Recollection: Retrospective Analysis of the Epidemiological Evolution of Brucellosis in Animals — China, 1951–1989 and 1996–2021

In this study, surveillance data from two epidemic phases (I: 1951–1989 and II: 2006–2021) of brucellosis in animals were collected and analyzed to illustrate the epidemiological profile. Epidemic data on animal brucellosis were collected from the Annals of Animal Diseases in China (1951–1989) and the Official Veterinary Bulletin (2006–2021). The seroprevalence of animal brucellosis and the number and biotypes of Brucella strains in different PLADs were extracted from Animal Diseases in China (1952–1989). Five epidemic items were extracted from the Official Veterinary Bulletin [2006–2021 (September), http://www.agri.gov.cn]: 1) the total number of outbreaks each month, 2) number of cases each month, 3) animal species (hosts), 4) number of animal deaths each month, and 5) number of animals destroyed each month. Excel 2016 (Microsoft, Redmond, WA, USA) was used for data curation, processing, analysis, and visualization. A semi-logarithmic curve was used to depicte the changing trends in the positive case rates and the culling rates. OmicShare tools (12) (https://www.omicshare.com/tools/) were used for Pearson correlation analysis of the incidence of human brucellosis, the infected rates, and the livestock breeding situation.

From 1951 to 1989, the seroprevalence of sheep brucellosis among 15 PLADs was 1.84% (993,609/54,068,364). The highest positive rate was 5.92% (520,140/8,788,690) in the 1960s (1960–1969), followed by 3.58% (234,154/6,543,382) in the 1950s (1951–1959), 2.18% in the 1970s (1970–1979), and 0.3% (95,582/32,129,518) in the 1980s (1980–1989) (Table 1). Sheep brucellosis was widespread from 1951 to 1959. The seroprevalence in Qinghai Province was 6.58% (16,280/247,365) from 1950 to 1959; in Heilongjiang Province was 8.5% from 1956 to 1958; and in Xinjiang Uygur Autonomous Region was 9.19% from 1956 to 1964. Sheep brucellosis was severe from 1961 to 1969, with seropositive rates in Qinghai and Xinjiang PLADs from 1960 to 1969 at 12.78% (16,280/247,365) and 4.16% (202,488/4,870,090), respectively. In Ningxia Hui Autonomous Region, the rate was 11.3% from 1963 to 1966.

Sheep brucellosis seroprevalence declined from 1970 to 1979. However, some regions remained heavily affected, with 9.26% seroprevalence in Qinghai Province and 3.98% in Xinjiang Uygur Autonomous Region. From 1980 to 1989, sheep brucellosis was gradually controlled in some initially high-epidemic regions. Seroprevalence decreased in Shaanxi, Gansu, Ningxia, Xizang, Jilin, Liaoning, and Qinghai PLADs. In Qinghai Province, the positive rate decreased from 9.26% in the 1970s to 3.06% in the 1980s, while in Gansu Province, it decreased from 4.66% in 1981 to 0.10% in 1986, and the positive rate decreased from 2.54% in the 1950s to 0.54% in the 1980s. Positive rate in Xinjiang Uygur Autonomous Region declined to 0.79% in the 1980s. From 1987 to 1989, the overall sheep seroprevalence in 30 PLADs (excluding Chongqing Municipality) was 0.59% (6,113/1,037,181), ranging from 0.10% (Jilin Province) to 7.44% (Jiangsu Province) (Table 2).

