Korean Journal of
Veterinary Service

Caseous lymphadenitis, caused by Corynebacterium pseudotuberculosis has been a predominant disease among small ruminants on farms, causing significant losses for farm producer in the larger part of goat rearing nations across the world, for over a century. However, the control measures have not been very effective due to the chronic and usually subclinical nature of the infection. This has caused significant financial losses due to chronic ill-thrift, carcass condemnation, decreased meat yields and low reproduction as well as animal welfare. The current status of caseous lymphadenitis, with updated reseach information to the etiology, pathogenesis, clinical signs, identification, prevalence, prevention and vaccination are delineated in the review.

Keywords Caseous lymphadenitis,Corynebacterium pseudotuberculosis,Goat,

1. Abebe D, Sisay Tessema T. 2015. Determination of Corynebacterium pseudotuberculosis prevalence and antimicrobial susceptibility pattern of isolates from lymph nodes of sheep and goats at an organic export abattoir, Modjo, Ethiopia. Lett Appl Microbiol 61: 469-476.
   
2. Al-Gaabary MH, Osman SA, Oreiby AF. 2009. Caseous lymphadenitis in sheep and goats: clinical, epidemiological and preventive studies. Small Rumin Res. 87: 116-121.
   
3. Al-Harbi KB. 2011. Prevalence and etiology of abscess disease of sheep and goats at Qassim region, Saudi Arabia. Vet World. 4: 495.
   
4. Alloui MN, Kaba J, Alloui N. 2011. Prevalence and risk factors of caseous lymphadenitis in sheep and goats of Batna area (Algeria). Res Opin Anim Vet Sci 1: 162-164.
5. Almeida S, Dorneles EMS, Diniz C, Abreu V, Sousa C, Alves J, Carneiro A, Bagano P, Spier S, Barh D, Lage AP, Figueiredo H, Azevedo V. 2017. Quadruplex PCR assay for identification of Corynebacterium pseudotuberculosis differentiating biovar Ovis and Equi. BMC Vet Res. 13:290.
   
6. Al-Qudah KM, Al-Majali AM, Obaidat MM. 2008. A study on pathological and microbiological conditions in goats in slaughterhouses in Jordan. Asian J Anim Vet Adv. 3: 269-274.
   
7. Anderson ML, Lean IJ, Blanchard PC. 1990. Corynebacterium pseudotuberculosis associated skin disease of holstein cattle in the San Joaquin Valley, California. Bov Pract 73-75.
8. Arsenault J, Girard C, Dubreuil P, Daignault D, Galarneau J-R, Boisclair J, Simard C, Belanger D. 2003. Prevalence of and carcass condemnation from maedi-visna, paratuberculosis and caseous lymphadenitis in culled sheep from Quebec, Canada. Prev Vet Med. 59: 67-81
   
9. Augustine JL, Renshaw HW. 1986. Survival of Corynebacterium pseudotuberculosis in axenic purulent exudate on common barnyard fomites. Am J Vet Res. 47:713-715.
10. Baird GJ, Fontaine MC. 2007. Corynebacterium pseudotuberculosis and its Role in Ovine Caseous Lymphadenitis. J Comp Pathol 137:179-210.
    
11. Binns SH, Green LE, Bailey M. 2002. Postal survey of ovine caseous lymphadenitis in the United Kingdom between 1990 and 1999. Vet Rec. 150: 263-268.
    
12. Björkroth J, Korkeala H, Funke G. 1999. rRNA gene RFLP as an identification tool for Corynebacterium species. Int J Syst Evol Microbiol 49:983-989.
    
13. Brown C, Olander HJ. 1987. Caseous lymphadenitis of goats and sheep:a review. Vet Bull. 57: 1-12.
14. Çetinkaya B, Karahan M, Atil E, Kalin R, de Baere T, Vaneechoutte M. 2002. Identification of Corynebacterium pseudotuberculosis isolates from sheep and goats by PCR. Vet Microbiol. 88:75-83.
    
15. Chirino-Zárraga C, Scaramelli A, Rey-Valeirón C. 2006. Bacteriological characterization of Corynebacterium pseudotuberculosis in Venezuelan goat flocks. Small Rumin Res. 65:170-175.
    
