Causative agents and epidemiology of diarrhea in Korean native calves

Sung-Hwan Lee; Ha-Young Kim; Eun Wha Choi; Doo Kim

doi:10.4142/jvs.2019.20.e64

Journal List > J Vet Sci > v.20(6) > 1148336

Go to TopGo to Top Go to BottomGo to Bottom

TOOLS

Lee, Kim, Choi, and Kim: Causative agents and epidemiology of diarrhea in Korean native calves

Original Article Internal Medicine

J Vet Sci 2019;20(6):e64.

Published online: 4 November 2019

DOI: https://doi.org/10.4142/jvs.2019.20.e64

Causative agents and epidemiology of diarrhea in Korean native calves

Sung-Hwan Lee¹, Ha-Young Kim², Eun Wha Choi³, Doo Kim^1,^*

¹Laboratory of Large Animal Medicine, College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University, Chuncheon 24341, Korea

²Animal Disease Diagnostic Division, Animal and Plant Quarantine Agency, Gimcheon 39660, Korea

³Department of Veterinary Clinical Pathology, College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University, Chuncheon 24341, Korea

^*Corresponding authors: Eun Wha Choi Department of Veterinary Clinical Pathology, College of Veterinary Medicine & Institute of Veterinary Science, Kangwon National University, 1 Kangwondaehak-gil, Chuncheon 24341, Korea. E-mail: ewchoi@kangwon.ac.kr

Received 5 July 2019 Revised 3 September 2019 Accepted 15 September 2019

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Calf diarrhea caused by infectious agents is associated with economic losses in the cattle industry. The purpose of this study was to identify the causative agents and epidemiological characteristics of diarrhea in Korean native calves (KNC). In total, 207 diarrheal KNC aged less than 7 months were investigated. Fecal samples collected from the rectum were examined for causative agents using polymerase chain reaction (PCR) or real-time PCR and the number of oocysts were counted. Fourteen causative agents were detected from 164 of the 207 diarrheal KNC. Rotavirus was the most common agent (34.8%), followed by Eimeria spp. (31.7%), Escherichia coli (22.0%), Giardia spp. (14.0%), Clostridium difficile (9.8%), bovine viral diarrhea virus (8.5%), coronavirus (7.9%), Cryptosporidium spp. (7.3%), torovirus (6.7%), parvovirus (5.5%), norovirus (4.9%), kobuvirus (1.8%), adenovirus (1.2%), and Salmonella spp. (0.6%). About 95 (57.9%) of 164 calves were infected with a single causative agent and 42.1% were infected by multiple agents. No significant difference was observed in mortality between calves infected with a single agent and multiple agents. The occurrence of diarrhea caused by rotavirus, Eimeria spp., kobuvirus, and Giardia spp. was significantly different based on onset age, and the prevalence of diarrhea caused by rotavirus or C. difficile was significantly different between seasons. This study help the understanding of KNC diarrhea for the development of an effective strategy for disease prevention and control, especially in Eastern provinces of South Korea.

Keywords: Diarrhea, calf, Korean native calves, causative agents, prevalence

References

1. Izzo MM, Kirkland PD, Mohler VL, Perkins NR, Gunn AA, House JK. Prevalence of major enteric pathogens in Australian dairy calves with diarrhoea. Aust Vet J. 2011; 89:167–173.

2. Hur TY, Jung YH, Choe CY, Cho YI, Kang SJ, Lee HJ, Ki KS, Baek KS, Suh GH. The dairy calf mortality: the causes of calf death during ten years at a large dairy farm in Korea. Korean J Vet Res. 2013; 53:103–108.

3. Kim D, Han HR. A quantitative study of the transfer of colostral immunoglobulins to the newborn Korean native calf. Korean J Vet Res. 1990; 29:75–81.

4. Kim D, Han HR. Changes in the serum immunoglobulin levels and viral antibody titers of colostrum – conferred Korean native calves during the first 12 weeks postpartum. Korean J Vet Res. 1990; 29:83–90.

5. Crouch CF, Oliver S, Francis MJ. Serological, colostral and milk responses of cows vaccinated with a single dose of a combined vaccine against rotavirus, coronavirus and Escherichia coli F5 (K99). Vet Rec. 2001; 149:105–108.

6. Bendali F, Bichet H, Schelcher F, Sanaa M. Pattern of diarrhoea in newborn beef calves in southwest France. Vet Res. 1999; 30:61–74.

7. Kirisawa R, Takeyama A, Koiwa M, Iwai H. Detection of bovine torovirus in fecal specimens of calves with diarrhea in Japan. J Vet Med Sci. 2007; 69:471–476.

