Skip to main content
SpringerLink
Log in

Antimicrobial Stewardship in Captive Monkeys

  • Chapter
  • First Online:
Neglected Diseases in Monkeys

Abstract

Antimicrobial resistance (AMR) is a growing threat in veterinary medicine, and although there is an expanding body of literature of the AMR prevalence in food animal and companion animal populations, little data on AMR exists in primate veterinary medicine. The monkey-human interface is extensive, especially in biomedical research and zoos, and these monkeys are frequently infected with bacteria that can be transmitted between monkeys and humans. The prevalence of antimicrobial resistant zoonotic bacteria has the potential to impact animal, human, and environmental health worldwide. Primate veterinarians frequently treat bidirectional zoonotic infections with antimicrobials classified as “critically important” by the World Health Organization, and such antimicrobial use (AMU) can influence AMR in humans and the environment. Consequently, medical primatologists have a public health obligation to use antimicrobials judiciously. Antimicrobial stewardship is especially important because the selective pressure of repeated AMU can promote the spread of AMR within and between monkeys and to humans with zoonotic transmission. Effective antimicrobial stewardship programs utilize a multi-modal approach involving a coordinated team with protocols for appropriate antimicrobial selection and practice and ongoing monitoring strategies for antimicrobial use, AMR, and patient outcomes. This multi-modal tactic is necessary to contest AMR on a One Health scale. Veterinarians are in a position to create comprehensive antimicrobial stewardship programs and reduce the threats of AMR on monkey and human health.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abee CR, Mansfield K, Tardif S, Morris T (eds) (2012) Nonhuman primates in biomedical research: diseases, 2nd edn. Elsevier/Academic, London

    Google Scholar 

  • Angulo FJ, Nunnery JA, Bair HD (2004) Antimicrobial resistance in zoonotic enteric pathogens. Rev Sci Tech Off Int Epizoot 23(2):485–496

    Article  CAS  Google Scholar 

  • Bailey C, Mansfield K (2010) Review paper: emerging and reemerging infectious diseases of nonhuman primates in the laboratory setting. Vet Pathol 47(3):462–481

    Google Scholar 

  • Banish LD, Sims R, Sack D, Montali RJ, Phillips L, Bush M (1993) Prevalence of shigellosis and other enteric pathogens in a zoologic collection of primates. J Am Vet Med Assoc 203(1):126–132

    CAS  PubMed  Google Scholar 

  • Blair JMA, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV (2014) Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol (Nat Publ Group) 13(1):42–51

    Article  CAS  Google Scholar 

  • Bourne GH (1975) The Rhesus monkey. Academic Press, New York

    Google Scholar 

  • Bowen A (2015) Shigellosis. CDC Heal Inf Int Travel

    Google Scholar 

  • Boyce JM, Pittet D, Healthcare Infection Control Practices Advisory Committee, HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force (2002) Guideline for hand hygiene in health-care settings. recommendations of the healthcare infection control practices advisory committee and the HICPAC/SHEA/APIC/IDSA hand hygiene task force. society for healthcare epidemiology of america/association for prof. MMWR 51(RR-16):1–45, quiz CE1-4

    Google Scholar 

  • Brack M, Hosefelder F (1992) In vitro characteristics of Yersinia pseudotuberculosis of nonhuman primate origin. Zentralbl Bakteriol 277:280–287

    Article  CAS  PubMed  Google Scholar 

  • Breed M, Kramer J, Perez H, McCully C, Warren K, Otto M et al (2016) Genotype and risk factors associated with MRSA colonization within a population of macaques. J Am Assoc Lab Anim Sci 55(1):110–114

    Google Scholar 

  • Bronson RT, May BD, Ruebner BH (1972) An outbreak of infection by Yersinia pseudotuberculosis in nonhuman primates. Am J Pathol 69(2):289–308

    Google Scholar 

  • Buhles WC, Vanderlip JE, Russell SW, Alexander NL (1981) Yersinia pseudotuberculosis infection: study of an epizootic in squirrel monkeys. J Clin Microbiol 13(0095–1137 (Print) LA–eng PT–Journal Article RN–0 (Antibodies, Bacterial) SB–IM):519–525

    Google Scholar 

  • Burstiner LC, Faires M, Weese JS (2010) Methicillin-resistant Staphylococcus aureus colonization in personnel attending a veterinary surgery conference. Vet Surg 39(2):150–157

    Article  PubMed  Google Scholar 

  • Carattoli A (2001) Importance of integrons in the diffusion of resistance. Vet Res 32(3–4):243–259

    Article  CAS  PubMed  Google Scholar 

  • Carattoli A (2003) Plasmid-mediated antimicrobial resistance in Salmonella enterica. Curr Issues Mol Biol 5(4):113–122

