Short-term gut microbiota's shift after laparoscopic Roux-en-Y vs one anastomosis gastric bypass: results of a multicenter randomized control trial.

Bariatric/metabolic surgery Gut microbiota Microbial diversity Morbid obesity One anastomosis gastric bypass Roux-en-Y gastric bypass

Journal

Surgical endoscopy
ISSN: 1432-2218
Titre abrégé: Surg Endosc
Pays: Germany
ID NLM: 8806653

Informations de publication

Date de publication:
18 Sep 2024
Historique:
received: 22 05 2024
accepted: 04 08 2024
medline: 19 9 2024
pubmed: 19 9 2024
entrez: 18 9 2024
Statut: aheadofprint

Résumé

Roux-en-Y (RYGB) and one anastomosis gastric bypass (OAGB) represent two of the most used bariatric/metabolic surgery (BMS) procedures. Gut microbiota (GM) shift after bypass surgeries, currently understated, may be a possible key driver for the short- and long-term outcomes. Prospective, multicenter study enrolling patients with severe obesity, randomized between OAGB or RYGB. Fecal and blood samples were collected, pre- (T0) and 24 months postoperatively (T1). GM was determined by V3-V4 16S rRNA regions sequencing and home-made bioinformatic pipeline based on Qiime2 plugin and R packages. To compare OAGB vs RYGB microbiota profile at T1 and its impact on metabolic and nutritional status. 54 patients completed the study, 27 for each procedure. An overall significant variation was detected in anthropometric and serum nutritional parameters at T1, with a significant, similar decrease in overall microbial alpha and beta diversity observed in both groups. An increase in relative abundances of Actinobacteria and Proteobacteria and a reduction of Bacteroidetes, no significant changes in Firmicutes and Verrucomicrobia, with an increase of the Firmicutes/Bacteroidetes ratio were observed. BMS promotes a dramatic change in GM composition. This is the first multicenter, RCT evaluating the impact of OAGB vs Roux-en-Y bypass on GM profile. The bypass technique per se did not impact differently on GM or other examined metabolic parameters. The emergence of slightly different GM profile postoperatively may be related to clinical conditions or may influence medium or long-term outcomes and as such GM profile may represent a biomarker for bariatric surgery's outcomes.

Sections du résumé

BACKGROUND BACKGROUND
Roux-en-Y (RYGB) and one anastomosis gastric bypass (OAGB) represent two of the most used bariatric/metabolic surgery (BMS) procedures. Gut microbiota (GM) shift after bypass surgeries, currently understated, may be a possible key driver for the short- and long-term outcomes.
METHODS METHODS
Prospective, multicenter study enrolling patients with severe obesity, randomized between OAGB or RYGB. Fecal and blood samples were collected, pre- (T0) and 24 months postoperatively (T1). GM was determined by V3-V4 16S rRNA regions sequencing and home-made bioinformatic pipeline based on Qiime2 plugin and R packages.
OBJECTS OBJECTIVE
To compare OAGB vs RYGB microbiota profile at T1 and its impact on metabolic and nutritional status.
RESULTS RESULTS
54 patients completed the study, 27 for each procedure. An overall significant variation was detected in anthropometric and serum nutritional parameters at T1, with a significant, similar decrease in overall microbial alpha and beta diversity observed in both groups. An increase in relative abundances of Actinobacteria and Proteobacteria and a reduction of Bacteroidetes, no significant changes in Firmicutes and Verrucomicrobia, with an increase of the Firmicutes/Bacteroidetes ratio were observed.
CONCLUSIONS CONCLUSIONS
BMS promotes a dramatic change in GM composition. This is the first multicenter, RCT evaluating the impact of OAGB vs Roux-en-Y bypass on GM profile. The bypass technique per se did not impact differently on GM or other examined metabolic parameters. The emergence of slightly different GM profile postoperatively may be related to clinical conditions or may influence medium or long-term outcomes and as such GM profile may represent a biomarker for bariatric surgery's outcomes.

Identifiants

pubmed: 39294316
doi: 10.1007/s00464-024-11154-6
pii: 10.1007/s00464-024-11154-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : European Association for Endoscopic Surgery and other Interventional Techniques
ID : Research Program 2018
Organisme : Sapienza Università di Roma
ID : Ateneo 2017

Informations de copyright

© 2024. The Author(s).

