine-based solutions were used on a standard basis for antiseptic skin preparation; vaginal disinfection is not routinely conducted. Uterine exteriorization after uterotomy was not performed on a standard basis. Cord traction is used to deliver the placenta.
Early infection was defined as new-onset postoperative infection occurring during days 1–4 after surgery; late infection was defined as infection on days 5–8. Fever was defined as an axillary temperature higher than 38.0 °C.
Statistical analyses
All data for continuous variables were checked for normal distribution (test of normality: Kolmogorov–Smirnov with Lilliefors significance correction, type I error = 10%) and for heteroscedasticity (Levene test, type I error = 5%). Since none of the variables fulfilled the criteria for parametric analysis, subgroup comparisons (infection vs. noninfection; early infection vs. late infection vs. noninfection) were carried out either using the Mann–Whitney U test or with Kruskal–Wallis one-way analysis of variance followed by Nemenyi’s multiple comparisons. Data for categorical variables were compared either using Fisher’s exact test or with the chi-square test (with provision of adjusted residuals).
The suitability of CRP values for predicting early and late infections was checked by means of receiver operating characteristic (ROC) curves; cut-off values were assessed using the Youden index. The robustness of the ROC results was investigated by means of modified bootstrapping approaches (1000 runs per calculation).
The type I error was not adjusted for multiple testing. The results of inferential statistics are therefore only descriptive. Statistical analysis was performed using the open-source R statistical software package, version 3.6.1 (R Foundation for Statistical Computing, Vienna, Austria).
Ethical approval
The study was approved by the local ethics committee of Upper Austria (K-32–13). Due to its retrospective design, the study was not registered in a public trial registry, but it was conducted in accordance with the EQUATOR (Enhancing the QUAlity and Transparency Of health Research) network guidelines.
Results
Study participants and characteristics
During the study period, 9981 deliveries took place at Kepler University Hospital, Linz, and 2186 CSs were performed (21.9%). After application of the exclusion criteria, 2056 patients were enrolled in the study. Postoperative infection was documented in 78 cases (3.8%), with 50 early infections (2.4%) and 28 late infections (1.4%). Out of this group, 42 patients (53.8%) had postoperative fever without any special focus of infection, 21 (26.9%) showed SSI or infected hematoma, mastitis occurred in eight patients (10.3%), and urinary tract infection in seven patients (9.0%). There were no documented cases of endometritis. The rate of infections was stable over the study period, varying from 3.1% to 4.9% (p = 0.22).
Of the 2056 patients, 973 (47.3%) underwent primary CS, 945 (46.0%) secondary CS, and 138 (6.7%) had an emergency CS. The prevalence of infection in the study group was lowest among emergency CSs, at four of 134 (2.9%), in comparison with 32 of 941 (3.4%) in the primary CS group and 42 of 903 (4.6%) in the secondary CS group, but there were no significant correlations (p = 0.35).
Associations between maternal and pregnancy characteristics and the occurrence of postoperative infection are presented in [Table 1]. A significant correlation was observed between postoperative complications such as hematoma, paralytic ileus, and wound dehiscence and infection (p < 0.01). There were no significant associations between other risk factors that were investigated.
Among the 2056 patients, 339 (16.5%) received antibiotics within the first four postoperative days and 184 (9.0%) within postoperative days 4–8.
Parameters and outcomes
Preoperative and postoperative CRP and leukocyte values are listed in [Table 2]. The mean CRP level was significantly higher in the infection group preoperatively and postoperatively (p = 0.01). A similar trend was seen in the leukocyte values, with significant results only being observed on the fourth day after CS (p = 0.01). In view of the unequal size samples, a subgroup analysis comparing postoperative CRP and leukocyte measurements between early and late infection was also conducted. The results are presented in [Table 3], showing significant results on the first postoperative day (p < 0.05).
The suitability of CRP values for predicting early and late infections was checked using ROC curves, which are shown in [Fig. 1] and [Fig. 2]. On the basis of the Youden index, a cut-off value of 6.7 mg/dl was calculated for the first postoperative day ([Fig. 1]), with a sensitivity of 68% (95% CI, 53.3 to 80.5) and a specificity of 60.87% (95% CI, 58.8 to 63.0) (p < 0.01). The cut-off value calculated for the fourth postoperative day ([Fig. 2]) was 7.3 mg/dl, with a sensitivity of 34.78% (95% CI, 16.4 to 57.3) and a specificity of 91.81% (95% CI, 90.4 to 93.1) (p = 0.02).