    CAS  PubMed  Google Scholar 

  • Carvalho VM, Gyles CL, Ziebell K, Ribeiro MA, Catão-Dias JL, Sinhorini IL et al (2003) Characterization of monkey enteropathogenic Escherichia coli (EPEC) and human typical and atypical EPEC serotype isolates from neotropical nonhuman primates. J Clin Microbiol

    Google Scholar 

  • CDC (2014) Campylobacter [Internet]. Available from: https://www.cdc.gov/foodsafety/diseases/campylobacter/index.html

    Google Scholar 

  • CDC (2017) Core elements of hospital antibiotic stewardship programs [Internet]. [cited 2017 Jan 1] Available from: https://www.cdc.gov/getsmart/healthcare/implementation/core-elements.html

  • Centers for Disease Control and Prevention (2016) National antimicrobial resistance monitoring system (NARMS): 2014 human isolates surveillance report, pp 1–83

    Google Scholar 

  • Centers for Disease Control and Prevention. Antibiotic resistance threats in the united states (2013) CDC 2013

    Google Scholar 

  • Chege GK, Warren RM, Gey van Pittius NC, Burgers W A, Wilkinson RJ, Shephard EG, et al (2008) Detection of natural infection with Mycobacterium intracellulare in healthy wild-caught Chacma baboons (Papio ursinus) by ESAT-6 and CFP-10 IFN-gamma ELISPOT tests following a tuberculosis outbreak. BMC Microbiol 8:27

    Google Scholar 

  • Cho SH, Lim YS, Park MS, Kim SH, Kang YH (2011) Prevalence of antibiotic resistance in Escherichia coli fecal isolates from healthy persons and patients with diarrhea. Osong Public Health and Research Perspectives

    Google Scholar 

  • Choi EW, Lee KW, Kim TM, Park H, Jeon MR, Cho CW, et al (2016) Mycobacterium tuberculosis infections in cynomolgus monkey transplant recipients and institution of a screening program for the prevention and control of tuberculosis. BMC Vet Res

    Google Scholar 

  • Clayton JB, Danzeisen JL, Trent AM, Murphy T, Johnson TJ (2014) Longitudinal characterization of Escherichia coli in healthy captive non-human primates. Front Vet Sci 1

    Google Scholar 

  • Cohen ML, Tauxe RV (1986) Drug-resistant Salmonella in the United States: an epidemiologic perspective. Science (80-. ) 234(4779):964–969

    Google Scholar 

  • Cooper JE, Needham JR (1976) An outbreak of shigellosis in laboratory marmosets and tamarins (family: Callitrichidae). J Hyg 76(3):415–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coscolla M, Lewin A, Metzger S, Maetz-Rennsing K, Calvignac-Spencer S, Nitsche A, et al (2013) Novel Mycobacterium tuberculosis complex isolate from a wild chimpanzee. Emerg Infect Dis 19(6):969–976

    Google Scholar 

  • Cristóbal-Azkarate J, Dunn JC, Day JMW, Amábile-Cuevas CF (2014) Resistance to antibiotics of clinical relevance in the fecal microbiota of Mexican wildlife. PLoS One 9(9)

    Google Scholar 

  • Crofts TS, Gasparrini AJ, Dantas G (2017) Next-generation approaches to understand and combat the antibiotic resistome. Nat Rev Microbiol (Nature Publishing Group) 15(7):422–434

    Article  CAS  Google Scholar 

  • D’Costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science (80-. ) 311(5759):374–377

    Google Scholar 

  • Department of Health and Human Services (2013) Department of health and human services 42 CFR part 71 control of communicable disease; foreign-requirements for importers of nonhuman primates (NHP); final rule

    Google Scholar 

  • Donato ACJ, Penna B, Consalter A, Carvalho DD, Lilenbaum W, Ferreira AMR (2017) Antibiotic resistance in Staphylococcus sp. isolated from the vaginal environment of squirrel monkeys (Saimiri spp.) bred ex situ. J Med Primatol 46(3):75–78

    Article  CAS  PubMed  Google Scholar 

  • Engel GA, Jones-Engel L (2012) Primates and primatologists: social contexts for interspecies pathogen transmission. Am J Primatol 74(6):543–550

    Article  CAS  PubMed  Google Scholar 

  • Fortman JD, Hewett TA, Halliday LC (2018) The laboratory nonhuman primate, 2nd edn. CRC Press, Boca Raton, FL

    Google Scholar 

  • Fourie PB, Odendaal MW (1983) Mycobacterium tuberculosis in a closed colony of baboons (Papio ursinus). Lab Anim 17(2):125–128

