Korean Journal of
Veterinary Service

Tuberculosis in mammals, caused by the Mycobacterium tuberculosis complex (MTBC), is a chronic bacterial disease affecting both animals and humans. This complex includes notable variants such as M. bovis, M. caprae, and M. tuberculosis. It significantly impacts cattle, various domesticated animals, and some wildlife, with zoonotic tuberculosis posing a notable public health concern due to human transmission (Cho et al, 2022; WOAH, 2022). Although, M. tuberculosis is predominantly associated with human TB globally, M. bovis is now a leading cause of zoonotic TB. In 2019, there were an estimated 140,000 new cases of zoonotic TB worldwide, with about 11,000 fatalities (WHO, 2020). Consequently, livestock tuberculosis is managed under the Act on the Prevention of Contagious Animal Diseases in Korea as a type II contagious animal disease. In Europe, it’s categorized as class B, while organizations like OIE (2022) and FAO (2022) list it under category B, and in Korea, it’s a class II legal infectious disease.

In Korea, bovine tuberculosis (BTB) was first officially reported in 1913. This study investigates the prevalence trend in Korean dairy cattle from 1961 to 2004, during which over 8.96 million dairy cows were tested, identifying 10,248 BTB cases. Despite a test-and-slaughter eradication policy initiated in 1964, BTB persists in Korean cattle and deer. This contrasts with nearly complete BTB eradication in the United States and Canada, thanks to effective long-term programs (Essey and Koller, 1994; Munroe et al, 2000; Suruiballi et al, 2002; O’Brien et al, 2023). Australia, too, successfully eradicated BTB based on a sound technical program with strong industrial and governmental support during a brucellosis and tuberculosis eradication campaign lasting more than 25 years (Radunz, 2006). Japan had been reported continuously since 1937, and saw a decline in BTB cases from 1962. Finally, the last outbreak was reported in Hyogo Prefecture in December 2014. In addition, there has been no evidence of infection with complex in wildlife in Japan. The WOAH Delegate of Japan declares that the country is free from infection with MTBC in bovids as of 1 April 2021 in compliance with the provisions of Article 8.11.4. of the Terrestrial Code (WOAH, 2022).

This study aims to analyze the epidemiological features of tuberculosis in Korean livestock from 2013 to 2022, providing insights into the effectiveness of tuberculosis prevention and eradication measures in Korea.

Data collection on livestock tuberculosis incidence

This study gathered data on tuberculosis occurrences in various animals, including different cattle breeds (dairy, beef, and Korean native cattle), deer, and elk. The data, spanning from 2013 to 2022, was confirmed by the Animal and Plant Quarantine Agency and recorded in the Korea Animal Health Integrated System (KAHIS, 2023). Additionally, to ensure accuracy, the KAHIS records were cross-validated with test results from provincial animal health laboratories.

Analysis of tuberculosis incidence data in livestock

For this analysis, farms were only considered if tuberculosis was identified there for the first time. The study included all repeat instances for calculating the number of infected animals. Data on the number of infected farms and individuals per farm were compiled annually and categorized by outbreak type. The yearly incidence rates for infected farms and individuals were also determined. The frequency of additional outbreaks was noted each time a positive test result was found on a newly affected farm, continuing until the disease was eradicated, as evidenced by negative test results upon retesting.

Statistical analysis

GraphPad Prism version 9.3.1 was employed for all statistical analyses. The significance of the findings was determined using Chi-square analysis, with a P-value of less than 0.05 indicating statistical significant.

