Prevalence of non-aureus staphylococci species causing intramammary infections in Canadian dairy herds

Journal of Dairy Science

Volumn 100, Issue 7, 2017, Pages 5592-5612

  Condas, Larissa A Z ^a,b   De Buck, Jeroen ^a,b   Nobrega, Diego B ^a,b   Carson, Domonique A ^a,b   Naushad, Sohail ^a,b   De Vliegher, Sarne ^c   Zadoks, Ruth N ^d   Middleton, John R ^e   Dufour, Simon ^b,f   Kastelic, John P ^a   Barkema, Herman W ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b Canadian Bovine Mastitis Research Network   (Canada)

^c GHENT UNIVERSITY   (Belgium)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e UNIVERSITY OF MISSOURI   (United States)

^f UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

coagulase negative staphylococci; dairy; intramammary infection; mastitis; prevalence

Indexed keywords

ANIMAL; BAYES THEOREM; BOVINE; BOVINE MASTITIS; CANADA; CATTLE DISEASE; CLASSIFICATION; FEMALE; ISOLATION AND PURIFICATION; MICROBIOLOGY; MILK; PREGNANCY; PREVALENCE; SPECIES DIFFERENCE; STAPHYLOCOCCUS; STAPHYLOCOCCUS INFECTION; UDDER; VETERINARY;

ANIMALS; BAYES THEOREM; CANADA; CATTLE; CATTLE DISEASES; FEMALE; MAMMARY GLANDS, ANIMAL; MASTITIS, BOVINE; MILK; PREGNANCY; PREVALENCE; SPECIES SPECIFICITY; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS;

EID: 85019373440     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2016-12478     Document Type: Article

References (77)

