Skip to main content
Top
Published in: Gut Pathogens 1/2020

01-12-2020 | Antibiotic | Research

Association of antimicrobial resistance and gut microbiota composition in human and non-human primates at an urban ecotourism site

Authors: C. W. Chong, A. H. S. Alkatheeri, N. Ali, Z. H. Tay, Y. L. Lee, S. J. Paramasivam, K. Jeevaratnam, W. Y. Low, S. H. E. Lim

Published in: Gut Pathogens | Issue 1/2020

Login to get access

Abstract

Background

The rise of nature-based ecotourism in the past decade has introduced unprecedented challenges in managing the increasing interaction between humans and animals. The potential transmission of antibiotic resistant microbes between humans and non-human primate populations is a concern due to their genetic similarity. Malaysia is well known for hotspots of wildlife diversity where non-human primates like monkeys and orangutans have become popular tourist attractions. In this study, we assessed the prevalence of antimicrobial resistant Staphylococcus aureus, Enterococcus species, and other Enterobacteriaceae in the faeces of human (HS) and two non-human primates (NHP) in Malaysia, the Long-tailed macaque (Macaca fascicularis, MF) and Silvered leaf monkey (Trachypithecus cristatus, TC). In addition, the faecal bacterial composition was profiled to evaluate the potential association between antibiotic resistant profiles and composition of gut microbiota.

Results

We tested the isolated bacteria using a selection of antibiotics. The results showed that both the number of antibiotic resistant strains and resistance level were higher in humans than NHPs. Overall, the composition of gut microbiome and pattern of antibiotic resistance showed that there was higher similarity between MF and TC, the two NHPs, than with HS. In addition, samples with higher levels of antibiotic resistance showed lower bacterial richness. Homo sapiens had the lowest bacterial diversity and yet it had higher abundance of Bacteroides. In contrast, NHPs displayed higher bacterial richness and greater prevalence of Firmicutes such as Ruminococceae and Oscillospira.