Discussion
In the group of patients included in the study, those with postoperative infection after CS were found to have significantly higher CRP values than those without infection. However, the clinical relevance of this is unclear. The mean CRP on the first postoperative day in the infection group was 7.91 mg/dl, in comparison with 6.44 mg/dl in the group with no infection, so that the differences are small. This might be due to unequal size samples, with only 78 infections out of a total of 2056 cesarean deliveries. A subgroup analysis of early infection versus late infection was carried out in addition, to provide similar sample sizes, but the differences in the CRP values were also negligible in that subgroup ([Table 3]).
An attempt was made using ROC analysis to identify an optimal cut-off value for CRP in order to rule out infection after CS. A bootstrap approach was used in view of the dissimilar sample sizes. As [Fig. 1] and [Fig. 2] show, there are no valid cut-off values for ruling out infection using CRP testing on either the first or fourth postoperative days.
In clinical management, CRP levels are frequently tested routinely after surgery. As the present data confirmed, an elevated CRP value does not always correlate with the occurrence of clinical infection. Preoperatively and on postoperative day 1, the maximum CRP values were observed in the group without infection. Clinicians’ awareness of postoperative CRP test values may influence their decision-making regarding antibiotic administration, and this should be avoided. In particular, inexperienced residents might initiate antibiotic therapy purely because of laboratory results, which would be inappropriate and could lead to the development of resistance mechanisms [29] [30]. This situation is also reflected in the data from the present study. Although only 78 patients had clinical signs of infection, antibiotics were administered in 339 cases during postoperative days 1–4 and in 184 cases during postoperative days 5–8. Whether or not to administer antibiotic therapy lies in the responsibility of the clinician who is on duty. Preoperatively initiated antibiotic therapy might therefore continue for several days after CS if there is a specific condition such as intrapartum fever, foul-smelling amniotic fluid or membranes, or PPROM [31]. In some cases, the clinician may also initiate antibiotic therapy due to raised postoperative inflammatory parameters, without any clinical signs of infection. Clinicians need to bear in mind that raised CRP levels may simply be evoked by tissue damage during the operation [17]. This study shows that postoperative CRP testing should in fact not be carried out routinely after CS, in order to avoid misinterpreting the laboratory results. A nonspecific increase in inflammation levels without a clinical focus is one of the main reasons for the administration of antibiotic therapy, which should be avoided if clinical grounds for it are lacking [32]. However, CRP does have an important role for monitoring or assessing the severity of confirmed infection and for guiding further therapy [25].
This study shows that infections after CS are rather rare, with an overall prevalence of 3.8% in this group of patients. It should be mentioned that urinary tract infections and puerperal mastitis were also included in the infection group, accounting for 19.3% of all infections. The fact that no cases of endometritis were diagnosed in the analysis is not reflected in the findings of other studies, in which endometritis appears to be a fairly frequent cause of postpartum infection [33]. The reason for this might be that in the present group of patients there were 42 women with fever, but without any specific focus of infection. Antibiotic therapy was started in these cases, leading to rapid recovery, so that classic symptoms of endometritis such as uterine tenderness or purulent lochia did not occur and the diagnosis was not confirmed.
The rate of CS during the study period was 21.9% of all deliveries. It should be mentioned that Kepler University Hospital is a tertiary center in Austria, in which many women with high-risk pregnancies are treated. In contrast to other studies that have suggested higher infection rates following emergency CS, the prevalence of infection among emergency cesarean sections was lowest in the study group, at four out of 134 (2.9%) [34]. This might be explained by the fact that 30 of 134 patients who underwent emergency cesareans (22.4%) had PROM/PPROM, so that antibiotics had already been administered before surgery.
Increasing rates of CS — leading to higher rates of repeat cesarean deliveries — should also be mentioned at this point. Severe intraperitoneal and intrauterine adhesions may occur more often after a history of postoperative infection, resulting in more intraoperative complications, prolonged hospital stays, and increased postoperative pain. In addition, intrauterine adhesions may lead to decreased pregnancy rates and require hysteroscopic treatment [35] [36].