    Google Scholar 

  • Fox JG (1975) Transmissible drug resistance in Shigella and Salmonella isolated from pet monkeys and their owners. J Med Primatol 4(3):165–171

    Article  CAS  PubMed  Google Scholar 

  • Fox JG, Anderson LC, Otto G, Pritchett-Corning KR, Whary MT (eds) (2015) Laboratory animal medicine, 3rd edn. Elsevier/Academic Press, Amsterdam

    Google Scholar 

  • Gillespie SH (2002) Evolution of drug resistance in Mycobacterium tuberculosis : clinical and molecular perspective. Antimicrob Agents Chemother

    Google Scholar 

  • Glynn MK, Bopp C, Dewitt W, Dabney P, Mokhtar M, Angulo FJ (1998) Emergence of multidrug-resistant Salmonella enterica serotype typhimurium DT104 infections in the United States. N Engl J Med 338(19):1333–1339

    Article  CAS  PubMed  Google Scholar 

  • Good RC, May BD, Kawatomari T (1969) Enteric pathogens in monkeys. J Bacteriol 97:1048–1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Good RC, May BD (1971) Respiratory pathogens in monkeys. Infect Immun 3(1):87–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hale TL, Keusch GT (1996) Shigella . Medical microbiology, 4th edn. Galveston

    Google Scholar 

  • Hanley PW, Barnhart KF, Abee CR, Lambeth SP, Weese JS (2015) Methicillin-resistant Staphylococcus aureus prevalence among captive Chimpanzees, Texas, USA, 2012(1). Emerg Infect Dis 21(12):2158–2160. [Internet] December [cited 2018 Jan 27]; Available from: http://wwwnc.cdc.gov/eid/article/21/12/14-2004_article.htm

  • Hardy A (1945) Studies of the acute diarrheal diseases: further cultural observations on the relative efficacy of sulfonamides in shigella infections. Public Health Rep 60:1037–1043

    Article  CAS  Google Scholar 

  • Hirschmann H, Fux L, Podusel J, Schindler K, Kundi M, Rotter M et al (2001) The influence of hand hygiene prior to insertion of peripheral venous catheters on the frequency of complications. J Hosp Infect 49(3):199–203

    Article  CAS  PubMed  Google Scholar 

  • Iwata T, Hayashidani H (2011) Epidemiological findings on yersiniosis in nonhuman primates in zoological gardens in Japan. Jpn Agric Res Q 45(1):83–90

    Article  Google Scholar 

  • Iwata T, Une Y, Okatani AT, Kaneko S, Namai S, Yoshida S et al (2005) Yersinia enterocolitica serovar O:8 infection in breeding monkeys in Japan. Microbiol Immunol 49(1):1–7

    Article  CAS  PubMed  Google Scholar 

  • Iwata T, Une Y, Okatani AT, Kato Y, Nakadai A, Lee KI et al (2008) Virulence characteristics of Yersinia pseudotuberculosis isolated from breeding monkeys in Japan. Vet Microbiol 129(3–4):404–409

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen JH, Ferraro MJ (2009) Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clin Inf Dis 49(11):1749–1755

    Article  CAS  Google Scholar 

  • Kaper JB, Nataro JP, HLT M (2004) Pathogenic Escherichia coli , review. Nat Rev Microbiol 2(2):123–140

    Article  CAS  PubMed  Google Scholar 

  • Kaplan SL, Mason EO (1998) Management of infections due to antibiotic-resistant Streptococcus pneumonia. Clin Microbiol Rev 11(4):628–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaufmann AF, Moulthrop JI, Moore RM (1975) A perspective of simian tuberculosis in the United States-1972. J Med Primatol 4(5):278–286

    Article  CAS  PubMed  Google Scholar 

  • Kelly KM, Wack AN, Bradway D, Simons BW, Bronson E, Osterhout G et al (2015) Identification of Mycobacterium genavense in a Diana monkey (Cercopithecus Diana) by polymerase chain reaction and high-performance liquid chromatography. J Zoo Wildl Med 46(2):339–344

    Google Scholar 

  • Kennedy FM, Astbury J, Xeedham R, Chhasty T, Sue EEII (1993) Shigellosis due to occupational contact with non-human primates. Epidemiol Infect 110(2):247–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Coble D, Salyards G, Bower J, Rinaldi W, Plauche G et al (2017a) Antimicrobial use for and resistance of zoonotic bacteria recovered from nonhuman primates. Comp Med 67(1):79–86

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim TM, Park H, Lee KW, Choi EW, Moon SH, Lee YS et al (2017b) A simple way to eradicate methicillin-resistant Staphylococcus aureus in cynomolgus macaques (macaca fascicularis). Comp Med 67(4):356–359

