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Acquisition of multidrug-resistant bacteria and encoding genes among French pilgrims during the 2017 and 2018 Hajj

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Abstract

The objective of this study is to determine the acquisition of multidrug-resistant (MDR) bacteria and antibiotic resistance-encoding genes by French Hajj pilgrims and associated risk factors. Pilgrims traveling during the 2017 and 2018 Hajj were recruited. All pilgrims underwent two successive systematic nasopharyngeal and rectal swabs, pre- and post-Hajj. Specific culture media were used to screen for MDR bacteria, including methicillin-resistant Staphylococcus aureus (MRSA), carbapenem-resistant bacteria, and extended spectrum beta-lactamase producing Enterobacteriaceae (ESBL-E). qPCR was used to identify antibiotic resistance-encoding genes from cultured isolates. Direct screening of genes encoding for colistin resistance (mcr-1, 2, 3, 4, 5, and 8) from nasopharyngeal and rectal swabs was performed using qPCR, and positive qPCR results were simultaneously tested by sequencing. There were 268 pilgrims included. The percentage of pilgrims acquiring MDR bacteria during the Hajj was 19.4%. A total of 81 strains were isolated (1 carbapenem-resistant Acinetobacter baumannii, 12 MRSA, and 68 ESBL-E). ESBL-E strains were found in rectal samples of 6.0% pilgrims pre-Hajj and of 16.4% pilgrims post-Hajj. Only 0.4% pilgrims were positive for CARB post-Hajj and 1.9% carried nasal MRSA pre- and post-Hajj. In addition, 23 (8.6%) post-Hajj rectal swabs were positive for mcr genes (19 mcr-1 gene and 4 mcr-4 gene). No significant association was found between co-factors and acquisition of MDR bacteria or mcr genes. MDR bacteria and genes are acquired by pilgrims during the Hajj mass gathering. Rationalization of antibiotic consumption and implementation of measures to prevent transmission of bacteria among pilgrims during the event are of paramount importance.

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Data availability

The datasets generated during and/or analyzed during the current study are available from corresponding author [P.G] on reasonable request.

References

  1. Memish ZA, Steffen R, White P, Dar O, Azhar EI, Sharma A, Zumla A (2019) Mass gatherings medicine: public health issues arising from mass gathering religious and sporting events. Lancet 393:2073–2084

    Article  PubMed  PubMed Central  Google Scholar 

  2. Yezli S, Bieh K, Khan A (2019) No measles cases during the 2019 Hajj. Lancet Infect Dis 19:1169–1170

    Article  PubMed  Google Scholar 

  3. Hoang V-T, Gautret P (2018) Infectious diseases and mass gatherings. Curr Infect Dis Rep 20:44

    Article  PubMed  PubMed Central  Google Scholar 

  4. Hoang V-T, Nguyen T-T-T, Belhouchat K, Meftah M, Sow D, Benkouiten S, Dao T-L, Anh Ly TD, Drali T, Yezli S, Alotaibi B, Raoult D, Parola P, Pommier de Santi V, Gautret P (2019) Antibiotic use for respiratory infections among Hajj pilgrims: a cohort survey and review of the literature. Travel Med Infect Dis 30:39–45

    Article  PubMed  Google Scholar 

  5. Leangapichart T, Rolain J-M, Memish ZA, Al-Tawfiq JA, Gautret P (2017) Emergence of drug resistant bacteria at the Hajj: a systematic review. Travel Med Infect Dis 18:3–17

    Article  PubMed  Google Scholar 

  6. Leangapichart T, Dia NM, Olaitan AO, Gautret P, Brouqui P, Rolain J-M (2016) Acquisition of extended-spectrum β-lactamases by Escherichia coli and Klebsiella pneumoniae in gut microbiota of pilgrims during the Hajj pilgrimage of 2013. Antimicrob Agents Chemother 60:3222–3226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Leangapichart T, Tissot-Dupont H, Raoult D, Memish ZA, Rolain J-M, Gautret P (2017) Risk factors for acquisition of CTX-M genes in pilgrims during Hajj 2013 and 2014. J Antimicrob Chemother 72:2627–2635

    Article  CAS  PubMed  Google Scholar 

  8. Leangapichart T, Gautret P, Griffiths K, Belhouchat K, Memish Z, Raoult D, Rolain J-M (2016) Acquisition of a High Diversity of Bacteria during the Hajj pilgrimage, including Acinetobacter baumannii with blaOXA-72 and Escherichia coli with blaNDM-5 Carbapenemase genes. Antimicrob Agents Chemother 60:5942–5948