Strengths and limitations
To the best of our knowledge, this study is the first to focus on CRP solely after CS. The strength of the study is that a large number of patients with CS were included, and the results can therefore be used to guide clinical management, avoiding testing for CRP routinely after CS when there are no signs of infection. The postpartum period is a vulnerable phase for all women, so that adequate management and treatment are indispensable. The present study also has inherent limitations associated with its retrospective design. The fact that endometritis is a common infection after CS is not reflected in the number of cases. This might be because of another limitation, as the clinicians treating the patients were not blinded to the CRP values. Their knowledge could potentially have influenced decision-making, which can be seen in the large number of patients receiving antibiotic therapy without clinical signs of infection. Another problem is that the dissimilar sample sizes only allow limited interpretation of the data collected. Prospective, randomized studies on CRP testing after cesarean section are warranted.
Conclusion
C-reactive protein testing after cesarean sections appears to have limited value for diagnosing postoperative infection. Clinicians should bear in mind that decision-making on initiating antibiotic therapy should be based on clinical criteria and not on laboratory findings alone. However, CRP can be used to monitor the clinical response to treatment and assess the severity of infection.
Statements and Declarations
Details of ethics approval
The study was approved by the local ethics committee of Upper Austria (K-32–13).
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Contributorsʼ Statement
SE: conceptualization, project administration, data curation, validating and writing original draft. PO: review and editing. RBM: conceptualization, methodology, and project administration. EB: data curation and writing original draft. PST: conceptualization, data curation, review, and editing.
Conflict of Interest
The authors declare that they have no conflict of interest.
Acknowledgement
The authors gratefully acknowledge the contribution of Eva Lunzer-Muehl and Georg Gruessenberger for their support in data collection.
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References
- 1 Betrán AP, Ye J, Moller AB. et al. The Increasing Trend in Caesarean Section Rates: Global, Regional and National Estimates: 1990–2014. PloS One 2016; 11: e0148343
- 2 Gastmeier P, Brandt C, Sohr D. et al. [Surgical site infections in hospitals and outpatient settings. Results of the German nosocomial infection surveillance system (KISS)]. Bundesgesundheitsbl – Gesundheitsforsch – Gesundheitsschutz 2004; 47: 339-344
- 3 Schneid-Kofman N, Sheiner E, Levy A. et al. Risk factors for wound infection following cesarean deliveries. Int J Gynaecol Obstet 2005; 90: 10-15
- 4 Mangram AJ, Horan TC, Pearson ML. et al. Guideline for Prevention of Surgical Site Infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control 1999; 27: 97-132
- 5 Wloch C, Wilson J, Lamagni T. et al. Risk factors for surgical site infection following caesarean section in England: results from a multicentre cohort study. BJOG 2012; 119: 1324-1333
- 6 Moulton LJ, Eric Jelovsek J, Lachiewicz M. et al. A model to predict risk of postpartum infection after Caesarean delivery. J Matern Fetal Neonatal Med 2018; 31: 2409-2417
- 7 Martin EK, Beckmann MM, Barnsbee LN. et al. Best practice perioperative strategies and surgical techniques for preventing caesarean section surgical site infections: a systematic review of reviews and meta-analyses. BJOG 2018; 125: 956-964
- 8 Hsu CD, Cohn I, Caban R. Reduction and sustainability of cesarean section surgical site infection: An evidence-based, innovative, and multidisciplinary quality improvement intervention bundle program. Am J Infect Control 2016; 44: 1315-1320
- 9 Bratzler DW, Dellinger EP, Olsen KM. American Society of Health-System Pharmacists, Infectious Disease Society of America, Surgical Infection Society, Society for Healthcare Epidemiology of America. et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Am J Health Syst Pharm 2013; 70: 195-283
- 10 Berríos-Torres SI, Umscheid CA, Bratzler DW. et al. Centers for Disease Control and Prevention Guideline for the Prevention of Surgical Site Infection, 2017. JAMA Surg 2017; 152: 784
- 11 Smaill FM, Grivell RM. Antibiotic prophylaxis versus no prophylaxis for preventing infection after cesarean section. Cochrane Database Syst Rev 2014; (10) CD007482
- 12 Practice Bulletin No. 199: Use of Prophylactic Antibiotics in Labor and Delivery: Correction. Obstet Gynecol [Anonym]. 2019; 134: 883-884
