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The epidemiology of human trichinellosis in China during 2004–2009
Acta Tropica 118 (2011) 1–5
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Review
The epidemiology of human trichinellosis in China during 2004–2009 J. Cui a , Z.Q. Wang a,∗ , B.L. Xu b a b
Department of Parasitology, Medical College, Zhengzhou University, Zhengzhou 450052, PR China Center for Disease Control of Henan Province, Zhengzhou 450003, PR China
a r t i c l e
i n f o
Article history: Received 21 July 2010 Received in revised form 3 February 2011 Accepted 7 February 2011 Available online 13 February 2011 Keywords: Trichinellosis Epidemiology Seroprevalence Outbreak China
a b s t r a c t The endemic foci of human trichinellosis are mainly located in southwestern China. Seroepidemiological surveys of Trichinella spiralis infection in humans were carried out in 10 out of 34 Provinces/Autonomous Regions/Municipals (P/A/M) of China during 2004–2009. The overall seroprevalence was 3.19% (3198/100,282). The highest seroprevalences were mainly located in western China: 8.43% in Yunnan, 6.37% in Inner Mongolia and 5.35% in Sichuan. The seroprevalence of Trichinella infection in humans was related to the habit of eating meat and differed among nationalities. From 2004 to 2009, 15 outbreaks of human trichinellosis, consisting of 1387 cases and four deaths, were reported in the three southwesternmost P/A of China (nine outbreaks in Yunnan, two in Sichuan and four in Tibet), where ethnic groups routinely eat raw meat. Pork is the predominant source of outbreaks of human trichinellosis in China. Out of 15 outbreaks, 12 (85.71%) were caused by eating raw or undercooked pork, and 2 (13.33%) resulted from the consumption of raw wild boar, suggesting the significance of game meat as a source of infection for human trichinellosis. An outbreak of imported trichinellosis involving 49 cases in Yunnan during December 2006 from Laos is the first recorded outbreak of imported trichinellosis in China, but the source of that outbreak could not be identified. The mandatory inspection of pork should be further strengthened in southwestern China. Crown Copyright © 2011 Published by Elsevier B.V. All rights reserved.
Contents 1. 2. 3. 4. 5. 6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Seroprevalence of human trichinellosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Outbreaks of human trichinellosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Source of infection for outbreak of trichinellosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Outbreak of imported trichinellosis in Yunnan from Laos . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Trichinellosis, a food-borne parasitic zoonosis, is caused by the tissue-dwelling nematode Trichinella. Humans acquire the disease by ingesting raw or insufficiently cooked meat of pigs or other animals containing the Trichinella larvae. The adult worms live in the duodenal and jejunal mucosa of flesh-eating animals and humans, while the larvae live in skeletal muscles of the same hosts. The clinical manifestations of trichinellosis can be divided into two phases: an enteral phase and a muscular (parenteral or
∗ Corresponding author. Tel.: +86 371 66181026; fax: +86 371 66997182. E-mail addresses: [email protected] (J. Cui), [email protected] (Z.Q. Wang).
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acute) phase, which can coexist for a period lasting from a few days to weeks. The hallmark of the intestinal phase is a nonspecific gastroenteritis. One or 2 days after ingesting the tainted meat, the newly matured adults penetrate the intestinal mucosa, resulting in nausea, abdominal pain, diarrhea, and vomiting. The muscular phase is associated with an inflammatory and allergic response to muscle invasion by the migrating larvae. Fever, eyelid or facial edema, myalgia, and eosinophilia are the most prominent manifestations (Pozio et al., 2003). Trichinellosis remains an important zoonotic disease worldwide. Of all of the countries of the world, Trichinella spp. infection has been documented in domestic animals (mainly pigs) and wildlife in 43 (21.9%) and 66 (33.3%) countries, respectively. Human trichinellosis has been documented in 55 (27.8%) countries
0001-706X/$ – see front matter. Crown Copyright © 2011 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.actatropica.2011.02.005
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Table 1 Seroprevalence of human infection with Trichinella spiralis in China during 2004–2009. Location Beijing Gongxi Heilongjiang Henan Hubei Inner Mongolia Jilin Liaoning Sichuan Yunnan Total
No. examined
No. positive
Positive rate (%)
Reference Jia et al. (2006) Yang et al. (2007) Ge et al. (2005) Xu et al. (2009) Chen et al. (2006) Song et al. (2007) Xu et al. (2009) Xu et al. (2009) Zheng et al. (2005) Wang et al. (2005)
12,064 9638 9960 10,102 9939 9956 10,006 10,092 8416 10,109
140 319 130 300 251 634 96 26 450 852
1.16 3.31 1.31 2.97 2.53 6.37 0.96 0.26 5.35 8.43
100,282
3198
3.19
around the world (Pozio, 2007). Most outbreaks of trichinellosis are related to the consumption of raw pork containing Trichinella spiralis larvae (Dupouy-Camet, 2009). Human cases of trichinellosis have been recorded in 17 out of 34 Provinces/Autonomous Regions/Municipals (P/A/M) of China since the first Chinese case was reported in Xizang (Tibet) in 1965. From 1964 to 1999, 548 outbreaks of trichinellosis, consisting of 23,004 cases and 236 deaths, occurred in 12 P/A/M of China (Wang and Cui, 2001). During 2000–2003, 17 outbreaks of human trichinellosis, consisting of 828 cases and 11 deaths, were recorded in 8 P/A of China. All 11 deaths occurred in southwestern China, where ethnic groups routinely eat raw meat (Wang et al., 2006a,b). Out of 565 outbreaks, 538 (95.22%) outbreaks were due to consumption of raw or poorly cooked pork, and pork is the predominant source of outbreaks of human trichinellosis in China. If uncontrolled, this zoonotic parasitosis could pose exceptional problems because China is the largest pork-producing country in the world. In fact, pork produced in China in 2008 accounted for 46% of the total pork output worldwide (http://www.21food.cn/html/news/35/509789.htm). Over the past 6 years, Chinese parasitologists have produced a number of reports regarding the epidemiology of human trichinellosis. Therefore, to clarify the nationwide status of human Trichinella infection in China, Chinese publications on human trichinellosis epidemiology in China since 2004 were collected and analyzed.