1. Aarestrup, F.M., Wegener, H.C., Rosdahl, V.T., Jensen, N.E., Staphylococcal and other bacterial species associated with intramammary infections in Danish dairy herds. Acta Vet. Scand. 36 (1995), 475–487 8669375.
2. Barkema, H.W., Schukken, Y.H., Lam, T.J., Galligan, D.T., Beiboer, M.L., Brand, A., Estimation of interdependence among quarters of the bovine udder with subclinical mastitis and implications for analysis. J. Dairy Sci. 80 (1997), 1592–1599 9276797.
3. Barkema, H.W., Von Keyserlingk, M.A.G., Kastelic, J.P., Lam, T.J.G.M., Luby, C., Roy, J.P., LeBlanc, S.J., Keefe, G.P., Kelton, D.F., Invited review: Changes in the dairy industry affecting dairy health and welfare. J. Dairy Sci. 98 (2015), 7426–7445 26342982.
4. Becker, K., Heilmann, C., Peters, G., Coagulase-negative staphylococci. Clin. Microbiol. Rev. 27 (2014), 870–926 25278577.
5. Braem, G., De Vliegher, S., Verbist, B., Heyndrickx, M., Leroy, F., De Vuyst, L., Culture-independent exploration of the teat apex microbiota of dairy cows reveals a wide bacterial species diversity. Vet. Microbiol. 157 (2012), 383–390 22266158.
6. Calcutt, M.J., Foecking, M.F., Fry, P.R., Hsieh, H.-Y., Perry, J., Stewart, G.C., Scholl, D.T., Messier, S., Middleton, J.R., Draft genome sequence of bovine mastitis isolate Staphylococcus agnetis CBMRN 20813338. Genome Announc., 2, 2014, e00883-14 25189590.
7. Canadian Dairy Information Centre. Dairy barns by type in Canada, 2016 Accessed December 17, 2016. http://www.dairyinfo.gc.ca/index_e.php?s1=dff-fcil&s2=farm-ferme&s3=db-el.
8. Capurro, A., Artursson, K., Waller, K.P., Bengtsson, B., Ericsson-Unnerstad, H., Aspán, A., Comparison of a commercialized phenotyping system, antimicrobial susceptibility testing, and tuf gene sequence-based genotyping for species-level identification of coagulase-negative staphylococci isolated from cases of bovine mastitis. Vet. Microbiol. 134 (2009), 327–333 18930604.
9. Chaffer, M., Leitner, G., Winkler, M., Glickman, A., Krifucks, O., Ezra, E., Saran, A., Coagulase-negative staphylococci and mammary gland infections in cows. Zentralbl. Veterinarmed. B. 46 (1999), 707–712 10676149.
10. Chakravorty, S., Helb, D., Burday, M., Connell, N., Alland, D., A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J. Microbiol. Methods 69 (2007), 330–339 17391789.
11. Crawley, M.J., The R Book, 2nd ed., 2013, Wiley, Chichester, United Kingdom.
12. De Visscher, A., Piepers, S., Haesebrouck, F., De Vliegher, S., Intramammary infection with coagulase-negative staphylococci at parturition: Species-specific prevalence, risk factors, and effect on udder health. J. Dairy Sci. 99 (2016), 6457–6469 27236763.
13. De Visscher, A., Piepers, S., Haesebrouck, F., Supré, K., De Vliegher, S., Coagulase-negative Staphylococcus species in bulk milk: Prevalence, distribution, and associated subgroup- and species-specific risk factors. J. Dairy Sci. 100 (2017), 629–642 27865514.
14. De Visscher, A., Supré, K., Haesebrouck, F., Zadoks, R.N., Piessens, V., Van Coillie, E., Piepers, S., De Vliegher, S., Further evidence for the existence of environmental and host-associated species of coagulase-negative staphylococci in dairy cattle. Vet. Microbiol. 172 (2014), 466–474 25008316.
15. De Vliegher, S., Fox, L.K., Piepers, S., McDougall, S., Barkema, H.W., Invited review: Mastitis in dairy heifers: Nature of the disease, potential impact, prevention, and control. J. Dairy Sci. 95 (2012), 1025–1040 22365187.
16. De Vliegher, S., Laevens, H., Opsomer, G., Leroy, J.L.M., Barkema, H.W., de Kruif, A., Prepartum teat apex colonization with Staphylococcus chromogenes in dairy heifers is associated with low somatic cell count in early lactation. Vet. Microbiol. 92 (2003), 245–252 12523986.
17. De Vliegher, S., Opsomer, G., Vanrolleghem, A., Devriese, L.A., Sampimon, O.C., Sol, J., Barkema, H.W., Haesebrouck, F., de Kruif, A., In vitro growth inhibition of major mastitis pathogens by Staphylococcus chromogenes originating from teat apices of dairy heifers. Vet. Microbiol. 101 (2004), 215–221 15223126.
18. Denwood, M., Plummer, M., Runjags: An R package providing interface utilities, model templates, parallel computing methods and additional distributions for MCMC models in JAGS. J. Stat. Softw. 71 (2016), 1–25.
19. Dohoo, I.R., Martin, S.W., Stryhn, H., Veterinary Epidemiologic Research. McPike, M.S., (eds.), 2010, Atlantic Veterinary College, Charlottetown, PE, Canada.