The overall seroprevalence of brucellosis in cattle from 22 PLADs was 1.4% (312,132/22,316,117) from 1952 to 1989. The seroprevalence in cattle gradually declined from 4.63% (59,701/1,289,667) from 1952 to 1959, to 2.97% (110,020/3,703,368) from 1960 to 1969, to 1.15% (89,214/7,733,531) from 1970 to 1979, and to 0.55% (53,197/9,589,551) from 1980 to 1989. In the 1950s, brucellosis in cattle was common in the north. The infection rates were 46.43%, 19.3%, 11.57%, and 12.27% in Ningxia, Qinghai, Gansu, and Xinjiang PLADs, respectively. Subsequently, the seroprevalence in cattle gradually declined from the 1950s to the 1980s, with rates of 1.60% in Xinjiang, 1.05% in Ningxia, and 8.9% in Qinghai in the 1980s. Epidemics and outbreaks gradually decreased and were controlled in regions with high seroprevalence. Brucellosis was still endemic in some previously low-epidemic regions from 1980 to 1984, at rates of 7.22% in Jiangxi, 6.66% in Liaoning, 5.20% in Hubei, 4.53% in Henan, 3.52% in Hunan, and 2.30% in Guizhou. Finally, the overall seroprevalence in cattle in all 30 PLADs (except Chongqing) decreased to 0.71% (5,727/803,782), with the lowest being 0.02% in Guangdong and the highest being 3.41% in Hunan Province.

Swine brucellosis seroprevalence was 3.7% (11,683/315,443) in 11 PLADs from 1955 to 1989, with rates of 24.38% (524/2,149) in the 1950s, 10.23% (687/6,714) in the 1960s, 4.36% (906/20,783) in the 1970s, and 3.35% (9,565/285,797) in the 1980s. Before the 1980s, swine brucellosis was atypical but locally endemic in Guangxi and Guangdong, where breeding swine production was prominent. In 1952, the Guilin Liangfeng swine farm in Guangxi introduced four Berkshire breeding pigs from Hong Kong Special Administrative Region (SAR), China, resulting in numerous infections and swine abortions. The seroprevalence in Guangxi in 1952 was 51.5% (381/739). In 1980, the swine brucellosis seroprevalence increased, peaking in 1985 at 8.15%, and subsequently declined continuously to 0.74% (2,300/310,394) from 1987 to 1989. Rates were 0.03% (2/6,585) in Henan and 4.06% (483/11,910) in Hunan (Table 2). In the late 1980s, Brucella canis brucellosis was reported, and B. canis was isolated and identified. The average positivity rate in 8 PLADs was 6.72% (141/2,099). Dog seroprevalence was 14.74% in Xinjiang from 1965 to 1989 and 22.5% in Qinghai. Seroprevalence in horses, deer, camels, poultry, and wildlife, such as yaks, has also been reported (13).

From 2006 to 2021, a total of 38,248 outbreak events were recorded. The number of outbreaks increased from 90 in 2006 to a maximum of 6,126 in 2011 and then declined to 3,133 in 2021 (Figure 1A). Outbreak events were observed each month, with 62.19% (23,787/38,248) recorded from June to October. Most outbreaks occurred in August (5,418), followed by September (n=5,181), July (n=4,710), and June (n=4,291), with the fewest occurring in February (n=794) (Figure 1B). The average number of reported outbreak events was 2,390.5 per year and 3,187.3 per month. Sheep and cattle accounted for approximately 99.2% of cases, with 218,168 in sheep, 11,625 in cattle, and 303,609 in both. The proportion of cases involving other animal species was low. Additionally, 1,759 cases included deaths caused by Brucella infection, accounting for 0.33% of deaths in Inner Mongolia, Shaanxi, and Xinjiang.

Figure 1. 

Brucellosis outbreak event in animals from 2006 to 2021. (A) Total number; (B) Seasonal distribution profile.

Note: Total outbreak number of brucellosis included the outbreak events from bovine, sheep, goats, and other hosts in this period.

Between 2006 and 2021, a total of 537,797 cases were reported. The number of cases was 2,031 in 2006, rapidly increased to 125,030 in 2011, and then declined to 59,494 in 2020. The lowest number of cases (n=1,280) was observed in 2007 (Figure 2A). Although the number of cases fluctuated and decreased after the 2011 peak, there were at least five times more cases in 2021 than in 2006. The range of case counts across months was 10,233–65,480, with 54.1% of cases reported from April to September. Most cases occurred in June, followed by August (n=54,828) and July (n=48,792), with the lowest number occurring in January (Figure 2B).

Figure 2. 

Reported brucellosis cases in animals from 2006 to 2021. (A) Total number; (B) Seasonal distribution profile.

Note: The total number of reported animal brucellosis cases included cases reported from bovine, sheep, goats, and other hosts in this period.