Between 2013 and 2022, tuberculosis cases in cattle and deer reached a high of 4,109 across 858 farms in 2019, then showed a decline to 1,869 cases in 431 farms by 2022 (Fig. 1, Table 1). The latest data from 2022 indicates 1,896 TB cases in livestock, spread across 431 herds. This includes 413 cattle herds (95.8%) with 1,741 cattle (91.8%) and 18 deer herds (4.2%) with 155 deer (8.2%) (Table 2, Fig. 2). Specifically, Korean native cattle represented a significant portion with 361 herds (87.4%) and 1,447 animals (83.1%), dairy cattle comprised 40 herds (9.69%) and 269 animals (15.5%), and beef cattle made up 12 herds (2.9%) and 25 animals (1.4%) (P<0.01) (Table 2). In the deer category, elk were predominant in 17 herds (94.4%) with 141 animals (91.0%) (P<0.01), while sika deer were in 1 herd (0.6%) with 14 animals (9.0%) (Table 2).

Table 1 . Prevalence of tuberculosis in livestock in Korea from 2013 to 2022.

Year	Region (province)																	Total
	Seoul	Busan	Daegu	Incheon	Gwangju	Daejeon	Ulsan	Sejong	Gyeonggi	Gwangwon	Chungbuk	Chungnam	Jeonbuk	Jeonnam	Gyeongbuk	Gyeongnam	Jeju
2013	2 (4)	0 (0)	0 (0)	11 (41)	14 (14)	4 (29)	10 (83)	14 (99)	139 (613)	36 (112)	50 (266)	117 (677)	51 (262)	86 (249)	104 (213)	83 (349)	2 (2)	713 (3,013)
2014	0 (0)	0 (0)	2 (6)	12 (57)	0 (0)	2 (4)	17 (58)	10 (47)	151 (616)	44 (193)	70 (431)	141 (657)	77 (296)	144 (928)	148 (813)	82 (479)	0 (0)	900 (4,585)
2015	0 (0)	0 (0)	7 (24)	17 (67)	1 (1)	0 (0)	2 (14)	8 (31)	101 (324)	20 (63)	29 (161)	111 (497)	89 (380)	120 (658)	121 (557)	55 (353)	2 (3)	683 (3,133)
2016	0 (0)	0 (0)	4 (7)	3 (3)	0 (0)	0 (0)	16 (60)	4 (5)	88 (362)	56 (233)	46 (204)	110 (709)	65 (327)	83 (461)	130 (588)	83 (462)	3 (3)	691 (3,424)
2017	0 (0)	1 (1)	5 (115)	2 (2)	1 (1)	0 (0)	23 (86)	10 (31)	88 (372)	30 (181)	57 (136)	153 (720)	119 (484)	108 (502)	116 (349)	104 (612)	12 (48)	829 (3,640)
2018	0 (0)	1 (1)	10 (24)	1 (2)	1 (1)	0 (0)	19 (54)	13 (55)	67 (261)	28 (66)	50 (136)	94 (628)	87 (335)	124 (336)	145 (630)	134 (431)	3 (6)	777 (2,966)
2019	0 (0)	1 (3)	1 (1)	6 (16)	1 (1)	0 (0)	8 (10)	2 (4)	102 (586)	47 (127)	78 (377)	110 (906)	100 (384)	135 (594)	123 (543)	143 (556)	1 (1)	858 (4,109)
2020	0 (0)	0 (0)	7 (42)	2 (4)	0 (0)	0 (0)	7 (30)	6 (26)	75 (353)	28 (172)	46 (193)	73 (632)	70 (286)	98 (473)	90 (202)	81 (584)	0 (0)	583 (2,997)
2021	0 (0)	1 (1)	14 (52)	1 (1)	0 (0)	0 (0)	11 (73)	12 (97)	62 (198)	17 (56)	26 (102)	61 (165)	26 (69)	122 (578)	51 (255)	67 (263)	6 (9)	477 (1,919)
2022	0 (0)	0 (0)	2 (13)	0 (0)	0 (0)	0 (0)	5 (15)	0 (0)	29 (170)	27 (89)	39 (194)	71 (206)	44 (249)	87 (510)	63 (132)	63 (317)	1 (1)	431 (1,896)
Total	2 (4)	4 (6)	52 (284)	55 (193)	5 (25)	2 (33)	52 (493)	37 (315)	532 (4,040)	174 (1,263)	252 (2,352)	573 (6,228)	375 (3,002)	588 (5,011)	590 (4,409)	466 (4,184)	20 (100)	6,942 (31,682)

* No. of TB cases (no. of TB livestock)..

