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BMC Infectious Diseases
Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Longitudinal study of Staphylococcus aureus colonization and infection in a cohort of swine veterinarians in the United States

Authors: Jisun Sun, My Yang, Srinand Sreevatsan, Jeffrey B. Bender, Randall S. Singer, Todd P. Knutson, Douglas G. Marthaler, Peter R. Davies

Published in: BMC Infectious Diseases | Issue 1/2017

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Abstract

Background

People working with pigs are at elevated risk of harboring methicillin resistant S. aureus (MRSA) in their nose, which is attributable to occupational exposure to animals harboring livestock adapted S. aureus. To obtain insight into the biological nature of occupationally related nasal culture positivity, we conducted a longitudinal study of 66 swine veterinarians in the USA.

Methods

The study cohort resided in 15 US states and worked predominantly with swine. Monthly for 18 months, participants self-collected nasal swabs and completed a survey to report recent exposure to pigs and other animals; the occurrence of work related injuries; and any relevant health events such as skin and soft tissue infections or confirmed staphylococcal infections. Nasal swabs were cultured using selective methods to determine the presence of MRSA and methicillin susceptible S. aureus (MSSA), and isolates were characterized by spa typing and MLST.

Results

Prevalences of S. aureus (64%, monthly range from 58 to 82%) and MRSA (9.5%; monthly range from 6 to15%) were higher than reported for the US population (30% and 1.5% respectively). Predominant spa types were t034 (ST398, 37%), t002 (ST5, 17%) and t337 (ST9/ST398 13%), a distribution similar to that found in a concurrent study in pigs in the USA. Veterinarians were classified into three groups: Persistent carriers (PC, 52%), Intermittent carriers (IC, 47%) and Non-carriers (NC, 1%). Persistent carriage of a single spa type was observed in 14 (21%) of participants, and paired (first and last) isolates from PC subjects had minor genetic differences. Swabs from PC veterinarians carried higher numbers of S. aureus. Among IC veterinarians, culture positivity was significantly associated with recent contact with pigs.