The seroprevalence of Trichinella infection in humans was related to the habit of eating meat and differed by nationality. In minor ethnic regions (Longchuang and Lianghe counties) of Yunnan Province, the seropositive rate of Trichinella infection in the Thais (one of the Chinese minor ethnic groups) is 16.72% (336/2009) and was statistically higher than the mean seropositive rate of 8.43% (852/10, 109) in this province (P < 0.01). The seroprevalence of the inhabitants who frequently ate raw pork (41.96%) was higher than those who did not (4.17%) (P < 0.01). The seroprevalence of the households using one set of knife and tableware for cooked food and raw meat was higher than that of those using two dinner sets (28.89% vs. 15.21%, respectively; P < 0.01) (Dong et al., 2005). In Danba county (the Tibetan ethnic minority region) of Sichuan Province, the seroprevalence of the Tibetans was 21.94% (111/506), which was higher than the provincial mean seropositive rate of 5.35% (450/8416) (P < 0.01). Out of the Tibetans with seropositivity, 98.2% had a history of eating raw or semi-cooked meat (such as pork, wild boar and bear). In addition, the seroprevalence of Trichinella infection in humans was different among occupations: the highest (93.69%) was observed in the farmers and herdsmen, followed by officers (4.51%) and students (1.80%) (Zheng et al., 2007a).
2. Seroprevalence of human trichinellosis
From 2004 to 2009, 15 outbreaks of human trichinellosis, consisting of 1387 cases and 4 deaths, were reported in three P/A of China (9 outbreaks in Yunnan, 2 in Sichuan and 4 in Tibet) (Table 2). Over the past 6 years, all epidemic foci of human trichinellosis outbreaks were located in southwestern China where the ethnic groups which eat raw meat are predominantly distributed. All four deaths occurred in southwestern China (one case in Yunnan, one case in Sichuan and two cases in Tibet). The occurrence of human trichinellosis during 2004–2009 had a clear seasonal variation, with outbreaks mainly occurring in winter. Out of 12 outbreaks with clear dates of onset of the diseases, 9 outbreaks occurred during January–February and 3 outbreaks occurred during April–May. At the present time, human trichinellosis is not a nationally reportable disease. The national trichinellosis surveillance system has not yet been established in China, and the reports on outbreaks of human trichinellosis are voluntary, relying on physicians, parasitologists or epidemiologists. This often results in fragmentary information. Thus, the data obtained from the papers published could merely be the tip of the iceberg. Additionally, because adequate diagnostic tools are not widely available, many patients with trichinellosis, especially those with light or atypical symptoms, are often undiagnosed or misdiagnosed as other diseases in rural clinics or town hospitals.
Seroepidemiological surveys of Trichinella infection in humans were carried out in 10 P/A/M of China during 2004–2009. The sites and population of surveys were sampled with the cluster random sampling method. A total of about 100,000 inhabitants from 200 sites (160 rural and 40 urban sites) in 80 counties/cities/districts of 10 P/A/M were selected. Specific anti-Trichinella antibodies (IgG) were determined by an ELISA kit using the excretory–secretory (ES) antigens of T. spiralis muscle larvae (Zhuhai Haitai Biological Pharmaceuticals Co. Ltd., China). Test sera/control sera OD values of less than 2.1 were regarded as negative, whereas those of 2.1 or greater were considered positive. The validation of ELISA and all seropositive samples were conducted by the Specialist Committee on Parasitic Diseases of Health Ministry of China (Wang, 2008). The overall seroprevalence was 3.19% (3198/100,282) (Table 1). The higher seroprevalences were mainly located in western parts of China. The highest seroprevalence (8.43%) was located in Yunnan Province, followed by Inner Mongolia (6.37%) and Sichuan (5.35%), and the lowest was in Liaoning (0.26%). Trichinella infection was observed in all age groups, but seroprevalence tended to increase with age ranging from 1.97% in children under 10 years of age to 3.81% in those between 30- and 40-year olds.
3. Outbreaks of human trichinellosis
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Table 2 Outbreaks of human trichinellosis in the Provinces/Municipalities (P/M) of China during 2004–2009. P/M
Area
Time of outbreaks
No. of outbreaks
No. of cases
No. of deaths
Source of outbreak
References
Yunnan
Dali
Feb. 2004
1
132
0
Raw pork
Wang and Li (2007)
Jan.–Feb. 2005
2
118
0
Raw pork
Wang and Liu (2006)
Feb. 2006
1
103
0
Raw pork
Wang et al. (2006a,b) Ke et al. (2007)
May 2007
1
841
0
Raw pork
Ma (2008)
Jan. 2006
1
56
0
Raw pork
Feng and Wang (2009)
Jan. 2007
1
49
0
?
Yao (2008)
Xishuangbanna
Apr. 2008
1
26
0
Raw wild boar
Wang et al. (2009)
Nujiang
Feb. 2009
1
9
1
Gangzhi
2006a
1
3
1
Semi-cooked pork Raw pork
www.yn.xinhuanet.com/ newscenter/2009-03/05 Zheng et al. (2008)
2006a
1
22
0
Raw wild boar
Zheng et al. (2008)
a
2006
1
5
0
Raw pork
Yang (2006)
May 2007
1
9
2
Gong et al. (2008)
Feb. 2008
1
12
0
Feb. 2009
1
2
0
Raw and semi-cooked pork Raw and semi-cooked pork Raw pork
15
1387
4
Puer
Sichuan
Tibet
Total a
Linzhi
Wang et al. (2008)
Ci et al. (2009)
Month of outbreak is not recorded in original report.