Table 2 . Prevalence of tuberculosis in cattle and deer by region in Korea in 2022.

Livestock	Species	Region (province)																	Sub total	Total
		Seoul	Busan	Daegu	Incheon	Gwangju	Daejeon	Ulsan	Sejong	Gyeonggi	Gangwon	Chungbuk	Chungnam	Jeonbuk	Jeonnam	Gyeongbuk	Gyeongnam	Jeju
Cattle	Korean native cattle	0 (0)	0 (0)	2 (13)	0 (0)	0 (0)	0 (0)	5 (15)	0 (0)	14* (70)	22* (72)	35* (179)	58* (123)	39* (232)	77* (412)	53* (105)	55* (225)	1 (1)	361* (1,447)	413 (1,741)
	Dairy cattle	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	13* (84)	5* (17)	0 (0)	3 (30)	0 (0)	0 (0)	7* (10)	2 (2)	0 (0)	40** (269)
	Beef cattle	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	3 (13)	0 (0)	0 (0)	7 (10)	2 (2)	0 (0)	12 (25)
Deer	Elk	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	2 (16)	0 (0)	4 (15)	6 (26)	1 (6)	2 (63)	2 (15)	0 (0)	0 (0)	17* (141)	18 (155)
	Sika	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	1 (14)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	1 (14)
Total		0 (0)	0 (0)	2 (13)	0 (0)	0 (0)	0 (0)	5 (15)	0 (0)	29* (170)	27* (89)	39* (194)	71* (206)	40* (238)	79* (475)	62* (140)	59* (229)	1 (1)	1 (14)	431 (1,896)

No. of TB cases (no. of TB livestock)..

*P<0.05, ** P<0.01..

Figure 1. Number of cases and livestock diagnosed as tuberculosis in Korea from 2013 to 2022.

Figure 2. Prevalence of tuberculosis in cattle and deer in Korea, 2022. (A) No. of farms. (B) No. of animals.

Analyzing TB diagnosis methods from 2018 to 2022, out of 2,975 cattle TB cases, 2,436 (81.9%) were diagnosed on farms using the tuberculin skin test (TST), and 639 cases (18.1%) were identified through post-mortem inspections at slaughterhouses, still a significant detection method (Table 3, Fig. 3). Of these 539 cases detected post-mortem, 29 (5.4%) were in dairy cattle, but the majority, 485 cases (90.0%), were in Korean native cattle (Table 3).

Table 3 . Number of tuberculosis cases at farms and slaughterhouses in cattle from 2018 to 2022 in Korea.

Livestock	Farm/slaughterhouses	Animals	Year					Total
			2018	2019	2020	2021	2022
Cattle	Farm	Korean native cattle	514** (1,957)	534** (2,719)	391** (1,951)	294** (1,203)	292** (1,317)	2,025** (9,147)
		Dairy cattle	68* (488)	126* (677)	60* (322)	56* (248)	37* (264)	347* (1,999)
		Beef cattle	8 (46)	25 (99)	10 (40)	10 (130)	11 (24)	64 (339)
		Subtotal	590 (2,491)	685 (3,495)	461 (2,316)	360 (1,581)	340 (1,605)	2,436 (11,485)
	Slaughter	Korean native cattle	158* (287)	122* (318)	86* (338)	50* (112)	69* (130)	485* (1,185)
		Dairy cattle	12 (37)	9 (32)	2 (5)	3 (30)	3 (5)	29 (109)
		Beef cattle	10 (103)	6 (6)	2 (2)	6 (6)	1 (1)	25 (118)
		Subtotal	180 (427)	137 (356)	90 (345)	59 (148)	73 (136)	539 (1,412)
	Subtotal	Korean native cattle	672** (2,244)	656** (3,037)	477** (2,289)	344** (1,315)	361** (1,447)	2,510** (10,332)
		Dairy cattle	80* (525)	135* (709)	62* (327)	59* (278)	40* (269)	376* (2,108)
		Beef cattle	18 (149)	31 (105)	12 (42)	16 (136)	12 (25)	89 (457)
	Total		770 (2,918)	822 (3,851)	551 (2,658)	419 (1,729)	413 (1,741)	2,975 (12,897)

No. of TB herds (no. of TB livestock)..

