DOI: 10.1111/1471-0528.12696

Systematic review

www.bjog.org

Chewing gum in preventing postoperative ileus in women undergoing caesarean section: a systematic review and meta-analysis of randomised controlled trials L Craciunas,a MS Sajid,a AS Ahmedb a Department of Laparoscopic Colorectal Surgery, Worthing Hospital, Worthing, UK b Department of Gynaecological Oncology, The Christie NHS Foundation Trust, Manchester, UK Correspondence: L Craciunas, Surgical Senior House Officer, Worthing Hospital, Worthing, West Sussex BN11 2DH, UK. Email [email protected]

Accepted 20 November 2013. Published Online 14 March 2014.

Background The incidence of postoperative ileus (POI) after

gynaecological surgery is 10–15% Chewing gum following general surgery improves outcomes, including early flatus, early bowel sounds, and shortening of hospitalisation periods. There is currently no guideline that supports the use of chewing gum after caesarean sections. Objectives To systematically analyse the published randomised

controlled trials regarding the effectiveness of chewing gum in preventing POI in women undergoing caesarean sections. Search strategy Systematic search of medical databases up to

March 2013. Selection criteria Randomised controlled trials that reported the

role of chewing gum in preventing POI in women undergoing caesarean sections. Data collection and analysis Two authors independently identified

and analysed it systematically using REVMAN. The combined outcome was expressed as an odds ratio and standardised mean difference. Main results Seven randomised controlled trials involving 1462 women (728 in the chewing gum group, 734 controls) were systematically analysed. There was significant heterogeneity (v2 = 29.02, df = 7; P < 0.0001; I2 = 76%) among the included trials. Among women undergoing caesarean sections, chewing gum reduced the risk of POI (odds ratio 0.36; 95% confidence interval 0.19–0.69; z = 3.08; P < 0.002) but did not affect duration of hospitalisation (P = 0.32). Conclusions Chewing gum for 30–60 minutes at least three times

a day appears to be effective in reducing the incidence and consequences of POI following caesarean sections. Keywords Caesarean section, chewing gum, postoperative ileus.

the relevant studies for inclusion, extracted outcome-related data, Please cite this paper as: Craciunas L, Sajid MS, Ahmed AS. Chewing gum in preventing postoperative ileus in women undergoing caesarean section: a systematic review and meta-analysis of randomised controlled trials. BJOG 2014;121:793–800.

Introduction Postoperative ileus (POI) refers to severe constipation and intolerance of oral intake resulting from a nonmechanical insult that disrupts the normal coordinated propulsive motor activity of the gastrointestinal tract.1–3 There is general consensus among surgeons that some degree of POI is a normal, obligatory and physiological response to abdominal surgery.3–5 Paralytic ileus may be caused by nonabdominal surgery and other mechanisms, such as knee surgery, pelvic surgery, spinal surgery, drug use, basal lung consolidation and localised or generalised peritonitis.3–5 In the USA, POI is estimated to cost between $5000 and

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$10 000 or a total of $1 billion per year due to discomfort, prolonged hospital stay and increased treatment costs.6 The incidence of POI after gynaecological surgery has a mean incidence of 10–15% (range of 5–25%).7–12 The aetiology and pathogenesis of POI is multifactorial; therefore, a multimodal approach is required to counteract the morbidity of POI. These measures include preoperative optimisation; gentle bowel handling; early feeding; avoidance of nonessential use of nasogastric tubes; thoracic epidural analgesia; use of pharmacological agents such as water-soluble contrast agents, alvimopan (a selective l-receptor opioid antagonist), misoprostol and ketorolac; and gum chewing.3,13–20

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Chewing gum has recently been used as a form of sham feeding to stimulate the acceleration of gut function after abdominal surgery,21,22 leading to both humoral and nervous stimulation of bowel motility. This response occurs after chewing to prepare the gut for food.23 Chewing gum after elective intestinal resection has been associated with various improved outcomes, including early flatus, early bowel sounds and shorter lengths of hospitalisation.21,22 Studies have reported conflicting results regarding the effectiveness of chewing gum for the prevention of POI. In addition, insufficient data are available on the reduced rate of clinical complications or reduced cost.21 There is currently no guideline to support the use of chewing gum for preventing POI in obstetrics and gynaecology despite an increasing interest towards its use in colorectal surgery. The objective of this study was to systematically analyse the published randomised controlled trials examining the effectiveness of chewing gum in preventing POI in women undergoing caesarean sections.

