ESBL-Type and AmpC-Type Beta-Lactamases in Third Generation Cephalosporin-Resistant Isolated from Animal Feces in Madagascar

Overview

Journal Animals (Basel)

Date 2024 Mar 13

PMID 38473126

Authors

Ulrich Schotte

Julian Ehlers

Johanna Nieter

Raphael Rakotozandrindrainy

Silver A Wolf

Torsten Semmler

Hagen Frickmann

Sven Poppert

Christa Ewers

Affiliations

Soon will be listed here.

Abstract

Third generation cephalosporin-resistant (3GCR) are known to be prevalent in Madagascar, with high colonization or infection rates in particular in Madagascan patients. Extended spectrum beta-lactamases (ESBLs) have been reported to be the predominant underlying resistance mechanism in human isolates. So far, little is known on antimicrobial resistance and its molecular determinants in and other bacteria causing enteric colonization of Madagascan wild animals. To address this topic, swabs from 49 animal stool droppings were collected in the Madagascan Tsimanapesotsa National Park and assessed by cultural growth of bacterial microorganisms on elective media. In addition to 7 spp., a total of 31 growing on elective agar for could be isolated and subjected to whole genome sequencing. spp. was the most frequently isolated genus, and AmpC-type beta-lactamases were the quantitatively dominating molecular resistance mechanism. In contrast, the gene, which has repeatedly been associated with 3GC-resistance in Madagascan from humans, was detected in a single isolate only. The identification of the fosfomycin-resistance gene in a high proportion of isolates is concerning, as fosfomycin is increasingly used to treat infections caused by multidrug-resistant bacteria. In conclusion, the proof-of-principle assessment indicated a high colonization rate of resistant bacteria in stool droppings of Madagascan wild animals with a particular focus on 3GCR . Future studies should confirm these preliminary results in a more systematic way and assess the molecular relationship of animal and human isolates to identify potential routes of transmission.

References

Rakotondrasoa A, Passet V, Herindrainy P, Garin B, Kermorvant-Duchemin E, Delarocque-Astagneau E . Characterization of Klebsiella pneumoniae isolates from a mother-child cohort in Madagascar. J Antimicrob Chemother. 2020; 75(7):1736-1746. DOI: 10.1093/jac/dkaa107. View

Osei Sekyere J, Reta M, Bernard Fourie P . Risk factors for, and molecular epidemiology and clinical outcomes of, carbapenem- and polymyxin-resistant Gram-negative bacterial infections in pregnant women, infants, and toddlers: a systematic review and meta-analyses. Ann N Y Acad Sci. 2021; 1502(1):54-71. DOI: 10.1111/nyas.14650. View

Ehlers J, Poppert S, Ratovonamana R, Ganzhorn J, Tappe D, Kruger A . Ectoparasites of endemic and domestic animals in southwest Madagascar. Acta Trop. 2019; 196:83-92. DOI: 10.1016/j.actatropica.2019.05.008. View

Tse H, Gu Q, Sze K, Chu I, Kao R, Lee K . A tricyclic pyrrolobenzodiazepine produced by is associated with cytotoxicity in antibiotic-associated hemorrhagic colitis. J Biol Chem. 2017; 292(47):19503-19520. PMC: 5702686. DOI: 10.1074/jbc.M117.791558. View

Merla C, Rodrigues C, Passet V, Corbella M, Thorpe H, Kallonen T . Description of sp. nov. and of sp. nov. Front Microbiol. 2019; 10:2360. PMC: 6824210. DOI: 10.3389/fmicb.2019.02360. View

Dos Santos A, Ferrari R, Conte-Junior C . Type three secretion system in Salmonella Typhimurium: the key to infection. Genes Genomics. 2020; 42(5):495-506. DOI: 10.1007/s13258-020-00918-8. View

Naas T, Cuzon G, Robinson A, Andrianirina Z, Imbert P, Ratsima E . Neonatal infections with multidrug-resistant ESBL-producing E. cloacae and K. pneumoniae in Neonatal Units of two different Hospitals in Antananarivo, Madagascar. BMC Infect Dis. 2016; 16:275. PMC: 4902894. DOI: 10.1186/s12879-016-1580-5. View