- 13 Tita AT, Szychowski JM, Boggess K. et al. Adjunctive Azithromycin Prophylaxis for Cesarean Delivery. N Engl J Med 2016; 375: 1231-1241
- 14 Bollig C, Nothacker M, Lehane C. et al. Prophylactic antibiotics before cord clamping in cesarean delivery: a systematic review. Acta Obstet Gynecol Scand 2018; 97: 521-535
- 15 Jyothirmayi CA, Halder A, Yadav B. et al. A randomized controlled double blind trial comparing the effects of the prophylactic antibiotic, Cefazolin, administered at caesarean delivery at two different timings (before skin incision and after cord clamping) on both the mother and newborn. BMC Pregnancy Childbirth 2017; 17: 340
- 16 Sproston NR, Ashworth JJ. Role of C-Reactive Protein at Sites of Inflammation and Infection. Front Immunol 2018; 9: 754
- 17 Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest 2003; 111: 1805-1812
- 18 Gans SL, Atema JJ, van Dieren S. et al. Diagnostic value of C-reactive protein to rule out infectious complications after major abdominal surgery: a systematic review and meta-analysis. Int J Colorectal Dis 2015; 30: 861-873
- 19 Noble F, Curtis NJ, Underwood TJ. C-reactive protein 2 days after laparoscopic gastric bypass surgery reliably indicates leaks and moderately predicts morbidity. J Gastrointest Surg 2013; 17: 844-845
- 20 Santonocito C, De Loecker I, Donadello K. et al. C-reactive protein kinetics after major surgery. Anesth Analg 2014; 119: 624-629
- 21 Colley CM, Fleck A, Goode AW. et al. Early time course of the acute phase protein response in man. J Clin Pathol 1983; 36: 203-207
- 22 Cole DS, Watts A, Scott-Coombes D. et al. Clinical utility of peri-operative C-reactive protein testing in general surgery. Ann R Coll Surg Engl 2008; 90: 317-321
- 23 Giannoudis PV, Smith MR, Evans RT. et al. Serum CRP and IL-6 levels after trauma. Not predictive of septic complications in 31 patients. Acta Orthop Scand 1998; 69: 184-188
- 24 Lindberg M, Hole A, Johnsen H. et al. Reference intervals for procalcitonin and C-reactive protein after major abdominal surgery. Scand J Clin Lab Invest 2002; 62: 189-194
- 25 Khan KS, Wojdyla D, Say L. et al. WHO analysis of causes of maternal death: a systematic review. Lancet 2006; 367: 1066-1074
- 26 Mertens K, Muys J, Jacquemyn Y. Postpartum C-Reactive Protein: A limited value to detect infection or inflammation. Facts Views Vis Obgyn 2019; 11: 243-250
- 27 Skarżyńska E, Zborowska H, Jakimiuk AJ. et al. Variations in serum concentrations of C-reactive protein, ceruloplasmin, lactoferrin and myeloperoxidase and their interactions during normal human pregnancy and postpartum period. J Trace Elem Med Biol 2018; 46: 83-87
- 28 AWMF Leitlinienprogramm, Deutsche Gesellschaft für Gynäkologie und Geburtshilfe (DGGG), Österreichische Gesellschaft für Gynäkologie und Geburtshilfe (OEGGG), Schweizerische Gesellschaft für Gynäkologie und Geburtshilfe (SGGG). Sectio caesarea. AWMF-Registernummer 015–084, Leitlinienklasse S3, Version 1.0. Berlin: Arbeitsgemeinschaft der Wissenschaftlichen Medizinischen Fachgesellschaften (AWMF). 2020 Accessed January 14, 2021 at: https://www.awmf.org/leitlinien/detail/ll/015–084.html
- 29 Mohr KI. History of Antibiotics Research. Curr Top Microbiol Immunol 2016; 398: 237-272
- 30 Karam G, Chastre J, Wilcox MH. et al. Antibiotic strategies in the era of multidrug resistance. Crit Care 2016; 20: 136
- 31 Romero R, Chaemsaithong P, Korzeniewski SJ. et al. Clinical chorioamnionitis at term III: how well do clinical criteria perform in the identification of proven intra-amniotic infection?. J Perinat Med 2016; 44: 23-32
- 32 Knoke J, Raab R, Geyer K. et al. Antibiotic Treatment During Pregnancy and the First Six Months Postpartum – a Secondary Analysis of the “Healthy Living in Pregnancy” (GeliS) Study. Geburtshilfe Frauenheilkd 2023; 83: 850-861
- 33 Mackeen AD, Packard RE, Ota E. et al. Antibiotic regimens for postpartum endometritis. Cochrane Database Syst Rev 2015; (02) CD001067
- 34 Martens MG, Kolrud BL, Faro S. et al. Development of wound infection or separation after cesarean delivery. Prospective evaluation of 2,431 cases. J Reprod Med 1995; 40: 171-175
- 35 Aboshama RA, Taha OT, Abdel Halim HW. et al. Prevalence and risk factor of postoperative adhesions following repeated cesarean section: A prospective cohort study. Int J Gynaecol Obstet 2023; 161: 234-240
- 36 Urman B, Yakin K, Ertas S. et al. Fertility and anatomical outcomes following hysteroscopic adhesiolysis: An 11-year retrospective cohort study to validate a new classification system for intrauterine adhesions (Urman-Vitale Classification System). Int J Gynaecol Obstet 2024; 165: 644-654
Correspondence
Publication History
Received: 14 July 2024
Accepted after revision: 10 September 2024
Article published online:
07 November 2024
© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/).