Methods The meta-analysis included appropriate prospective, randomised controlled trials (irrespective of type, language, blinding, sample size or publication status) on the use of postoperative gum chewing following caesarean sections. The trials were indexed before March 2013, The databases searched were The Cochrane Pregnancy and Childbirth Group Controlled Trial Register, the Cochrane Central Register of Controlled Trials (CENTRAL) in The Cochrane Library, Medline, EMBASE and the Science Citation Index. The search was performed up to March 2013. The medical subject headings (MeSH) terms used were ‘chewing gum’, ‘caesarean section’ and ‘postoperative ileus’. The ‘related citations’ function was used to broaden the search criteria and to include additional studies in order to screen all abstracts, comparative studies and nonrandomised trials to allow a complete literature search. Further search of the reference lists of the included studies was conducted to find additional trials. Two of the authors independently performed the literature search, extracted data related to the outcomes, and stored the data on a secured database. A third author found no discrepancies when the data were assessed. Data analysis was performed using the software package 24 REVMAN 5.2, provided by the Cochrane Collaboration.25 For binary data variables, the odds ratio (OR) with a 95% confidence interval (CI) was calculated and the summated outcomes of the continuous variables were expressed as a standardised mean difference (SMD). The guidelines of the Cochrane Collaboration25 were used to calculate the standard deviation (SD) in cases where it was not available.

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Heterogeneity was evaluated using the chi-square test, with significance set at P < 0.05, and quantified26 using I2. In case of significant heterogeneity only the results of the random effects model were reported. The Mantel–Haenszel method was used for the calculation of OR under the fixed effect model.27 The estimate of the difference between both techniques was pooled depending upon the effect weights in the results, as determined by each trial estimate variance. The results from the meta-analysis were presented as forest plots. The quality of the included trials was assessed using the Cochrane Risk of Bias tool and later on the summary of the evidence was generated using GRADEPRO,28 a tool provided by the Cochrane Collaboration.

Results The PRISMA flow chart to explain the study methodology, literature search and trial selection is shown in Figure 1. The summary of the evidence generated using GRADEPRO is presented in Figure 2. Seven randomised controlled trials29–35 evaluating a total of 1462 women allocated to either a chewing gum group or a control group for reporting the role of chewing gum in the prevention of POI following caesarean sections were retrieved from electronic databases. There were 728 women in the chewing gum groups and 734 women in the control groups. The characteristics of the included trials are shown in Table S1 (see the Supporting information), and the treatment protocols used for the women in all of the trials are shown in Table S2 (see the Supporting information). Variables used to achieve a combined outcome are shown in Table S3 (see the Supporting information). We used the published data of one trial31 reporting data on three arms (control, sugar-free gum and sugar-substituted gum) as two trials. Other confounding factors of early recovery such as early mobilisation, physiotherapy and other associated comorbidities were not adequately reported in the included trials.

Methodological quality of included studies Based upon the use of the Cochrane Risk of Bias tool, the quality of most of the included studies was moderate to poor because of inadequate concealment technique and blinding (see the Supporting information, Table S4). The combined outcome of all of the variables is given below.

Time to first flatus There was significant heterogeneity (v2 = 29.02, df = 7; P < 0.0001; I2 = 76%) among the trials. The time to first flatus following chewing gum use was significantly less than that in the control group (SMD 0.52; 95% CI 0.75 to 0.28; z = 4.27; P < 0.0001; see the Supporting information, Figure S1A).

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Identification

Role of chewing gum following caesarean section

Records identified through database searching (n = 216)

Additional records identified through other sources (n = 33)

Eligibility

Screening

Records after duplicates removed (n = 224)

Records screened (n = 68)

Full-text articles assessed for eligibility (n = 46)

Records excluded (n = 22)

Full-text articles excluded (n = 27; not relevant to study) (n = 12; involved non-caesarean section patients)

Included

Studies included in qualitative synthesis (n = 7)

Studies included in quantitative synthesis (meta-analysis) (n = 7)

Figure 1. PRISMA flow chart showing trial selection methodology.