16. Connor KM, Fontaine MC, Rudge K, Baird G, Donachie W. 2007. Molecular genotyping of multinational ovine and caprine Corynebacterium pseudotuberculosis isolates using pulsed-field gel electrophoresis. Vet Res 38:613-623.
    
17. Connor KM, Quirie MM, Baird G, Donachie W. 2000. Characterization of United Kingdom Isolates ofCorynebacterium pseudotuberculosis Using Pulsed-Field Gel Electrophoresis. J Clin Microbiol 38:2633-2637.
    
18. Costa LRR, Spier SJ, Hirsh DC. 1998. Comparative molecular characterization of Corynebacterium pseudotuberculosis of different origin. Vet Microbiol 62:135-143.
    
19. D’Afonseca V, Prosdocimi F, Dorella FA, Pacheco LGC, Moraes PM, Izabela Pena I, Ortega JM, Teixeira S, Oliveira SC, Coser EM, Oliveira LM, de Oliveira GC, Meyer R, Miyoshi A, Vasco Azevedo V. 2010. Survey of genome organization and gene content of Corynebacterium pseudotuberculosis. Microbiol Res 165:312-320.
    
20. da Costa Barnabé NN, Alves JRA, de Farias AEM, Alves FSF, Faccioli-Martins PY, Pinheiro RR, de Azevedo SS, Alves CJ. 2020. Assessment of caseous lymphadenitis in goats in a slaughterhouse in the Brazilian semi-arid region and estimates of economic losses due to carcass condemnation. Semin Ciências Agrárias. 41: 2655-2668.
    
21. de la Fuente R, de las Heras M, Torrijos C, de Tejada PD, Perez-Sancho M, Carrion FC, Order JA, Dominguez- Bernal G. 2017. Isolation frequency of bacteria causing lymphadenitis and abscesses in small ruminants in central Spain. Small Rumin Res. 154:5-8.
    
22. de Pinho RB, de Oliveira Silva MT, Bezerra FSB, Borsuk S. 2021. Vaccines for caseous lymphadenitis: up-to-date and forward-looking strategies. Appl Microbiol Biotechnol. 105: 2287-2296.
    
23. de Sá Guimarães A, do Carmo FB, Pauletti RB, Seyffert N, Ribeiro D, Lage AP, Heinemann MB, Miyoshi A, Azevedo V, Gouveira AMG. 2011. Caseous lymphadenitis: Epidemiology, diagnosis, and control. IIOAB J 2: 33-43.
24. Dercksen DP, Brinkhof JMA, Dekker-Nooren T, van Maanen K, Bode CF, Baird G, Kamp EM. 2000. A comparison of four serological tests for the diagnosis of caseous lymphadenitis in sheep and goats. Vet Microbiol 75:167- 175.
    
25. Dorella FA, Pacheco LGC, Oliveira SC, Miyoshi A, Axevedo V. 2006. Corynebacterium pseudotuberculosis: microbiology, biochemical properties, pathogenesis and molecular studies of virulence. Vet Res 37:201-218.
    
26. Foley JE, Spier SJ, Mihalyi J, Drazenovich N, Leutenegger CM. 2004. Molecular epidemiologic features of Corynebacterium pseudotuberculosis isolated from horses. Am J Vet Res 65:1734-1737.
    
27. Fontaine MC, Baird GJ. 2008. Caseous lymphadenitis. Small Rumin Res 76:42-48.
    
28. Goldberger AC, Lipsky BA, Plorde JJ. 1981. Suppurative Granulomatous Lymphadenitis Caused by Corynebacterlum ovis (Pseudotuberculosis). Am J Clin Pathol 76:486-490.
    
29. Gonçalves JL, Tomazi T, Barreiro JR, de Campos Braga PA, Ferreira CR, Junior JPA, Eberlin MN, dos Santod MV. 2014. Identification of Corynebacterium spp. isolated from bovine intramammary infections by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Vet Microbiol 173:147-151.
    