*P<0.05, **P<0.01..

Figure 3. Number of tuberculosis cases at farms and slaughterhouses in cattle from 2018 to 2022 in Korea. (A) No. of farms. (B) No. of animals.

The incidence rates of BTB per 1,000 farms and per 10,000 cattle from 2018 to 2022 are detailed in Table 4 and 5. The herd incidence per 1,000 herds peaked from 7.26 in 2018 to 7.97 in 2019, then dropped to 4.10 by 2022 (Table 5). This trend was mirrored in dairy cattle, where the incidence rose from 12.58 in 2018 to 21.89 in 2019, before decreasing (Table 5). The incidence per 10,000 animals also increased from 8.29 in 2018 to 10.53 in 2019, then gradually fell to 4.23 in 2022 (Table 5).

Table 4 . Statistics on the number of herds and number of cattle in South Korea from 2018 to 2022.

Animals	Year
	2018	2019	2020	2021	2022
Korean native cattle	92,238* (2,961,521)	89,731* (3,078,184)	88,994* (3,227,181)	89,824* (3,415,332)	87,852* (3,557,185)
Dairy cattle	6,360 (407,894)	6,168 (408,135)	6,106 (409,790)	6,105 (409,798)	5,888 (389,860)
Beef cattle	7,474 (151,471)	7,276 (158,871)	7,174 (168,005)	7,153 (174,127)	6,924 (169,362)
Total	106,072 (3,520,886)	103,175 (3,645,190)	102,274 (3,804,976)	103,082 (3,999,257)	100,664 (4,116,407)

*No. of farm herds (no. of cattle)..

Data of the total number of herds and cattle (in total, by dairy, beef and Korean native) were derived from Korea Statistical Information Services..

Table 5 . The annual herd and animal incidence rate of tuberculosis in cattle 2018 to 2022 in Korea.

Classification	Cattle	Year
		2018	2019	2020	2021	2022
Herd incidence (per 1,000 herds)	Korean native cattle	7.29	7.31	5.36	3.83	4.11
	Dairy cattle	12.58*	21.89*	10.15*	9.66*	6.79*
	Beef cattle	2.41	4.26	1.67	2.24	1.73
	Total	7.26	7.97	5.39	4.06	4.10
Animal incidence (per 10,000 animals)	Korean native cattle	7.58	9.87	7.09*	3.85	4.07
	Dairy cattle	12.87*	17.37*	7.98*	6.78*	6.90*
	Beef cattle	9.84	6.61	2.50	7.81*	1.48
	Total	8.29	10.53	6.99	4.32	4.23

No. of farm herds (no. of cattle)..

Data of the total number of herds and cattle (in total, by dairy, beef and Korean native) were derived from Korea Statistical Information Services..

Herd incidence: (number of infected dairy herds/number of total herds) ×100..

Animal incidence: (number of infected cattle/number of total cattle) ×100..

*P<0.05..

The ongoing challenge of tuberculosis in cattle and deer, despite over 40 years of an eradication program in Korea, highlights the complexities and resilience of this disease. Initiated in 1964, the test-and-slaughter policy with compensation aimed to curb tuberculosis, yet its persistence underscores the need for revisiting and adapting strategies.