Time to first bowel sounds 29–31,33–35

Six trials contributed to the combined calculation of this outcome. There was significant heterogeneity (v2 = 95.91, df = 6; P < 0.00001; I2 = 94%) among the trials. The time to first bowel sounds in the chewing gum group was significantly less than that in the control group (SMD 0.96; 95% CI 1.43 to 0.49; z = 3.97; P < 0.0001; Figure S1B).

Time to first defaecation Five trials29–31,34,35 contributed to the combined calculation of this outcome. There was significant heterogeneity (v2 = 54.33, df = 5; P < 0.00001; I2 = 91%) among the included trials. Compared with the control group, the chewing gum group was associated with a significantly shorter time to first defaecation (SMD 0.53; 95% CI 0.94 to 0.12; z = 2.54; P < 0.01; Figure S1C).

Requirement of enemas for flatus and antiemetics Only one trial33 reported on these outcomes. The requirement for an enema to enable passing the first flatus and antiemetics was significantly less in the chewing gum group than in the control group.

df = 2; P = 0.27; I2 = 24%) among these trials. Compared with control groups, chewing gum was associated with significantly fewer occurrences of ileus (OR 0.36; 95% CI 0.19–0.69; z = 3.08; P < 0.002; Figure S1D).

Length of hospital stay Five trials29,31–33,35 contributed to the combined calculation of this outcome. There was significant heterogeneity (v2 = 57.47, df = 5; P < 0.00001; I2 = 91%) among the trials. Compared with the control groups, chewing gum was associated with shorter lengths of hospitalisation (SMD 0.26; 95% CI 0.76 to 0.25; z = 1.00; P = 0.32; Figure S1E), but the difference was not statistically significant.

Subgroup analysis We analysed all high-quality trials29,32,34,35 and we did not find any difference in overall conclusion. Data were insufficient for subgroup analysis based on causes of heterogeneity (Table 1).

Discussion

Postoperative ileus

Main findings

Three trials29,30,35 contributed to the combined calculation of this outcome. There was no heterogeneity (v2 = 2.63,

The findings of this review suggest that chewing gum may be effective for shortening the time to first flatus,

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Figure 2. Summary and strength of the evidence from trials analysed on GradePro.

time to first bowel sounds and time to first defaecation following caesarean sections. In addition, it reduces the requirement for enemas and antiemetics. The use of chewing gum in women undergoing caesarean sections also reduces the risk of POI, but does not affect the length of hospitalisation.

Strengths and limitations We hope that this systematic review will help obstetricians to consider the use of chewing gum as part of their postop-

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erative recommendations. The results of this review are consistent with those of previously published studies in general and colorectal surgical patients.6,21,22,36–41 Trials involving colorectal patients concluded that the use of chewing gum is associated with a decreased time to first flatus and first defaecation, which indirectly lowered the incidence of POI. However, there were mixed results in terms of length of hospitalisation.6,21,22,36–41 A previous meta-analysis42 of 17 randomised controlled trials included a subgroup analysis of four trials assessing

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Role of chewing gum following caesarean section

Table 1. Causes of heterogeneity Clinical

Methodological

• Recruitment of nulliparous versus multiparous women • Previous surgery • Various age groups • Variable inclusion and exclusion criteria

• Different primary and second variables • Different technique of randomisation • Lack of power calculation • Lack of blinding • Different statistic methods to report outcomes

collection as well as that of the assessor and operating surgeon should be considered. Further trials differentiating between sugar-substituted gums and sugar-free gums should also be considered to determine which type of chewing gum would be most effective, based on a robust cost-effectiveness analysis. Until then, this review may facilitate decision-making in obstetricians because chewing gum is well accepted in most cultures, so it may represent a simple and cost-effective method for reducing POI following caesarean sections.