    Google Scholar 

  • Kim J, Coble DJ, Salyards GW, Habing GG (2018) Comparative review of antimicrobial resistance in humans and nonhuman primates. Comp Med 68(2):124–130

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klein H, Hasselschwert D, Handt L, Kastello M (2008) A pharmacokinetic study of enrofloxacin and its active metabolite ciprofloxacin after oral and intramuscular dosing of enrofloxacin in rhesus monkeys (macaca mulatta ). J Med Primatol 37(4):177–183

    Article  CAS  PubMed  Google Scholar 

  • Klugman KP (1990) Pneumococcal resistance to antibiotics. Clin Microbiol Rev 3(2):171–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolappaswamy K, Shipley ST, Tatarov II, DeTolla LJ (2008) Methicillin-resistant Staphylococcus non-aureus infection in an irradiated rhesus macaque (Macaca mulatta ). J Am Assoc Lab Anim Sci 47(3):64–67

    Google Scholar 

  • Kolappaswamy K, Nazareno J, Porter WP, Klein HJ (2014) Outbreak of pathogenic Escherichia coli in an outdoor-housed non-human primate colony. J Med Primatol 43(2):122–124

    Google Scholar 

  • Kozak GK, Boerlin P, Janecko N, Reid-Smith RJ, Jardine C (2009) Antimicrobial resistance in Escherichia coli isolates from swine and wild small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl Env Microbiol 75(3):559–566

    Article  CAS  Google Scholar 

  • Kumar HBC, Lokesha KM, Madhavaprasad CB, Shilpa VT, Karabasanavar NS, Kumar A (2013) Occupational zoonoses in zoo and wildlife veterinarians in India: a review. Vet World 6(9):605–613

    Article  Google Scholar 

  • Kyaw MH, Lynfield R, Schaffner W, Craig AS, Hadler J, Reingold A, Thomas AR, Harrison LH, Bennett NM, Farley MM, Facklam RR, Jorgensen JH, Besser J, Zell ER, Schuchat A, Whitney CG (2006) Effect of introduction of the pneumococcal conjugate vaccine on drug-resistant. N Engl J Med 354(14):1455–1463

    Article  CAS  PubMed  Google Scholar 

  • La Plante K, Cunha C, Morrill H, Rice L, Mylonakis E (eds) (2017) Antimicrobial stewardship: principles and practice. CABI, Oxfordshire

    Google Scholar 

  • Lankau EW, Turner PV, Mullan RJ, Galland GG (2014) Use of nonhuman primates in research in North America. J Am Assoc Lab Anim Sci 53(3):278–282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leathers CW, Hamm TEJ (1976) Naturally occurring tuberculosis in a squirrel monkey and a cebus monkey. J Am Vet Med Assoc 169(9):909–911

    CAS  PubMed  Google Scholar 

  • Lederer I, Much P, Allerberger F, Voracek T, Vielgrader H (2005) Outbreak of shigellosis in the Vienna zoo affecting human and non-human primates. Int J Infect Dis 9(5):290–291

    Article  PubMed  Google Scholar 

  • Leekha S, Terrell CL, Edson RS (2011) General principles of antimicrobial therapy. Mayo Clin Proc 86(2):156–167

    Article  PubMed  PubMed Central  Google Scholar 

  • Leekitcharoenphon P, Hendriksen RS, Le Hello S, Weill F-X, Baggesen DL, Jun S-R et al (2016) Global genomic epidemiology of Salmonella enterica serovar typhimurium DT104. Appl Env Microbiol 82(8):2516–2526

    Article  CAS  Google Scholar 

  • Levy SB, FitzGerald GB, Macone AB (1976) Changes in intestinal flora of farm personnel after introduction of a tetracycline-supplemented feed on a farm. N Engl J Med 295(11):583–588

    Article  CAS  PubMed  Google Scholar 

  • Lhermie G, Dupouy V, El Garch F, Ravinet N, Toutain P-L, Bousquet-Mélou A et al (2017) Impact of low and high doses of marbofloxacin on the selection of resistant enterobacteriaceae in the commensal gut flora of young cattle: discussion of data from 2 study populations. Foodborne Pathog Dis 14(3):152–159

    Article  CAS  PubMed  Google Scholar 

  • Lipsitch M, Siber GR (2016) How can vaccines contribute to solving the antimicrobial resistance problem. MBio 7(3)

    Google Scholar 

  • MacArthur JA, Wood M (1983) Yersiniosis in a breeding unit of Macaca fascicularis (cynomolgus monkeys ). Lab Anim 17(2):151–155

    Article  CAS  PubMed  Google Scholar 

  • Mair NS (1973) Yersiniosis in wildlife and its public health implications. J Wildl Dis 9(1):64–71