20. Dohoo, I.R., Smith, J., Andersen, S., Kelton, D.F., Godden, S., Diagnosing intramammary infections: Evaluation of definitions based on a single milk sample. J. Dairy Sci. 94 (2011), 250–261 21183035.
21. Drancourt, M., Raoult, D., rpoB gene sequence-based identification of Staphylococcus species. J. Clin. Microbiol. 40 (2002), 1333–1338 11923353.
22. Dufour, S., Dohoo, I.R., Barkema, H.W., Descoteaux, L., Devries, T.J., Reyher, K.K., Roy, J.P., Scholl, D.T., Epidemiology of coagulase-negative staphylococci intramammary infection in dairy cattle and the effect of bacteriological culture misclassification. J. Dairy Sci. 95 (2012), 3110–3124 22612947.
23. Dufour, S., Fréchette, A., Barkema, H.W., Mussell, A., Scholl, D.T., Invited review: Effect of udder health management practices on herd somatic cell count. J. Dairy Sci. 94 (2011), 563–579 21257026.
24. Fox, L.K., Prevalence, incidence and risk factors of heifer mastitis. Vet. Microbiol. 134 (2009), 82–88 18930610.
25. Fry, P.R., Middleton, J.R., Dufour, S., Perry, J., Scholl, D., Dohoo, I., Association of coagulase-negative staphylococcal species, mammary quarter milk somatic cell count, and persistence of intramammary infection in dairy cattle. J. Dairy Sci. 97 (2014), 4876–4885 24931524.
26. Gillespie, B.E., Headrick, S.I., Boonyayatra, S., Oliver, S.P., Prevalence and persistence of coagulase-negative Staphylococcus species in three dairy research herds. Vet. Microbiol. 134 (2009), 65–72 18950962.
27. Hogan, J.S., Gonzales, R.N., Harmon, R.J., Nickerson, S.P., Oliver, J.W., Pankey, J.W., Smith, K.L., Laboratory Handbook on Bovine Mastitis, 2009, National Mastitis Council, Madison, WI.
28. Koop, G., De Vliegher, S., De Visscher, A., Supré, K., Haesebrouck, F., Nielen, M., van Werven, T., Differences between coagulase-negative Staphylococcus species in persistence and in effect on somatic cell count and milk yield in dairy goats. J. Dairy Sci. 95 (2012), 5075–5084 22916911.
29. Matos, J.S., White, D.G., Harmon, R.J., Langlois, B.E., Isolation of Staphylococcus aureus from sites other than the lactating mammary gland. J. Dairy Sci. 74 (1991), 1544–1549 1880263.
30. Matthews, K.R., Harmon, R.J., Langlois, B.E., Prevalence of Staphylococcus species during the periparturient period in primiparous and multiparous cows. J. Dairy Sci. 75 (1992), 1835–1839 1500579.
31. Matthews, K.R., Harmon, R.J., Smith, B.A., Protective effect of Staphylococcus chromogenes infection against Staphylococcus aureus infection in the lactating bovine mammary gland. J. Dairy Sci. 73 (1990), 3457–3462 2099367.
32. McInturff, P., Johnson, W.O., Cowling, D., Gardner, I.A., Modelling risk when binary outcomes are subject to error. Stat. Med. 23 (2004), 1095–1109 15057880.
33. Mellmann, A., Becker, K., von Eiff, C., Keckevoet, U., Schumann, P., Harmsen, D., Sequencing and staphylococci identification. Emerg. Infect. Dis. 12 (2006), 333–336 16494767.
34. Mørk, T., Jorgensen, H.J., Sunde, M., Kvitle, B., Sviland, S., Waage, S., Tollersrud, T., Persistence of staphylococcal species and genotypes in the bovine udder. Vet. Microbiol. 159 (2012), 171–180 22503603.
35. Myllys, V., Staphylococci in heifer mastitis before and after parturition. J. Dairy Res. 62 (1995), 51–60 7738245.
36. Naushad, S., Barkema, H.W., Luby, C., Condas, L.A.Z., Carson, D.A., Nobrega, D.B., De Buck, J., Comprehensive phylogenetic analysis of bovine non-aureus Staphylococcus species based on whole genome sequencing. Front. Microbiol., 7, 2016, 1990 28066335.
37. Nickerson, S.C., Control of heifer mastitis: Antimicrobial treatment—An overview. Vet. Microbiol. 134 (2009), 128–135 18963599.
38. Olde Riekerink, R.G.M., Barkema, H.W., Kelton, D.F., Scholl, D.T., Incidence rate of clinical mastitis on Canadian dairy farms. J. Dairy Sci. 91 (2008), 1366–1377 18349229.
39. Olde Riekerink, R.G., Barkema, H.W., Veenstra, S., Poole, D.E., Dingwell, R.T., Keefe, G.P., Prevalence of contagious mastitis pathogens in bulk tank milk in Prince Edward Island. Can. Vet. J. 47 (2006), 567–572 16808229.
40. Oliver, S.P., Jayarao, B.M., Coagulase-negative staphylococcal intramammary infections in cows and heifers during the nonlactating and periparturient periods. J. Vet. Med. B 44 (1997), 355–363 9283286.