8. Park SI, Jeong C, Kim HH, Park SH, Park SJ, Hyun BH, Yang DK, Kim SK, Kang MI, Cho KO. Molecular epidemiology of bovine noroviruses in South Korea. Vet Microbiol. 2007; 124:125–133.

9. Mauroy A, Scipioni A, Mathijs E, Saegerman C, Mast J, Bridger JC, Ziant D, Thys C, Thiry E. Epidemiological study of bovine norovirus infection by RT-PCR and a VLP-based antibody ELISA. Vet Microbiol. 2009; 137:243–251.

10. Jeoung HY, Lim JA, Jeong W, Oem JK, An DJ. Three clusters of bovine kobuvirus isolated in Korea, 2008–2010. Virus Genes. 2011; 42:402–406.

11. Gülaçtı I, Işıdan H, Sözdutmaz I. Detection of bovine torovirus in fecal specimens from calves with diarrhea in Turkey. Arch Virol. 2014; 159:1623–1627.

12. Kailasan S, Halder S, Gurda B, Bladek H, Chipman PR, McKenna R, Brown K, Agbandje-McKenna M. Structure of an enteric pathogen, bovine parvovirus. J Virol. 2015; 89:2603–2614.

13. Peter SG, Gitau GK, Richards S, Vanleeuwen JA, Uehlinger F, Mulei CM, Kibet RR. Risk factors associated with Cryptosporidia, Eimeria, and diarrhea in smallholder dairy farms in Mukurwe-ini Sub-County, Nyeri County, Kenya. Vet World. 2016; 9:811–819.

14. Rodriguez-Palacios A, Stämpfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, Brazier JS, Weese JS. Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis. 2006; 12:1730–1736.

15. Berge AC, Besser TE, Moore DA, Sischo WM. Evaluation of the effects of oral colostrum supplementation during the first fourteen days on the health and performance of preweaned calves. J Dairy Sci. 2009; 92:286–295.

16. Hensgens MP, Keessen EC, Squire MM, Riley TV, Koene MG, de Boer E, Lipman LJ, Kuijper EJ; European Society of Clinical Microbiology and Infectious Diseases Study Group for Clostridium difficile (ESGCD). Clostridium difficile infection in the community: a zoonotic disease? Clin Microbiol Infect. 2012; 18:635–645.

17. Lyoo YS. Detection of Torovirus-like particles from calves with diarrhea. Korean J Vet Res. 1997; 37:155–159.

18. Gül A, Ciçek M, Kilinç O. Prevalence of Eimeria spp., Cryptosporidium spp. and Giardia spp. in calves in the Van province. Turkiye Parazitol Derg. 2008; 32:202–204.

19. Heo JH, Cho MH, Lee KC, Park MN, Cho EJ, Choi MS, Kim CH, Kang JB, Kim EK, Kim JS. An epidemiological study on the calves with clinical diarrhea in southern Gyeonnam. Korean J Vet Serv. 2008; 31:305–313.

20. Koutny H, Joachim A, Tichy A, Baumgartner W. Bovine Eimeria species in Austria. Parasitol Res. 2012; 110:1893–1901.

21. Gillhuber J, Rügamer D, Pfister K, Scheuerle MC. Giardiosis and other enteropathogenic infections: a study on diarrhoeic calves in Southern Germany. BMC Res Notes. 2014; 7:112.

22. Jeong MH, Lee MK, Kim HS, Lee SU, Seong MH, Park DY, Hwang BW, Park HJ, Cho JH. Detection of etiologic agents in diarrhea fecal samples from calves in Gyeongnam province, Korea. Korean J Vet Serv. 2012; 35:339–342.

23. Sibley SD, Goldberg TL, Pedersen JA. Detection of known and novel adenoviruses in cattle wastes via broad-spectrum primers. Appl Environ Microbiol. 2011; 77:5001–5008.

24. Yamashita T, Ito M, Kabashima Y, Tsuzuki H, Fujiura A, Sakae K. Isolation and characterization of a new species of kobuvirus associated with cattle. J Gen Virol. 2003; 84:3069–3077.

25. Park SJ, Oh EH, Park SI, Kim HH, Jeong YJ, Lim GK, Hyun BH, Cho KO. Molecular epidemiology of bovine toroviruses circulating in South Korea. Vet Microbiol. 2008; 126:364–371.

26. Franck SM, Bosworth BT, Moon HW. Multiplex PCR for enterotoxigenic, attaching and effacing, and Shiga toxin-producing Escherichia coli strains from calves. J Clin Microbiol. 1998; 36:1795–1797.