    Article  CAS  PubMed  Google Scholar 

  • Mandell LA, Peterson LR, Wise R, Hooper D, Low DE, Schaad UB, Klugman KP, Courvalin P (2002) The battle against emerging antibiotic resistance: should Fluoroquinolones be used to treat children? Clin Infect Dis 35(6):721–727

    Article  CAS  PubMed  Google Scholar 

  • Mansfield KG, Lin KC, Xia D, Newman JV, Schauer DB, MacKey J et al (2001) Enteropathogenic Escherichia coli and ulcerative colitis in cotton-top tamarins (Saguinus oedipus ). J Infect Dis 184(6):803–807

    Article  CAS  PubMed  Google Scholar 

  • Mather AE, Reid SWJ, Maskell DJ, Parkhill J, Fookes MC, Harris SR (2013) Distinguishable epidemics within different hosts of the multidrug resistant zoonotic pathogen Salmonella typhimurium. Science (80-.) 341(6153):1514–1517

    Google Scholar 

  • McAndrew R, Helms Tillery SI (2016) Laboratory primates: their lives in and after research. Temperature 3(4):502–508

    Article  Google Scholar 

  • McClure HM (1986) Bacterial infections of nonhuman primates. Primates. Springer, pp 531–556

    Google Scholar 

  • McClure HM, Alford P, Swenson B (1976) Nonenteric shigella infections in nonhuman primates. J Am Vet Med Assoc 169(9):938–939

    CAS  PubMed  Google Scholar 

  • McDermott PF, Tyson GH, Kabera C, Chen Y, Li C, Folster JP, et al (2016) Whole-genome sequencing for detecting antimicrobial resistance in nontyphoidal Salmonella . Antimicrob Agents Chemother (American Society for Microbiology) 60(9):5515–5520

    Google Scholar 

  • McEachran AD, Blackwell BR, Hanson JD, Wooten KJ, Mayer GD, Cox SB et al (2015) Antibiotics, bacteria, and antibiotic resistance genes: aerial transport from cattle feed yards via particulate matter. Env Health Perspect (National Institute of Environmental Health Science) 123(4):337–343

    Article  Google Scholar 

  • Miller-Spiegel C (2011) Primates by the numbers. The use and importation of nonhuman primates for research and testing in the United States

    Google Scholar 

  • Morgan M (2008) Methicillin-resistant Staphylococcus aureus and animals: zoonosis or humanosis? J Antimicrob Chemother 62(6):1181–1187

    Article  CAS  PubMed  Google Scholar 

  • Mulder JB (1971) Shigellosis in nonhuman primates: a review. Lab Anim Sci 21(5):734–738

    CAS  PubMed  Google Scholar 

  • Munita JM, Arias CA (2016) Mechanisms of antibiotic resistance. Microbiol Spectr 4(2):1–37

    Article  CAS  Google Scholar 

  • Nakamura S, Hayashidani H, Iwata T, Namai S, Une Y (2010) Pathological changes in captive monkeys with spontaneous yersiniosis due to infection by Yersinia enterocolitica serovar O8. J Comp Pathol Elsevier Ltd 143(2–3):150–156

    Article  CAS  Google Scholar 

  • Nastaly P, Grinholc M, Bielawski KP (2010) Molecular characteristics of community-associated methicillin-resistant Staphylococcus aureus strains for clinical medicine. Arch Microbiol 192(8):603–617

    Google Scholar 

  • Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli . Clin Microbiol Rev

    Google Scholar 

  • National Research Council of the National Academies (2003) Occupational health and safety in the care and use of nonhuman primates, 1st edn. Occupational and health safe care and use of nonhuman primates. The National Academic Press, Washington, DC

    Google Scholar 

  • O’Brien TF, Hopkins JD, Gilleece ES, Medeiros AA, Kent RL, Blackburn BO et al (1982) Molecular epidemiology of antibiotic resistance in Salmonella from animals and human beings in the United States. N Engl J Med 307(1):1–6

    Article  PubMed  Google Scholar 

  • O’Toole R (2010) Experimental models used to study human tuberculosis . Adv Appl Microbiol 71

    Google Scholar 

  • OIE (World Organization for Animal Health) (2007) OIE list of antimicrobials of veterinary importance

    Google Scholar 

  • Olson LC, Bergquist DY, Fitzgerald DL (1986) Control of Shigella flexneri in celebes black macaques (Macaca nigra). Lab Anim Sci 36(3):240–242

    Google Scholar 

  • Omenn GS (2010) Evolution and public health. Proc Natl Acad Sci U S A 107(suppl_1):1702–1709