Références

Chooi YC, Ding C, Magkos F (2019) The epidemiology of obesity. Metabolism 92:6–10
pubmed: 30253139 doi: 10.1016/j.metabol.2018.09.005
Apovian CM (2016) Obesity: definition, comorbidities, causes, and burden. Am J Manag Care 22:s176–s185
pubmed: 27356115
Asadi A, Shadab Mehr N, Mohamadi MH, Shokri F, Heidary M, Sadeghifard N, Khoshnood S (2022) Obesity and gut-microbiota-brain axis: a narrative review. J Clin Lab Anal 36:e24420
pubmed: 35421277 pmcid: 9102524 doi: 10.1002/jcla.24420
Vallianou N, Stratigou T, Christodoulatos GS, Dalamaga M (2019) Understanding the role of the gut microbiome and microbial metabolites in obesity and obesity-associated metabolic disorders: current evidence and perspectives. Curr Obes Rep 8:317–332
pubmed: 31175629 doi: 10.1007/s13679-019-00352-2
Fujisaka S, Watanabe Y, Tobe K (2023) The gut microbiome: a core regulator of metabolism. J Endocrinol. https://doi.org/10.1530/JOE-22-0111
doi: 10.1530/JOE-22-0111 pubmed: 36458804 pmcid: 9874984
Arterburn DE, Telem DA, Kushner RF, Courcoulas AP (2020) Benefits and risks of bariatric surgery in adults: a review. JAMA 324:879–887
pubmed: 32870301 doi: 10.1001/jama.2020.12567
Coimbra VOR, Crovesy L, Ribeiro-Alves M, Faller ALK, Mattos F, Rosado EL (2022) Gut microbiota profile in adults undergoing bariatric surgery: a systematic review. Nutrients. https://doi.org/10.3390/nu14234979
doi: 10.3390/nu14234979 pubmed: 36558475 pmcid: 9783872
Juarez-Fernandez M, Roman-Saguillo S, Porras D, Garcia-Mediavilla MV, Linares P, Ballesteros-Pomar MD, Urioste-Fondo A, Alvarez-Cuenllas B, Gonzalez-Gallego J, Sanchez-Campos S, Jorquera F, Nistal E (2021) Long-term effects of bariatric surgery on gut microbiota composition and faecal metabolome related to obesity remission. Nutrients. https://doi.org/10.3390/nu13082519
doi: 10.3390/nu13082519 pubmed: 34444679 pmcid: 8397959
Eisenberg D, Shikora SA, Aarts E, Aminian A, Angrisani L, Cohen RV, De Luca M, Faria SL, Goodpaster KPS, Haddad A, Himpens JM, Kow L, Kurian M, Loi K, Mahawar K, Nimeri A, O’Kane M, Papasavas PK, Ponce J, Pratt JSA, Rogers AM, Steele KE, Suter M, Kothari SN (2022) American society for metabolic and bariatric surgery (ASMBS) and international federation for the surgery of obesity and metabolic disorders (IFSO): indications for metabolic and bariatric surgery. Surg Obes Relat Dis 18(2022):1345–1356
pubmed: 36280539 doi: 10.1016/j.soard.2022.08.013
Cosentino C, Marchetti C, Monami M, Mannucci E, Cresci B (2021) Efficacy and effects of bariatric surgery in the treatment of obesity: Network meta-analysis of randomized controlled trials. Nutr Metab Cardiovasc Dis 31:2815–2824
pubmed: 34348877 doi: 10.1016/j.numecd.2021.06.018
Angrisani L, Santonicola A, Iovino P, Ramos A, Shikora S, Kow L, Survey BS (2018) Similarities and disparities among the 5 IFSO chapters. Obes Surg 31(2021):1937–1948
Salminen P, Gronroos S, Helmio M, Hurme S, Juuti A, Juusela R, Peromaa-Haavisto P, Leivonen M, Nuutila P, Ovaska J (2022) Effect of laparoscopic sleeve gastrectomy vs roux-en-Y gastric bypass on weight loss, comorbidities, and reflux at 10 years in adult patients with obesity: the SLEEVEPASS randomized clinical trial. JAMA Surg 157:656–666
pubmed: 35731535 pmcid: 9218929 doi: 10.1001/jamasurg.2022.2229
Rutledge R (2001) The mini-gastric bypass: experience with the first 1,274 cases. Obes Surg 11:276–280
pubmed: 11433900 doi: 10.1381/096089201321336584
Rutledge R, Walsh TR (2005) Continued excellent results with the mini-gastric bypass: six-year study in 2,410 patients. Obes Surg 15:1304–1308
pubmed: 16259892 doi: 10.1381/096089205774512663
Deitel M (2019) History of the MGB and OAGB operations. Int J Surg 66:79–83