Disclosure of interest None to declare. the effect of chewing gum following caesarean sections and reported similar results in terms of time to first flatus, time to first bowel movement and length of hospital stay. The authors are fully aware of several limitations in this review. First, the quality of included trials was not necessarily high because of limitations associated with randomisation techniques, allocation concealment, blinding, intention-to-treat analyses and power calculations, which are potential sources of bias. Second, there were significant differences regarding the inclusion and exclusion criteria among the included trials. Third, variable degrees of difference also existed among the included trials regarding the definition of ‘postoperative ileus’ and ‘measurement scales for postoperative pain’. Fourth, the studies with a relatively small number of women in this review may not have been sufficient to recognise small differences between groups.

Contribution to authorship CL conceived the idea for the study, performed the literature search, collected data and drafted the article. SMS performed the literature search, collected data and performed statistical analyses. AAS contributed to the design of the study, confirmed statistical analyses and supervised the study. All authors reviewed and edited the article.

Details of ethics approval Not required.

Funding None to declare.

Acknowledgements None to declare.

Interpretation

Supporting Information

Based upon this study chewing gum may be used in women following caesarean section to reduce the incidence of POI. All the included trials have used different gums and doses so it is difficult to recommend a specific one. We are recommending chewing gum for 30–60 minutes at least three times per day because this regimen has been studied by the majority of the trials. However, because of several limitations, the authors consider a major randomised, control trial to be mandatory to validate these findings.

Additional Supporting Information may be found in the online version of this article: Figure S1. A: The forest plot showing time to first flatus in women following C-section. Standardised mean difference is shown with 95% confidence interval. B: The forest plot showing time to first bowel sounds in women following C-section. Standardised mean difference is shown with 95% confidence interval. C: The forest plot showing time to first defecation in women following C-section. Standardised mean difference is shown with 95% confidence interval. D: The forest plot showing incidence of postoperative ileus in women following C-section. Odds ratio is shown with 95% confidence interval. E: The forest plot showing length of hospitalisation periods in women following C-section. Standardised mean difference is shown with 95% confidence interval. Table S1. Characteristics of included trials. Table S2. Treatment protocol adopted in included trials. Table S3. Variables used for meta-analysis.

Conclusion The conclusion of this review may be considered weak based upon the strength of the evidence; however, we believe that this study will provide the impetus for further investigations in the form of a major multicentre randomised controlled trial. Future trials should be powered adequately and should be conducted according to the CONSORT guidelines. From the technical viewpoint, achieving multiple level blinding is impossible because of the nature of the trial. However, the blinding of the data

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Table S4. Quality assessment of included trials. Data S1. Powerpoint slides summarising the study. &