Animal brucellosis outbreaks were reported in 28 PLADs from 2006 to 2021, excluding Tianjin, Hainan, and Xizang PLADs. Inner Mongolia reported the highest number of outbreaks (21,860) between 2006 and 2021 (Figure 3), with a dramatic increase from 215 in 2010 to 5,464 in 2011, followed by a decline to 609 in 2021. Xinjiang reported 8,985 cases during the study period, with the number of outbreaks gradually increasing annually from 2 in 2006 to 1,543 in 2021. A similar trend was observed in Shaanxi Province, with outbreaks gradually increasing from 3 in 2006 to 744 in 2021. In the south, Hubei (n=931) and Zhejiang (n=518) reported the most outbreaks, both exhibiting an initial increasing trend followed by a gradual annual decline. The fewest cases were reported in Anhui (n=11), followed by Sichuan (n=24), Beijing (n=39), Shanghai (n=43), Guangxi (n=52), Ningxia (n=57), and Guangdong (n=59). Other regions reported between 60 and 454 outbreaks. Approximately 40% of outbreaks occurred from 2011 to 2013, with 6,136 in 2011, 5,346 in 2012, and 3,604 in 2013. A total of 537,797 animal cases tested positive across 28 PLADs. Of these, 6.34% (34,070/537,797) were in the south and 93.67% (503,727/537,797) were in the north (Figure 4). Most cases were reported in Inner Mongolia (n=346,785), Xinjiang (n=105,367), and Shanxi (n=23,399), while Beijing reported the fewest (n=171). In the north, cases continuously increased from 1,797 in 2006 to 58,369 in 2020 before declining to 18,419 in 2021. In the south, Hubei reported the most cases (n=10,839), followed by Yunnan (n=5,888), Henan (n=4,841), and Zhejiang (n=4,536). Conversely, Sichuan recorded the lowest number (n=91). Southern cases rose from 234 in 2006, peaked in 2016 (n=8,014), and then fluctuated before declining to 741 in 2021. Notably, cases in the south increased with a lag of two to five years compared to the north. The peak occurred in the north in 2011 and in the south in 2016 (Figure 4).

Figure 3. 

The distribution of reported brucellosis cases in animals at the PLADs level from 2006 to 2021.

Note: Number of cases reported in each province included those from bovine, sheep, goats, and other hosts in this period. Abbreviation: PLADs=provincial-level administrative divisions.

Figure 4. 

Distribution profile of reported brucellosis cases in animals between southern and northern regions from 2006 to 2021.

Note: Number of reported cases in southern and northern included cases from bovine, sheep, goats, and other hosts in this period.

The total culling rate of positive animals was 70.14% (377,230/537,797). The culling rate gradually declined from 103.3% in 2006 to 4.32% in 2017 and then fluctuated between 40.4% and 109.3% from 2017 to 2021 (Figure 5A). The trends in culling and infection rates between 2006 and 2021 were almost reversed. The culling rate of positive animals declined with an increase in the infection rate (Figure 5B). These data provide irrefutable evidence that the source of brucellosis infection is persistent and may move between herds and regions. Sichuan Province had the highest culling rate of positive animals (170.33%), followed by Anhui (157.29%), Beijing (156.73%), and Guangxi (155.35%) (Figure 5A). Additionally, the culling rates in nine PLADs were above 100%: Fujian, Shanghai, Jiangxi, Guangdong, Jiangsu, Jilin, Yunnan, Heilongjiang, and Guizhou (Figure 5A). However, the culling rates in 15 others PLADs were below 100%, with the lowest culling rate in Hubei [61.75% (6,693/10,839)], followed by 66.70% in Xinjiang, 68.98% in Ningxia, 70.77% in Shanxi, 78.26% in Shandong, 84.32% in Liaoning, and 84.69% in Inner Mongolia (Figure 5A). Furthermore, correlation analysis showed that the number of sheep and the infection rate of animal brucellosis were significantly correlated with the incidence rate and number of human brucellosis cases (P≤0.001) (Figure 6).

Figure 5. 