4. Source of infection for outbreak of trichinellosis As shown in Table 2, pork is still the predominant source of infection of outbreaks of human trichinellosis in China. Out of 15 outbreaks, 12 (85.71%) were caused by eating raw or undercooked pork and 2 (13.33%) resulted from the consumption of raw wild boar. (The source of an imported outbreak could not be identified.) The Bai ethnic minority inhabitants in Dali prefecture of Yunnan Province eat raw meat and usually add condiments (salt, oil, vinegar, ginger, soy, etc.) into the raw pork to prepare salted, fermented pork or toasted swine skin. The largest trichinellosis outbreak occurred in Dali (the Bai minor ethnic area) of Yunnan Province in May of 2007 and was caused by eating raw skin (roast pig leg, cooked until the skin color changes to yellow with the meat under the skin still raw). The inhabitants slaughtered the selfraised swine at home without veterinary inspection and invited the villagers to dinner containing raw pork. These events caused an outbreak involving 841 cases (Ma, 2008). A trichinellosis outbreak associated with wild boar occurred in Batang county in the Ganzhi prefecture of Sichuan Province in 2006. The wild boar were illegally captured by the local villagers and clandestinely slaughtered. Twenty-two people were infected with Trichinella after eating the boar (Zheng et al., 2008). Another outbreak of trichinellosis resulting from the consumption of wild boar occurred in Xishuangbanna of Yunnan in April 2008. After two wild boars were captured, the boar meat was prepared as “chop raw” (in which the boar is broken into small pieces) and distributed to the villagers as gifts. This led to an outbreak of 26 cases (Wang et al., 2009). 5. Outbreak of imported trichinellosis in Yunnan from Laos A group of Puer city (Yunnan Province) government officials visited in Laos during 15–23 December 2006. The group was con-
sisted of 57 officers, actors, traders, drivers, security guards and doctors. Out of the 57 visitors, 49 developed symptoms of acute trichinellosis 15–20 days after returning to Puer city from Laos. The main clinical manifestations of the 49 cases were fevers of 38–40 ◦ C (49 cases), gastrointestinal symptoms (10 cases), facial and/or general edema (32 cases), general myalgia (42 cases), skin rash (28 cases), hematuria (24 cases), myocarditis (14 cases) and lobular pneumonia (27 cases). All patients developed eosinophilia and serum anti-Trichinella IgG antibody titers were positive by ELISA. The encapsulated Trichinella larvae were observed in five cases by microscopic examination of muscle biopsies. All 49 patients were cured with a 7-day course of albendazole (20 mg/kg/d) plus dexamethasone (10 mg/d) (Yao, 2008). During the visit, the group ate raw and poorly cooked meat but the exact source of the infection could not be identified. To our knowledge, this is the first reported outbreak of imported trichinellosis in China.
6. Discussion The higher seroprevalences of human Trichinella infection continue to be located mainly in western China (Yunnan, Inner Mongolia and Sichuan), especially in ethnic minority regions. The seroprevalence tended to increase with age could be related with the accumulation of recurrent Trichinella infection or seropositivity in the population due to long lasting antibody production in humans, since anti-Trichinella antibodies may remain positive for many years and even up to 19 years after the end of the acute phase of human Trichinella infection (Harms et al., 1993; Pozio et al., 1993). Seroprevalence was related to the habit of eating raw meat in some ethnic minorities. Foods and preparation methods of some minor ethnic groups in western China are associated with Trichinella infection, including: (1) raw skin, (2) chop raw, (3) cross bridge rice line
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(raw pork mixed with noodles and scalded for 1–3 min, which is inadequate heating time for large cubes of meat), and (4) acidic meat (fermented raw pork) (Dong et al., 2006). Another important mode of human Trichinella infection in China is when the same knife and tableware set is used for both cooked food and raw meat. Most households, and even some small restaurants, have one set of tableware, one knife and one chopping board, that are used for both cooked and raw food. Out of 15 outbreaks in this paper, 2 (1 with 56 cases and another with 9 cases) were caused by eating raw vegetables contained within raw pork (Feng and Wang, 2009; www.yn.xinhuanet.com/newscenter/200903/05/content15869299.htm). Along with the development of tourism, some ethnic restaurants serve special food, such as “acidic meat” to attract the customers, resulting in an increase of infected persons and local outbreaks of trichinellosis (Cui et al., 2006a,b). Between 2004 and 2009, all 15 outbreaks of human trichinellosis, with 1387 cases and four deaths, occurred in southwestern China where the ethnic groups which eat raw or lightly processed meat are predominantly distributed. Out of 15 outbreaks, 12 (85.71%) were caused by eating raw or undercooked pork, the predominant source of outbreaks of human trichinellosis in China. The higher incidence of trichinellosis around the New Year is believed to result from local inhabitants slaughtering pigs and preparing food containing raw pork for celebrations such as New Year’s Day and the Tibetan Spring Festival. Trichinellosis often correlated with groups taking part in various parties during winter festivals (Wang et al., 1998). At present, swine trichinellosis in China still is mainly transmitted by garbage (i.e., feeding pigs with swills containing raw pork scraps). In some rural and mountainous areas of southwestern China, pigs are raised in backyards under poor hygienic condition or in open areas where they feed on raw waste products or animal carcasses and are exposed to rodents and wildlife (Cui et al., 2006a,b). The appearance of ecological (organic or green) pig farms, where pigs were fed outdoors and pastured freely, may