Evaluation and cluster analysis of inflammatory reactions of dairy cattle mastitis pathogens in milk samples submitted for microbiological examination

  1. Diaz-Cao, Jose M. 1
  2. Barreal, María L. 2
  3. Pombo, Belén 2
  4. Prieto, Alberto 1
  5. Alonso, José M.
  6. Iglesias, Antonio 4
  7. Lorenzana, Roberto 2
  8. López-Novo, Cynthia 1
  9. Díez-Baños, Pablo 1
  10. Fernández, Gonzalo 1
  1. 1 Universidade de Santiago de Compostela, Faculty of Veterinary Sciences, Dept. Animal Pathology. 27002 Lugo
  2. 2 Laboratorio Interprofesional Gallego de Análisis de la Leche (LIGAL), Edificio de Laboratorios Agrarios. 15318 Abegondo, A Coruña
  3. 3 Universidade de Santiago de Compostela, Faculty of Sciences, Dept. Statistics, Mathematical Analysis and Optimization. 27002 Lugo
  4. 4 niversidade de Santiago de Compostela, Faculty of Veterinary Sciences, Dept. Anatomy, Animal Production and Clinical Veterinary Sciences. 27002 Lugo
Spanish journal of agricultural research

ISSN: 1695-971X 2171-9292

Ano de publicación: 2019

Volume: 17

Número: 4

Tipo: Artigo

DOI: 10.5424/SJAR/2019174-15316 DIALNET GOOGLE SCHOLAR lock_openAcceso aberto editor

Outras publicacións en: Spanish journal of agricultural research


Aim of study: We have classified into homogenous groups a wide spectrum of mammary pathogens according to their frequency of isolation in clinical mastitis and their somatic cell counts in non-clinical mastitis.Area of study: The study was conducted in Galicia (NW Spain)Material and methods: 163,741 dairy cattle quarter milk samples were analyzed. We identified mastitis pathogens to the species level and performed a cluster analysis to classify these microorganisms by their median of Linear Score (mLS), percentage of isolation in clinical mastitis samples (%ICS) and percentage of isolation in samples with somatic cell counts under 100,000 cells/mL (%ISU100).Main results: Forty-three different species were isolated. Cluster analysis identified 4 groups of pathogens; mLS and %ICS progressively increased from Group I to Group IV and %ISU100 decreased. However, several pathogens included in groups II and III showed %ISU100 values higher than 2% and 3%. Minor pathogens were mainly clustered in Group I (e.g., Corynebacterium spp. and most of Staphylococcus spp.), while known major pathogens were included in Groups II, III y IV. Species of the same family, genus or microbiological group like Enterobacteriaceae or Enterococcus spp. were frequently separated into different groups, thus showing heterogeneity among the members of these groups.Research highlights: Results obtained here may aid in assessing the pathogenicity of sporadic pathogens in relation to more well-known pathogens and suggest that the traditional classification between minor and major pathogens is an oversimplification of the reality, especially for the latter category.