27. Arnold T, Scholz HC, Marg H, Rösler U, Hensel A. Impact of invA-PCR and culture detection methods on occurrence and survival of salmonella in the flesh, internal organs and lymphoid tissues of experimentally infected pigs. Vet Med B Infect Dis Vet Public Health. 2004; 51:459–463.

28. Shabana II, Zaraket H, Suzuki H. Molecular studies on diarrhea-associated Escherichia coli isolated from humans and animals in Egypt. Vet Microbiol. 2013; 167:532–539.

29. Cortés C, De la Fuente R, Blanco J, Blanco M, Blanco JE, Dhabi G, Mora A, Justel P, Contreras A, Sánchez A, Corrales JC, Orden JA. Serotypes, virulence genes and intimin types of verotoxin-producing Escherichia coli and enteropathogenic E. coli isolated from healthy dairy goats in Spain. Vet Microbiol. 2005; 110:67–76.

30. Kato H, Kato N, Watanabe K, Iwai N, Nakamura H, Yamamoto T, Suzuki K, Kim SM, Chong Y, Wasito EB. Identification of toxin A-negative, toxin B-positive Clostridium difficile by PCR. J Clin Microbiol. 1998; 36:2178–2182.

31. Section 1. Diagnostic parasitology. Foreyt WJ, editor. (ed.).Veterinary Parasitology Reference Manual. 5th ed.pp.p. 3–10. Blackwell Publishing;Ames: 2013.

32. Lee SH, VanBik D, Kim HY, Lee YR, Kim JW, Chae M, Oh SI, Goo YK, Kwon OD, Kwak D. Multilocus typing of Cryptosporidium spp. in young calves with diarrhea in Korea. Vet Parasitol. 2016; 229:81–89.

33. Lee SH, VanBik D, Kim HY, Cho A, Kim JW, Byun JW, Oem JK, Oh SI, Kwak D. Prevalence and molecular characterisation of Giardia duodenalis in calves with diarrhoea. Vet Rec. 2016; 178:633.

34. Lee BS. A study of natural seasons in Korea. J Korean Geogr Soc. 1979; 14:1–11.

35. Gebeyehu EB, Seon MG, Jung BY, Byun JW, Oem JK, Kim HY, Kwak D. Prevalence of gastrointestinal parasites in Korean native goats (Capra hircus aegarus). J Anim Plant Sci. 2013; 23:986–989.

36. Björkman C, Svensson C, Christensson B, de Verdier K. Cryptosporidium parvum and Giardia intestinalis in calf diarrhoea in Sweden. Acta Vet Scand. 2003; 44:145–152.

37. Brandão PE, Villarreal LY, de Souza SL, Richtzenhain LJ, Jerez JA. Mixed infections by bovine coronavirus, rotavirus and Cryptosporidium parvum in an outbreak of neonatal diarrhea in beef cattle. Arq Inst Biol (Sao Paulo). 2007; 74:33–34.

38. Barry AF, Alfieri AF, Stipp DT, Alfieri AA. Bovine coronavirus detection in a collection of diarrheic stool samples positive for group A bovine rotavirus. Braz Arch Biol Technol. 2009; 52:45–49.

39. Enemark HL, Dahl J, Enemark JM. Eimeriosis in Danish dairy calves–correlation between species, oocyst excretion and diarrhoea. Parasitol Res. 2013; 112(Suppl 1):169–176.

40. Cho YI, Yoon KJ. An overview of calf diarrhea – infectious etiology, diagnosis, and intervention. J Vet Sci. 2014; 15:1–17.

Table 1.

Prevalence of calves infected with a single causative agent (n = 95) among diarrheal Korean native calves (n = 164)

Causative agents	No. of calves	Prevalence (%)
Virus
Rotavirus	28	17.1
Coronavirus	5	3.0
Parvovirus	5	3.0
BVDV	3	1.8
Norovirus	3	1.8
Torovirus	3	1.8
Kobuvirus	1	0.6
Subtotal	48	29.1
Bacteria
E. coli	13	7.9
C. difficile	4	2.4
Salmonella spp.	1	0.6
Subtotal	18	10.9
Protozoa
Eimeria spp.	20	12.2
Giardia spp.	8	4.9
Cryptosporidium spp.	1	0.6
Subtotal	29	17.7
Total	95	57.9

BVDV, bovine viral diarrhea virus.

Table 2.