    Article  PubMed  PubMed Central  Google Scholar 

  9. Hoang VT, Dao TL, Ly TDA, Sow D, Belhouchat K, Larbi Chaht K, Ninove L, Drali T, Yezli S, Alotaibi B, Raoult D, Parola P, de Santi VP, Gautret P (2020) Gastrointestinal symptoms and the acquisition of enteric pathogens in Hajj pilgrims: a 3-year prospective cohort study. Eur J Clin Microbiol Infect Dis. https://doi.org/10.1007/s10096-020-04018-z

  10. Haut Conseil de la santé publique. Bull Epidemiol Hebdo (2017) Recommandations sanitaires pour les voyageurs. http://opac.invs.sante.fr/doc_num.php?explnum_id=10785. Accessed 5 Dec 2020

  11. Direction Générale de la Santé. Ministère des Affaires sociales, de la Santé et des Droits des femmes (2017) Calendrier des vaccinations et recommandations vaccinales 2017 https://www.mesvaccins.net/textes/calendrier_vaccinations_2017.pdf. Accessed 5 Dec 2020

  12. Haut Conseil de la santé publique. Bull Epidemiol Hebdo (2018) Recommandations sanitaires pour les voyageurs https://invs.santepubliquefrance.fr/content/.../62/file/Recommandations_voyageurs_2018.pdf. Accessed 5 Dec 2020

  13. Direction Générale de la Santé. Ministère des Affaires sociales, de la Santé et des Droits des femmes (2018) Calendrier des vaccinations et recommandations vaccinales 2018, https://solidarites-sante.gouv.fr/IMG/pdf/calendrier_vaccinations_2018.pdf. Accessed 5 Dec 2020

  14. Rashid H, Shafi S, El Bashir H, Haworth E, Memish ZA, Ali KA, Booy R (2008) Influenza and the Hajj: defining influenza-like illness clinically. Int J Infect Dis 12:102–103

    Article  PubMed  Google Scholar 

  15. WHO. Body mass index – BMI (2020) http://www.euro.who.int/en/health-topics/disease-prevention/nutrition/a-healthy-lifestyle/body-mass-index-bmi. Accessed 5 Dec 2020

  16. Hoang V-T, Dao T-L, Ly TDA, Belhouchat K, Chaht KL, Gaudart J, Mrenda BM, Drali T, Yezli S, Alotaibi B, Fournier P-E, Raoult D, Parola P, de Santi VP, Gautret P (2019) The dynamics and interactions of respiratory pathogen carriage among French pilgrims during the 2018 Hajj. Emerg Microbes Infect 8:1701–1710

    Article  PubMed  PubMed Central  Google Scholar 

  17. Galia L, Ligozzi M, Bertoncelli A, Mazzariol A (2019) Real-time PCR assay for detection of Staphylococcus aureus, Panton-Valentine Leucocidin and methicillin resistance directly from clinical samples. AIMS Microbiol 5:138–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Nijhuis RHT, van Maarseveen NM, van Hannen EJ, van Zwet AA, Mascini EM (2014) A rapid and high-throughput screening approach for methicillin-resistant Staphylococcus aureus based on the combination of two different real-time PCR assays. J Clin Microbiol 52:2861–2867

    Article  PubMed  PubMed Central  Google Scholar 

  19. Roschanski N, Fischer J, Guerra B, Roesler U (2014) Development of a multiplex real-time PCR for the rapid detection of the predominant beta-lactamase genes CTX-M, SHV, TEM and CIT-type AmpCs in Enterobacteriaceae. PLoS One 9:e100956

    Article  PubMed  PubMed Central  Google Scholar 

  20. Mesli E, Berrazeg M, Drissi M, Bekkhoucha SN, Rolain J-M (2013) Prevalence of carbapenemase-encoding genes including New Delhi metallo-β-lactamase in Acinetobacter species, Algeria. Int J Infect Dis 17:e739–e743

