Abstract
Purpose
Candida spp. cause opportunistic infections in conditions of immunodeficiency. Here, we investigated the relationship between colonization of the gastric juice by Candida spp. and surgical site infection (SSI) in hepatectomy.
Methods
Consecutive hepatectomy cases between November 2019 and April 2021 were enrolled. Gastric juice samples (collected intraoperatively through a nasogastric tube) were cultured. We compared factors related to patient background, blood test findings, surgical findings, and postoperative complications between the Candida + group (positive for colonization of the gastric juice by Candida spp.) and the Candida − group (negative). In addition, we identified the factors that contribute to SSI.
Results
There were 29 and 71 patients in the Candida + and Candida − groups, respectively. The Candida + group was significantly older (average age: Candida + 74 years vs. Candida − 69 years; p = 0.02) and contained more patients negative for the hepatitis B and C virus (Candida + 93% vs. Candida − 69%; p = 0.02). SSI was significantly more common in the Candida + group (Candida + 31% vs. Candida − 9%; p = 0.01). Postoperative bile leakage and colonization of the gastric juice by Candida spp. were independent predictors of SSI.
Conclusion
Colonization of the gastric juice by Candida spp. is a risk factor for SSI after hepatectomy.
Similar content being viewed by others
Data availability
The protocol or datasets used during the current study are available from the corresponding author on reasonable request.
References
Kaibori M, Matsui K, Ishizaki M, Saito T, Kitade H, Matsui Y, Kwon AH (2009) Hepatic resection for hepatocellular carcinoma in the elderly. J Surg Oncol 99(3):154–160. https://doi.org/10.1002/jso.21221
Iida H, Kaibori M, Matsui K, Ishizaki M, Kon M (2017) Assessing the feasibility of clinicopathological features of hepatic resection for hepatocellular carcinoma in patients over 80 years of age. Mol Clin Oncol 6(1):29–38. https://doi.org/10.3892/mco.2016.1079
Mirici-Cappa F, Gramenzi A, Santi V, Zambruni A, Di Micoli A, Frigerio M, Maraldi F, Di Nolfo MA, Del Poggio P, Benvegnù L, Rapaccini G, Farinati F, Zoli M, Borzio F, Giannini EG, Caturelli E, Bernardi M, Trevisani F (2010) Treatments for hepatocellular carcinoma in elderly patients are as effective as in younger patients: a 20-year multicentre experience. Gut 59(3):387–396. https://doi.org/10.1136/gut.2009.194217
Sugawara G, Nagino M, Nishio H, Ebata T, Takagi K, Asahara T, Nomoto K, Nimura Y (2006) Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg 244(5):706–714. https://doi.org/10.1097/01.sla.0000219039.20924.88
Usami M, Miyoshi M, Kanbara Y, Aoyama M, Sakaki H, Shuno K, Hirata K, Takahashi M, Ueno K, Tabata S, Asahara T, Nomoto K (2011) Effects of perioperative synbiotic treatment on infectious complications, intestinal integrity, and fecal flora and organic acids in hepatic surgery with or without cirrhosis. JPEN J Parenter Enteral Nutr 35(3):317–328. https://doi.org/10.1177/0148607110379813
Iida H, Sasaki M, Maehira H, Mori H, Yasukawa D, Takebayashi K, Kurihara M, Bamba S, Tani M (2020) The effect of preoperative synbiotic treatment to prevent surgical-site infection in hepatic resection. J Clin Biochem Nutr 66(1):67–73. https://doi.org/10.3164/jcbn.19-46
Owens WD, Felts JA, Spitznagel EL Jr (1978) ASA physical status classifications: a study of consistency of ratings. Anesthesiology 49(4):239–243. https://doi.org/10.1097/00000542-197810000-00003
Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, Carbone PP (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5(6):649–655