    Article  CAS  PubMed  Google Scholar 

  • Panarella ML, Bimes RS (2010) A naturally occurring outbreak of tuberculosis in a group of imported cynomolgus monkeys (Macaca fascicularis). J Am Assoc Lab Anim Sci

    Google Scholar 

  • Papp R, Popovic A, Kelly N, Tschirret-Guth R (2010) Pharmacokinetics of cefovecin in squirrel monkey (Saimiri sciureus ), rhesus macaques (Macaca mulatta ), and cynomolgus macaques (Macaca fascicularis). J Am Assoc Lab Anim Sci 49(6):805–808

    Google Scholar 

  • Parsons SDC, de Villiers C, van Pittius NC, Warren RM, van Helden PD (2010) Detection of Mycobacterium kansasii infection in a rhesus macaque (Macaca mulatta ) using a modified QuantiFERON-TB gold assay. Vet Immunol Immunopathol

    Google Scholar 

  • Paul M, Lador A, Grozinsky-Glasberg S, Leibovici L (2014) Beta lactam antibiotic monotherapy versus beta lactam-aminoglycoside antibiotic combination therapy for sepsis. Cochrane Database Syst Rev 1

    Google Scholar 

  • Raabe BM, Lovaglio J, Grover GS, Brown SA, Boucher JF, Yuan Y et al (2011) Pharmacokinetics of cefovecin in cynomolgus macaques (Macaca fascicularis), olive baboons (Papio anubis), and rhesus macaques (Macaca mulatta ). J Am Assoc Lab Anim Sci 50(3):389–395

    Google Scholar 

  • Renner M, Bartholomew W (1974) Mycobacteriologic data from two outbreaks of bovine tuberculosis in nonhuman Primates. Am Rev Respir Dis 109:11–16

    CAS  PubMed  Google Scholar 

  • Roberts JA, Andrews K (2008) Nonhuman primate quarantine: its evolution and practice. ILAR J (Oxf Univ Press) 49(2):145–156

    Article  CAS  Google Scholar 

  • Rosenbaum M, Mendoza P, Ghersi BM, Wilbur AK, Perez-Brumer A, Cavero Yong N et al (2015) Detection of Mycobacterium tuberculosis Complex in New World Monkeys in Peru. Ecohealth

    Google Scholar 

  • Rosenberg DP, Lerche NW, Henrickson RV (1980) Yersinia pseudotuberculosis infection in a group of Macaca fascicularis. J Am Vet Med Assoc 177(9):818–819

    Google Scholar 

  • Ross S, Controni G, Khan W (1972) Resistance of shigellae to ampicillin and other antibiotics. Its clinical and epidemiological implications. J Am Vet Med Assoc 221(1):45–47

    Article  CAS  Google Scholar 

  • Russell RG, DeTolla LJ (1993) Nonhuman primates, 1. In: Jones TC, Mohr U, Hunt RD, Shigellosis. Springer, Berlin, pp 46–53

    Google Scholar 

  • Russell RG, Rosenkranz SL, Lee LA, Howard H, DiGiacomo RF, Bronsdon MA et al (1987) Epidemiology and etiology of diarrhea in colony-born Macaca nemestrina. Lab Anim Sci 37(3):309–316

    CAS  PubMed  Google Scholar 

  • Salyards GW, Knych HK, Hill AE, Kelly KR, Christe KL (2015) Pharmacokinetics of ceftiofur crystalline free acid in male rhesus macaques (Macaca mulatta ) after subcutaneous administration. J Am Assoc Lab Anim Sci 54(5):557–563

    Google Scholar 

  • Salyards GW, Lemoy M-J, Knych HK, Hill AE, Christe KL (2017) Pharmacokinetics of a novel, transdermal fentanyl solution in rhesus macaques (Macaca mulatta ). J Am Assoc Lab Anim Sci 56(4):443–451

    Google Scholar 

  • Schaumburg F, Mugisha L, Peck B, Becker K, Gillespie TR, Peters G et al (2012) Drug-resistant human Staphylococcus aureus in sanctuary apes pose a threat to endangered wild ape populations. Am J Primatol 74(12):1071–1075

    Article  PubMed  Google Scholar 

  • Seelig D, Truitt A (1999) Postresearch retirement of monkeys and other nonhuman primates. Lab Primate Newsl 38(2)

    Google Scholar 

  • Shea A, Shaw S (2012) Evaluation of an educational campaign to increase hand hygiene at a small animal veterinary teaching hospital. J Am Vet Med Assoc 240(1):61–64

    Article  PubMed  Google Scholar 

  • Smith T, Wolff KA, Nguyen L (2013) Molecular biology of drug resistance in Mycobacterium tuberculosis . Pathogen mycobacterium tuberculosis its interact with Host Org