Conclusions

Exposure to pigs did not lead to prolonged colonization in most subjects, and the higher numbers of S. aureus in PC subjects suggests that unknown host factors may determine the likelihood of prolonged colonization by S. aureus of livestock origin. Exposure to S. aureus and persistent colonization of swine veterinarians was common but rarely associated with S. aureus disease.
Appendix
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Literature
1.
2.
Chuang YY, Huang YC. Livestock-associated meticillin-resistant Staphylococcus Aureus in Asia: an emerging issue? Int J Antimicrob Agents. 2015;45(4):334–40.CrossRefPubMed
3.
Khanna T, Friendship R, Dewey C, Weese JS. Methicillin resistant Staphylococcus Aureus colonization in pigs and pig farmers. Vet Microbiol. 2008;128(3–4):298–303.CrossRefPubMed
4.
Smith TC, Gebreyes WA, Abley MJ, Harper AL, Forshey BM, Male MJ, Martin HW, Molla BZ, Sreevatsan S, Thakur S, Thiruvengadam M, Davies PR. Methicillin-resistant Staphylococcus Aureus in pigs and farm workers on conventional and antibiotic-free swine farms in the USA. PLoS One. 2013;8(5):e63704.CrossRefPubMedPubMedCentral
5.
Graveland H, Wagenaar JA, Heesterbeek H, Mevius D, van Duijkeren E, Heederik D. Methicillin resistant Staphylococcus Aureus ST398 in veal calf farming: human MRSA carriage related with animal antimicrobial usage and farm hygiene. PLoS One. 2010;5(6):e10990.CrossRefPubMedPubMedCentral
6.
Van den Eede A, Martens A, Lipinska U, Struelens M, Deplano A, Denis O, Haesebrouck F, Gasthuys F, Hermans K. High occurrence of methicillin-resistant Staphylococcus Aureus ST398 in equine nasal samples. Vet Microbiol. 2009;133(1–2):138–44.CrossRefPubMed
7.
Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, Devriese LA, Pasmans F, Haesebrouck F. Antimicrobial resistance of old and recent Staphylococcus Aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob Agents Chemother. 2008;52(10):3817–9.CrossRefPubMedPubMedCentral
8.
Sun J, Yang M, Sreevatsan S, Davies PR. Prevalence and characterization of Staphylococcus Aureus in growing pigs in the USA. PLoS One. 2015;10(11):e0143670.CrossRefPubMedPubMedCentral
9.
Alba P, Feltrin F, Cordaro G, Porrero MC, Kraushaar B, Argudin MA, Nykasenoja S, Monaco M, Stegger M, Aarestrup FM, Butaye P, Franco A, Battisti A. Livestock-associated methicillin resistant and methicillin susceptible Staphylococcus Aureus sequence type (CC)1 in European farmed animals: high genetic relatedness of isolates from Italian cattle herds and humans. PLoS One. 2015;10(8):e0137143.CrossRefPubMedPubMedCentral
10.
Feltrin F, Alba P, Kraushaar B, Ianzano A, Argudin MA, Di Matteo P, Porrero MC, Aarestrup FM, Butaye P, Franco A, Battisti A. A livestock-associated, multidrug-resistant, methicillin-resistant Staphylococcus Aureus clonal complex 97 lineage spreading in dairy cattle and pigs in Italy. Appl Environ Microbiol. 2015;82(3):816–21.CrossRefPubMed
11.
12.
den Heijer CD, van Bijnen EM, Paget WJ, Pringle M, Goossens H, Bruggeman CA, Schellevis FG, Stobberingh EE, Study Team APRES. Prevalence and resistance of commensal Staphylococcus Aureus, including meticillin-resistant S aureus, in nine European countries: a cross-sectional study. Lancet Infect Dis. 2013;13(5):409–15.CrossRefPubMed
13.
Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, Jensen BJ, Killgore G, Tenover FC, Kuehnert MJ. Changes in the prevalence of nasal colonization with Staphylococcus Aureus in the United States, 2001-2004. J Infect Dis. 2008;197(9):1226–34.CrossRefPubMed
14.
Muthukrishnan G, Lamers RP, Ellis A, Paramanandam V, Persaud AB, Tafur S, Parkinson CL, Cole AM: Longitudinal genetic analyses of Staphylococcus aureus nasal carriage dynamics in a diverse population. BMC Infect Dis 2013, 13:221–2334–13-221.
15.
Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus Aureus infections. Lancet Infect Dis. 2005;5(12):751–62.CrossRefPubMed