41. Osterås, O., Sølverød, L., Reksen, O., Milk culture results in a large Norwegian survey—Effects of season, parity, days in milk, resistance, and clustering. J. Dairy Sci. 89 (2006), 1010–1023 16507696.
42. Piccart, K., Verbeke, J., De Visscher, A., Piepers, S., Haesebrouck, F., De Vliegher, S., Local host response following an intramammary challenge with Staphylococcus fleurettii and different strains of Staphylococcus chromogenes in dairy heifers. Vet. Res., 47, 2016, 56 27176792.
43. Piepers, S., De Meulemeester, L., de Kruif, A., Opsomer, G., Barkema, H.W., De Vliegher, S., Prevalence and distribution of mastitis pathogens in subclinically infected dairy cows in Flanders, Belgium. J. Dairy Res. 74 (2007), 478–483 17931457.
44. Piepers, S., De Vliegher, S., de Kruif, A., Opsomer, G., Barkema, H.W., Impact of intramammary infections in dairy heifers on future udder health, milk production, and culling. Vet. Microbiol. 134 (2009), 113–120 18930608.
45. Piepers, S., Opsomer, G., Barkema, H.W., de Kruif, A., De Vliegher, S., Heifers infected with coagulase-negative staphylococci in early lactation have fewer cases of clinical mastitis and higher milk production in their first lactation than noninfected heifers. J. Dairy Sci. 93 (2010), 2014–2024 20412915.
46. Piepers, S., Peeters, K., Opsomer, G., Barkema, H.W., Frankena, K., De Vliegher, S., Pathogen group specific risk factors at herd, heifer and quarter levels for intramammary infections in early lactating dairy heifers. Prev. Vet. Med. 99 (2011), 91–101 21411160.
47. Piepers, S., Schukken, Y.H., Passchyn, P., De Vliegher, S., The effect of intramammary infection with coagulase-negative staphylococci in early lactating heifers on milk yield throughout first lactation revisited. J. Dairy Sci. 96 (2013), 5095–5105 23769365.
48. Piessens, V., De Vliegher, S., Verbist, B., Braem, G., Van Nuffel, A., De Vuyst, L., Heyndrickx, M., Van Coillie, E., Intra-species diversity and epidemiology varies among coagulase-negative Staphylococcus species causing bovine intramammary infections. Vet. Microbiol. 155 (2012), 62–71 21889271.
49. Piessens, V., Van Coillie, E., Verbist, B., Supré, K., Braem, G., Van Nuffel, A., De Vuyst, L., Heyndrickx, M., De Vliegher, S., Distribution of coagulase-negative Staphylococcus species from milk and environment of dairy cows differs between herds. J. Dairy Sci. 94 (2011), 2933–2944 21605763.
50. Pitkälä, A., Haveri, M., Pyörälä, S., Myllys, V., Honkanen-Buzalski, T., Bovine mastitis in Finland 2001—Prevalence, distribution of bacteria, and antimicrobial resistance. J. Dairy Sci. 87 (2004), 2433–2441 15328265.
51. Pyörälä, S., Taponen, S., Coagulase-negative staphylococci-emerging mastitis pathogens. Vet. Microbiol. 134 (2009), 3–8 18848410.
52. Rainard, P., Ducelliez, M., Poutrel, B., The contribution of mammary infections by coagulase-negative staphylococci to the herd bulk milk somatic cell count. Vet. Res. Commun. 14 (1990), 193–198 2382403.
53. Reksen, O., Gröhn, Y.T., Barlow, J.W., Schukken, Y.H., Transmission dynamics of intramammary infections with coagulase-negative staphylococci. J. Dairy Sci. 95 (2012), 4899–4910 22916894.
54. Reyher, K.K., Dohoo, I.R., Muckle, C.A., Evaluation of clustering of new intramammary infections in the bovine udder, including the impact of previous infections, herd prevalence, and somatic cell count on their development. J. Dairy Sci. 96 (2013), 219–233.
55. Reyher, K.K., Dufour, S., Barkema, H.W., Des Coteaux, L., Devries, T.J., Dohoo, I.R., Keefe, G.P., Roy, J.P., Scholl, D.T., The National Cohort of Dairy Farms—A data collection platform for mastitis research in Canada. J. Dairy Sci. 94 (2011), 1616–1626 21338829.
56. Sampimon, O.C., Barkema, H.W., Berends, I.M.G.A., Sol, J., Lam, T.J.G.M., Prevalence and herd-level risk factors for intramammary infection with coagulase-negative staphylococci in Dutch dairy herds. Vet. Microbiol. 134 (2009), 37–44 18977613.
57. Sampimon, O.C., Zadoks, R.N., De Vliegher, S., Supré, K., Haesebrouck, F., Barkema, H.W., Sol, J., Lam, T.J., Performance of API Staph ID 32 and Staph-Zym for identification of coagulase-negative staphylococci isolated from bovine milk samples. Vet. Microbiol. 136 (2009), 300–305 19110383.
58. Schukken, Y.H., González, R.N., Tikofsky, L.L., Schulte, H.F., Santisteban, C.G., Welcome, F.L., Bennett, G.J., Zurakowski, M.J., Zadoks, R.N., CNS mastitis: Nothing to worry about?. Vet. Microbiol. 134 (2009), 9–14 18842362.