Referencias bibliográficas

  • Bexiga R, Pereira H, Pereira O, Leitão A, Carneiro C, Ellis KA, Vilela CL, 2011. Observed reduction in recovery of Corynebacterium spp. from bovine milk samples by use of a teat cannula. J Dairy Res 78: 9-14. https://doi.org/10.1017/S0022029910000609
  • Bradley AJ, 2002. Bovine mastitis: An evolving disease. Vet J 164: 116-128. https://doi.org/10.1053/tvjl.2002.0724
  • Brown BW, Barnum DA, Jasper DE, McDonald JS, Schultze WD, 1981. Microbiological procedures for use in the diagnosis of bovine mastitis, 2nd ed. National Mastitis Council, Iowa, USA.
  • Clarke KR, Somerfield PJ, Gorley RN, 2008. Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Bio Ecol 366: 56-69. https://doi.org/10.1016/j.jembe.2008.07.009
  • Condas LAZ, De Buck J, Nobrega DB, Carson DA, Roy JP, Keefe GP, DeVries TJ, Middleton JR, Dufour S, Barkema HW, 2017. Distribution of non- aureus staphylococci species in udder quarters with low and high somatic cell count, and clinical mastitis. J Dairy Sci 100: 5613-5627. https://doi.org/10.3168/jds.2016-12479
  • Damm M, Holm C., Blaabjerg M, Bro MN, Schwarz D, 2017. Differential somatic cell count -A novel method for routine mastitis screening in the frame of dairy herd improvement testing programs. J Dairy Sci 100: 4926-4940. https://doi.org/10.3168/jds.2016-12409
  • de Haas Y, De Veerkamp R, Barkema H, Gröhn YT, Schukken YH, 2004. Associations between pathogen-specific cases of clinical mastitis and somatic cell count patterns. J Dairy Sci 87: 95-105. https://doi.org/10.3168/jds.S0022-0302(04)73146-X
  • Devriese LA, Hommez J, Laevens H, Pot B, Vandamme P, Haesebrouck F, 1999. Identification of aesculin-hydrolyzing streptococci, lactococci, aerococci and enterococci from subclinical intramammary infections in dairy cows. Vet Microbiol 70: 87-94. https://doi.org/10.1016/S0378-1135(99)00124-8
  • Djabri B, Bareille N, Beaudeau F, Seegers H, 2002. Quarter milk somatic cell count in infected dairy cows: a meta-analysis. Vet Res 33: 335-357. https://doi.org/10.1051/vetres:2002021
  • Dohoo IR, Meek AH, 1982. Somatic cell counts in bovine milk. Can Vet J 23: 119-125.
  • Dohoo IR, Smith J, Andersen S, Kelton DF, Godden S, 2011. Diagnosing intramammary infections: evaluation of definitions based on a single milk sample. J Dairy Sci 94: 250-261. https://doi.org/10.3168/jds.2010-3559
  • Fernández G, Barreal ML, Pombo MB, Ginzo-Villamayor MJ, González-Manteiga W, Prieto A, Lago N, González-Palencia J, 2013. Comparison of the epidemiological behavior of mastitis pathogens by applying time-series analysis in results of milk samples submitted for microbiological examination. Vet Res Commun 37: 259-267. https://doi.org/10.1007/s11259-013-9570-1
  • Fry PR, Middleton JR, Dufour S, Perry J, Scholl D, Dohoo I, 2014. Association of coagulase-negative staphylococcal species, mammary quarter milk somatic cell count, and persistence of intramammary infection in dairy cattle. J Dairy Sci 97: 4876-4885. https://doi.org/10.3168/jds.2013-7657
  • Guélat-Brechbuehl M, Thomann A, Albini S, Moret-Stalder S, Reist M, Bodmer M, Michel A, Niederberger MD, Kaufmann T, 2010. Cross-sectional study of Streptococcus species in quarter milk samples of dairy cows in the canton of Bern, Switzerland. Vet Rec 167: 211-215. https://doi.org/10.1136/vr.167.6.211
  • Harmon RJ, 1994. Physiology of mastitis and factors affecting somatic cell counts. J Dairy Sci 77: 2103-2112. https://doi.org/10.3168/jds.S0022-0302(94)77153-8
  • Hogan JS, Smith KL, Hoblet KH, Schoenberger PS, Todhunter DA, Hueston WD, Pritchard DE, Bowman GL, Heider LE, Brockett BL, Conrad HR, 1989. Field survey of clinical mastitis in low somatic cell count herds. J Dairy Sci 72: 1547-1556. https://doi.org/10.3168/jds.S0022-0302(89)79266-3