16.
Sollid JU, Furberg AS, Hanssen AM, Johannessen M. Staphylococcus Aureus: determinants of human carriage. Infect Genet Evol. 2014;21:531–41.CrossRefPubMed
17.
Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR. The human nasal microbiota and Staphylococcus Aureus carriage. PLoS One. 2010;5(5):e10598.CrossRefPubMedPubMedCentral
18.
Zipperer A, Konnerth MC, Laux C, Berscheid A, Janek D, Weidenmaier C, Burian M, Schilling NA, Slavetinsky C, Marschal M, Willmann M, Kalbacher H, Schittek B, Brotz-Oesterhelt H, Grond S, Peschel A, Krismer B. Human commensals producing a novel antibiotic impair pathogen colonization. Nature. 2016;535(7613):511–6.CrossRefPubMed
19.
Guinane CM, Ben Zakour NL, Tormo-Mas MA, Weinert LA, Lowder BV, Cartwright RA, Smyth DS, Smyth CJ, Lindsay JA, Gould KA, Witney A, Hinds J, Bollback JP, Rambaut A, Penades JR, Fitzgerald JR. Evolutionary genomics of Staphylococcus Aureus reveals insights into the origin and molecular basis of ruminant host adaptation. Genome Biol Evol. 2010;2:454–66.CrossRefPubMedPubMedCentral
20.
Lowder BV, Fitzgerald JR. Human origin for avian pathogenic Staphylococcus Aureus. Virulence. 2010;1(4):283–4.CrossRefPubMed
21.
Viana D, Comos M, McAdam PR, Ward MJ, Selva L, Guinane CM, Gonzalez-Munoz BM, Tristan A, Foster SJ, Fitzgerald JR, Penades JR. A single natural nucleotide mutation alters bacterial pathogen host tropism. Nat Genet. 2015;47(4):361–6.CrossRefPubMedPubMedCentral
22.
23.
van Cleef BA, Verkade EJ, Wulf MW, Buiting AG, Voss A, Huijsdens XW, van Pelt W, Mulders MN, Kluytmans JA. Prevalence of livestock-associated MRSA in communities with high pig-densities in The Netherlands. PLoS One. 2010;5(2):e9385.CrossRefPubMedPubMedCentral
24.
Verkade E, van Benthem B, den Bergh MK, van Cleef B, van Rijen M, Bosch T, Kluytmans J. Dynamics and determinants of Staphylococcus Aureus carriage in livestock veterinarians: a prospective cohort study. Clin Infect Dis. 2013;57(2):e11–7.CrossRefPubMed
25.
Cuny C, Nathaus R, Layer F, Strommenger B, Altmann D, Witte W. Nasal colonization of humans with methicillin-resistant Staphylococcus Aureus (MRSA) CC398 with and without exposure to pigs. PLoS One. 2009;4(8):e6800.CrossRefPubMedPubMedCentral
26.
Bisdorff B, Scholholter JL, Claussen K, Pulz M, Nowak D, Radon K. MRSA-ST398 in livestock farmers and neighbouring residents in a rural area in Germany. Epidemiol Infect. 2012;140(10):1800–8.CrossRefPubMed
27.
Fang HW, Chiang PH, Huang YC. Livestock-associated methicillin-resistant Staphylococcus Aureus ST9 in pigs and related personnel in Taiwan. PLoS One. 2014;9(2):e88826.CrossRefPubMedPubMedCentral
28.
Frana TS, Beahm AR, Hanson BM, Kinyon JM, Layman LL, Karriker LA, Ramirez A, Smith TC. Isolation and characterization of methicillin-resistant Staphylococcus Aureus from pork farms and visiting veterinary students. PLoS One. 2013;8(1):e53738.CrossRefPubMedPubMedCentral
29.
Armand-Lefevre L, Ruimy R, Andremont A. Clonal comparison of Staphylococcus Aureus isolates from healthy pig farmers, human controls, and pigs. Emerg Infect Dis. 2005;11(5):711–4.CrossRefPubMedPubMedCentral
30.
Gibbs SG, Green CF, Tarwater PM, Mota LC, Mena KD, Scarpino PV. Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environ Health Perspect. 2006;114(7):1032–7.CrossRefPubMedPubMedCentral
31.
Friese A, Schulz J, Hoehle L, Fetsch A, Tenhagen BA, Hartung J, Roesler U. Occurrence of MRSA in air and housing environment of pig barns. Vet Microbiol. 2012;158(1–2):129–35.CrossRefPubMed
32.
van Cleef BA, Graveland H, Haenen AP, van de Giessen AW, Heederik D, Wagenaar JA, Kluytmans JA. Persistence of livestock-associated methicillin-resistant Staphylococcus Aureus in field workers after short-term occupational exposure to pigs and veal calves. J Clin Microbiol. 2011;49(3):1030–3.CrossRefPubMedPubMedCentral
33.