    Article  CAS  PubMed  Google Scholar 

  21. Sow D, Parola P, Sylla K, Ndiaye M, Delaunay P, Halfon P, Camiade S, Dieng T, Tine RCK, Faye B, Ndiaye JL, Dieng Y, Gaye O, Raoult D, Bittar F (2017) Performance of real-time polymerase chain reaction assays for the detection of 20 gastrointestinal parasites in clinical samples from Senegal. Am J Trop Med Hyg 97:173–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Edouard S, Prudent E, Gautret P, Memish ZA, Raoult D (2015) Cost-effective pooling of DNA from nasopharyngeal swab samples for large-scale detection of bacteria by real-time PCR. J Clin Microbiol 53:1002–1004

    Article  PubMed  PubMed Central  Google Scholar 

  23. Dandachi I, Fayad E, Sleiman A, Daoud Z, Rolain J-M (2020) Dissemination of multidrug-resistant and mcr-1 gram-negative bacilli in broilers, farm workers, and the surrounding environment in Lebanon. Microb Drug Resist 26:368–377

    Article  CAS  PubMed  Google Scholar 

  24. Nabti LZ, Sahli F, Ngaiganam EP, Radji N, Mezaghcha W, Lupande-Mwenebitu D, Baron SA, Rolain J-M, Diene SM (2020) Development of real-time PCR assay allowed describing the first clinical Klebsiella pneumoniae isolate harboring plasmid-mediated colistin resistance mcr-8 gene in Algeria. J Glob Antimicrob Resist 20:266–271

    Article  PubMed  Google Scholar 

  25. Chabou S, Leangapichart T, Okdah L, Le Page S, Hadjadj L, Rolain J-M (2016) Real-time quantitative PCR assay with Taqman(®) probe for rapid detection of MCR-1 plasmid-mediated colistin resistance. New Microbes New Infect 13:71–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Rebelo AR, Bortolaia V, Kjeldgaard JS, Pedersen SK, Leekitcharoenphon P, Hansen IM, Guerra B, Malorny B, Borowiak M, Hammerl JA, Battisti A, Franco A, Alba P, Perrin-Guyomard A, Granier SA, De Frutos EC, Malhotra-Kumar S, Villa L, Carattoli A, Hendriksen RS (2018) Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Euro Surveill 23:17–00672

    Article  PubMed Central  Google Scholar 

  27. Haseeb A, Faidah HS, Bakhsh AR, Malki WHA, Elrggal ME, Saleem F, Rahman SU, Khan TM, Hassali MA (2016) Antimicrobial resistance among pilgrims: a retrospective study from two hospitals in Makkah, Saudi Arabia. Int J Infect Dis 47:92–94

    Article  PubMed  Google Scholar 

  28. Memish ZA, Balkhy HH, Almuneef MA, Al-Haj-Hussein BT, Bukhari AI, Osoba AO (2006) Carriage of Staphylococcus aureus among Hajj pilgrims. Saudi Med J 27:1367–1372

    PubMed  Google Scholar 

  29. Tham J, Odenholt I, Walder M, Brolund A, Ahl J, Melander E (2010) Extended-spectrum beta-lactamase-producing Escherichia coli in patients with travellers’ diarrhoea. Scand J Infect Dis 42:275–280

    Article  CAS  PubMed  Google Scholar 

  30. Kuenzli E, Jaeger VK, Frei R, Neumayr A, DeCrom S, Haller S, Blum J, Widmer AF, Furrer H, Battegay M, Endimiani A, Hatz C (2014) High colonization rates of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in Swiss travellers to South Asia– a prospective observational multicentre cohort study looking at epidemiology, microbiology and risk factors. BMC Infect Dis 14:528

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kantele A, Lääveri T, Mero S, Vilkman K, Pakkanen SH, Ollgren J, Antikainen J, Kirveskari J (2015) Antimicrobials increase travelers’ risk of colonization by extended-spectrum betalactamase-producing Enterobacteriaceae. Clin Infect Dis 60:837–846

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kantele A, Mero S, Kirveskari J, Lääveri T (2017) Fluoroquinolone antibiotic users select fluoroquinolone-resistant ESBL-producing Enterobacteriaceae (ESBL-PE) - data of a prospective traveller study. Travel Med Infect Dis 16:23–30

    Article  PubMed  Google Scholar 

  33. Bell M (2014) Antibiotic misuse: a global crisis. JAMA Intern Med 174:1920–1921

    Article  PubMed  Google Scholar 

  34. Qureshi H, Gessner BD, Leboulleux D, Hasan H, Alam SE, Moulton LH (2000) The incidence of vaccine preventable influenza-like illness and medication use among Pakistani pilgrims to the Haj in Saudi Arabia. Vaccine 18:2956–2962