Conclusion

Higher antibiotic susceptibility in NHPs is likely related to low direct exposure to antibiotics. The lack of resistance may also suggest limited antimicrobial resistance transmission between humans and NHP. Nonetheless, continued monitoring over a long period will help mitigate the risk of anthropozoonosis and zooanthroponosis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Akyol M, Tatoğlu FY, Ustaoğlu M. Financing economic growth by dual banking in Malaysia: Empirical Evidence. In: Ustaoğlu M, İNcekara A, editors. Balancing Islamic and conventional banking for economic growth: empirical evidence from emerging economies. Cham: Springer; 2017. p. 69–84.CrossRef Akyol M, Tatoğlu FY, Ustaoğlu M. Financing economic growth by dual banking in Malaysia: Empirical Evidence. In: Ustaoğlu M, İNcekara A, editors. Balancing Islamic and conventional banking for economic growth: empirical evidence from emerging economies. Cham: Springer; 2017. p. 69–84.CrossRef
2.
go back to reference Carne C, Semple S, MacLarnon A, Majolo B, Maréchal L. Implications of tourist-Macaque interactions for disease transmission. EcoHealth. 2017;14(4):704–17.CrossRef Carne C, Semple S, MacLarnon A, Majolo B, Maréchal L. Implications of tourist-Macaque interactions for disease transmission. EcoHealth. 2017;14(4):704–17.CrossRef
3.
go back to reference Muehlenbein MP, Martinez LA, Lemke AA, Ambu L, Nathan S, Alsisto S, Sakong R. Unhealthy travelers present challenges to sustainable primate ecotourism. Travel Med Infecti Dis. 2010;8(3):169–75.CrossRef Muehlenbein MP, Martinez LA, Lemke AA, Ambu L, Nathan S, Alsisto S, Sakong R. Unhealthy travelers present challenges to sustainable primate ecotourism. Travel Med Infecti Dis. 2010;8(3):169–75.CrossRef
4.
go back to reference Lee WH, Moscardo G. Understanding the impact of ecotourism resort experiences on tourists’ environmental attitudes and behavioural intentions. J Sustain Tour. 2005;13(6):546–65.CrossRef Lee WH, Moscardo G. Understanding the impact of ecotourism resort experiences on tourists’ environmental attitudes and behavioural intentions. J Sustain Tour. 2005;13(6):546–65.CrossRef
5.
go back to reference Buckley RC, Morrison C, Castley JG. Net effects of ecotourism on threatened species survival. PLoS ONE. 2016;11(2):e0147988.CrossRef Buckley RC, Morrison C, Castley JG. Net effects of ecotourism on threatened species survival. PLoS ONE. 2016;11(2):e0147988.CrossRef
6.
go back to reference Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol. 2010;8:251.CrossRef Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol. 2010;8:251.CrossRef
7.
go back to reference Trinh P, Zaneveld JR, Safranek S, Rabinowitz PM. One health relationships between human, animal, and environmental microbiomes: a mini-review. Front Public Health. 2018;6:235.CrossRef Trinh P, Zaneveld JR, Safranek S, Rabinowitz PM. One health relationships between human, animal, and environmental microbiomes: a mini-review. Front Public Health. 2018;6:235.CrossRef
8.
go back to reference Ducarmon QR, Zwittink RD, Hornung BVH, van Schaik W, Young VB, Kuijper EJ. Gut microbiota and colonization resistance against bacterial enteric infection. Microbiol Mol Biol Rev. 2019;83(3):e00007–00019.CrossRef Ducarmon QR, Zwittink RD, Hornung BVH, van Schaik W, Young VB, Kuijper EJ. Gut microbiota and colonization resistance against bacterial enteric infection. Microbiol Mol Biol Rev. 2019;83(3):e00007–00019.CrossRef
9.
go back to reference Blancou J, Chomel BB, Belotto A, Meslin FX. Emerging or re-emerging bacterial zoonoses: factors of emergence, surveillance and control. Vet Res. 2005;36(3):507–22.CrossRef Blancou J, Chomel BB, Belotto A, Meslin FX. Emerging or re-emerging bacterial zoonoses: factors of emergence, surveillance and control. Vet Res. 2005;36(3):507–22.CrossRef
10.
go back to reference Unwin T, Smith A. Behavioral differences between provisioned and non-provisioned Barbary macaques (Macaca sylvanus). Anthrozoös. 2010;23(2):109–18.CrossRef Unwin T, Smith A. Behavioral differences between provisioned and non-provisioned Barbary macaques (Macaca sylvanus). Anthrozoös. 2010;23(2):109–18.CrossRef
11.
go back to reference McLennan MR, Spagnoletti N, Hockings KJ. The implications of primate behavioral flexibility for sustainable human-primate coexistence in anthropogenic habitats. Int J Primatol. 2017;38(2):105–21.CrossRef McLennan MR, Spagnoletti N, Hockings KJ. The implications of primate behavioral flexibility for sustainable human-primate coexistence in anthropogenic habitats. Int J Primatol. 2017;38(2):105–21.CrossRef