pubmed: 31054329 doi: 10.1016/j.ijsu.2019.04.018
De Luca M, Piatto G, Merola G, Himpens J, Chevallier JM, Carbajo MA, Mahawar K, Sartori A, Clemente N, Herrera M, Higa K, Brown WA, Shikora S (2021) IFSO update position statement on one anastomosis gastric bypass (OAGB). Obes Surg 31:3251–3278
pubmed: 33939059 doi: 10.1007/s11695-021-05413-x
Uhe I, Douissard J, Podetta M, Chevallay M, Toso C, Jung MK, Meyer J (2022) Roux-en-Y gastric bypass, sleeve gastrectomy, or one-anastomosis gastric bypass? A systematic review and meta-analysis of randomized-controlled trials. Obesity (Silver Spring) 30:614–627
pubmed: 35137548 doi: 10.1002/oby.23338
Alexandrou A, Davis PA, Law S, Whooley BP, Murthy SC, Wong J (2002) Esophageal cancer in patients with a history of distal gastrectomy. Arch Surg 137:1238–1242
pubmed: 12413309 doi: 10.1001/archsurg.137.11.1238
Parmar C, Zakeri R, Abouelazayem M, Shin TH, Aminian A, Mahmoud T, Abu Dayyeh BK, Wee MY, Fischer L, Daams F, Mahawar K, Group OS (2022) Esophageal and gastric malignancies after bariatric surgery: a retrospective global study. Surg Obes Relat Dis 18:464–472
pubmed: 35065887 doi: 10.1016/j.soard.2021.11.024
Salman MA, Salman A, Assal MM, Elsherbiney M, Tourky M, Elewa A, Khalaf AM, Gadallah MA, Gebril M, Khalid S, Shaaban H, Mohammed AA, Osman MHA, Hassan H (2023) One anastomosis gastric bypass (OAGB) with a 150-cm biliopancreatic limb (BPL) versus a 200-cm BPL, a systematic review and meta-analysis. Obes Surg 33:1846–1856
pubmed: 37022609 pmcid: 10234867 doi: 10.1007/s11695-023-06556-9
Kong LC, Tap J, Aron-Wisnewsky J, Pelloux V, Basdevant A, Bouillot JL, Zucker JD, Dore J, Clement K (2013) Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. Am J Clin Nutr 98:16–24
pubmed: 23719559 doi: 10.3945/ajcn.113.058743
Yadav J, Liang T, Qin T, Nathan N, Schwenger KJP, Pickel L, Xie L, Lei H, Winer DA, Maughan H, Robertson SJ, Woo M, Lou W, Banks K, Jackson T, Okrainec A, Hota SS, Poutanen SM, Sung HK, Allard JP, Philpott DJ, Gaisano HY (2023) Gut microbiome modified by bariatric surgery improves insulin sensitivity and correlates with increased brown fat activity and energy expenditure. Cell Rep Med 4:101051
pubmed: 37196633 pmcid: 10213984 doi: 10.1016/j.xcrm.2023.101051
De Maio F, Boru CE, Avallone M, Velotti N, Bianco DM, Capoccia D, Greco F, Guarisco G, Nogara M, Sanguinetti M, Verrastro O, Capaldo B, Musella M, Raffaelli M, Delogu G, Silecchia G, Leonetti F (2021) Characterization of gut microbiota in patients with metabolic syndrome candidates for bariatric/metabolic surgery: preliminary findings of a multi-center prospective study. Diabetes Res Clin Pract 180:109079
pubmed: 34599974 doi: 10.1016/j.diabres.2021.109079
Schulz KF, Altman DG, Moher D, CONSORT Group (2010) CONSORT 2010 Statement: updated guidelines for reporting parallel group randomised trials. BMC Med 24(8):18. https://doi.org/10.1186/1741-7015-8-18
doi: 10.1186/1741-7015-8-18
Di Lorenzo N, Antoniou SA, Batterham RL, Busetto L, Godoroja D, Iossa A, Carrano FM, Agresta F, Alarcon I, Azran C, Bouvy N, Balague Ponz C, Buza M, Copaescu C, De Luca M, Dicker D, Di Vincenzo A, Felsenreich DM, Francis NK, Fried M, Gonzalo Prats B, Goitein D, Halford JCG, Herlesova J, Kalogridaki M, Ket H, Morales-Conde S, Piatto G, Prager G, Pruijssers S, Pucci A, Rayman S, Romano E, Sanchez-Cordero S, Vilallonga R, Silecchia G (2020) Clinical practice guidelines of the European Association for Endoscopic Surgery (EAES) on bariatric surgery: update 2020 endorsed by IFSO-EC, EASO and ESPCOP. Surg Endosc 34:2332–2358
pubmed: 32328827 pmcid: 7214495 doi: 10.1007/s00464-020-07555-y
