Impact of the Ileal microbiota on surgical site infections in Crohn’s disease: a nationwide prospective cohort

Clément Julien (1) , Emré Anakok (2, 3) , Xavier Treton (4) , Maria Nachury (5) , Stéphane Nancey (6) , Anthony Buisson (7, 8) , Mathurin Fumery (9, 10) , Jérôme Filippi (11) , Léon Maggiori (12) , Yves Panis (13) , Philippe Zerbib (14) , Yves François (15) , Anne Dubois (16) , Charles Sabbagh (17, 18) , Amine Rahili (11) , Philippe Seksik (3, 19) , Matthieu Allez (12) , Jérémie Lefevre (20, 19) , Pierre Cattan (12) , Mircea Chirica (21) , Nicolas Munoz-Bongrand (12) , Hélène Corte (12) , Nathan Beaupel , Jonathan Catry , Jean-Marc Gornet (12) , Clotilde Baudry (12) , Nelson Lourenco (12) , Mariane Maillet , My-Linh Tran-Minh (12) , Victor Chardiny , Joelle Bonnet , Leila Chedouba , Andrée Nisard (12) , Laurent Beaugerie (22) , Anne Bourrier (22) , Isabelle Nion-Larmurier , Julien Kirchgesner (22) , Cécilia Landman (22) , Elodie Quevrain , Loic Brot , Najim Chafai , Yann Parc , Clothilde Debove , Magali Svreck (22) , Camille Vincent , Nathalie Guedj (23) , Marianne Ferron , Yoram Bouhnik (23) , Olivier Corcos (24) , Carmen Stefanescu (23) , Sarah Khabil , Philippe Marteau (25) , Xavier Dray , Ulrika Chaput , Gilles Bommelaer (16) , Marion Goutte (16) , Jérémie Denizot (7) , Nicolas Barnich (7) , Dilek Coban (16) , Pierre Desreumaux , Benjamin Pariente (26) , Coralie Sommeville , Jean-Louis Dupas , Julien Loreau (27) , Franck Brazier (27) , Denis Chatelain (28, 27) , Christophe Attencourt (27, 28) , Martine Leconte , Gilles Boschetti (6) , Bernard Flourié , Eddy Cotte (29) , Anne-Laure Charlois , Peggy Falgon , Helena Hadjisavvas , Driffa Moussata , Marion Chauvenet (29) , Sarah Boyer , Xavier Hebuterne (30) , Nadia Arab , Raja Barhoumi , Paul Hofmann , Sylvain Le Corff (31, 32) , Anna Bonnet (2, 19) , Laura Beyer-Berjot (1, 33, 34) , Harry Sokol (3, 19, 34)

1 Service de Chirurgie viscérale et disgestive
2 LPSM (UMR_8001) - Laboratoire de Probabilités, Statistique et Modélisation
3 CRSA - Centre de Recherche Saint-Antoine
4 Service de Gastroentérologie [Hôpital Beaujon]
5 INFINITE (Ex-Liric) - Institute for Translational Research in Inflammation - U 1286
6 CHLS - Centre Hospitalier Lyon Sud [CHU - HCL]
7 M2iSH - Microbes, Intestin, Inflammation et Susceptibilité de l'Hôte
8 Service d'Hépatologie Gastro-entérologie [CHU Clermont-Ferrand]
9 Service d'Hépato Gastroenterologie [CHU Amiens-Picardie]
10 PERITOX - Périnatalité et Risques Toxiques - UMR INERIS_I 1
11 CHU Nice - Centre Hospitalier Universitaire de Nice
12 AP-HP - Hopital Saint-Louis [AP-HP]
13 Service de Chirurgie colorectale [Hôpital Beaujon]
14 Hôpital Claude Huriez [Lille]
15 Service de chirurgie digestive et oncologique [Centre Hôspitalier Lyon Sud]
16 CHU Clermont-Ferrand
17 Chirurgie digestive [CHU Amiens]
18 SSPC - Simplification des soins chez les patients complexes - UR UPJV 7518
19 FHU PaCeMM - Paris Center for Microbiome Medicine
20 Service de chirurgie générale et digestive [CHU Saint-Antoine]
21 CHU Grenoble
22 CHU Saint-Antoine [AP-HP]
23 Hôpital Beaujon [AP-HP]
24 AP-HP - Assistance publique - Hôpitaux de Paris (AP-HP)
25 Hôpital Lariboisière-Fernand-Widal [APHP]
26 CHRU Lille - Centre Hospitalier Régional Universitaire [Lille]
27 CHU Amiens-Picardie
28 CHIMERE - CHirurgie, IMagerie et REgénération tissulaire de l’extrémité céphalique - Caractérisation morphologique et fonctionnelle - UR UPJV 7516
29 HCL - Hospices Civils de Lyon
30 Servcie Hépato-gastroentérolgie et Nutrition clinique [CHU Nice]
31 TSP - Télécom SudParis
32 IP Paris - Institut Polytechnique de Paris
33 LBA UMR T24 - Laboratoire de Biomécanique Appliquée
34 MICALIS - MICrobiologie de l'ALImentation au Service de la Santé

Abstract Background and Aims Surgery is performed in 50–70% of Crohn’s disease [CD] patients, and its main risk is surgical site infection [SSI]. The microbiota has been extensively assessed in CD but not as a potential risk factor for septic morbidity. The objective of this study was to assess the impact of the gut microbiota on SSI in CD. Methods We used the multicentric REMIND prospective cohort to identify all patients who experienced SSI after ileocolonic resection for CD, defined as any postoperative local septic complication within 90 days after surgery: wound abscess, intra-abdominal collection, anastomotic leakage or enterocutaneous fistula. The mucosa-associated microbiota of the ileal resection specimen was analysed by 16S gene sequencing in 149 patients. The variable selection and prediction were performed with random forests [R package VSURF] on clinical and microbiotal data. The criterion of performance that we considered was the area under the Receiver Operating Characteristic [ROC] curve [AUC]. Results SSI occurred in 24 patients [16.1%], including 15 patients [10.1%] with major morbidity. There were no significant differences between patients with or without SSI regarding alpha and beta diversity. The top selected variables for the prediction of SSI were all microbiota-related. The maximum AUC [0.796] was obtained with a model including 14 genera, but an AUC of 0.78 had already been obtained with a model including only six genera [Hungatella, Epulopiscium, Fusobacterium, Ruminococcaceae_ucg_009, Actinomyces and Ralstonia]. Conclusion The gut microbiota has the potential to predict SSI after ileocolonic resection for CD. It might play a role in this frequent postoperative complication.

Mots clés: gut microbiota; Crohn’s disease; prediction

Domaines: Sciences du Vivant [q-bio]; Médecine humaine et pathologie; Chirurgie; Sciences du Vivant [q-bio]; Médecine humaine et pathologie; Hépatologie et Gastroentérologie

Clément Julien, Emré Anakok, Xavier Treton, Maria Nachury, Stéphane Nancey, et al.. Impact of the Ileal microbiota on surgical site infections in Crohn’s disease: a nationwide prospective cohort. Journal of Crohn's and Colitis, 2022, ⟨10.1093/ecco-jcc/jjac026⟩. ⟨hal-03638385⟩