increase the risk of transmission of Trichinlla from wildlife to domestic swine (Murrell and Pozio, 2000). Although a policy that pigs must be collectively slaughtered and quarantined for trichinellosis in the appointed public abattoirs was established in China in 1996, some pigs were clandestinely slaughtered at home in rural and mountainous areas of southwestern China without veterinary inspection. The mandatory inspection of pork should be further strengthened in these areas. The first outbreak caused by eating game (raw bear meat), consisting of 70 cases and three deaths, occurred in Heshui county of Sichuan Province in December 1968. Another outbreak caused by raw bear meat occurred in the same county, which led to 58 cases and 1 death in 1972 (Wang and Luo, 1981). Since the 1970s, the fauna of wild animals decreased sharply due to an increase in the human population and deforestation. No outbreak of trichinellosis resulting from the consumption of game took place in Sichuan Province during 1973–1992. However, from the 1990s to the present, the increase in fallow land and returning land for forestry have led to an increase in wildlife populations in some mountainous areas and highlands in southwestern China, including Sichuan, Chongqing, Yunnan and Tibet (Cui and Wang, 2003). Furthermore, some farmers in mountainous areas of southwestern China have recently begun to domesticate wild boar which were fed with domestic pigs in pig farms, increasing the risk of direct transmission of Trichinella from boar to domestic pigs possibly due to tail or ear bites or to eating boar carcasses that are not promptly removed from the herd (Pozio, 2001). In addition, wildlife in China is protected by the law and hunting is prohibited. Illegal hunting has resulted in wild boars and bears being killed by poachers. It is likely that the poached wild boars and bears are not examined for Trichinella and such game meat is another source of outbreaks.
Three outbreaks of trichinellosis caused by eating wild boar, with 48 cases and three deaths, have been registered in Sichuan during 1993–2006 (Ye et al., 2003; Zheng et al., 2008). Because hunting is illegal in China, patients usually deny their history of eating game and are often misdiagnosed with other diseases. For example, one male Tibetan patient from Litang county of Sichuan poached a wild boar and ate boar meat on 25 September 2005, developed disease on 30 September, and was admitted to hospital with fever, muscle pain, and general edema on 25 November. The patient and family members repeatedly denied the history of eating wild boar as they were afraid of being punished for poaching by the government. He did not confess to eating wild boar until Trichinella larvae were observed by muscle biopsies on 3 December (Zheng et al., 2007b). Although the outbreaks of trichinellosis in China are mainly associated with consumption of raw or improperly cooked pork, outbreaks involving wild game meat emphasize the significance of game as source for human trichinellosis. The outbreak of trichinellosis involving 49 cases in Yunnan during December 2006 is the first recorded outbreak of imported trichinellosis in China from Laos on the Yunnan border. In recent years, two outbreaks of trichinellosis occurred in central Laos in 2003 (22 cases) and in northern Laos in 2005 (650 cases) (Sayasone et al., 2006; Barennes et al., 2008). Consumption of uncooked or fermented pork at funeral and wedding ceremonies was the main source of infection. Similar to Yunnan, the major source of infection in Laos is due to local inhabitants eating raw pork. Therefore, it is speculated that the outbreak of imported trichinellosis in Yunnan was likely caused by the consumption of raw or uncooked pork. In another of China’s neighboring countries, Korea, two outbreaks of trichinellosis have been recorded since 2000 (Sohn et al., 2000, 2003). On 9 February 2007, a Korean inhabitant with seven dog carcasses arrived in the JiAn port located between Jilin Province of China and Korea, and Trichinella larvae were observed in two (28.5%) of the carcasses by microscopy (Wu et al., 2008). Korean inhabitants in northeastern China eat raw or scalded dog meat, and from 1974 to 2003, nine outbreaks of human trichinellosis associated with dog meat occurred in this area (Cui and Wang, 2001; Wang et al., 2006a,b). Hence, the introduction of Trichinellainfected dog meat would add a new origin of infection. Because human trichinellosis is relatively rare in areas of low endemicity, local physicians are unfamiliar with its symptoms and signs and consequently misdiagnosis is likely. The number of travelers going abroad will be increased along with the increase of inhabitants’ income and development of tourism. Hence, residents and travelers need to be educated about cooking all pork and game adequately. Proper food preparation steps should be taken to prevent from the infection. Pork must be heated to at least 70 ◦ C in the center of meat, which is above the death point for Trichinella larvae (Gamble et al., 2000). In addition, the inspection for Trichinella larvae in meat products imported, mailed, or brought back by travelers from endemic areas should be further strengthened at port. Acknowledgements This work was supported by the National Basic Research Program of China (no. 2010CB530000), the National Natural Science Foundation of China (no. 30972492) and the Major Public Research Project of Henan Province (no. 2008-145). References Barennes, H., Sayasone, S., Odermatt, P., De Bruyne, A., Hongsakhone, S., Newton, P.N., Vongphrachanh, P., Martinez-Aussel, B., Strobel, M., Dupouy-Camet, J., 2008. A major trichinellosis outbreak suggesting a high endemicity of Trichinella infection in northern Laos. Am. J. Trop. Med. Hyg. 78, 40–44. Chen, G.Y., Zhang, H.X., Chen, J.S., Yu, P.H., Huang, G.Q., Pei, S.J., Gui, A.F., Zuo, S.L., Yuan, F.Y., 2006. Analysis on seroepidemiological investigation of human trichinellosis in Hubei Province. J. Pub. Health Prev. Med. 17, 39–40.