Posteraro B, De Maio F, Gasbarrini A (2021) Profiling the gastrointestinal microbiota. Methods Mol Biol 2283:83–92
pubmed: 33765312 doi: 10.1007/978-1-0716-1302-3_10
De Pascale G, De Maio F, Carelli S, De Angelis G, Cacaci M, Montini L, Bello G, Cutuli SL, Pintaudi G, Tanzarella ES, Xhemalaj R, Grieco DL, Tumbarello M, Sanguinetti M, Posteraro B, Antonelli M (2021) Staphylococcus aureus ventilator-associated pneumonia in patients with COVID-19: clinical features and potential inference with lung dysbiosis. Crit Care 25:197
pubmed: 34099016 pmcid: 8182737 doi: 10.1186/s13054-021-03623-4
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodriguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vazquez-Baeza Y, Vogtmann E, von Hippel M, Walters W et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857
pubmed: 31341288 pmcid: 7015180 doi: 10.1038/s41587-019-0209-9
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, GregoryCaporaso J (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90
pubmed: 29773078 pmcid: 5956843 doi: 10.1186/s40168-018-0470-z
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217
pubmed: 23630581 pmcid: 3632530 doi: 10.1371/journal.pone.0061217
Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73:1576–1585
pubmed: 17220268 pmcid: 1828774 doi: 10.1128/AEM.01996-06
Mechanick JI, Apovian C, Brethauer S, Garvey WT, Joffe AM, Kim J, Kushner RF, Lindquist R, Pessah-Pollack R, Seger J, Urman RD, Adams S, Cleek JB, Correa R, Figaro MK, Flanders K, Grams J, Hurley DL, Kothari S, Seger MV, Still CD (2019) Clinical Practice Guidelines for the Perioperative Nutrition, Metabolic, and Nonsurgical Support of Patients Undergoing Bariatric Procedures - 2019 Update: Cosponsored by American Association of Clinical Endocrinologists/ American College of Endocrinology, the Obesity Society, American Society for Metabolic & Bariatric Surgery, Obesity Medicine Association, and American Society of Anesthesiologists - Executive Summary. Endocr Pract 25:1346–1359
pubmed: 31682518 doi: 10.4158/GL-2019-0406
Robert M, Espalieu P, Pelascini E, Caiazzo R, Sterkers A, Khamphommala L, Poghosyan T, Chevallier JM, Malherbe V, Chouillard E, Reche F, Torcivia A, Maucort-Boulch D, Bin-Dorel S, Langlois-Jacques C, Delaunay D, Pattou F, Disse E (2019) Efficacy and safety of one anastomosis gastric bypass versus Roux-en-Y gastric bypass for obesity (YOMEGA): a multicentre, randomised, open-label, non-inferiority trial. Lancet 393:1299–1309
pubmed: 30851879 doi: 10.1016/S0140-6736(19)30475-1
Kermansaravi M, DavarpanahJazi AH, ShahabiShahmiri S, Carbajo M, Vitiello A, Parmar CD, Musella M (2021) Areas of non-consensus around one anastomosis/mini gastric bypass (OAGB/MGB): a narrative review. Obes Surg 31:2453–2463
pubmed: 33598845 doi: 10.1007/s11695-021-05276-2
Bhandari M, Fobi MAL, Buchwald JN (2019) Bariatric metabolic surgery standardization working, standardization of bariatric metabolic procedures: world consensus meeting statement. Obes Surg 29:309–345
pubmed: 31297742 doi: 10.1007/s11695-019-04032-x
Kaniel O, Sherf-Dagan S, Szold A, Langer P, Khalfin B, Kessler Y, Raziel A, Sakran N, Motro Y, Goitein D, Moran-Gilad J (2022) The effects of one anastomosis gastric bypass surgery on the gastrointestinal tract. Nutrients. https://doi.org/10.3390/nu14020304
doi: 10.3390/nu14020304 pubmed: 35057486 pmcid: 8778673
Ben Izhak M, Eshel A, Cohen R, Madar-Shapiro L, Meiri H, Wachtel C, Leung C, Messick E, Jongkam N, Mavor E, Sapozhnikov S, Maharshak N, Abu-Abeid S, Alis A, Mahler I, Meoded A, Meron Eldar S, Koren O, Louzoun Y (2021) Projection of gut microbiome pre- and post-bariatric surgery to predict surgery outcome. mSystems 6:e0136720
pubmed: 34100636 doi: 10.1128/mSystems.01367-20