Brucellosis in animals from 2006 to 2021. (A) Change trend of culling rates; (B) Infection rates.

Note: Total number of culls in seropositive animals included bovine, sheep, goats, and other hosts each year.

Figure 6. 

Pearson correlation analysis of incidence of human brucellosis and livestock breeding situation.

** P≤0.01;

*** P≤0.001.

From 1951 to 1989, 2,015 Brucella strains were collected from animals, including 1,523 B. melitensis strains, 250 B. abortus strains, 208 B. suis strains, 32 B. canis strains, and 2 B. ovis strains. During this period, B. melitensis was mainly found in Xinjiang (n=286), followed by Shaanxi (n=217), Jilin (n=207), Henan (n=109), Sichuan (n=25), and fewer strains in Guangxi, Yunnan, and Fujian PLADs. B. abortus strains were dominant in Sichuan (n=122), Xinjiang (n=56), and Jilin (n=30). B. suis strains were distributed in Guangxi (n=98) and Guangdong (n=90). Fewer B. canis strains were observed in Sichuan, Fujian, Guangdong, and Guangxi PLADs (Supplementary Table S1). Additionally, only two B. ovis strains were isolated from Urumqi, Xinjiang. However, from 1996 to 2021, only 303 Brucella strains were isolated and identified from animals, with 254 B. melitensis, 26 B. abortus, and 23 B. suis strains. During this period, most B. melitensis strains were found in Xinjiang (n=101), Inner Mongolia (n=78), and Gansu (n=26). B. abortus strains were distributed in Hebei (n=11), Heilongjiang (n=10), and Xinjiang (n=5) PLADs. Additionally, 22 B. suis strains were isolated from animals in Inner Mongolia. The number and diversity of species/biotypes have gradually decreased, indicating a significant difference between the current serious epidemic situation of brucellosis and the number of strains in humans. Furthermore, the species/biotype distribution pattern of Brucella showed a pronounced shift from multiple co-driven species before the 2000s to a single dominant species, B. melitensis, after the 2000s.

This study involved a retrospective epidemiological evolution analysis of brucellosis in animals from the 1950s to the 2020s; the epidemic pattern was similar to that of human brucellosis (10). Two epidemic stages were identified during the examined period: the first from the 1950s to the 1980s and the second from 2006 to 2021. Almost all PLADs were involved in both stages, resulting in substantial harm to human health, the farming industry, and socioeconomic development (9). This study showed that brucellosis in sheep, goats, and cattle is dominant in mainland China, endemic areas are widespread in most PLADs, and swine brucellosis is predominant in Guangdong and Guangxi. Sheep, goats, and bovines were the only means of production and livelihood for thousands of people from the 1950s to the 1990s; cattle were the main production factor, including for farmland, cultivation, and transportation. After 2000, along with economic development, production pattern changes, and elevated living standards, sheep and goat breeding has continuously increased and expanded, and the incidence of brucellosis has worsened. Swine brucellosis was potentially introduced to mainland China and was dominant in Guangdong and Guangxi, where the breeding industry is large. Surveys showed that swine brucellosis became epidemic on farms and gradually spread to rural areas, further increasing the difficulty of control. In Guangxi, the seropositivity by SAT from 22,127 serum samples from breeding pigs between 2009 and 2011 was under 2.0%, but some historical epidemic areas have a re-emerging risk due to multiple factors (14). Currently, the epidemic features of brucellosis display a pronounced change in Guangxi; previously dominant circulating B. suis and B. canis strains have been replaced by B. melitensis strains (15).