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Review
The epidemiology of human trichinellosis in China during 2004–2009 J. Cui a , Z.Q. Wang a,∗ , B.L. Xu b a b
Department of Parasitology, Medical College, Zhengzhou University, Zhengzhou 450052, PR China Center for Disease Control of Henan Province, Zhengzhou 450003, PR China
a r t i c l e
i n f o
Article history: Received 21 July 2010 Received in revised form 3 February 2011 Accepted 7 February 2011 Available online 13 February 2011 Keywords: Trichinellosis Epidemiology Seroprevalence Outbreak China
a b s t r a c t The endemic foci of human trichinellosis are mainly located in southwestern China. Seroepidemiological surveys of Trichinella spiralis infection in humans were carried out in 10 out of 34 Provinces/Autonomous Regions/Municipals (P/A/M) of China during 2004–2009. The overall seroprevalence was 3.19% (3198/100,282). The highest seroprevalences were mainly located in western China: 8.43% in Yunnan, 6.37% in Inner Mongolia and 5.35% in Sichuan. The seroprevalence of Trichinella infection in humans was related to the habit of eating meat and differed among nationalities. From 2004 to 2009, 15 outbreaks of human trichinellosis, consisting of 1387 cases and four deaths, were reported in the three southwesternmost P/A of China (nine outbreaks in Yunnan, two in Sichuan and four in Tibet), where ethnic groups routinely eat raw meat. Pork is the predominant source of outbreaks of human trichinellosis in China. Out of 15 outbreaks, 12 (85.71%) were caused by eating raw or undercooked pork, and 2 (13.33%) resulted from the consumption of raw wild boar, suggesting the significance of game meat as a source of infection for human trichinellosis. An outbreak of imported trichinellosis involving 49 cases in Yunnan during December 2006 from Laos is the first recorded outbreak of imported trichinellosis in China, but the source of that outbreak could not be identified. The mandatory inspection of pork should be further strengthened in southwestern China. Crown Copyright © 2011 Published by Elsevier B.V. All rights reserved.
Contents 1. 2. 3. 4. 5. 6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Seroprevalence of human trichinellosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Outbreaks of human trichinellosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Source of infection for outbreak of trichinellosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Outbreak of imported trichinellosis in Yunnan from Laos . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction Trichinellosis, a food-borne parasitic zoonosis, is caused by the tissue-dwelling nematode Trichinella. Humans acquire the disease by ingesting raw or insufficiently cooked meat of pigs or other animals containing the Trichinella larvae. The adult worms live in the duodenal and jejunal mucosa of flesh-eating animals and humans, while the larvae live in skeletal muscles of the same hosts. The clinical manifestations of trichinellosis can be divided into two phases: an enteral phase and a muscular (parenteral or
∗ Corresponding author. Tel.: +86 371 66181026; fax: +86 371 66997182. E-mail addresses: [email protected] (J. Cui), [email protected] (Z.Q. Wang).
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acute) phase, which can coexist for a period lasting from a few days to weeks. The hallmark of the intestinal phase is a nonspecific gastroenteritis. One or 2 days after ingesting the tainted meat, the newly matured adults penetrate the intestinal mucosa, resulting in nausea, abdominal pain, diarrhea, and vomiting. The muscular phase is associated with an inflammatory and allergic response to muscle invasion by the migrating larvae. Fever, eyelid or facial edema, myalgia, and eosinophilia are the most prominent manifestations (Pozio et al., 2003). Trichinellosis remains an important zoonotic disease worldwide. Of all of the countries of the world, Trichinella spp. infection has been documented in domestic animals (mainly pigs) and wildlife in 43 (21.9%) and 66 (33.3%) countries, respectively. Human trichinellosis has been documented in 55 (27.8%) countries
0001-706X/$ – see front matter. Crown Copyright © 2011 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.actatropica.2011.02.005
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J. Cui et al. / Acta Tropica 118 (2011) 1–5
Table 1 Seroprevalence of human infection with Trichinella spiralis in China during 2004–2009. Location Beijing Gongxi Heilongjiang Henan Hubei Inner Mongolia Jilin Liaoning Sichuan Yunnan Total
No. examined
No. positive
Positive rate (%)
Reference Jia et al. (2006) Yang et al. (2007) Ge et al. (2005) Xu et al. (2009) Chen et al. (2006) Song et al. (2007) Xu et al. (2009) Xu et al. (2009) Zheng et al. (2005) Wang et al. (2005)
12,064 9638 9960 10,102 9939 9956 10,006 10,092 8416 10,109
140 319 130 300 251 634 96 26 450 852
1.16 3.31 1.31 2.97 2.53 6.37 0.96 0.26 5.35 8.43
100,282
3198
3.19
around the world (Pozio, 2007). Most outbreaks of trichinellosis are related to the consumption of raw pork containing Trichinella spiralis larvae (Dupouy-Camet, 2009). Human cases of trichinellosis have been recorded in 17 out of 34 Provinces/Autonomous Regions/Municipals (P/A/M) of China since the first Chinese case was reported in Xizang (Tibet) in 1965. From 1964 to 1999, 548 outbreaks of trichinellosis, consisting of 23,004 cases and 236 deaths, occurred in 12 P/A/M of China (Wang and Cui, 2001). During 2000–2003, 17 outbreaks of human trichinellosis, consisting of 828 cases and 11 deaths, were recorded in 8 P/A of China. All 11 deaths occurred in southwestern China, where ethnic groups routinely eat raw meat (Wang et al., 2006a,b). Out of 565 outbreaks, 538 (95.22%) outbreaks were due to consumption of raw or poorly cooked pork, and pork is the predominant source of outbreaks of human trichinellosis in China. If uncontrolled, this zoonotic parasitosis could pose exceptional problems because China is the largest pork-producing country in the world. In fact, pork produced in China in 2008 accounted for 46% of the total pork output worldwide (http://www.21food.cn/html/news/35/509789.htm). Over the past 6 years, Chinese parasitologists have produced a number of reports regarding the epidemiology of human trichinellosis. Therefore, to clarify the nationwide status of human Trichinella infection in China, Chinese publications on human trichinellosis epidemiology in China since 2004 were collected and analyzed.