van den Broek IV, van Cleef BA, Haenen A, Broens EM, van der Wolf PJ, van den Broek MJ, Huijsdens XW, Kluytmans JA, van de Giessen AW, Tiemersma EW. Methicillin-resistant Staphylococcus Aureus in people living and working in pig farms. Epidemiol Infect. 2009;137(5):700–8.
34.
van Cleef BA, van Benthem BH, Verkade EJ, van Rijen MM, Kluytmans-van den Bergh MF, Graveland H, Bosch T, Verstappen KM, Wagenaar JA, Bos ME, Heederik D, Kluytmans JA. Livestock-associated MRSA in household members of pig farmers: transmission and dynamics of carriage, a prospective cohort study. PLoS One. 2015;10(5):e0127190.CrossRefPubMedPubMedCentral
35.
Linhares LL, Yang M, SreevatsanS, Munoz-Zanzi CA, Torremorell M, Davies PR. The effect of anatomic site and age on detection of Staphylococcus Aureus in pigs. J Vet Diagn Invest 2015;27(1):55-60.
36.
Harmsen D, Claus H, Witte W, Rothganger J, Claus H, Turnwald D, Vogel U. Typing of methicillin-resistant Staphylococcus Aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003;41(12):5442–8.CrossRefPubMedPubMedCentral
37.
Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus Aureus. J Clin Microbiol. 2000;38(3):1008–15.PubMedPubMedCentral
38.
Mehrotra M, Wang G, Johnson WM. Multiplex PCR for detection of genes for Staphylococcus Aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol. 2000;38(3):1032–5.PubMedPubMedCentral
39.
van Cleef BA, van Benthem BH, Verkade EJ, van Rijen M, Kluytmans-van den Bergh MF, Schouls LM, Duim B, Wagenaar JA, Graveland H, Bos ME, Heederik D, Kluytmans JA. Dynamics of methicillin-resistant Staphylococcus Aureus and methicillin-susceptible Staphylococcus Aureus carriage in pig farmers: a prospective cohort study. Clin Microbiol Infect. 2014; 20(10):O764-71.
40.
Dierikx CM, Hengeveld PD, Veldman KT, de Haan A, van der Voorde S, Dop PY, Bosch T, van Duijkeren E. Ten years later: still a high prevalence of MRSA in slaughter pigs despite a significant reduction in antimicrobial usage in pigs the Netherlands. J Antimicrob Chemother. 2016;71(9):2414–8.CrossRefPubMed
41.
Sun J, Singer RS, Hau SJ, Nicholson TL, Davies PR. Antimicrobial resistance of Staphylococcus Aureus isolated from swine and swine veterinarians in the USA. 2016.
42.
Cuny C, Abdelbary M, Layer F, Werner G, Witte W. Prevalence of the immune evasion gene cluster in Staphylococcus Aureus CC398. Vet Microbiol. 2015;177(1–2):219–23.CrossRefPubMed
43.
Stegger M, Liu CM, Larsen J, Soldanova K, Aziz M, Contente-Cuomo T, Petersen A, Vandendriessche S, Jimenez JN, Mammina C, van Belkum A, Salmenlinna S, Laurent F, Skov RL, Larsen AR, Andersen PS, Price LB. Rapid differentiation between livestock-associated and livestock-independent Staphylococcus Aureus CC398 clades. PLoS One. 2013;8(11):e79645.CrossRefPubMedPubMedCentral
44.
Votintseva AA, Miller RR, Fung R, Knox K, Godwin H, Peto TE, Crook DW, Bowden R, Walker AS. Multiple-strain colonization in nasal carriers of Staphylococcus Aureus. J Clin Microbiol. 2014;52(4):1192–200.CrossRefPubMedPubMedCentral
45.
Goerge T, Lorenz MB, van Alen S, Hubner NO, Becker K, Kock R. MRSA colonization and infection among persons with occupational livestock exposure in Europe: prevalence, preventive options and evidence. Vet Microbiol. 2017;200:6–12.
46.
Ritchie SR, Isdale E, Priest P, Rainey PB, Thomas MG. The turnover of strains in intermittent and persistent nasal carriers of Staphylococcus Aureus. J Inf Secur. 2016;72(3):295–301.
47.
Williams REO. Healthy carriage of Staphylococcus Aureus: its prevalence and importance. Bacteriol Rev. 1963;27(1):56–71.
48.
Verhoeven PO, Gagnaire J, Botelho-Nevers E, Grattard F, Carricajo A, Lucht F, Pozzetto B, Berthelot P. Detection and clinical relevance of Staphylococcus Aureus nasal carriage: an update. Expert Rev Anti-Infect Ther. 2014;12(1):75–89.CrossRefPubMed
49.
von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus Aureus bacteremia. Study group. N Engl J Med. 2001;344(1):11–6.CrossRefPubMed