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19 Harms BA, Heise CP. Pharmacologic management of post operative ileus: the next chapter in GI surgery. Ann Surg 2007;245:364–5. 20 Fanning J, Valea FA. Perioperative bowel management for gynecologic surgery. Am J Obstet Gynecol 2011;205:309–14. 21 Noble EJ, Harris R, Hosie KB, Thomas S, Lewis SJ. Gum chewing reduces postoperative ileus? A systematic review and meta-analysis. Int J Surg 2009;7:100–5. 22 Purkayastha S, Tilney HS, Darzi AW, Tekkis PP. Meta-analysis of randomized studies evaluating chewing gum to enhance postoperative recovery following colectomy. Arch Surg 2008;143:788–93. 23 Guyton A, Hall J. Textbook of Medical Physiology, 10th edn. Philadelphia, PA: Saunders; 2000. 24 Review Manager (RevMan) [Computer program]. Version 5.0. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration; 2008. 25 Higgins JPT, Green S (eds). Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.0 (updated February 2008). The Cochrane Collaboration, 2008. [http://www.cochrane-handbook.org]. Accessed 21 March 2013. 26 Higgins JP. Thompson SG Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539–58. 27 Egger M, Smith GD, Altman DG. Systematic Reviews in Healthcare. London: BMJ Publishing; 2006. 28 GRADEpro. [Computer program]. Version 3.2 for Windows. Jan €nemann 2008. [http://ims. Brozek, Andrew Oxman, Holger Schu cochrane.org/revman/other-resources/gradepro/download]. Accessed 21 March 2013. 29 Abd-El-Maeboud KH, Ibrahim MI, Shalaby DA, Fikry MF. Gum chewing stimulates early return of bowel motility after caesarean section. BJOG 2009;116:1334–9. 30 Garshasbi A, Behboudi S. The effect of Gum chewing on postoperative ileus after cesarean section. Society for Obstetric Anesthesia and Perinatology (SOAP) 42nd Annual Meeting. [http:// soap.org/abstracts-uploads-spring-2011/1011411033345The_effect_ of_Gum_c.pdf]. Accessed 21 March 2013. 31 Harma MI, Barut A, Arikan II, Harma M. Gum-chewing speeds return of first bowel sounds but not first defecation after cesarean section. Anatol J Obstet Gynecol 2009;1:1–3. 32 Jakkaew B, Charoenkwan K. Effects of gum chewing on recovery of bowel function following cesarean section: a randomized controlled trial. Arch Gynecol Obstet 2013;288:255–60. €zdemir E, Simavli S, Onaran Y, Keskin E. 33 Kafali H, Duvan CI, Go Influence of gum chewing on postoperative bowel activity after cesarean section. Gynecol Obstet Invest 2010;69:84–7. 34 Ledari FM, Barat S, Delavar MA. Chewing gums has stimulatory effects on bowel function in patients undergoing cesarean section: a randomized controlled trial. Bosn J Basic Med Sci 2012;12: 265–8. 35 Shang H, Yang Y, Tong X, Zhang L, Fang A, Hong L. Gum chewing slightly enhances early recovery from postoperative ileus after cesarean section: results of a prospective, randomized, controlled trial. Am J Perinatol 2010;27:387–91. 36 Hocevar BJ, Robinson B, Gray M. Does chewing gum shorten the duration of postoperative ileus in patients undergoing abdominal surgery and creation of a stoma? J Wound Ostomy Continence Nurs 2010;37:140–6. 37 Yin Z, Sun J, Liu T, Zhu Y, Peng S, Wang J. Gum chewing: another simple potential method for more rapid improvement of postoperative gastrointestinal function. Digestion 2013;87:67–74. 38 V asquez W, Hern andez AV, Garcia-Sabrido JL. Is gum chewing useful for ileus after elective colorectal surgery? A systematic review and meta-analysis of randomized clinical trials. J Gastrointest Surg 2009;13:649–56.

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39 de Castro SM, van den Esschert JW, van Heek NT, Dalhuisen S, Koelemay MJ, Busch OR, et al. A systematic review of the efficacy of gum chewing for the amelioration of postoperative ileus. Dig Surg 2008;25:39–45. 40 Chan MK, Law WL. Use of chewing gum in reducing postoperative ileus after elective colorectal resection: a systematic review. Dis Colon Rectum 2007;50:2149–57.

41 Leier H. Does gum chewing help prevent impaired gastric motility in the postoperative period? J Am Acad Nurse Pract 2007;19:133–6. 42 Li S, Liu Y, Peng Q, Xie L, Wang J, Qin X. Chewing gum reduces postoperative ileus following abdominal surgery: a meta-analysis of 17 randomized controlled trials. J Gastroenterol Hepatol 2013;28: 1122–32.

Sham feeding with gum following caesarian section: something to chew on S Smith G7 Newcastle Private Medical Suites New Lambton Heights, NSW, 2300, Australia

Mini commentary on ‘Chewing gum in preventing postoperative ileus in women undergoing caesarean section: a systematic review and meta-analysis of randomised controlled trials’ The concept of postoperative sham feeding with chewing gum is to enable faster return of gastrointestinal function, by stimulating the cephalovagal pathway (Lunding et al. Neurogastroenterol Motil 2008;20: 618–24). This is a relatively simple and inexpensive concept, and certainly one worth considering. Craciunas et al. have performed a systematic review and meta-analysis, on the use of chewing gum in preventing postoperative ileus, following caesarean section. Given the morbidity and cost associated with postoperative ileus, this would appear to be an important topic to review. Although there appear to be some limitations with the quality of the trials included in the review, as well as significant heterogeneity between them, the findings appear to indicate clinically relevant advantages associated with gum chewing: half a day reduction in time to return of flatus and time to first defaecation, and approximately a two-thirds reduction in rates of ileus. The potential causes of heterogeneity between the trials that make up