The seroprevalence of Trichinella infection in humans was related to the habit of eating meat and differed by nationality. In minor ethnic regions (Longchuang and Lianghe counties) of Yunnan Province, the seropositive rate of Trichinella infection in the Thais (one of the Chinese minor ethnic groups) is 16.72% (336/2009) and was statistically higher than the mean seropositive rate of 8.43% (852/10, 109) in this province (P < 0.01). The seroprevalence of the inhabitants who frequently ate raw pork (41.96%) was higher than those who did not (4.17%) (P < 0.01). The seroprevalence of the households using one set of knife and tableware for cooked food and raw meat was higher than that of those using two dinner sets (28.89% vs. 15.21%, respectively; P < 0.01) (Dong et al., 2005). In Danba county (the Tibetan ethnic minority region) of Sichuan Province, the seroprevalence of the Tibetans was 21.94% (111/506), which was higher than the provincial mean seropositive rate of 5.35% (450/8416) (P < 0.01). Out of the Tibetans with seropositivity, 98.2% had a history of eating raw or semi-cooked meat (such as pork, wild boar and bear). In addition, the seroprevalence of Trichinella infection in humans was different among occupations: the highest (93.69%) was observed in the farmers and herdsmen, followed by officers (4.51%) and students (1.80%) (Zheng et al., 2007a).
2. Seroprevalence of human trichinellosis
From 2004 to 2009, 15 outbreaks of human trichinellosis, consisting of 1387 cases and 4 deaths, were reported in three P/A of China (9 outbreaks in Yunnan, 2 in Sichuan and 4 in Tibet) (Table 2). Over the past 6 years, all epidemic foci of human trichinellosis outbreaks were located in southwestern China where the ethnic groups which eat raw meat are predominantly distributed. All four deaths occurred in southwestern China (one case in Yunnan, one case in Sichuan and two cases in Tibet). The occurrence of human trichinellosis during 2004–2009 had a clear seasonal variation, with outbreaks mainly occurring in winter. Out of 12 outbreaks with clear dates of onset of the diseases, 9 outbreaks occurred during January–February and 3 outbreaks occurred during April–May. At the present time, human trichinellosis is not a nationally reportable disease. The national trichinellosis surveillance system has not yet been established in China, and the reports on outbreaks of human trichinellosis are voluntary, relying on physicians, parasitologists or epidemiologists. This often results in fragmentary information. Thus, the data obtained from the papers published could merely be the tip of the iceberg. Additionally, because adequate diagnostic tools are not widely available, many patients with trichinellosis, especially those with light or atypical symptoms, are often undiagnosed or misdiagnosed as other diseases in rural clinics or town hospitals.
Seroepidemiological surveys of Trichinella infection in humans were carried out in 10 P/A/M of China during 2004–2009. The sites and population of surveys were sampled with the cluster random sampling method. A total of about 100,000 inhabitants from 200 sites (160 rural and 40 urban sites) in 80 counties/cities/districts of 10 P/A/M were selected. Specific anti-Trichinella antibodies (IgG) were determined by an ELISA kit using the excretory–secretory (ES) antigens of T. spiralis muscle larvae (Zhuhai Haitai Biological Pharmaceuticals Co. Ltd., China). Test sera/control sera OD values of less than 2.1 were regarded as negative, whereas those of 2.1 or greater were considered positive. The validation of ELISA and all seropositive samples were conducted by the Specialist Committee on Parasitic Diseases of Health Ministry of China (Wang, 2008). The overall seroprevalence was 3.19% (3198/100,282) (Table 1). The higher seroprevalences were mainly located in western parts of China. The highest seroprevalence (8.43%) was located in Yunnan Province, followed by Inner Mongolia (6.37%) and Sichuan (5.35%), and the lowest was in Liaoning (0.26%). Trichinella infection was observed in all age groups, but seroprevalence tended to increase with age ranging from 1.97% in children under 10 years of age to 3.81% in those between 30- and 40-year olds.
3. Outbreaks of human trichinellosis
J. Cui et al. / Acta Tropica 118 (2011) 1–5
3
Table 2 Outbreaks of human trichinellosis in the Provinces/Municipalities (P/M) of China during 2004–2009. P/M
Area
Time of outbreaks
No. of outbreaks
No. of cases
No. of deaths
Source of outbreak
References
Yunnan
Dali
Feb. 2004
1
132
0
Raw pork
Wang and Li (2007)
Jan.–Feb. 2005
2
118
0
Raw pork
Wang and Liu (2006)
Feb. 2006
1
103
0
Raw pork
Wang et al. (2006a,b) Ke et al. (2007)
May 2007
1
841
0
Raw pork
Ma (2008)
Jan. 2006
1
56
0
Raw pork
Feng and Wang (2009)
Jan. 2007
1
49
0
?