Nishigori T, Tsunoda S, Okabe H, Tanaka E, Hisamori S, Hosogi H, Shinohara H, Sakai Y (2016) Impact of sarcopenic obesity on surgical site infection after laparoscopic total gastrectomy. Ann Surg Oncol 23:524–531. https://doi.org/10.1245/s10434-016-5385-y
Namm JP, Thakrar KH, Wang CH, Stocker SJ, Sur MD, Berlin J, Dale W, Talamonti MS, Roggin KK (2017) A semi-automated assessment of sarcopenia using psoas area and density predicts outcomes after pancreaticoduodenectomy for pancreatic malignancy. J Gastrointest Oncol 8(6):936–944. https://doi.org/10.21037/jgo.2017.08.09
Kato H, Iizawa Y, Kishiwada M, Usui M, Nakamura A, Murata Y, Tanemura A, Kuriyama N, Azumi Y, Mizuno S, Sakurai H, Isaji S (2016) Negative impact of biliary candidiasis on early and late postoperative complications after pancreatoduodenectomy usefulness of the CHROMagar Candida plate for identification. Pancreas 45(9):e45-47. https://doi.org/10.1097/mpa.0000000000000682
Sato A, Masui T, Nakano K, Sankoda N, Anazawa T, Takaori K, Kawaguchi Y, Uemoto S (2017) Abdominal contamination with Candida albicans after pancreaticoduodenectomy is related to hemorrhage associated with pancreatic fistulas. Pancreatology 17(3):484–489. https://doi.org/10.1016/j.pan.2017.03.007
Kato H, Iizawa Y, Nakamura K, Gyoten K, Hayasaki A, Fujii T, Murata Y, Tanemura A, Kuriyama N, Azumi Y, Kishiwada M, Mizuo S, Usui M, Sakurai H, Isaji S (2018) The critical role of biliary candidiasis in development of surgical site infections after pancreatoduodenectomy: results of prospective study using a selective culture medium for Candida species. Biomed Res Int 2018:5939724. https://doi.org/10.1155/2018/5939724
National Healthcare Safety Network (2023) Centers for Disease Control and Prevention. Surgical site infection (SSI) event. (9):1–41. http://www.cdc.gov/nhsn/pdfs/pscmanual/9pscssicurrent.pdf
Rahbari NN, Garden OJ, Padbury R, Brooke-Smith M, Crawford M, Adam R, Koch M, Makuuchi M, Dematteo RP, Christophi C, Banting S, Usatoff V, Nagino M, Maddern G, Hugh TJ, Vauthey JN, Greig P, Rees M, Yokoyama Y, Fan ST, Nimura Y, Figueras J, Capussotti L, Büchler MW, Weitz J (2011) Posthepatectomy liver failure: a definition and grading by the International Study Group of Liver Surgery (ISGLS). Surgery 149(5):713–724. https://doi.org/10.1016/j.surg.2010.10.001
Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, Fan ST, Yokoyama Y, Crawford M, Makuuchi M, Christophi C, Banting S, Brooke-Smith M, Usatoff V, Nagino M, Maddern G, Hugh TJ, Vauthey JN, Greig P, Rees M, Nimura Y, Figueras J, DeMatteo RP, Büchler MW, Weitz J (2011) Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery 149(5):680–688. https://doi.org/10.1016/j.surg.2010.12.002
Baumgartner C, Freydiere AM, Gille Y (1996) Direct identification and recognition of yeast species from clinical material by using albicans ID and CHROMagar Candida plates. J Clin Microbiol 34(2):454–456. https://doi.org/10.1128/jcm.34.2.454-456.1996
Hirokawa K, Utsuyama M, Ishikawa T, Kikuchi Y, Kitagawa M, Fujii Y, Nariuchi H, Uetake H, Sugihara K (2009) Decline of T cell-related immune functions in cancer patients and an attempt to restore them through infusion of activated autologous T cells. Mech Ageing Dev 130(1–2):86–91. https://doi.org/10.1016/j.mad.2008.05.001
Hirokawa K, Utsuyama M, Hayashi Y, Kitagawa M, Makinodan T, Fulop T (2013) Slower immune system aging in women versus men in the Japanese population. Immun Ageing 10(1):19. https://doi.org/10.1186/1742-4933-10-19
Hayashi K, Tooyama H, Tanaka H, Aizawa H, Shimane T, Kurashina K, Yamada SI, Kurita H (2017) Relationship between the quantity of oral Candida and immunological vigor. J Oral Maxillof Surg Med Pathol 29(1):65–70. https://doi.org/10.1016/j.ajoms.2016.09.011