59. Supré, K., Haesebrouck, F., Zadoks, R.N., Vaneechoutte, M., Piepers, S., De Vliegher, S., Some coagulase-negative Staphylococcus species affect udder health more than others. J. Dairy Sci. 94 (2011), 2329–2340 21524522.
60. Taponen, S., Bjorkroth, J., Pyorala, S., Coagulase-negative staphylococci isolated from bovine extramammary sites and intramammary infections in a single dairy herd. J. Dairy Res. 75 (2008), 422–429 18700996.
61. Taponen, S., Koort, J., Bjorkroth, J., Saloniemi, H., Pyorala, S., Bovine intramammary infections caused by coagulase-negative staphylococci may persist throughout lactation according to amplified fragment length polymorphism-based analysis. J. Dairy Sci. 90 (2007), 3301–3307 17582115.
62. Taponen, S., Pyörälä, S., Coagulase-negative staphylococci as cause of bovine mastitis—Not so different from Staphylococcus aureus?. Vet. Microbiol. 134 (2009), 29–36 18977615.
63. Taponen, S., Simojoki, H., Haveri, M., Larsen, H.D., Pyörälä, S., Clinical characteristics and persistence of bovine mastitis caused by different species of coagulase-negative staphylococci identified with API or AFLP. Vet. Microbiol. 115 (2006), 199–207 16527434.
64. Taponen, S., Supre, K., Piessens, V., Van Coillie, E., De Vliegher, S., Koort, J.M., Staphylococcus agnetis sp. nov., a coagulase-variable species from bovine subclinical and mild clinical mastitis. Int. J. Syst. Evol. Microbiol. 62 (2012), 61–65 21335502.
65. ten Napel, J., de Haas, Y., de Jong, G., Lam, T.J., Ouweltjes, W., Windig, J.J., Characterization of distributions of somatic cell counts. J. Dairy Sci. 92 (2009), 1253–1264 19233818.
66. Tenhagen, B.A., Köster, G., Wallmann, J., Heuwieser, W., Prevalence of mastitis pathogens and their resistance against antimicrobial agents in dairy cows in Brandenburg, Germany. J. Dairy Sci. 89 (2006), 2542–2551 16772573.
67. Thorberg, B.M., Danielsson-Tham, M.L., Emanuelson, U., Persson Waller, K., Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. J. Dairy Sci. 92 (2009), 4962–4970 19762813.
68. Tomazi, T., Gonçalves, J.L., Barreiro, J.R., Arcari, M.A., dos Santos, M.V., Bovine subclinical intramammary infection caused by coagulase-negative staphylococci increases somatic cell count but has no effect on milk yield or composition. J. Dairy Sci. 98 (2015), 3071–3078 25726098.
69. Trinidad, P., Nickerson, S.C., Alley, T.K., Adkinson, R.W., Efficacy of intramammary treatment in unbred and primigravid dairy heifers. J. Am. Vet. Med. Assoc. 197 (1990), 465–470 2211291.
70. Vanderhaeghen, W., Piepers, S., Leroy, F., Van Coillie, E., Haesebrouck, F., De Vliegher, S., Invited review: Effect, persistence, and virulence of coagulase-negative Staphylococcus species associated with ruminant udder health. J. Dairy Sci. 97 (2014), 5275–5293 24952781.
71. Vanderhaeghen, W., Piepers, S., Leroy, F., Van Coillie, E., Haesebrouck, F., De Vliegher, S., Identification, typing, ecology and epidemiology of coagulase negative staphylococci associated with ruminants. Vet. J. 203 (2015), 44–51 25467994.
72. White, D.G., Harmon, R.J., Matos, J.E., Langlois, B.E., Isolation and identification of coagulase-negative Staphylococcus species from bovine body sites and streak canals of nulliparous heifers. J. Dairy Sci. 72 (1989), 1886–1892 2778172.
73. Woodward, W.D., Besser, T.E., Ward, A.C., Corbeil, L.B., In vitro growth inhibition of mastitis pathogens by bovine teat skin normal flora. Can. J. Vet. Res. 51 (1987), 27–31 3552170.
74. Woodward, W.D., Ward, A.C.S., Fox, L.K., Corbeil, L.B., Teat skin normal flora and colonization with mastitis pathogen inhibitors. Vet. Microbiol. 17 (1988), 357–365 3188374.
75. Zadoks, R.N., Barkema, H.W., Sampimon, O.C., Wellenberg, G.J., Gröhn, Y.T., Schukken, Y.H., Cow- and quarter-level risk factors for Streptococcus uberis and Staphylococcus aureus mastitis. J. Dairy Sci. 84 (2001), 2649–2663 11814021.
76. Zadoks, R.N., Middleton, J.R., McDougall, S., Katholm, J., Schukken, Y.H., Molecular epidemiology of mastitis pathogens of dairy cattle and comparative relevance to humans. J. Mammary Gland Biol. Neoplasia 16 (2011), 357–372 21968538.
77. Zadoks, R.N., Watts, J.L., Species identification of coagulase-negative staphylococci: Genotyping is superior to phenotyping. Vet. Microbiol. 134 (2009), 20–28 18930607.