30. Guerrero J, Oca-Jiménez R, Dibarrat J, Leon F, Morales-Erasto V, Salazar H. 2018. Isolation and molecular characterization of Corynebacterium pseudotuberculosis from sheep and goats in Mexico. Microb Pathog 117:304-309.
    
31. Gyles CL, Prescott JF, Songer JG, Thoen CO. 2008. Pathogenesis of bacterial infections in animals. John Wiley & Sons.
32. Hodgson AL, Tachedjian M, Corner LA, Radford AJ. 1994. Protection of sheep against caseous lymphadenitis by use of a single oral dose of live recombinant Corynebacterium pseudotuberculosis. Infect Immun 62:5275-5280.
    
33. Hodgson ALM, Carter K, Tachedjian M, Krywult J, Corner LA, McColl M, Cameron A. 1999. Efficacy of an ovine caseous lymphadenitis vaccine formulated using a genetically inactive form of the Corynebacterium pseudotuberculosis phospholipase D. Vaccine 17:802-808.
    
34. House RW, Schousboe M, Allen JP, Grant CC. 1986. Corynebacterium ovis (pseudo-tuberculosis) lymphadenitis in a sheep farmer: a new occupational disease in New Zealand. N Z Med J 99:659-662.
35. Jones D. 1986. Irregular, nonsporing Gram-positive rods. Bergey’s Man Syst Bacteriol 1261-1282.
36. Jung BY, Lee SH, Kim HY, Byun JW, Shin DH, Kim D, Kwak D. 2015. Serology and clinical relevance of Corynebacterium pseudotuberculosis in native Korean goats (Capra hircus coreanae). Trop Anim Health Prod 47:657-661.
    
37. Khamis A, Raoult D, La Scola B. 2004. rpoB Gene Sequencing for Identification of Corynebacterium Species. J Clin Microbiol 42:3925-3931.
    
38. Kong JY, Lee K, Jung JY, Kim JW, Yoon NS, So BJ, Choi EJ. 2019. Clinical case of internal caseous lymphadenitis in a native Korean goat (Capra hircus coreanae). J Prev Vet Med 43:58-61.
    
39. Kumar J, Singh F, Tripathi BN, Kumar R, Dixit SK, Sonawane GG. 2012. Epidemiological, bacteriological and molecular studies on caseous lymphadenitis in Sirohi goats of Rajasthan, India. Trop Anim Health Prod 44:1319-1322.
    
40. Kumaresan G, Singh DD, Pawaiya R, Andani D, Gangwar NK, Mishra AK, Chaturvedi V, Kumar A. 2018. Investigation of an outbreak of caseous lymphadenitis in goats. Indian J Small Ruminants 24: 95-100.
    
41. Li H, Yang H, Zhou Z, Li X, Yi W, Xu Y, Wang Z, Hu S. 2018. Isolation, antibiotic resistance, virulence traits and phylogenetic analysis of Corynebacterium pseudotuberculosis from goats in southwestern China. Small Rumin Res 168:69-75.
    
42. Lopes Bastos B, Dias portela RW, Dorella FA, Rebeiro D, Seyeffert N, de Paula Castro TL, Miyoshi A, oliveira SC, Meyer R, Azevedo V. 2012. Corynebacterium pseudotuberculosis: Immunological Responses in Animal Models and Zoonotic Potential. J Clin Cell Immunol, S4.
    
43. Menzies P., Hwang YT, Prescott J. 2004. Comparison of an interferon-g to a phospholipase D enzyme-linked immunosorbent assay for diagnosis of Corynebacterium pseudotuberculosis infection in experimentally infected goats. Vet Microbiol 100:129-137.
    
44. Middleton MJ, Epstein VM, Gregory GG. 1991. Caseous lymphadenitis on Flinders Island: prevalence and management surveys. Aust Vet J 68:311-312.
    
45. Miers KC, Ley WB. 1980. Corynebacterium pseudotuberculosis infection in the horse: study of 117 clinical cases and consideration of etiopathogenesis. J Am Vet Med Assoc 177:250-253.
46. Min TG, Kong KO, Song HB. 1999. The marketing of the goat in Korea. College of Natural Resources, Taegu University, South Korea.
47. Minozzi G, Mattiello S, Grosso L, Crepaldi P, Chessa S, Pagnacco G. 2017. First insights in the genetics of caseous lymphadenitis in goats. Ital J Anim Sci 16: 31-38.
    