Yao (2008)
Xishuangbanna
Apr. 2008
1
26
0
Raw wild boar
Wang et al. (2009)
Nujiang
Feb. 2009
1
9
1
Gangzhi
2006a
1
3
1
Semi-cooked pork Raw pork
www.yn.xinhuanet.com/ newscenter/2009-03/05 Zheng et al. (2008)
2006a
1
22
0
Raw wild boar
Zheng et al. (2008)
a
2006
1
5
0
Raw pork
Yang (2006)
May 2007
1
9
2
Gong et al. (2008)
Feb. 2008
1
12
0
Feb. 2009
1
2
0
Raw and semi-cooked pork Raw and semi-cooked pork Raw pork
15
1387
4
Puer
Sichuan
Tibet
Total a
Linzhi
Wang et al. (2008)
Ci et al. (2009)
Month of outbreak is not recorded in original report.
4. Source of infection for outbreak of trichinellosis As shown in Table 2, pork is still the predominant source of infection of outbreaks of human trichinellosis in China. Out of 15 outbreaks, 12 (85.71%) were caused by eating raw or undercooked pork and 2 (13.33%) resulted from the consumption of raw wild boar. (The source of an imported outbreak could not be identified.) The Bai ethnic minority inhabitants in Dali prefecture of Yunnan Province eat raw meat and usually add condiments (salt, oil, vinegar, ginger, soy, etc.) into the raw pork to prepare salted, fermented pork or toasted swine skin. The largest trichinellosis outbreak occurred in Dali (the Bai minor ethnic area) of Yunnan Province in May of 2007 and was caused by eating raw skin (roast pig leg, cooked until the skin color changes to yellow with the meat under the skin still raw). The inhabitants slaughtered the selfraised swine at home without veterinary inspection and invited the villagers to dinner containing raw pork. These events caused an outbreak involving 841 cases (Ma, 2008). A trichinellosis outbreak associated with wild boar occurred in Batang county in the Ganzhi prefecture of Sichuan Province in 2006. The wild boar were illegally captured by the local villagers and clandestinely slaughtered. Twenty-two people were infected with Trichinella after eating the boar (Zheng et al., 2008). Another outbreak of trichinellosis resulting from the consumption of wild boar occurred in Xishuangbanna of Yunnan in April 2008. After two wild boars were captured, the boar meat was prepared as “chop raw” (in which the boar is broken into small pieces) and distributed to the villagers as gifts. This led to an outbreak of 26 cases (Wang et al., 2009). 5. Outbreak of imported trichinellosis in Yunnan from Laos A group of Puer city (Yunnan Province) government officials visited in Laos during 15–23 December 2006. The group was con-
sisted of 57 officers, actors, traders, drivers, security guards and doctors. Out of the 57 visitors, 49 developed symptoms of acute trichinellosis 15–20 days after returning to Puer city from Laos. The main clinical manifestations of the 49 cases were fevers of 38–40 ◦ C (49 cases), gastrointestinal symptoms (10 cases), facial and/or general edema (32 cases), general myalgia (42 cases), skin rash (28 cases), hematuria (24 cases), myocarditis (14 cases) and lobular pneumonia (27 cases). All patients developed eosinophilia and serum anti-Trichinella IgG antibody titers were positive by ELISA. The encapsulated Trichinella larvae were observed in five cases by microscopic examination of muscle biopsies. All 49 patients were cured with a 7-day course of albendazole (20 mg/kg/d) plus dexamethasone (10 mg/d) (Yao, 2008). During the visit, the group ate raw and poorly cooked meat but the exact source of the infection could not be identified. To our knowledge, this is the first reported outbreak of imported trichinellosis in China.
6. Discussion The higher seroprevalences of human Trichinella infection continue to be located mainly in western China (Yunnan, Inner Mongolia and Sichuan), especially in ethnic minority regions. The seroprevalence tended to increase with age could be related with the accumulation of recurrent Trichinella infection or seropositivity in the population due to long lasting antibody production in humans, since anti-Trichinella antibodies may remain positive for many years and even up to 19 years after the end of the acute phase of human Trichinella infection (Harms et al., 1993; Pozio et al., 1993). Seroprevalence was related to the habit of eating raw meat in some ethnic minorities. Foods and preparation methods of some minor ethnic groups in western China are associated with Trichinella infection, including: (1) raw skin, (2) chop raw, (3) cross bridge rice line
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(raw pork mixed with noodles and scalded for 1–3 min, which is inadequate heating time for large cubes of meat), and (4) acidic meat (fermented raw pork) (Dong et al., 2006). Another important mode of human Trichinella infection in China is when the same knife and tableware set is used for both cooked food and raw meat. Most households, and even some small restaurants, have one set of tableware, one knife and one chopping board, that are used for both cooked and raw food. Out of 15 outbreaks in this paper, 2 (1 with 56 cases and another with 9 cases) were caused by eating raw vegetables contained within raw pork (Feng and Wang, 2009; www.yn.xinhuanet.com/newscenter/200903/05/content15869299.htm). Along with the development of tourism, some ethnic restaurants serve special food, such as “acidic meat” to attract the customers, resulting in an increase of infected persons and local outbreaks of trichinellosis (Cui et al., 2006a,b). Between 2004 and 2009, all 15 outbreaks of human trichinellosis, with 1387 cases and four deaths, occurred in southwestern China where the ethnic groups which eat raw or lightly processed meat are predominantly distributed. Out of 15 outbreaks, 12 (85.71%) were caused by eating raw or undercooked pork, the predominant source of outbreaks of human trichinellosis in China. The higher incidence of trichinellosis around the New Year is believed to result from local inhabitants slaughtering pigs and preparing food containing raw pork for celebrations such as New Year’s Day and the Tibetan Spring Festival. Trichinellosis often correlated with groups taking part in various parties during winter festivals (Wang et al., 1998). At present, swine trichinellosis in China still is mainly transmitted by garbage (i.e., feeding pigs with swills containing raw pork scraps). In some rural and mountainous areas of southwestern China, pigs are raised in backyards under poor hygienic condition