Prevalence of calves infected with mixed causative agents (n = 69) among diarrheal Korean native calves (n = 164)

Mixed form	No.	Causative agents	Prevalence (%)
Double	7	E. coli, Eimeria spp.
	6	Rotavirus, coronavirus
	5	Rotavirus, E. coli
	5	Rotavirus, C. difficile
	3	Rotavirus, Eimeria spp.
	3	Rotavirus, Giardia spp.
	3	Eimeria spp., Giardia spp.
	2	Rotavirus, BVDV
	2	Coronavirus, Eimeria spp.
	2	Norovirus, E. coli
	2	Torovirus, E. coli
	2	Eimeria spp., Cryptosporidium spp.
	1	Rotavirus, parvovirus
	1	Rotavirus, norovirus
	1	BVDV, C. difficile
	1	BVDV, Eimeria spp.
	1	Parvovirus, norovirus
	1	Parvovirus, torovirus
	1	Parvovirus, Eimeria spp.
	1	Kobuvirus, Eimeria spp.
	1	Kobuvirus, Giardia spp.
	1	Torovirus, Eimeria spp.
	1	C. difficile, Giardia spp.
Subtotal	53		32.3
Triple	2	BVDV, Eimeria spp., Cryptosporidium spp.
	1	BVDV, adenovirus, Eimeria spp.
	1	BVDV, E. coli, C. difficile
	1	Rotavirus, torovirus, E. coli
	1	Rotavirus, E. coli, C. difficile
	1	Adenovirus, torovirus, Eimeria spp.
	1	Torovirus, E. coli, C. difficile
	1	Eimeria spp., Cryptosporidium spp., Giardia spp.
Subtotal	9		5.5
Quadruple	3	BVDV, Eimeria spp, Cryptosporidium spp., Giardia spp.
	1	Rotavirus, torovirus, E coli, Cryptosporidium spp.
	1	E. coli, C. difficile, Eimeria spp., Giardia spp.
	1	C. difficile, Eimeria spp., Cryptosporidium spp., Giardia spp.
Subtotal	6		3.7
Quintuple	1	Norovirus, E. coli, Eimeria spp., Cryptosporidium spp., Giardia spp.
Subtotal	1		0.6
Total	69		42.1

BVDV, bovine viral diarrhea virus.

Table 3.

Prevalence of calves infected with a single or multiple causative agents (n = 257) among diarrheal Korean native calves (n = 164)

Causative agents	No. of tested causative agents	No. of calves with single agent	No. of calves with mixed agents
Virus
Rotavirus	57	28	29
BVDV	14	3	11
Coronavirus	13	5	8
Torovirus	11	3	8
Parvovirus	9	5	4
Norovirus	8	3	5
Kobuvirus	3	1	2
Adenovirus	2	0	2
Subtotal (%)	117 (45.5)	48 (18.7)	69 (26.8)
Bacteria
E. coli	36	13	23
C. difficile	16	4	12
Salmonella spp.	1	1	0
Subtotal (%)	53 (20.6)	18 (7.0)	35 (13.6)
Protozoa
Eimeria spp.	52	20	32
Giardia spp.	23	8	15
Cryptosporidium spp.	12	1	11
Subtotal (%)	87 (33.9)	29 (11.3)	58 (22.6)
Total (%)	257 (100.0)	95(37.0)	162 (63.0)

BVDV, bovine viral diarrhea virus.

Table 4.