48. Nozaki CN, Faria MAR, Machado TMM.2000. Surgical extirpation of abscesses of caseous lymphadenitis in goats. Arq Inst Biol 67:187-189.
49. Olson ME, Ceri H, Morck DW, Buret AG, Read RR. 2002. Biofilm bacteria: formation and comparative susceptibility to antibiotics. Can J Vet Res 66:86-92.
50. Osman AY, Abdullah F, Saharee AA. 2012. Sero-Prevalence of Caseous Lymphadenitis Evaluated by Agar Gel Precipitation Test among Small Ruminant Flocks in East Coast Economic Regions in Peninsular Malaysia. J Anim Vet Adv 11: 3474-3480.
    
51. Pacheco LGC, Pena RR, Castro TLP, Dorella FA, Bahia RC, Carminati R, Frota MNL, Oliveira SC, meyer R, Alves FSF, Miyoshi A, Azevedo V. 2007. Multiplex PCR assay for identification of Corynebacterium pseudotuberculosis from pure cultures and for rapid detection of this pathogen in clinical samples. J Med Microbiol 56:480- 486.
    
52. Paton MW, Walker SB, Rose IR, Watt GF. 2003. Prevalence of caseous lymphadenitis and usage of caseous lymphadenitis vaccines in sheep flocks. Aust Vet J 81:91-95.
    
53. Pavan ME, Robles C, Cairo FM, Marcellino R, Petttinari MJ. 2012. Identification of Corynebacterium pseudotuberculosis from sheep by PCR-restriction analysis using the RNA polymerase b-subunit gene (rpoB). Res Vet Sci 92:202-206.
    
54. Peel MM, Palmer GG, Stacpoole AM, Kerr TG 1997. Human lymphadenitis due to Corynebacterium pseudotuberculosis: report of ten cases from Australia and review. Clin Infect Dis 24:185-191.
    
55. Pekelder JJ. 2003. Caseous lymphadenitis. In: Martin, W.B.; Aitken, I.D. Diseases of Sheep. 3rd edn, Blackwell Science, Oxford.
56. Piontkowski MD, Shivvers DW. 1998. Evaluation of a commercially available vaccine against Corynebacterium pseudotuberculosis for use in sheep. J Am Vet Med Assoc 212: 1765-1768.
57. Poonacha KB, Donahue JM. 1995. Abortion in a mare associated with Coryrtebacterium pseudotuberculosis infection. J Vet Diagnostic Investig 7:563-564.
    
58. Pugh DG, Baird NN. 2012. Sheep & Goat Medicine-E-Book. Elsevier Health Sciences.
59. Pulina G, Milán MJ, Lavín MP, Theodoridis A, Morin E, Capote J, Thomas DL, Francesconi AHD, Caja G. 2018. Invited review: Current production trends, farm structures, and economics of the dairy sheep and goat sectors. J Dairy Sci. 101: 6715-6729.
    
60. Radostits OM, Gay CC, Blood DC, Hinchcliff, Kenneth W, McKenzie RA. 2002. Veterinary Clinic: a treatise on diseases of cattle, sheep pigs, goats and horses, 9th ed. Guanabara Koogan, Rio de Janeiro.
61. Rizvi S, Green LE, Glover MJ. 1997. Caseous lymphadenitis: an increasing cause for concern. Vet Rec. 140: 586-7.
62. Sá M da CA de, Gouveia GV, Krewer C da C, Veschi JLA, Mattos-Guaraldi AL de, Costa MM da. 2013. Distribution of PLD and FagA, B, C and D genes in Corynebacterium pseudotuberculosis isolates from sheep and goats with caseus lymphadenitis. Genet Mol Biol. 36: 265-268.
    