Since the 1950s, some PLADs with high seroprevalence of animal brucellosis have organized and established institutes and groups for brucellosis surveillance and control according to government planning to implement surveillance and control strategies (16). From the 1950s to the 1960s, a set of comprehensive prevention and control measures primarily based on serological testing and vaccine immunization was implemented, including the culling and isolation of positive animals (16). In the 1970s, animal immunization was the main control tool, and all animals were vaccinated with the M5 (17) or B. suis strain 2 (S2) vaccine (18). In the 1980s, epidemic surveillance improved at the national and provincial levels, with the exception of vaccinated animals. Animal brucellosis has been preliminarily controlled since 1986 based on comprehensive control strategies, including immunization, quarantine, elimination, and culling, implemented over the past four decades (9,19). The incidence of human brucellosis has significantly decreased, and only a few cases have been reported. These data demonstrate that persistent immunization and quarantine measures for animals nationwide are still a priority for stopping human brucellosis (20). However, because current detection technology cannot discriminate between infection and vaccine immunization in animals, surveillance in animal immune zones present some puzzles. Therefore, we suggest that the implementation of mass vaccination in small ruminants in high-epidemic areas, and the surveillance and elimination of positive animals, is an option for control measures in zones with a low epidemic (21). In Kyrgyzstan, the introduction of mass vaccination in small ruminants has contributed to brucellosis control, thereby reducing the number of infections in animals and humans (22). Additionally, a vital reason for brucellosis control in the 1980s was that all breeding farms were collectively owned by the state, facilitating the implementation and purification of prevention and control strategies. Currently, the majority of livestock is owned by individuals, and transportation and transactions are extremely frequent, posing a severe challenge to brucellosis prevention and control (23). However, there was a considerable discrepancy in the reported cases between animals and humans, even though there was an almost reversed epidemic trend from 2006 to 2021. The incidence rate of human brucellosis increased during this period; however, the number of reported cases in the animal population gradually declined. These data revealed that testing and surveillance capacity for animal brucellosis was insufficient, and control measures were severely lacking. Testing and culling are very effective measures for animal disease prevention and control (24). There was a low positive animal culling rate in some regions with a high incidence rate, meaning that infected animals were not completely eliminated, resulting in the persistent circulation of the disease. The increased infection rate in the south was driven by the introduction of infected animals from the north, implying that control of the infected animal trade and transfer was inadequate. Currently, circulating Brucella species have obviously changed. Although a few B. abrotus, B. suis, and B. canis strains were occasionally isolated (25-26), B. melitensis strains were the predominant species in China and have expanded southward (27). B. ovis has only been historically isolated from Xinjiang; its epidemic situation needs further evaluation (28).

Despite incomplete surveillance data hindering accurate and timely prediction of brucellosis trends in animals, the nationwide growth of the animal breeding industry has increased the demand for animal products. Furthermore, the pursuit of economic benefits has driven changes in sheep breeding practices, which is another important factor to consider. For example, the “Small Tailed Han Sheep” breed gained recognition in China for its early maturity, high birth rates, and multiple offspring. This popularity increased the likelihood and frequency of human contact with infected sheep, contributing to the spread and rise in brucellosis infections.

In the Black Sea basin, ruminant health has been hindered by informal animal trade due to economic factors, insufficient support for developing formal trade, and sociocultural drivers (29). Animal trade movements were identified as a major transmission route for brucellosis spread between farms (30). Therefore, restricting the movement and trade of infected animals and implementing mass vaccination of small ruminants in regions with high incidence have been urged. Furthermore, strengthening surveillance, information exchange, risk assessment, and coordinated response capacity for animal brucellosis is urgent (31). In particular, grassroots veterinary departments must screen for and eliminate infected animals in a timely manner. Comprehensive intervention measures against brucellosis incidence in humans and animals are recommended. These measures include public awareness, effective hygiene management, and adequate quarantine or serological detection (e.g., SAT) for newly introduced animals (32-33). Given the high baseline prevalence, these measures should be based on vaccination combined with measures to promote hygiene and husbandry practices that minimize the risk of brucellosis spreading to low-endemic regions.

This study provides an updated epidemiological overview of animal brucellosis nationwide, which will aid government sectors in strengthening routine surveillance and vaccination to reduce disease occurrence and public health risks in China. Additionally, a vast discrepancy was observed in the incidences of animal and human brucellosis after the 2000s. Therefore, strengthening the surveillance and control of diseased in animals is the most effective strategy. This includes persistent vaccination in high-incidence areas, implementing routine surveillance plans, and using strict animal movement restrictions to restrain further spread.

All authors who have previously published research data on animal brucellosis nationwide and are working on animal brucellosis control and prevention.