Dhir A, Huang D (2021) Gut microbiome and bariatric surgery. Indian J Surg 83:395–397
doi: 10.1007/s12262-021-02927-7
Stojanov S, Berlec A, Strukelj B (2020) The influence of probiotics on the firmicutes/bacteroidetes ratio in the treatment of obesity and inflammatory bowel DISEASE. Microorganisms. https://doi.org/10.3390/microorganisms8111715
doi: 10.3390/microorganisms8111715 pubmed: 33139627 pmcid: 7692443
Palmas V, Pisanu S, Madau V, Casula E, Deledda A, Cusano R, Uva P, Vascellari S, Loviselli A, Manzin A, Velluzzi F (2021) Gut microbiota markers associated with obesity and overweight in Italian adults. Sci Rep 11:5532
pubmed: 33750881 pmcid: 7943584 doi: 10.1038/s41598-021-84928-w
Lau E, Belda E, Picq P, Carvalho D, Ferreira-Magalhaes M, Silva MM, Barroso I, Correia F, Vaz CP, Miranda I, Barbosa A, Clement K, Dore J, Freitas P, Prifti E (2021) Gut microbiota changes after metabolic surgery in adult diabetic patients with mild obesity: a randomised controlled trial. Diabetol Metab Syndr 13:56
pubmed: 34020709 pmcid: 8139007 doi: 10.1186/s13098-021-00672-1
Koliada A, Syzenko G, Moseiko V, Budovska L, Puchkov K, Perederiy V, Gavalko Y, Dorofeyev A, Romanenko M, Tkach S, Sineok L, Lushchak O, Vaiserman A (2017) Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population. BMC Microbiol 17:120
pubmed: 28532414 pmcid: 5440985 doi: 10.1186/s12866-017-1027-1
Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P, Balamurugan R (2020) The firmicutes/bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients? Nutrients. https://doi.org/10.3390/nu12051474
doi: 10.3390/nu12051474 pubmed: 32438689 pmcid: 7285218
Finotello F, Mastrorilli E, Di Camillo B (2018) Measuring the diversity of the human microbiota with targeted next-generation sequencing. Brief Bioinform 19:679–692
pubmed: 28025179
Anhe FF, Schertzer JD, Marette A (2019) Bacteria to alleviate metabolic syndrome. Nat Med 25:1031–1033
pubmed: 31263287 doi: 10.1038/s41591-019-0516-1
Deluca HF, Cantorna MT (2001) Vitamin D: its role and uses in immunology. FASEB J 15:2579–2585
pubmed: 11726533 doi: 10.1096/fj.01-0433rev
Gurung M, Li Z, You H, Rodrigues R, Jump DB, Morgun A, Shulzhenko N (2020) Role of gut microbiota in type 2 diabetes pathophysiology. EBioMedicine 51:102590
pubmed: 31901868 pmcid: 6948163 doi: 10.1016/j.ebiom.2019.11.051
Bellerba F, Muzio V, Gnagnarella P, Facciotti F, Chiocca S, Bossi P, Cortinovis D, Chiaradonna F, Serrano D, Raimondi S, Zerbato B, Palorini R, Canova S, Gaeta A, Gandini S (2021) The association between vitamin D and gut microbiota: a systematic review of human studies. Nutrients. https://doi.org/10.3390/nu13103378
doi: 10.3390/nu13103378 pubmed: 34684379 pmcid: 8540279
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv. https://doi.org/10.1016/0006-3207(92)91201-3
doi: 10.1016/0006-3207(92)91201-3
Faith DP, Lozupone CA, Nipperess D, Knight R (2009) The cladistic basis for the phylogenetic diversity (PD) measure links evolutionary features to environmental gradients and supports broad applications of microbial ecology’s “phylogenetic beta diversity” framework. Int J Mol Sci 10:4723–4741
pubmed: 20087461 pmcid: 2808007 doi: 10.3390/ijms10114723
Azim S, Kashyap SR (2016) Bariatric surgery: pathophysiology and outcomes. Endocrinol Metab Clin North Am 45(4):905–921. https://doi.org/10.1016/j.ecl.2016.06.011
doi: 10.1016/j.ecl.2016.06.011 pubmed: 27823611 pmcid: 9075538
Karami R, Kermansaravi M, Pishgahroudsari M et al (2021) Changes in gut microbial flora after Roux-en-Y gastric bypass and sleeve gastrectomy and their effects on post-operative weight loss. Updates Surg 73:1493–1499
pubmed: 33067675 doi: 10.1007/s13304-020-00900-9