or in open areas where they feed on raw waste products or animal carcasses and are exposed to rodents and wildlife (Cui et al., 2006a,b). The appearance of ecological (organic or green) pig farms, where pigs were fed outdoors and pastured freely, may increase the risk of transmission of Trichinlla from wildlife to domestic swine (Murrell and Pozio, 2000). Although a policy that pigs must be collectively slaughtered and quarantined for trichinellosis in the appointed public abattoirs was established in China in 1996, some pigs were clandestinely slaughtered at home in rural and mountainous areas of southwestern China without veterinary inspection. The mandatory inspection of pork should be further strengthened in these areas. The first outbreak caused by eating game (raw bear meat), consisting of 70 cases and three deaths, occurred in Heshui county of Sichuan Province in December 1968. Another outbreak caused by raw bear meat occurred in the same county, which led to 58 cases and 1 death in 1972 (Wang and Luo, 1981). Since the 1970s, the fauna of wild animals decreased sharply due to an increase in the human population and deforestation. No outbreak of trichinellosis resulting from the consumption of game took place in Sichuan Province during 1973–1992. However, from the 1990s to the present, the increase in fallow land and returning land for forestry have led to an increase in wildlife populations in some mountainous areas and highlands in southwestern China, including Sichuan, Chongqing, Yunnan and Tibet (Cui and Wang, 2003). Furthermore, some farmers in mountainous areas of southwestern China have recently begun to domesticate wild boar which were fed with domestic pigs in pig farms, increasing the risk of direct transmission of Trichinella from boar to domestic pigs possibly due to tail or ear bites or to eating boar carcasses that are not promptly removed from the herd (Pozio, 2001). In addition, wildlife in China is protected by the law and hunting is prohibited. Illegal hunting has resulted in wild boars and bears being killed by poachers. It is likely that the poached wild boars and bears are not examined for Trichinella and such game meat is another source of outbreaks.
Three outbreaks of trichinellosis caused by eating wild boar, with 48 cases and three deaths, have been registered in Sichuan during 1993–2006 (Ye et al., 2003; Zheng et al., 2008). Because hunting is illegal in China, patients usually deny their history of eating game and are often misdiagnosed with other diseases. For example, one male Tibetan patient from Litang county of Sichuan poached a wild boar and ate boar meat on 25 September 2005, developed disease on 30 September, and was admitted to hospital with fever, muscle pain, and general edema on 25 November. The patient and family members repeatedly denied the history of eating wild boar as they were afraid of being punished for poaching by the government. He did not confess to eating wild boar until Trichinella larvae were observed by muscle biopsies on 3 December (Zheng et al., 2007b). Although the outbreaks of trichinellosis in China are mainly associated with consumption of raw or improperly cooked pork, outbreaks involving wild game meat emphasize the significance of game as source for human trichinellosis. The outbreak of trichinellosis involving 49 cases in Yunnan during December 2006 is the first recorded outbreak of imported trichinellosis in China from Laos on the Yunnan border. In recent years, two outbreaks of trichinellosis occurred in central Laos in 2003 (22 cases) and in northern Laos in 2005 (650 cases) (Sayasone et al., 2006; Barennes et al., 2008). Consumption of uncooked or fermented pork at funeral and wedding ceremonies was the main source of infection. Similar to Yunnan, the major source of infection in Laos is due to local inhabitants eating raw pork. Therefore, it is speculated that the outbreak of imported trichinellosis in Yunnan was likely caused by the consumption of raw or uncooked pork. In another of China’s neighboring countries, Korea, two outbreaks of trichinellosis have been recorded since 2000 (Sohn et al., 2000, 2003). On 9 February 2007, a Korean inhabitant with seven dog carcasses arrived in the JiAn port located between Jilin Province of China and Korea, and Trichinella larvae were observed in two (28.5%) of the carcasses by microscopy (Wu et al., 2008). Korean inhabitants in northeastern China eat raw or scalded dog meat, and from 1974 to 2003, nine outbreaks of human trichinellosis associated with dog meat occurred in this area (Cui and Wang, 2001; Wang et al., 2006a,b). Hence, the introduction of Trichinellainfected dog meat would add a new origin of infection. Because human trichinellosis is relatively rare in areas of low endemicity, local physicians are unfamiliar with its symptoms and signs and consequently misdiagnosis is likely. The number of travelers going abroad will be increased along with the increase of inhabitants’ income and development of tourism. Hence, residents and travelers need to be educated about cooking all pork and game adequately. Proper food preparation steps should be taken to prevent from the infection. Pork must be heated to at least 70 ◦ C in the center of meat, which is above the death point for Trichinella larvae (Gamble et al., 2000). In addition, the inspection for Trichinella larvae in meat products imported, mailed, or brought back by travelers from endemic areas should be further strengthened at port. Acknowledgements This work was supported by the National Basic Research Program of China (no. 2010CB530000), the National Natural Science Foundation of China (no. 30972492) and the Major Public Research Project of Henan Province (no. 2008-145). References Barennes, H., Sayasone, S., Odermatt, P., De Bruyne, A., Hongsakhone, S., Newton, P.N., Vongphrachanh, P., Martinez-Aussel, B., Strobel, M., Dupouy-Camet, J., 2008. A major trichinellosis outbreak suggesting a high endemicity of Trichinella infection in northern Laos. Am. J. Trop. Med. Hyg. 78, 40–44. Chen, G.Y., Zhang, H.X., Chen, J.S., Yu, P.H., Huang, G.Q., Pei, S.J., Gui, A.F., Zuo, S.L., Yuan, F.Y., 2006. Analysis on seroepidemiological investigation of human trichinellosis in Hubei Province. J. Pub. Health Prev. Med. 17, 39–40.
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