this review are many, and have been listed by the authors. One cause of heterogeneity not listed is the variety of feeding regimens given to patients following abdominal surgery in the different trials. Presumably if sham feeding is effective, in improving postoperative gut function, one would anticipate regular feeding to also be effective. The traditional regimen of not feeding until signs of gut function returns, has been replaced in the era of enhanced recovery, with rapid postoperative feeding. When one analyses the colorectal literature on this subject, it becomes clear that the more modern trials on sham feeding, where rapid postoperative feeding is employed, reveal minimal or no improvement with the addition of chewing gum (Lim et al. Ann Surg 2013;257:1016–24, Zaghiyan et al. Dis Colon Rectum 2013;56:328– 35). One can assume from this, that it is the postoperative act of mastication that prepares the stomach for food, and helps hasten gut emptying. Patients that can tolerate food immediately following on from their surgery should be fed early, and fed a

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diet that encourages mastication. Indeed, it may be that chewing gum is most useful in the group of patients who do develop an ileus, or who suffer from postoperative nausea and cannot tolerate a diet. While complications and cost were not assessed in this review, studies have shown that the intervention of chewing gum is a relatively safe one: Noble et al. (Int J Surg 2009;7:100– 5), while common sense suggests it to be an inexpensive one. Given the findings of this review, in addition to the simplicity, ease and low cost of this intervention, the authors’ conclusion that chewing gum should be used routinely following caesarean section seems valid, and should be strongly considered in patients that cannot tolerate an early return to feeding, for any reason.

Disclosure of interests All the information contained in this mini commentary represents solely the thoughts and work of Dr Stephen Smith, whom has no pecuniary interest in the topic. &

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Journal club Papers for discussion Craciunas L, Sajid MS, Ahmed AS. A systematic review and meta-analysis of randomised controlled trials reporting the role of chewing gum in preventing postoperative ileus in women undergoing caesarean section. BJOG 2014; DOI: 10.1111/1471-0528.12696. Yi-Ping Zhu YP, Yao XD, Wang WJ, Zhang SL, Dai B, Ye DW. Effects of gum chewing on postoperative ileus after cesarean section: a meta-analysis of randomised controlled trials. BJOG 2014; DOI: 10.1111/1471-0528.12662.

Scenario A woman who previously suffered from postoperative ileus after her first caesarean section has undergone an elective caesarean section for her second child. She asks immediately after the operation, ‘is there any way to help my bowel move?’

Description of research Participants Intervention Comparison Outcomes Study design

Women who have undergone caesarean section Chewing gum alongside routine management Routine management alone Time to first flatus, time to first bowel movement, time to first stool and length of hospital stay Meta-analyses of randomised controlled trials

Discussion points • • • •

How common is postoperative ileus in your practice? How would you currently manage this woman at risk of postoperative ileus in the scenario? Compare the methodology of these meta-analyses using the MOOSE and/or PRISMA checklists. Most included trials had used surrogate outcomes (e.g. time to bowel movement)—are these surrogates good proxies for ileus? • What are the problems of overlapping meta-analyses? How can we solve them? (see suggested reading) • Can you briefly summarise the results of the two meta-analyses? Have they changed your practice? (Data S1)

Suggested reading • Chien PF, Khan KS, Siassakos D. Registration of systematic reviews: PROSPERO. BJOG 2012;119:903–5. • Siontis KC, Hernandez-Boussard T, Ioannidis JPA. Overlapping meta-analyses on the same topic: survey of published studies. BMJ 2013;347:f4501. EYL Leung Women’s Health Research Unit, Queen Mary, University of London, London, UK Join us at #BlueJC: Follow @BJOGTweets to stay updated on #BlueJC sessions or email [email protected] to host a journal club on Twitter. Find out more on our journal club page by visiting bjog.org.&

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Chewing gum in preventing postoperative ileus in women undergoing caesarean section: a systematic review and meta-analysis of randomised controlled trials.

The incidence of postoperative ileus (POI) after gynaecological surgery is 10-15% Chewing gum following general surgery improves outcomes, including e...
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