Korting HC, Ollert M, Georgii A, Fröschl M (1988) In vitro susceptibilities and biotypes of Candida albicans isolates from the oral cavities of patients infected with human immunodeficiency virus. J Clin Microbiol 26(12):2626–2631. https://doi.org/10.1128/jcm.26.12.2626-2631.1988
Gyoten K, Kato H, Hayasaki A, Fujii T, Iizawa Y, Murata Y, Tanemura A, Kuriyama N, Kishiwada M, Mizuno S, Usui M, Sakurai H, Isaji S (2021) Association between gastric Candida colonization and surgical site infections after high-level hepatobiliary pancreatic surgeries: the results of prospective observational study. Langenbecks Arch Surg 406(1):109–119. https://doi.org/10.1007/s00423-020-02006-7
Shirtliff ME, Peters BM, Jabra-Rizk MA (2009) Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett 299(1):1–8. https://doi.org/10.1111/j.1574-6968.2009.01668.x
Carlson E (1983) Enhancement by Candida albicans of Staphylococcus aureus, Serratia marcescens, and Streptococcus faecalis in the establishment of infection in mice. Infect Immun 39(1):193–197. https://doi.org/10.1128/iai.39.1.193-197.1983
Sokol H, Leducq V, Aschard H, Pham HP, Jegou S, Landman C, Cohen D, Liguori G, Bourrier A, Nion-Larmurier I, Cosnes J, Seksik P, Langella P, Skurnik D, Richard ML, Beaugerie L (2017) Fungal microbiota dysbiosis in IBD. Gut 66(6):1039–1048. https://doi.org/10.1136/gutjnl-2015-310746
Yang AM, Inamine T, Hochrath K, Chen P, Wang L, Llorente C, Bluemel S, Hartmann P, Xu J, Koyama Y, Kisseleva T, Torralba MG, Moncera K, Beeri K, Chen CS, Freese K, Hellerbrand C, Lee SML, Hoffman HM, Mehal WZ, Garcia-Tsao G, Mutlu EA, Keshavarzian A, Brown GD, Ho SB, Bataller R, Stärkel P, Fouts DE, Schnabl B (2017) Intestinal fungi contribute to development of alcoholic liver disease. J Clin Investig 127(7):2829–2841. https://doi.org/10.1172/JCI90562
Shindo K, Fukumura M (1995) Effect of H2-receptor antagonists on bile acid metabolism. J Invest Med : Off Publ Am Fed Clin Res 43(2):170–177
Shindo K, Machida M, Fukumura M, Koide K, Yamazaki R (1998) Omeprazole induces altered bile acid metabolism. Gut 42(2):266–271. https://doi.org/10.1136/gut.42.2.266
Brzozowski T, Zwolinska-Wcislo M, Konturek PC, Kwiecien S, Drozdowicz D, Konturek SJ, Stachura J, Budak A, Bogdal J, Pawlik WW, Hahn EG (2005) Influence of gastric colonization with Candida albicans on ulcer healing in rats: effect of ranitidine, aspirin and probiotic therapy. Scand J Gastroenterol 40(3):286–296. https://doi.org/10.1080/00365520510011524
Martinsen TC, Bergh K, Waldum HL (2005) Gastric juice: a barrier against infectious diseases. Basic Clin Pharmacol Toxicol 96(2):94–102. https://doi.org/10.1111/j.1742-7843.2005.pto960202.x
Author information
Authors and Affiliations
Contributions
HI and MK designed the research and analyzed the patient data. HI, HM, HM, NN, TM, KT, SK, TM, and MT collected the data. HI drafted the manuscript. All authors have read and approved the final version of the manuscript.
Corresponding author
Ethics declarations
This prospective observational study conformed to the Clinical Research Guidelines and was approved by the ethics committee of our institution (institutional approval number: R2019-138). Written informed consent was obtained from all patients. In addition, this study was registered with UMIN-CTR (identifying number: UMIN 000048860).
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Iida, H., Kaibori, M., Maehira, H. et al. Colonization of the gastric juice by Candida spp. promotes surgical site infection after hepatectomy. Langenbecks Arch Surg 408, 240 (2023). https://doi.org/10.1007/s00423-023-02978-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00423-023-02978-2