12.
go back to reference Maréchal L, MacLarnon A, Majolo B, Semple S. Primates’ behavioural responses to tourists: evidence for a trade-off between potential risks and benefits. Sci Rep. 2016;6:32465.CrossRef Maréchal L, MacLarnon A, Majolo B, Semple S. Primates’ behavioural responses to tourists: evidence for a trade-off between potential risks and benefits. Sci Rep. 2016;6:32465.CrossRef
13.
go back to reference Rousham EK, Unicomb L, Islam MA. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: integrating behavioural, epidemiological and one health approaches. Proc Biol Sci. 1876;2018(285):20180332. Rousham EK, Unicomb L, Islam MA. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: integrating behavioural, epidemiological and one health approaches. Proc Biol Sci. 1876;2018(285):20180332.
14.
go back to reference Grassotti TT, de Angelis Zvoboda D, da Fontoura Xavier Costa L, de Araújo AJG, Pereira RI, Soares RO, Wagner PGC, Frazzon J, Frazzon APG. Antimicrobial resistance profiles in Enterococcus spp. isolates from fecal samples of wild and captive black Capuchin monkeys (Sapajus nigritus) in South Brazil. Front Microbiol. 2018;9:2366.CrossRef Grassotti TT, de Angelis Zvoboda D, da Fontoura Xavier Costa L, de Araújo AJG, Pereira RI, Soares RO, Wagner PGC, Frazzon J, Frazzon APG. Antimicrobial resistance profiles in Enterococcus spp. isolates from fecal samples of wild and captive black Capuchin monkeys (Sapajus nigritus) in South Brazil. Front Microbiol. 2018;9:2366.CrossRef
15.
go back to reference Vittecoq M, Godreuil S, Prugnolle F, Durand P, Brazier L, Renaud N, Arnal A, Aberkane S, Jean-Pierre H, Gauthier-Clerc M, et al. Antimicrobial resistance in wildlife. J Appl Ecol. 2016;53(2):519–29.CrossRef Vittecoq M, Godreuil S, Prugnolle F, Durand P, Brazier L, Renaud N, Arnal A, Aberkane S, Jean-Pierre H, Gauthier-Clerc M, et al. Antimicrobial resistance in wildlife. J Appl Ecol. 2016;53(2):519–29.CrossRef
16.
go back to reference Fuentes A. Human culture and monkey behavior: assessing the contexts of potential pathogen transmission between macaques and humans. Am J Primatol. 2006;68(9):880–96.CrossRef Fuentes A. Human culture and monkey behavior: assessing the contexts of potential pathogen transmission between macaques and humans. Am J Primatol. 2006;68(9):880–96.CrossRef
17.
go back to reference Soulsbury CD, White PCL. Human–wildlife interactions in urban areas: a review of conflicts, benefits and opportunities. Wildl Res. 2015;42(7):541–53.CrossRef Soulsbury CD, White PCL. Human–wildlife interactions in urban areas: a review of conflicts, benefits and opportunities. Wildl Res. 2015;42(7):541–53.CrossRef
18.
go back to reference Harding LE. Trachypithecus cristatus (Primates: Cercopithecidae). Mammal Species. 2010;42(1):149–65.CrossRef Harding LE. Trachypithecus cristatus (Primates: Cercopithecidae). Mammal Species. 2010;42(1):149–65.CrossRef
19.
go back to reference Atiqah Tahir N, Ismail A, Rahman F. Daily activity budget of silver leaf monkeys (Trachypithcus cristatus) in Kuala Selangor Nature Park (KSNP), Peninsular Malaysia Malay. Nature J. 2017;69:337–43. Atiqah Tahir N, Ismail A, Rahman F. Daily activity budget of silver leaf monkeys (Trachypithcus cristatus) in Kuala Selangor Nature Park (KSNP), Peninsular Malaysia Malay. Nature J. 2017;69:337–43.
20.
go back to reference Bachiri T, Bakour S, Ladjouzi R, Thongpan L, Rolain JM, Touati A. High rates of CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae in wild boars and Barbary macaques in Algeria. J Glob Antimicrobia Resist. 2017;8:35–40.CrossRef Bachiri T, Bakour S, Ladjouzi R, Thongpan L, Rolain JM, Touati A. High rates of CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae in wild boars and Barbary macaques in Algeria. J Glob Antimicrobia Resist. 2017;8:35–40.CrossRef
21.
go back to reference Gonzalez BE, Martinez-Aguilar G, Hulten KG, Hammerman WA, Coss-Bu J, Avalos-Mishaan A, Mason EO Jr, Kaplan SL. Severe Staphylococcal sepsis in adolescents in the era of community-acquired methicillin-resistant Staphylococcus aureus. Pediatrics. 2005;115(3):642–8.CrossRef Gonzalez BE, Martinez-Aguilar G, Hulten KG, Hammerman WA, Coss-Bu J, Avalos-Mishaan A, Mason EO Jr, Kaplan SL. Severe Staphylococcal sepsis in adolescents in the era of community-acquired methicillin-resistant Staphylococcus aureus. Pediatrics. 2005;115(3):642–8.CrossRef
22.