63. Selim SA. 2001. Oedematous skin disease of buffalo in Egypt. J Vet Med Ser B. 48: 241-258.
    
64. Seyffert N, Guimarães AS, Pacheco LGC, Portela RW, Bastos BL, Dorella FA, Heinemann MB, Lage AP, Gouveia AMG, Meyer R, Miyoshi A, Azeveda V. 2010. High seroprevalence of caseous lymphadenitis in Brazilian goat herds revealed by Corynebacterium pseudotuberculosis secreted proteins-based ELISA. Res Vet Sci 88: 50-55.
    
65. Shin DH, Song YK, Byun JW, Kim HY, Kim HS, Woo GH, Lee OS, Jung BY. 2010. Caseous lymphadenitis by Corynebacterium pseudotuberculosis in a Saanen dairy goat (Capra hircus aegagrus). Korean J Vet Res. 50:25-28.
66. Shpigel NY, Elad D, Yeruham I, Winkler M, Saran A. 1993. An outbreak of Corynebacterium pseudotuberculosis infection in an Israeli dairy herd. Vet Rec. 133:89-94.
    
67. Skalka B, Literrak I, Michalik I, Skrivanek M. 1998. Corynebacterium pseudotuberculosis Infection in Goats in the Czech Republic. J Vet hied B 45: 31-35.
    
68. Smith MC, Sherman DM. 2009. Goat Medicine, 2nd Edition. Wiley-Black, Ames, Iowa.
    
69. Solaiman SG. 2010. Goat science and production, pp 221. John Wiley & Sons.
70. Stanford K, Brogden KA, McClelland LA, Kozub GC, Audibert F. 1998. The incidence of caseous lymphadenitis in Alberta sheep and assessment of impact by vaccination with commercial and experimental vaccines. Can J Vet Res. 62:38-43.
71. Stefańska I, Rzewuska M, Binek M. 2008. Evaluation of three methods for DNA fingerprinting of Corynebacterium pseudotuberculosis strains isolated from goats in Poland. Pol J Microbiol. 57:105-112.
72. Steinman A, Elad D, Shpigel NY. 1999. Ulcerative lymphangitis and coronet lesions in an Israeli dairy herd infected with Corynebacterium pseudotuberculosis. Vet. Rec. 145: 604- 606.
    
73. Thongkwow S, Poosiripinyo N, Pongkornkumpon N, Saengsakchai S, Klinkhiew N, Chalatan T, Kanistanon K, Lerk-u-suke S, Rerkyusuke S. 2019. Distribution and risk factors of clinical caseous lymphadenitis in small-holder goat herds in Northeastern Thailand. Thai J Vet Med 49: 343-351.
74. Tripathi BN, Kumar J, Sonawane GG, Kumar Rajiv, Dixit Sk. 2016. Microbiological and Molecular Investigation of Clinically Suspected Caseous Lymphadenitis Cases in Goats. Agric Res. 5:413-419.
    
75. Wan-Choul K, Hyoung-seok Y, Ko JA, Lee S, Lee DS, Son WG. 2015. Prevalence of Johne’s disease of Korean native cattle in Jeju Province, Korea. 38: 221-225.
    
76. Williamson LH. 2001. Caseous Lymphadenitis in Small Ruminants. Vet Clin North Am Food Anim Pract. 17: 359-371.
    
77. Yeruham I, Braverman Y, Shpigel NY, Chizov-Ginzbury A, Saran A, Winkler M. 1996. Mastitis in dairy cattle caused by Corynebacterium pseudotuberculosis and the feasibility of transmission by houseflies I. Vet Q. 18: 87-89.
    
78. Yeruham I, Elad D, Van-Ham M, Shipigel NY Perl S. 1997. Corynebacterium pseudotuberculosis infection in Israeli cattle: clinical and epidemiological studies. Vet Rec. 140: 423-427.
    
79. Yitagesu E, Alemnew E, Olani A, Asfaw T, Demis C. 2020. Survival Analysis of Clinical Cases of Caseous Lymphadenitis of Goats in North Shoa, Ethiopia. Vet Med Int 2020.
    
80. Zeru F, Kahsay AG. 2014. Caseous lymphadenitis in goats from Borena range Land South Ethiopia slaughtered at luna export abattoir. J Vet Med Anim Heal. 6: 168-173.