    Google Scholar 

  • Snyder S, Peace T, Soave O, Lund J (1970) Tuberculosis in an owl monkey (Aotus trivirgatus ). J Am Vet Med Assoc

    Google Scholar 

  • Soge OO, No D, Michael KE, Dankoff J, Lane J, Vogel K et al (2016) Transmission of MDR MRSA between primates, their environment and personnel at a United States primate Centre. J Antimicrob Chemother 71(10):2798–2803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soto E, Griffin M, Verma A, Castillo-Alcala F, Beierschmitt A, Beeler-Marfisi J et al (2013) An outbreak of Yersinia enterocolitica in a captive colony of african green monkeys (Chlorocebus aethiops sabaeus) in the caribbean. Comp Med 63(5):439–444

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stirling J, Griffith M, Blair I, Cormican M, Dooley JSG, Goldsmith CE et al (2008) Prevalence of gastrointestinal bacterial pathogens in a population of zoo animals. Zoonoses Public Health 55(3):166–172

    Article  CAS  PubMed  Google Scholar 

  • Taffs LF, Dunn G (1983) An outbreak of Yersinia pseudotuberculosis infection in a small indoor breeding colony of red-bellied (Saguinus labiatus ) tamarins. Lab Anim 17:311–320

    Google Scholar 

  • Taylor WM, Grady AW (1998) Catheter-tract infections in rhesus macaques (Macaca mulatta ) with indwelling intravenous catheters. Lab Anim Sci 48(5):448–454

    CAS  PubMed  Google Scholar 

  • Torres AG, Zhou X, Kaper JB (2005) Adherence of Diarrheagenic Escherichia coli strains to epithelial cells MINIREVIEW adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infect Immun 73(1):18–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tribe GW, Fleming MP (1983) Biphasic enteritis in imported cynomolgus (Macaca fascicularis) monkeys infected with Shigella , Salmonella and campylobacter species. Lab Anim 17(1):65–69

    Google Scholar 

  • Tyson GH, McDermott PF, Li C, Chen Y, Tadesse DA, Mukherjee S et al (2015) WGS accurately predicts antimicrobial resistance in Escherichia coli . J Antimicrob Chemother 70(10):2763–2769

    Article  CAS  PubMed  Google Scholar 

  • Uma B, Prabhakar K, Rajendran S, Kavitha K, Sarayu Y (2009) Antibiotic sensitivity and plasmid profiles of Escherichia coli isolated from pediatric diarrhea. J Glob Infect Dis 1(2):107

    Google Scholar 

  • US Food and Drug Administration (2015) NARMS integrated report 2015

    Google Scholar 

  • van den Berg S, van Wamel WJB, Snijders SV, Ouwerling B, de Vogel CP, Boelens HA et al (2011) Rhesus macaques (Macaca mulatta ) are natural hosts of specific Staphylococcus aureus lineages. Fowler VG (ed). PLoS One 6(10):e26170

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wachtman LM, Miller AD, Xia D, Curran EH, Mansfield KG (2011) Colonization with nontuberculous mycobacteria is associated with positive tuberculin skin test reactions in the common marmoset (Callithrix jacchus ). Comp Med 61(3):278–284

    Google Scholar 

  • Ward GS, Elwell MR, Tingpalapong M, Pomsdhit J (1985) Use of streptomycin and isoniazid during a tuberculosis epizootic in a rhesus and cynomolgus breeding colony. Lab Anim Sci 35(4):395–399

    CAS  PubMed  Google Scholar 

  • Weese JS (2010) Methicillin-resistant Staphylococcus aureus in animals. ILAR 51(3):233–244

    Google Scholar 

  • Weese SJ, Page SW, Prescott JF (2013) Antimicrobial stewardship in animals. In: Giguère S, Prescott JF, Dowling PM (eds) Antimicrobial therapy in veterinary medicine, 5th edn. Wiley, Hoboken, pp 117–132

    Google Scholar 

  • Weller R (1994) Infectious and noninfectious diseases of owl monkeys. In: Baer J, Weller R, Kakoma I (eds) Aotus Owl monkey. Acadmeic Press, San Diego, pp 178–215

    Google Scholar 

  • WHO (2012) The global view of campylobacteriosis

    Google Scholar 

  • Wilbur AK, Engel GA, Rompis A, Putra IGAA, Lee BPYH, Aggimarangsee N et al (2012) From the mouths of monkeys: detection of Mycobacterium tuberculosis complex DNA from buccal swabs of Synanthropic macaques. Am J Primatol

    Google Scholar 

  • Wolf RH, Gibson SV, Watson EA, Baskin GB (1988) Multidrug chemotherapy of tuberculosis in rhesus monkeys. Lab Anim Sci 38(1):25–33