Shibu P, McCuaig F, McCartney A, Kujawska M, Hall L, Hoyles L . Improved molecular characterization of the complex reveals the prevalence of the kleboxymycin biosynthetic gene cluster. Microb Genom. 2021; 7(6). PMC: 8461473. DOI: 10.1099/mgen.0.000592. View

Toy T, Pak G, Pham Duc T, Campbell J, El Tayeb M, von Kalckreuth V . Multicountry Distribution and Characterization of Extended-spectrum β-Lactamase-associated Gram-negative Bacteria From Bloodstream Infections in Sub-Saharan Africa. Clin Infect Dis. 2019; 69(Suppl 6):S449-S458. PMC: 6821266. DOI: 10.1093/cid/ciz450. View

10.

Randrianirina F, Vaillant L, Ramarokoto C, Rakotoarijaona A, Andriamanarivo M, Razafimahandry H . Antimicrobial resistance in pathogens causing nosocomial infections in surgery and intensive care units of two hospitals in Antananarivo, Madagascar. J Infect Dev Ctries. 2010; 4(2):74-82. DOI: 10.3855/jidc.454. View

11.

Randrianirina F, Ratsima E, Ramparany L, Randremanana R, Rakotonirina H, Andriamanantena T . Antimicrobial resistance of bacterial enteropathogens isolated from stools in Madagascar. BMC Infect Dis. 2014; 14:104. PMC: 3937528. DOI: 10.1186/1471-2334-14-104. View

12.

Hanson N, Sanders C . Regulation of inducible AmpC beta-lactamase expression among Enterobacteriaceae. Curr Pharm Des. 1999; 5(11):881-94. View

13.

Mattioni Marchetti V, Hrabak J, Bitar I . Fosfomycin resistance mechanisms in : an increasing threat. Front Cell Infect Microbiol. 2023; 13:1178547. PMC: 10352792. DOI: 10.3389/fcimb.2023.1178547. View

14.

Andriamanantena T, Ratsima E, Rakotonirina H, Randrianirina F, Ramparany L, Carod J . Dissemination of multidrug resistant Acinetobacter baumannii in various hospitals of Antananarivo Madagascar. Ann Clin Microbiol Antimicrob. 2010; 9:17. PMC: 2910008. DOI: 10.1186/1476-0711-9-17. View

15.

Conde-Perez K, Vazquez-Ucha J, Alvarez-Fraga L, Ageitos L, Rumbo-Feal S, Martinez-Guitian M . In-Depth Analysis of the Role of the Acinetobactin Cluster in the Virulence of . Front Microbiol. 2021; 12:752070. PMC: 8524058. DOI: 10.3389/fmicb.2021.752070. View

16.

Herindrainy P, Randrianirina F, Ratovoson R, Hariniana E, Buisson Y, Genel N . Rectal carriage of extended-spectrum beta-lactamase-producing gram-negative bacilli in community settings in Madagascar. PLoS One. 2011; 6(7):e22738. PMC: 3146483. DOI: 10.1371/journal.pone.0022738. View

17.

Randrianirina F, Soares J, Carod J, Ratsima E, Thonnier V, Combe P . Antimicrobial resistance among uropathogens that cause community-acquired urinary tract infections in Antananarivo, Madagascar. J Antimicrob Chemother. 2006; 59(2):309-12. DOI: 10.1093/jac/dkl466. View

18.

Rakotonirina H, Garin B, Randrianirina F, Richard V, Talarmin A, Arlet G . Molecular characterization of multidrug-resistant extended-spectrum β-lactamase-producing Enterobacteriaceae isolated in Antananarivo, Madagascar. BMC Microbiol. 2013; 13:85. PMC: 3639105. DOI: 10.1186/1471-2180-13-85. View

19.

Ahmad I, Nadeem A, Mushtaq F, Zlatkov N, Shahzad M, Zavialov A . Csu pili dependent biofilm formation and virulence of Acinetobacter baumannii. NPJ Biofilms Microbiomes. 2023; 9(1):101. PMC: 10721868. DOI: 10.1038/s41522-023-00465-6. View

20.

Jacoby G . Mechanisms of resistance to quinolones. Clin Infect Dis. 2005; 41 Suppl 2:S120-6. DOI: 10.1086/428052. View