    Article  CAS  PubMed  Google Scholar 

  35. Mustafa AN, Gessner BD, Ismail R, Yusoff AF, Abdullah N, Ishak I, Abdullah N, Merican MI (2003) A case-control study of influenza vaccine effectiveness among Malaysian pilgrims attending the Haj in Saudi Arabia. Int J Infect Dis 7:210–214

    Article  PubMed  Google Scholar 

  36. Angelin M, Forsell J, Granlund M, Evengård B, Palmgren H, Johansson A (2015) Risk factors for colonization with extended-spectrum beta-lactamase producing Enterobacteriaceae in healthcare students on clinical assignment abroad: a prospective study. Travel Med Infect Dis 13:223–229

    Article  PubMed  Google Scholar 

  37. Schaumburg F, Sertic SM, Correa-Martinez C, Mellmann A, Köck R, Becker K (2019) Acquisition and colonization dynamics of antimicrobial-resistant bacteria during international travel: a prospective cohort study. Clin Microbiol Infect 25:1287.e1–1287.e7

    Article  CAS  Google Scholar 

  38. Lübbert C, Straube L, Stein C, Makarewicz O, Schubert S, Mössner J, Pletz MW, Rodloff AC (2015) Colonization with extended-spectrum beta-lactamase-producing and carbapenemase-producing Enterobacteriaceae in international travelers returning to Germany. Int J Med Microbiol 305:148–156

    Article  PubMed  Google Scholar 

  39. Leangapichart T, Gautret P, Brouqui P, Memish ZA, Raoult D, Rolain J-M (2016) Acquisition of mcr-1 plasmid-mediated colistin resistance in Escherichia coli and Klebsiella pneumoniae during Hajj 2013 and 2014. Antimicrob Agents Chemother 60:6998–6999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu L-F, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu J-H, Shen J (2016) Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16:161–168

    Article  PubMed  Google Scholar 

  41. Hadjadj L, Riziki T, Zhu Y, Li J, Diene SM, Rolain J-M (2017) Study of mcr-1 gene-mediated colistin resistance in Enterobacteriaceae isolated from humans and animals in different countries. Genes (Basel) 8:394

    Article  Google Scholar 

  42. Rapoport M, Faccone D, Pasteran F, Ceriana P, Albornoz E, Petroni A, MCR Group, Corso A (2016) First description of mcr-1-mediated colistin resistance in human infections caused by Escherichia coli in Latin America. Antimicrob Agents Chemother 60:4412–4413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Elbediwi M, Li Y, Paudyal N, Pan H, Li X, Xie S, Rajkovic A, Feng Y, Fang W, Rankin SC, Yue M (2019) Global burden of colistin-resistant bacteria: mobilized colistin resistance genes study (1980–2018). Microorganisms 7:461

    Article  CAS  PubMed Central  Google Scholar 

  44. Olaitan AO, Thongmalayvong B, Akkhavong K, Somphavong S, Paboriboune P, Khounsy S, Morand S, Rolain J-M (2015) Clonal transmission of a colistin-resistant Escherichia coli from a domesticated pig to a human in Laos. J Antimicrob Chemother 70:3402–3404

    CAS  PubMed  Google Scholar 

  45. Zhang X-F, Doi Y, Huang X, Li H-Y, Zhong L-L, Zeng K-J, Zhang Y-F, Patil S, Tian G-B (2016) Possible transmission of mcr-1-harboring Escherichia coli between companion animals and human. Emerg Infect Dis 22:1679–1681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Carattoli A, Villa L, Feudi C, Curcio L, Orsini S, Luppi A, Pezzotti G, Magistrali CF (2017) Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Euro Surveill 22:30589

    Article  PubMed  PubMed Central  Google Scholar 

  47. Cienfuegos AV, Ocampo AM, Higuita LF, Jiménez N (2016) Risk factors for the acquisition of colistin and carbapenem-resistant Klebsiella pneumoniae in Medellín-Colombia, an endemic region for carbapenem resistance. Int J Infect Dis 53:39–40

    Article  Google Scholar 

  48. Hoang V-T, Sow D, Belhouchat K, Dao T-L, Ly TDA, Fenollar F, Yezli S, Alotaibi B, Raoult D, Parola P, Pommier de Santi V, Gautret P (2020) Environmental investigation of respiratory pathogens during the Hajj 2016 and 2018. Travel Med Infect Dis 33:101500