    CAS  PubMed  Google Scholar 

  • Wolfensohn S (1998) Shigella infection in macaque colonies: case report of an eradication and control program. Lab Anim Sci 48(4):330–333

    CAS  PubMed  Google Scholar 

  • World Health Organization (2011) Critically important antimicrobials for human medicine (3rd ed). (AGISAR) WAG on IS of AR, editor. World Health Organisation

    Google Scholar 

  • World Health Organization (2016) Campylobacter [Internet]. Available from: http://www.who.int/mediacentre/factsheets/fs255/en/

  • World Health Organization. MDR-TB surveillance [Internet]. Available from: http://www.who.int/tb/areas-of-work/monitoring-evaluation/mdr-tb-surveillance/en/

  • World Health Organization. Drug-resistant TB [Internet]. [cited 2017, January 1] Available from: http://www.who.int/tb/areas-of-work/drug-resistant-tb/en/

  • Zhang Y, Yew W (2015) Mechanisms of drug resistance in Mycobacterium tuberculosis : update 2015. Int J Tuberc Lung Dis

    Google Scholar 

  • Zhao S, Tyson GH, Chen Y, Li C, Mukherjee S, Young S, et al (2015) Whole-genome sequencing analysis accurately predicts antimicrobial resistance phenotypes in Campylobacter spp. Appl Env Microb Am Soc Microbiol 82(2):459–466

    Google Scholar 

  • Zhao N, Li M, Amer S, Liu S, Luo J, Wang S et al (2016) Mortality in captive rhesus monkeys (Macaca mulatta ) in China due to infection with Yersinia pseudotuberculosis serotype O:1a. Ecohealth (Springer US) 13(3):597–601

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Immunology, and Pathology, Colorado State University, College of Veterinary Medicine and Biomedical Sciences, Fort Collins, CO, USA

    Jeffrey Kim

  2. Department of Veterinary Preventive Medicine, The Ohio State University, College of Veterinary Medicine, Columbus, OH, USA

    Gregory G. Habing

  3. Division of Veterinary Resources, National Institutes of Health, Office of Research Services, Bethesda, MD, USA

    Gregory W. Salyards

  4. Abigail Wexner Research Institute at Nationwide Children’s Hospital, Columbus, OH, USA

    Dondrae J. Coble

Authors
  1. Jeffrey Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gregory G. Habing
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gregory W. Salyards
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dondrae J. Coble
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregory G. Habing .

Editor information

Editors and Affiliations

  1. Workgroup Neglected Tropical Diseases, Infection Biology Unit, Deutsches Primatenzentrum GmbH, Leibniz Institute for Primate Research, Goettingen, Germany

    Sascha Knauf

  2. Department of Anthropology and Center for Studies in Demography and Ecology, University of Washington, Seattle, WA, USA

    Lisa Jones-Engel

Glossary

Anthropozoonosis

transmissibility of infectious pathogens from human to vertebrate animal. Also known as “reverse zoonosis”

Antimicrobial resistance

also known as antibiotic resistance or drug resistance, it is the ability of microbes to resist the effects of drugs

Antimicrobial susceptibility test

a diagnostic test measuring the degree of bacterial resistance to antimicrobials

Antimicrobial selective pressure

an influence exerted by the presence of an antimicrobial, killing susceptible bacteria and promoting the growth and spread of bacteria resistant to the antimicrobial present

Commensal organism

a microbe that benefits from the presence of another organism, which is unaffected by the microbe

Competitive exclusion

the elimination of an organism by another that shares identical resources

Empiric antimicrobial therapy

initiation of antimicrobial treatment prior to microbial test results

Fomite

object or material that can carry infectious pathogens

Horizontal transmission

spread of an infectious agent among individuals of the same generation

Mean inhibitory concentration

lowest concentration of antimicrobial that prevents bacterial growth

Medical primatology

the study of the medical management and care of nonhuman primates with the purpose to maximize their well-being, conserve their species, and research comparative knowledge for human pathology and biology

Nosocomial

infection or disease contracted from a hospital setting

Reverse zoonosis

see anthropozoonosis

Resistome

the collection of all antimicrobial resistance genes and the precursors

Shedding

the act of expelling pathogens from the body

Zoonosis

transmissibility of infectious pathogens from vertebrate animal to human

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kim, J., Habing, G.G., Salyards, G.W., Coble, D.J. (2020). Antimicrobial Stewardship in Captive Monkeys. In: Knauf, S., Jones-Engel, L. (eds) Neglected Diseases in Monkeys. Springer, Cham. https://doi.org/10.1007/978-3-030-52283-4_7

Download citation

Publish with us

Policies and ethics

Search

Navigation