50.
Verhoeven PO, Grattard F, Carricajo A, Lucht F, Cazorla C, Garraud O, Pozzetto B, Berthelot P. An algorithm based on one or two nasal samples is accurate to identify persistent nasal carriers of Staphylococcus Aureus. Clin Microbiol Infect. 2012;18(6):551–7.CrossRefPubMed
51.
Ghasemzadeh-Moghaddam H, Neela V, van Wamel W, Hamat RA, Shamsudin MN, Hussin NS, Aziz MN, Haspani MS, Johar A, Thevarajah S, Vos M, van Belkum A. Nasal carriers are more likely to acquire exogenous Staphylococcus aureus strains than non-carriers. Clin Microbiol Infect. 2015;21(11):998.e1–7.CrossRef
52.
Bos ME, Verstappen KM, van Cleef BA, Dohmen W, Dorado-Garcia A, Graveland H, Duim B, Wagenaar JA, Kluytmans JA, Heederik DJ. Transmission through air as a possible route of exposure for MRSA. J Expo Sci Environ Epidemiol. 2016;26(3):263–9.CrossRefPubMed
53.
Graveland H, Wagenaar JA, Bergs K, Heesterbeek H, Heederik D. Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS One. 2011;6(2):e16830.CrossRefPubMedPubMedCentral
54.
Bosch T, Verkade E, van Luit M, Landman F, Kluytmans J, Schouls LM. Transmission and persistence of livestock-associated methicillin-resistant Staphylococcus Aureus among veterinarians and their household members. Appl Environ Microbiol. 2015;81(1):124–9.CrossRefPubMed
55.
Verkade E, Kluytmans-van den Bergh M, van Benthem B, van Cleef B, van Rijen M, Bosch T, Schouls L, Kluytmans J. Transmission of methicillin-resistant Staphylococcus Aureus CC398 from livestock veterinarians to their household members. PLoS One. 2014;9(7):e100823.CrossRefPubMedPubMedCentral
56.
Grontvedt CA, Elstrom P, Stegger M, Skov RL, Skytt Andersen P, Larssen KW, Urdahl AM, Angen O, Larsen J, Amdal S, Lotvedt SM, Sunde M, Bjornholt JV. Methicillin-resistant Staphylococcus Aureus CC398 in humans and pigs in Norway: a "one health" perspective on introduction and transmission. Clin Infect Dis. 2016;63(11):1431–8.CrossRefPubMedPubMedCentral
57.
Nair R, Wu J, Carrel M, O'Brien A, Quick M, Farina S, Wardyn S, Thapaliya D, Grenier D, Smith TC. Prospective multicenter surveillance identifies Staphylococcus Aureus infections caused by livestock-associated strains in an agricultural state. Diagn Microbiol Infect Dis. 2016;85(3):360-366.
58.
Larsen J, Petersen A, Sorum M, Stegger M, van Alphen L, Valentiner-Branth P, Knudsen LK, Larsen LS, Feingold B, Price LB, Andersen PS, Larsen AR, Skov RL: Meticillin-resistant Staphylococcus aureus CC398 is an increasing cause of disease in people with no livestock contact in Denmark, 1999 to 2011. Euro Surveill 2015, 20(37). doi:10.​2807/​1560–7917.​ES.​2015.​20.​37.​30021.
59.
Omland O, Hoffmann L. Occupational acquisition of methicillin-resistant Staphylococcus Aureus in humans--a description of MRSA carrier and infected cases from the region of North Jutland in Denmark. Ann Agric Environ Med. 2012;19(4):637–40.PubMed
60.
VAN Cleef BA, VAN Benthem BH, Verkade EJ, VAN Rijen MM, Kluytmans-VAN DEN Bergh MF, Graveland H, Bosch T, Verstappen KM, Wagenaar JA, Heederik D, Kluytmans JA: Health and health-related quality of life in pig farmers carrying livestock-associated methicillin-resistant Staphylococcus Aureus. Epidemiol Infect 2016, 144(8):1774–1783.
61.
Nielsen RT, Kemp M, Holm A, Skov MN, Detlefsen M, Hasman H, Aarestrup FM, Kaas RS, Nielsen JB, Westh H, Kolmos HJ. Fatal septicemia linked to transmission of MRSA clonal complex 398 in hospital and nursing home, Denmark. Emerg Infect Dis. 2016;22(5):900–2.CrossRefPubMedPubMedCentral
Metadata
Title
Longitudinal study of Staphylococcus aureus colonization and infection in a cohort of swine veterinarians in the United States
Authors
Jisun Sun
My Yang
Srinand Sreevatsan
Jeffrey B. Bender
Randall S. Singer
Todd P. Knutson
Douglas G. Marthaler
Peter R. Davies
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2802-1

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