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References
- 1 Betrán AP, Ye J, Moller AB. et al. The Increasing Trend in Caesarean Section Rates: Global, Regional and National Estimates: 1990–2014. PloS One 2016; 11: e0148343
- 2 Gastmeier P, Brandt C, Sohr D. et al. [Surgical site infections in hospitals and outpatient settings. Results of the German nosocomial infection surveillance system (KISS)]. Bundesgesundheitsbl – Gesundheitsforsch – Gesundheitsschutz 2004; 47: 339-344
- 3 Schneid-Kofman N, Sheiner E, Levy A. et al. Risk factors for wound infection following cesarean deliveries. Int J Gynaecol Obstet 2005; 90: 10-15
- 4 Mangram AJ, Horan TC, Pearson ML. et al. Guideline for Prevention of Surgical Site Infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control 1999; 27: 97-132
- 5 Wloch C, Wilson J, Lamagni T. et al. Risk factors for surgical site infection following caesarean section in England: results from a multicentre cohort study. BJOG 2012; 119: 1324-1333
- 6 Moulton LJ, Eric Jelovsek J, Lachiewicz M. et al. A model to predict risk of postpartum infection after Caesarean delivery. J Matern Fetal Neonatal Med 2018; 31: 2409-2417
- 7 Martin EK, Beckmann MM, Barnsbee LN. et al. Best practice perioperative strategies and surgical techniques for preventing caesarean section surgical site infections: a systematic review of reviews and meta-analyses. BJOG 2018; 125: 956-964
- 8 Hsu CD, Cohn I, Caban R. Reduction and sustainability of cesarean section surgical site infection: An evidence-based, innovative, and multidisciplinary quality improvement intervention bundle program. Am J Infect Control 2016; 44: 1315-1320
- 9 Bratzler DW, Dellinger EP, Olsen KM. American Society of Health-System Pharmacists, Infectious Disease Society of America, Surgical Infection Society, Society for Healthcare Epidemiology of America. et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Am J Health Syst Pharm 2013; 70: 195-283
- 10 Berríos-Torres SI, Umscheid CA, Bratzler DW. et al. Centers for Disease Control and Prevention Guideline for the Prevention of Surgical Site Infection, 2017. JAMA Surg 2017; 152: 784
- 11 Smaill FM, Grivell RM. Antibiotic prophylaxis versus no prophylaxis for preventing infection after cesarean section. Cochrane Database Syst Rev 2014; (10) CD007482
- 12 Practice Bulletin No. 199: Use of Prophylactic Antibiotics in Labor and Delivery: Correction. Obstet Gynecol [Anonym]. 2019; 134: 883-884
- 13 Tita AT, Szychowski JM, Boggess K. et al. Adjunctive Azithromycin Prophylaxis for Cesarean Delivery. N Engl J Med 2016; 375: 1231-1241
- 14 Bollig C, Nothacker M, Lehane C. et al. Prophylactic antibiotics before cord clamping in cesarean delivery: a systematic review. Acta Obstet Gynecol Scand 2018; 97: 521-535
- 15 Jyothirmayi CA, Halder A, Yadav B. et al. A randomized controlled double blind trial comparing the effects of the prophylactic antibiotic, Cefazolin, administered at caesarean delivery at two different timings (before skin incision and after cord clamping) on both the mother and newborn. BMC Pregnancy Childbirth 2017; 17: 340
- 16 Sproston NR, Ashworth JJ. Role of C-Reactive Protein at Sites of Inflammation and Infection. Front Immunol 2018; 9: 754
- 17 Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest 2003; 111: 1805-1812
- 18 Gans SL, Atema JJ, van Dieren S. et al. Diagnostic value of C-reactive protein to rule out infectious complications after major abdominal surgery: a systematic review and meta-analysis. Int J Colorectal Dis 2015; 30: 861-873