  • Husson F, Josse J, Pagès J, 2010. Principal component methods - hierarchical clustering - partitional clustering: why would we need to choose for visualizing data? Tech Rep 1-17.
  • IDF, 2013. Guidelines for the use and interpretation of bovine milk somatic cell counts (SCC) in the dairy industry. Bull Int Dairy Feder: 466
  • Jarp J, 1991. Classification of coagulase-negative staphylococci isolated from bovine clinical and subclinical mastitis. Vet Microbiol 27: 151-158. https://doi.org/10.1016/0378-1135(91)90006-2
  • Kalmus P, Aasmäe B, Kärssin A, Orro T, Kask K, 2011. Udder pathogens and their resistance to antimicrobial agents in dairy cows in Estonia. Acta Vet Scand 53: 4. https://doi.org/10.1186/1751-0147-53-4
  • Lê S, Josse J, Husson F, 2008. FactoMineR : An R package for multivariate analysis. J Stat Softw 25: 1-18. https://doi.org/10.18637/jss.v025.i01
  • Makovec JA, Ruegg PL, 2003. Results of milk samples submitted for microbiological examination in Wisconsin from 1994 to 2001. J Dairy Sci 86: 3466-3472. https://doi.org/10.3168/jds.S0022-0302(03)73951-4
  • Malinowski E, Lassa H, Ossowska AKŁ, Markiewicz H, Kaczmarowski MŁ, Smulski S, 2006. Relationship between mastitis agents and somatic cell count in foremilk samples. Bull Vet Inst Pulawy 50: 349-352.
  • Middleton JR, Fox LK, 2002. Influence of Staphylococcus aureus strain on mammary quarter milk production. Vet Rec 150: 411-413. https://doi.org/10.1136/vr.150.13.411
  • Nam HM, Kim JM, Lim SK, Jang KC, Jung SC, 2010. Infectious aetiologies of mastitis on Korean dairy farms during 2008. Res Vet Sci 88: 372-374. https://doi.org/10.1016/j.rvsc.2009.12.008
  • Oliveira CSF, Hogeveen H, Botelho AM, Maia PV, Coelho SG, Haddad JPA, 2015. Cow-specific risk factors for clinical mastitis in Brazilian dairy cattle. Prev Vet Med 121: 297-305. https://doi.org/10.1016/j.prevetmed.2015.08.001
  • Packer RA, 1977. Bovine mastitis produced by corynebacteria. J Am Vet Med Assoc 170: 1164-1165.
  • Piepers S, De Meulemeester L, de Kruif A, Opsomer G, Barkema HW, De Vliegher S, 2007. Prevalence and distribution of mastitis pathogens in subclinically infected dairy cows in Flanders, Belgium. J Dairy Res 74: 478-483. https://doi.org/10.1017/S0022029907002841
  • Pitkälä A, Haveri M, Pyorälä S, Myllys V, Honkanen-Buzalski T, 2004. Bovine mastitis in Finland 2001-prevalence, distribution of bacteria, and antimicrobial resistance. J Dairy Sci 87: 2433-2441. https://doi.org/10.3168/jds.S0022-0302(04)73366-4
  • Pyörälä S, Taponen S, 2009. Coagulase-negative staphylococci-Emerging mastitis pathogens. Vet Microbiol 134: 3-8. https://doi.org/10.1016/j.vetmic.2008.09.015
  • Quinn PJ, Markey BK, Leonard FC, Fitzpatrick ES, Fanning S, Hartigan PJ, 2011. Veterinary microbiology and microbial disease, 2nd ed. Wiley-Blackwell, Oxford, UK.
  • Richard JL, McDonald JS, Fichtner RE, Anderson AJ, 1980. Identification of yeasts from infected bovine mammary glands and their experimental infectivity in cattle. Am J Vet Res 41: 1991-1994.
  • Sampimon OC, Barkema HW, Berends IMGA, Sol J, Lam TJGM, 2009. Prevalence and herd-level risk factors for intramammary infection with coagulase-negative staphylococci in Dutch dairy herds. Vet Microbiol 134: 37-44. https://doi.org/10.1016/j.vetmic.2008.09.010
  • Scaccabarozzi L, Turchetti B, Buzzini P, Pisoni G, Bertocchi L, Arrigoni N, Boettcher P, Bronzo V, Moroni P, 2008. Short communication: isolation of Prototheca species strains from environmental sources in dairy herds. J Dairy Sci 91: 3474-3477. https://doi.org/10.3168/jds.2008-1115
