The incidence of human brucellosis is surging dramatically in southern provinces of China (1-3), including provincial-level administrative divisions (PLADs) along and to the south of the Yangtze River①, and no brucellosis outbreaks were reported in southern Hubei Province before this investigation (4-5). An eradication program of brucellosis has been put into action in Hubei since 2017.
On June 3, 2019, 2 clusters of brucellosis involving 5 cases in Xianning, a prefecture-level city in southern Hubei, were reported to the National Public Health Emergency Reporting Information System (NPHERIS), and 1 cluster involved 3 employees of L mutton restaurant in Chongyang County, Xianning with the other involving 2 goat keepers of J goat farm in Jiayu County, Xianning. A field investigation was initiated to identify the infection source and risk factors.
Suspected cases were defined as residents of Chongyang County and suppliers of the L mutton restaurant who developed two or more of the following symptoms from January 1 to June 31, 2019: fever (≥37.5 ℃), fatigue, night sweats, and joint pain excluding patients with confirmed diagnosis for other diseases. Confirmed cases were defined as suspected cases with positive 1∶100 (+ +) or above serum agglutination test (SAT) for Brucella.
Case finding was carried out by interviewing cases, doctors, restaurant managers, and others employees, reviewing Infectious Disease Reporting Management Information System and medical records, and implementing symptom surveillance in local major hospitals.
Serum samples of all suspect cases were collected and tested. If the Rose Bengal plate agglutination test (RBPT) or SAT was positive, detailed demographic information, clinical information, eating habits, occupational history, preventive measures, and sources of animal products were collected. A field investigation was also initiated to ascertain possible polluted environments which these patients were exposed to.
A total of 8 cases (including 5 initial cases mentioned above) of brucellosis were identified with 6 patients experiencing onset of illness in April and 2 patients in May. All cases were confirmed. The most commonly reported symptoms were fever (88%), joint pain (75%), and fatigue (75%), and they were all discharged after a treatment of doxycycline and rifampin (42 d). Of these patients, 6 came from Chongyang County, and 2 from Jiayu County, and their ages ranged from 26 to 57 years old with a median age of 49 years. Their suspected exposures included goat-slaughtering, abortive ewes, and environmental exposure. Time intervals between onset of symptoms and diagnosis varied from 6 to 43 days, and the onset-to-diagnosis intervals of 6 cases exceeded 1 month.
The trade relationship among the work sites was further investigated. In Hubei, mutton consumption peaks between October and February of the next year, and L mutton restaurant mainly engaged in mutton hot pots and mutton noodles. During the off-season, the restaurant bought frozen mutton from B wholesale market in Wuhan, whose mutton originated from a market in Huanghua, Hebei Province of Northern China. During the peak months, it bought live goats from J goat farm and then slaughtered them in a back room of the restaurant. J goat farm bought live goats from M live goat market in Fang County, Shiyan City, northern Hubei Province (Figure 1).
During the investigation, a total of 19 serum samples were collected and 8 of them tested positive for RBPT and SAT. A strain of Brucella melitensis was isolated (Table 1).
Source of samples Samples collected RBPT positive SAT positive Brucella strain isolated L mutton restaurant 9 5 5 1 J goat farm 2 2 2 − D butcher’s 2 1 1 − M live goat market 1 0 0 − Relatives 5 0 0 − Total 19 8 8 1 Abbreviations: RBPT=Rose Bengal plate agglutination test, SAT=Serum agglutination test.
Table 1. Laboratory results of an outbreak of brucellosis in Hubei Province, China, 2019.
Given that most cases had a suspected exposure to goat-slaughtering, we hypothesized that slaughtering was a key risk factor of infection. Subsequently, we investigated the exposure histories of 21 individuals, including all employees of L mutton restaurant, J goat farm, and D butcher's. No employees wore any personal protective equipment at work, and no patients had a history of consuming unpasteurized contaminated animal products or a history of travelling to endemic areas beforehand. The results showed that slaughtering without protective measures was a risk factor (RR=11.38, 95%CI: 1.70–76.14) (Table 2), and 6 of the 8 patients had not heard of brucellosis before and no patients had an awareness of clinical signs and symptoms of human brucellosis.
Factors Exposed Unexposed Attack rate (%) RR (95%CI) Total Cases Total Cases Exposed Unexposed Slaughtering without precautions 8 7 13 1 87.50 7.69 11.38 (1.70–76.14) In slaughterhouse without precautions 5 1 16 7 20.00 43.75 0.46 (0.07–2.88) Processing frozen mutton without precautions 8 0 13 8 0 61.54 0* Abbreviations: RR=Relative Risk.
Table 2. A cohort study of an outbreak of brucellosis in Hubei Province, China, 2019.
Further field investigation revealed that the slaughterhouse of L mutton restaurant was a low-roofed room of nine square meters with a door connecting the lobby of the restaurant. There were no windows, ventilation, or disinfection facilities, and the conditions in D butcher’s were similar.
J goat farm is located beside the Yangtze River and separated from residential areas. In the off season, the farm kept about 200 self-bred goats. In November 2018, the farm bought about 100 goats from M live goat market and kept them with self-bred goats, which might have led to cross-infection. Several pregnant ewes were aborted between December 2018 and January 2019 but were still sold. There were no inspections or quarantine measures while in transit since these goats were transported through a rural road. All the goats in the farm were sold for the first time in nearly a decade in January 2019 without any inspection measure.
|①||These include Jiangsu, Anhui, Shanghai, Hubei, Sichuan, Zhejiang, Chongqing, Jiangxi, Hunan, Guizhou, Fujian, Yunnan, Guangdong, Guangxi, and Hainan of the mainland of China.|