- 19 Noble F, Curtis NJ, Underwood TJ. C-reactive protein 2 days after laparoscopic gastric bypass surgery reliably indicates leaks and moderately predicts morbidity. J Gastrointest Surg 2013; 17: 844-845
- 20 Santonocito C, De Loecker I, Donadello K. et al. C-reactive protein kinetics after major surgery. Anesth Analg 2014; 119: 624-629
- 21 Colley CM, Fleck A, Goode AW. et al. Early time course of the acute phase protein response in man. J Clin Pathol 1983; 36: 203-207
- 22 Cole DS, Watts A, Scott-Coombes D. et al. Clinical utility of peri-operative C-reactive protein testing in general surgery. Ann R Coll Surg Engl 2008; 90: 317-321
- 23 Giannoudis PV, Smith MR, Evans RT. et al. Serum CRP and IL-6 levels after trauma. Not predictive of septic complications in 31 patients. Acta Orthop Scand 1998; 69: 184-188
- 24 Lindberg M, Hole A, Johnsen H. et al. Reference intervals for procalcitonin and C-reactive protein after major abdominal surgery. Scand J Clin Lab Invest 2002; 62: 189-194
- 25 Khan KS, Wojdyla D, Say L. et al. WHO analysis of causes of maternal death: a systematic review. Lancet 2006; 367: 1066-1074
- 26 Mertens K, Muys J, Jacquemyn Y. Postpartum C-Reactive Protein: A limited value to detect infection or inflammation. Facts Views Vis Obgyn 2019; 11: 243-250
- 27 Skarżyńska E, Zborowska H, Jakimiuk AJ. et al. Variations in serum concentrations of C-reactive protein, ceruloplasmin, lactoferrin and myeloperoxidase and their interactions during normal human pregnancy and postpartum period. J Trace Elem Med Biol 2018; 46: 83-87
- 28 AWMF Leitlinienprogramm, Deutsche Gesellschaft für Gynäkologie und Geburtshilfe (DGGG), Österreichische Gesellschaft für Gynäkologie und Geburtshilfe (OEGGG), Schweizerische Gesellschaft für Gynäkologie und Geburtshilfe (SGGG). Sectio caesarea. AWMF-Registernummer 015–084, Leitlinienklasse S3, Version 1.0. Berlin: Arbeitsgemeinschaft der Wissenschaftlichen Medizinischen Fachgesellschaften (AWMF). 2020 Accessed January 14, 2021 at: https://www.awmf.org/leitlinien/detail/ll/015–084.html
- 29 Mohr KI. History of Antibiotics Research. Curr Top Microbiol Immunol 2016; 398: 237-272
- 30 Karam G, Chastre J, Wilcox MH. et al. Antibiotic strategies in the era of multidrug resistance. Crit Care 2016; 20: 136
- 31 Romero R, Chaemsaithong P, Korzeniewski SJ. et al. Clinical chorioamnionitis at term III: how well do clinical criteria perform in the identification of proven intra-amniotic infection?. J Perinat Med 2016; 44: 23-32
- 32 Knoke J, Raab R, Geyer K. et al. Antibiotic Treatment During Pregnancy and the First Six Months Postpartum – a Secondary Analysis of the “Healthy Living in Pregnancy” (GeliS) Study. Geburtshilfe Frauenheilkd 2023; 83: 850-861
- 33 Mackeen AD, Packard RE, Ota E. et al. Antibiotic regimens for postpartum endometritis. Cochrane Database Syst Rev 2015; (02) CD001067
- 34 Martens MG, Kolrud BL, Faro S. et al. Development of wound infection or separation after cesarean delivery. Prospective evaluation of 2,431 cases. J Reprod Med 1995; 40: 171-175
- 35 Aboshama RA, Taha OT, Abdel Halim HW. et al. Prevalence and risk factor of postoperative adhesions following repeated cesarean section: A prospective cohort study. Int J Gynaecol Obstet 2023; 161: 234-240
- 36 Urman B, Yakin K, Ertas S. et al. Fertility and anatomical outcomes following hysteroscopic adhesiolysis: An 11-year retrospective cohort study to validate a new classification system for intrauterine adhesions (Urman-Vitale Classification System). Int J Gynaecol Obstet 2024; 165: 644-654