go back to reference Senghore M, Bayliss SC, Kwambana-Adams BA, Foster-Nyarko E, Manneh J, Dione M, Badji H, Ebruke C, Doughty EL, Thorpe HA, et al. Transmission of Staphylococcus aureus from humans to green monkeys in the Gambia as revealed by whole-genome sequencing. Appl Environ Microbiol. 2016;82(19):5910.CrossRef Senghore M, Bayliss SC, Kwambana-Adams BA, Foster-Nyarko E, Manneh J, Dione M, Badji H, Ebruke C, Doughty EL, Thorpe HA, et al. Transmission of Staphylococcus aureus from humans to green monkeys in the Gambia as revealed by whole-genome sequencing. Appl Environ Microbiol. 2016;82(19):5910.CrossRef
23.
go back to reference Soge OO, No D, Michael KE, Dankoff J, Lane J, Vogel K, Smedley J, Roberts MC. Transmission of MDR MRSA between primates, their environment and personnel at a United States primate centre. J Antimicrob Chemother. 2016;71(10):2798–803.CrossRef Soge OO, No D, Michael KE, Dankoff J, Lane J, Vogel K, Smedley J, Roberts MC. Transmission of MDR MRSA between primates, their environment and personnel at a United States primate centre. J Antimicrob Chemother. 2016;71(10):2798–803.CrossRef
24.
go back to reference Menni C, Jackson MA, Pallister T, Steves CJ, Spector TD, Valdes AM. Gut microbiome diversity and high-fibre intake are related to lower long-term weight gain. Int J Obes. 2017;41:1099.CrossRef Menni C, Jackson MA, Pallister T, Steves CJ, Spector TD, Valdes AM. Gut microbiome diversity and high-fibre intake are related to lower long-term weight gain. Int J Obes. 2017;41:1099.CrossRef
25.
go back to reference Konikoff T, Gophna U. Oscillospira: a Central, Enigmatic Component of the Human Gut Microbiota. Trends Microbiol. 2016;24(7):523–4.CrossRef Konikoff T, Gophna U. Oscillospira: a Central, Enigmatic Component of the Human Gut Microbiota. Trends Microbiol. 2016;24(7):523–4.CrossRef
26.
go back to reference David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2013;505:559.CrossRef David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2013;505:559.CrossRef
27.
go back to reference Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell. 2010;141(7):1241–52.CrossRef Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell. 2010;141(7):1241–52.CrossRef
28.
go back to reference McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci. 2013;110(9):3229–366.CrossRef McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci. 2013;110(9):3229–366.CrossRef
29.
go back to reference Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13:790.CrossRef Buffie CG, Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol. 2013;13:790.CrossRef
30.
go back to reference Bahrndorff S, Alemu T, Alemneh T, Lund Nielsen J. The microbiome of animals: implications for conservation biology. Int J Genomics. 2016;2016:7.CrossRef Bahrndorff S, Alemu T, Alemneh T, Lund Nielsen J. The microbiome of animals: implications for conservation biology. Int J Genomics. 2016;2016:7.CrossRef
31.
go back to reference van Schaik W. The human gut resistome. Philos Trans R Soc Lond B Biol Sci. 2015;370(1670):20140087–20140087.CrossRef van Schaik W. The human gut resistome. Philos Trans R Soc Lond B Biol Sci. 2015;370(1670):20140087–20140087.CrossRef
32.
go back to reference Brown DF. Detection of methicillin/oxacillin resistance in Staphylococci. J Antimicrob Chemother. 2001;48(Suppl 1):65–70.CrossRef Brown DF. Detection of methicillin/oxacillin resistance in Staphylococci. J Antimicrob Chemother. 2001;48(Suppl 1):65–70.CrossRef
33.
go back to reference Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. App Environ Microbiol. 2009;75(23):7537.CrossRef Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. App Environ Microbiol. 2009;75(23):7537.CrossRef
34.
go back to reference Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(Database):D590–D596596.PubMed Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(Database):D590–D596596.PubMed
35.
go back to reference McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8(4):e61217.CrossRef McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8(4):e61217.CrossRef
36.
go back to reference Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.PubMedPubMedCentral Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.PubMedPubMedCentral
Metadata
Title
Association of antimicrobial resistance and gut microbiota composition in human and non-human primates at an urban ecotourism site
Authors
C. W. Chong
A. H. S. Alkatheeri
N. Ali
Z. H. Tay
Y. L. Lee
S. J. Paramasivam
K. Jeevaratnam
W. Y. Low
S. H. E. Lim
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2020
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-020-00352-x

Other articles of this Issue 1/2020

Gut Pathogens 1/2020 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.