Historically, the incidence of tuberculosis in cattle was notably high, around 15%, until the 1940s. With continuous testing and culling policies, this rate decreased to 1.6% from 1950. However, a resurgence in the 2000s, particularly in deer, calls for a critical evaluation of these policies. This fluctuation in prevalence indicates the influence of varying testing programs (Yoon et al, 2008).

A significant observation is the prioritization of bovine tuberculosis control in dairy cattle over Korean native and beef cattle. This oversight might have contributed to the sustained presence of tuberculosis, especially considering the lesser focus on tuberculin testing in these cattle breeds. The study’s findings advocate for a more inclusive and urgent approach towards tuberculosis testing, particularly in breeding farms of Korean native and beef cattle.

The study’s data from 2018 to 2022 show a peak in bovine TB incidence rates, with notable contributions from dairy cattle. However, the presence of the disease in native Korean and beef cattle, often unchecked for head and neck TB, is a concerning trend. The domestic BTB herd incidence per 1,000 heads increased from 11.2 in 2000 to 16.1 in 2003, and the BTB incidence per 10,000 animals was very high at 21.5 in 2001 and 22.6 in 2002 (Nam et al, 2012). The increase in positive cases since the introduction of the gamma interferon test in 2013 and mandatory TB testing in traded cattle over 12 months old since 2016 signifies a shift in detection strategies.

Furthermore, the current landscape in 2022, dominated by cattle TB cases, especially in Korean native cattle, calls for a comprehensive prevention policy. This includes thorough inspections and possibly rethinking the testing methodologies, as the high incidence in slaughterhouses suggests insufficient pre-testing.

Beyond cattle, addressing TB in goats, wildlife, and companion animals like dogs and cats is essential for a holistic approach to TB eradication in Korea (Lee et al, 2015; Cho et al, 2022). TB in household pets, particularly in Korea, warrants attention. The possibility of widespread TB infections in companion animals like dogs and cats is highlighted by recent incidents, such as the M. bovis outbreak among dogs (Cho et al, 2022). This situation underscores the need for comprehensive surveys and studies in this area.

A recent survey of goat farming in South Korea found that 432,765 goats were raised by 10,073 farms as of December 2022 (MAFRA, 2023). However, the lack of a TB screening system for these goats is also an important issue that needs to be addressed in order to eradicate TB in South Korea. Meanwhile, M. bovis, the causative agent of BTB, is susceptible to a variety of wild and zoo animals, such as wild bores, wild cats, foxes, possums, river otter and badgers (Fitzgerald and Kaneene, 2013; Pesciaroli et al, 2014; Lee et al, 2015). The possum and badger are considered maintenance hosts of M. bovis in New Zealand, as well as in the United Kingdom, Spain, Portugal, Ireland and France (Palmer, 2013), whereas wild boar is considered a maintenance host of M. bovis in Spain, Portugal and the United Kingdom (Naranjo et al, 2008; Santos et al, 2009; Barasona et al, 2014). Therefore, with a substantial goat farming industry and the susceptibility of various animals to M. bovis, a comprehensive TB testing protocol becomes imperative.

The test-and-slaughter strategy, while historically effective, requires adaptation to current challenges. Learning from successful eradication stories like Australia’s (Lehane, 1996), Korea can aim for a swift and efficient eradication of TB in livestock. Australia successfully eliminated BTB within a span of 27 years, starting with the initiation of the Brucellosis and Tuberculosis Eradication Campaign (BTEC) in 1970. This successful eradication campaign culminated on December 31, 1997, when the country officially declared itself free from BTB. To replicate this success, Korea would benefit from an enhanced surveillance system that covers a broader spectrum of animal species. Such an endeavor would require the active involvement of the private sector along with strong support from the government, creating a collaborative effort towards the efficient eradication of TB in livestock.

This work was supported by Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) through Agriculture, Food and Rural Affairs Convergence Technologies Program for Educating Creative Global Leader, funded by Ministry of Agriculture, Food and Rural Affairs (MAFRA) (320005-04).

No potential conflict of interest relevant to this article was reported.