    Article  PubMed  Google Scholar 

  49. Khedher MB, Baron SA, Riziki T, Ruimy R, Raoult D, Diene SM, Rolain J-M (2020) Massive analysis of 64,628 bacterial genomes to decipher water reservoir and origin of mobile colistin resistance genes: is there another role for these enzymes? Sci Rep 10:5970

    Article  PubMed  PubMed Central  Google Scholar 

  50. Benkouiten S, Brouqui P, Gautret P (2014) Non-pharmaceutical interventions for the prevention of respiratory tract infections during Hajj pilgrimage. Travel Med Infect Dis 12:429–442

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by the Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, the French National Research Agency under the “Investissements d’avenir” program, reference ANR-10-IAHU-03, the Région Provence Alpes Côte d’Azur, and European ERDF PRIMI funding.

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Authors and Affiliations

  1. IRD, AP-HM, SSA, VITROME, Aix Marseille University, Marseille, France

    Van-Thuan Hoang, Thi-Loi Dao, Tran Duc Anh Ly, Khadidja Belhouchat, Kamel Larbi Chaht, Philippe Parola, Vincent Pommier de Santi & Philippe Gautret

  2. Institut Hospitalo-Universitaire Méditerranée Infection, 19-21 Boulevard Jean Moulin, 13385, Marseille Cedex 05, France

    Van-Thuan Hoang, Thi-Loi Dao, Tran Duc Anh Ly, Frédérique Gouriet, Linda Hadjadj, Khadidja Belhouchat, Kamel Larbi Chaht, Didier Raoult, Philippe Parola, Sophie Alexandra Baron, Vincent Pommier de Santi, Jean-Marc Rolain & Philippe Gautret

  3. Thai Binh University of Medicine and Pharmacy, Thai Binh, Vietnam

    Van-Thuan Hoang & Thi-Loi Dao

  4. IRD, AP-HM, MEPHI, Aix Marseille University, Marseille, France

    Frédérique Gouriet, Linda Hadjadj, Didier Raoult, Sophie Alexandra Baron & Jean-Marc Rolain

  5. The Global Centre for Mass Gatherings Medicine, Ministry of Health, Riyadh, Saudi Arabia

    Saber Yezli & Badriah Alotaibi

  6. French Military Center for Epidemiology and Public Health Marseille, Marseille, France

    Vincent Pommier de Santi

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  1. Van-Thuan Hoang
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  2. Thi-Loi Dao
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  3. Tran Duc Anh Ly
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  13. Vincent Pommier de Santi
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Contributions

Conceptualization: Van Thuan Hoang, Philippe Gautret, Vincent Pommier de Santi, and Jean-Marc Rolain.

Methodology: Jean-Marc Rolain, Frédérique Gouriet, Linda Hadjadj, Sophie Alexandra Baron, and Philippe Gautret.

Laboratory technic: Van Thuan Hoang, Thi-Loi Dao, and Tran Duc Anh Ly.

Data collection: Khadidja Belhouchat and Kamel Larbi Chaht.

Formal analysis and investigation: Van Thuan Hoang, Sophie Alexandra Baron, Jean-Marc Rolain, and Philippe Gautret.

Writing original draft and preparation: Van Thuan Hoang and Philippe Gautret.

Writing—review and editing: Thi-Loi Dao, Tran Duc Anh Ly, Frédérique Gouriet, Linda Hadjadj, Khadidja Belhouchat, Kamel Larbi Chaht, Saber Yezli, Badriah Alotaibi, Didier Raoult, Philippe Parola, Sophie Alexandra Baron, Vincent Pommier de Santi, and Jean-Marc Rolain.

Supervision: Philippe Gautret.

Corresponding author

Correspondence to Philippe Gautret.

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The authors declare that they have no conflict of interest.

Ethical approval

The protocol was performed according to the good clinical practices recommended by the Declaration of Helsinki and its amendments and approved by the Aix-Marseille University institutional review board (July 23, 2013; reference No. 2013-A00961-44).

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Written informed consent was obtained from all individual participants included in the study.

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Hoang, VT., Dao, TL., Ly, T.D.A. et al. Acquisition of multidrug-resistant bacteria and encoding genes among French pilgrims during the 2017 and 2018 Hajj. Eur J Clin Microbiol Infect Dis 40, 1199–1207 (2021). https://doi.org/10.1007/s10096-020-04122-0

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