  • Schukken YH, González RN, Tikofsky LL, Schulte HF, Santisteban CG, Welcome FL, Bennett GJ, Zurakowski MJ, Zadoks RN, 2009. CNS mastitis: Nothing to worry about? Vet Microbiol 134: 9-14. https://doi.org/10.1016/j.vetmic.2008.09.014
  • Schukken Y, Chuff M, Moroni P, Gurjar A, Santisteban C, Welcome F, Zadoks R, 2012. The "other" gram-negative bacteria in mastitis. Klebsiella, Serratia, and more. Vet Clin North Am - Food Anim Pract 28: 239-256. https://doi.org/10.1016/j.cvfa.2012.04.001
  • Schwarz D, Diesterbeck US, Failing K, König S, Brügemann K, Zschöck M, Wolter W, Czerny CP, 2010. Somatic cell counts and bacteriological status in quarter foremilk samples of cows in Hesse, Germany -a longitudinal study. J Dairy Sci 93: 5716-5728. https://doi.org/10.3168/jds.2010-3223
  • Shook GE, 1982. A linear scale for scoring somatic cell count. J Dairy Sci 65: 1108.
  • Steeneveld W, Hogeveen H, Barkema HW, van den Broek J, Huirne RBM, 2008. The influence of cow factors on the incidence of clinical mastitis in dairy cows. J Dairy Sci 91: 1391-1402. https://doi.org/10.3168/jds.2007-0705
  • Supré K, Haesebrouck F, Zadoks RN, Vaneechoutte M, Piepers S, De Vliegher S, 2011. Some coagulase-negative Staphylococcus species affect udder health more than others. J Dairy Sci 94: 2329-2340. https://doi.org/10.3168/jds.2010-3741
  • Taponen S, Simojoki H, Haveri M, Larsen HD, Pyörälä S, 2006. Clinical characteristics and persistence of bovine mastitis caused by different species of coagulase-negative staphylococci identified with API or AFLP. Vet Microbiol 115: 199-207. https://doi.org/10.1016/j.vetmic.2006.02.001
  • Taponen S, Koort J, Björkroth J, Saloniemi H, Pyörälä S, 2007. Bovine intramammary infections caused by coagulase-negative staphylococci may persist throughout lactation according to amplified fragment length polymorphism-based analysis. J Dairy Sci 90: 3301-3307. https://doi.org/10.3168/jds.2006-860
  • Tarabla H, Zurbriggen M, Canavesio V, Vitulich C, Calvinho L, 1993. Nocardia asteroides mastitis in a small Argentinian herd. Vet Rec 132: 303-303. https://doi.org/10.1136/vr.132.12.303-a
  • Tenhagen BA, Köster G, Wallmann J, Heuwieser W, 2006. Prevalence of mastitis pathogens and their resistance against antimicrobial agents in dairy ows in Brandenburg, Germany. J Dairy Sci 89: 2542-2551. https://doi.org/10.3168/jds.S0022-0302(06)72330-X
  • Thorberg BM, Danielsson-Tham ML, Emanuelson U, Persson Waller K, 2009. Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. J Dairy Sci 92: 4962-4970. https://doi.org/10.3168/jds.2009-2184
  • Todhunter DA, Smith KL, Hogan JS, 1995. Environmental streptococcal intramammary infections of the bovine mammary gland. J Dairy Sci 78: 2366-2374. https://doi.org/10.3168/jds.S0022-0302(95)76864-3
  • Ward Jr JH, 1963. Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58: 236-244. https://doi.org/10.1080/01621459.1963.10500845
  • Zadoks RN, van Leeuwen WB, Kreft D, Fox LK, Barkema HW, Schukken YH, van Belkum, 2002. Comparison of Staphylococcus aureus isolates from bovine and human skin, milking equipment, and bovine milk by phage typing, pulsed-field gel electrophoresis, and binary typing. J Clin Microbiol 40: 3894-3902. https://doi.org/10.1128/JCM.40.11.3894-3902.2002
  • Zadoks R, Fitzpatrick J, 2009. Changing trends in mastitis. Ir Vet J 62: S59. https://doi.org/10.1186/2046-0481-62-S4-S59
  • Zadoks RN, Middleton JR, McDougall S, Katholm J, Schukken YH, 2011. Molecular epidemiology of mastitis pathogens of dairy cattle and comparative relevance to humans. J Mammary Gland Biol Neoplasia 16: 357-372. https://doi.org/10.1007/s10911-011-9236-y