Auteurs

Flavio De Maio (F)

Dipartimento Di Scienze Di Laboratorio E Infettivologiche, Fondazione Policlinico A. Gemelli IRCCS, Università Cattolica del Sacro Cuore, Rome, Italy.

Cristian Eugeniu Boru (CE)

General Surgery Division, Sant'Andrea Hospital, Department of Medical Surgical Sciences and Translational Medicine and Department of Medical-Surgical Sciences and Biotechnologies, University "La Sapienza" of Rome, Via Di Grottarossa N. 1035, 00189, Rome, Italy. cristian.boru@uniroma1.it.

Nunzio Velotti (N)

Department of Advanced Biomedical Sciences, University of Naples "Federico II", Naples, Italy.

Danila Capoccia (D)

General Surgery Division, Sant'Andrea Hospital, Department of Medical Surgical Sciences and Translational Medicine and Department of Medical-Surgical Sciences and Biotechnologies, University "La Sapienza" of Rome, Via Di Grottarossa N. 1035, 00189, Rome, Italy.

Giulia Santarelli (G)

Dipartimento Di Scienze Biotecnologiche Di Base, Cliniche Intensivologiche e Perioperatorie - Sezione di Microbiologia, Università Cattolica del Sacro Cuore, Rome, Italy.

Ornella Verrastro (O)

Division of Endocrine and Metabolic Surgery, Fondazione Policlinico A. Gemelli IRCCS, Università Cattolica del Sacro Cuore, Rome, Italy.

Delia Mercedes Bianco (DM)

Dipartimento Di Scienze Biotecnologiche Di Base, Cliniche Intensivologiche e Perioperatorie - Sezione di Microbiologia, Università Cattolica del Sacro Cuore, Rome, Italy.

Brunella Capaldo (B)

Department of Clinical Medicine and Surgery, University of Naples ''Federico II", Naples, Italy.

Maurizio Sanguinetti (M)

Dipartimento Di Scienze Di Laboratorio E Infettivologiche, Fondazione Policlinico A. Gemelli IRCCS, Università Cattolica del Sacro Cuore, Rome, Italy.
Dipartimento Di Scienze Biotecnologiche Di Base, Cliniche Intensivologiche e Perioperatorie - Sezione di Microbiologia, Università Cattolica del Sacro Cuore, Rome, Italy.

Mario Musella (M)

Department of Advanced Biomedical Sciences, University of Naples "Federico II", Naples, Italy.

Marco Raffaelli (M)

Division of Endocrine and Metabolic Surgery, Fondazione Policlinico A. Gemelli IRCCS, Università Cattolica del Sacro Cuore, Rome, Italy.

Frida Leonetti (F)

General Surgery Division, Sant'Andrea Hospital, Department of Medical Surgical Sciences and Translational Medicine and Department of Medical-Surgical Sciences and Biotechnologies, University "La Sapienza" of Rome, Via Di Grottarossa N. 1035, 00189, Rome, Italy.

Giovani Delogu (G)

Dipartimento Di Scienze Biotecnologiche Di Base, Cliniche Intensivologiche e Perioperatorie - Sezione di Microbiologia, Università Cattolica del Sacro Cuore, Rome, Italy.
Mater Olbia Hospital, Olbia, Italy.

Gianfranco Silecchia (G)

General Surgery Division, Sant'Andrea Hospital, Department of Medical Surgical Sciences and Translational Medicine and Department of Medical-Surgical Sciences and Biotechnologies, University "La Sapienza" of Rome, Via Di Grottarossa N. 1035, 00189, Rome, Italy.

Classifications MeSH