Distribution of major causative agents according to onset age of diarrhea

Onset age	Rota	Corona	BVDV	Adeno	Parvo	Kobu	Noro	Toro	E. coli	Salmonella	C. difficile	Eimeria	Cryptosporidium	Giardia
< 1 weeks	22	4	3	0	1	0	4	4	10	1	4	0	1	0
(n = 38)	38.6%	30.8%	21.4%	0.0%	11.1%	0.0%	50.0%	36.4%	27.8%	100.0%	25.0%	0.0%	8.3%	0.0%
1–2 weeks	17	3	1	0	1	1	2	2	7	0	3	0	1	2
(n = 26)	29.8%	23.1%	7.1%	0.0%	11.1%	33.3%	25.0%	18.2%	19.4%	0.0%	18.8%	0.0%	8.3%	8.7%
3–4 weeks	8	1	5	1	4	0	0	0	6	0	5	12	4	5
(n = 30)	14.0%	7.7%	35.7%	50.0%	44.4%	0.0%	0.0%	0.0%	16.7%	0.0%	31.3%	23.1%	33.3%	21.7%
5–6 weeks	7	1	2	1	1	0	2	2	5	0	2	19	4	7
(n = 30)	12.3%	7.7%	14.3%	50.0%	11.1%	0.0%	25.0%	18.2%	13.9%	0.0%	12.5%	36.5%	33.3%	30.4%
7–8 weeks	3	1	2	0	0	0	0	0	1	0	2	5	2	6
(n = 14)	5.3%	7.7%	14.3%	0.0%	0.0%	0.0%	0.0%	0.0%	2.8%	0.0%	12.5%	9.6%	16.7%	26.1%
9–10 weeks	0	1	0	0	0	2	0	1	4	0	0	7	0	3
(n = 12)	0.0%	7.7%	0.0%	0.0%	0.0%	66.7%	0.0%	9.1%	11.1%	0.0%	0.0%	13.5%	0.0%	13.0%
11–12 weeks	0	0	0	0	0	0	0	0	1	0	0	3	0	0
(n = 3)	0.0%	0.0%	0.0%	0.0%	0.0%	0.0%	0.0%	0.0%	2.8%	0.0%	0.0%	5.8%	0.0%	0.0%
≥ 13 weeks	0	2	1	0	2	0	0	2	2	0	0	6	0	0
(n = 11)	0.0%	15.4%	7.1%	0.0%	22.2%	0.0%	0.0%	18.2%	5.6%	0.0%	0.0%	11.5%	0.0%	0.0%
Total	57	13	14	2	9	3	8	11	36	1	16	52	12	23
(n = 164)	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%	100.0%
Pearson's χ², p	< 0.001	0.732	0.608	0.834	0.208	0.014	0.444	0.464	0.736	0.852	0.634	< 0.001	0.337	0.002
Linear by linear association	< 0.001	0.963	0.887	0.922	0.422	0.261	0.052	0.873	0.519	0.244	0.164	< 0.001	0.920	0.050
Onset age (mean ± standard deviation, days)	4	44.0 ± 62.7	30.1 ± 31.6	5	58.4 ± 78.2		13.4 ± 11.9	48.9 ± 67.8	33.1 ± 45.3		20.1 ± 15.0 5	57.0 ± 49.7	28.3 ± 13.1	38.1 ± 15.0
Onset age (range, days)		2–180	3–129		7–210		3–34	3–180	3–210		3–55	20–210	7–52	10–70
Single infection, onset age (range, days)	3–45	2–180	3–129		16–210		3–12	7–180	5–60		15–55	22–210	7	13–64

BVDV, bovine viral diarrheea virus.

Table 5.

Seasonal distribution of causative agents (n = 257) detected in diarrheal Korean native calves (n = 164)

Causative agents	Spring (Mar–May)	Summer (Jun–Aug)	Fall (Sep–Nov)	Winter (Dec–Feb)	p value
Rotavirus	33 (20.1)	2 (1.2)	6 (3.7)	16 (9.8)	0.017
Coronavirus	5 (3.0)	0 (0.0)	1 (0.6)	7 (4.3)	0.250
BVDV	3 (1.8)	4 (2.4)	0 (0.0)	7 (4.3)	0.061
Adenovirus	1 (0.6)	1 (0.6)	0 (0.0)	0 (0.0)	0.417
Parvovirus	4 (2.4)	1 (0.6)	0 (0.0)	4 (2.4)	0.745
Kobuvirus	0 (0.0)	0 (0.0)	1 (0.6)	2 (1.2)	0.143
Norovirus	1 (0.6)	1 (0.6)	0 (0.0)	6 (3.7)	0.058
Torovirus	5 (3.0)	0 (0.0)	2 (1.2)	4 (2.4)	0.361
E. coli	20 (12.2)	6 (3.7)	3 (1.8)	7 (4.3)	0.310
Salmonella spp.	0 (0.0)	1 (0.6)	0 (0.0)	0 (0.0)	0.090
C. difficile	7 (4.3)	3 (1.8)	5 (3.0)	1 (0.6)	0.001
Eimeria spp.	19 (11.6)	10 (6.1)	4 (2.4)	19 (11.6)	0.270
Cryptosporidium spp.	2 (1.2)	1 (0.6)	1 (0.6)	8 (4.9)	0.059
Giardia spp.	9 (5.5)	2 (1.2)	3 (1.8)	9 (5.5)	0.570
Total	109 (66.5)	32 (16.5)	26 (8.5)	90 (54.9)

Values are presented as number of patients (%). The χ² test was used to analyse the differences in the prevalence of diarrhea caused by each causative agent across seasons.

BVDV, bovine viral diarrhea virus.

TOOLS

Similar articles