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Review

Food-borne parasitic zoonoses in


China: perspective for control
Peng Zhou1*, Ning Chen1*, Ren-Li Zhang2, Rui-Qing Lin1 and Xing-Quan Zhu1
1
Department of Parasitology, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Street, Tianhe
District, Guangzhou 510642, Guangdong Province, The People’s Republic of China
2
Laboratory of Molecular Biology, Shenzhen Center for Disease Control and Prevention, 21 Tian Bai No. 1 Street, Shenzhen 518020,
Guangdong Province, The People’s Republic of China

Food-borne parasitic zoonoses (FBPZs) cause death and re-emerging in some areas of China, such as Qinghai
serious diseases in humans and animals worldwide, and Province, because of the ‘Western Development Project’
are of both public health significance and socioeconomic and the developing tourist industry [15].
importance. The FBPZ problem is severe in mainland Infected pork is the main source of human infection with
China, where 150 million people are suffering from T. spiralis, and dog meat is the source of human infection
FBPZs and more people are at risk. Here, the current with T. nativa [16]. The prevalence of Trichinella in pigs
status of the FBPZ problem in mainland China is and dogs is still high in some provinces (Table 1).
reviewed and strategies and measures for effective con-
trol of FBPZs are proposed. Major parasitic zoonoses Cysticercosis and taeniasis
transmitted through consumption of infected or con- Human and pig cysticercosis is caused by Taenia solium
taminated meat, fish, plants and/or water will be dis- larvae when T. solium eggs that are released from infected
cussed. patients are accidentally ingested. Cysticercosis has been
established in 29 provinces [7,8] (Table 1). In the Yunnan,
Significance of food-borne parasitic zoonoses Guizhou and Sichuan provinces, several minorities prefer
Food-borne parasitic zoonoses (FBPZs) are human and to eat raw pork and, hence, are at high risk of developing
animal diseases caused by helminths and protozoans cysticercosis [17]. For instance, the mean prevalence of
through the consumption of infected or contaminated cysticercosis in the Bai and Miao minorities is 2.7% and
meat, fish, plants and/or water; they pose significant public 1.1%, respectively [8].
health and socioeconomic problems [1–4]. An example of In China, human taeniasis is caused by the tapeworms
the FBPZ problem is the continuing prevalence of human T. solium, Taenia saginata and Taenia asiatica [8,18]. It is
and animal trichinellosis in many countries [5]. Cysticer- estimated that 550 000 people are infected nationwide [8].
cosis and echinococcosis also cause human death and Human infection with T. asiatica is endemic in Duyun,
suffering in many countries, as well as considerable Guizhou Province [19] and Lanping, Yunnan Province [20].
economic losses in the meat industry [2]. The problem is Swine cysticercosis is prevalent in all of the 31 mainland
particularly severe in mainland China, where FBPZs cause provinces [17,21] (Table 1).
considerable socioeconomic and public health problems [6–
10]. There have been several review articles on FBPZs in Toxoplasmosis
general [2–4], on a particular FBPZ [11,12] or focusing on Human infection with Toxoplasma gondii has been
the FBPZ problem in particular countries [13], but there reported in each mainland province, with a mean infection
has been no previously published overview on FBPZs in rate of 7.9% nationwide, as revealed by ELISA [8] (Table 1).
mainland China in the English literature. The Guizhou, Guangxi and Jiangxi provinces have higher
prevalence rates [8]. Prevalence in these provinces has
Meat-borne parasitic zoonoses increased sharply in comparison with the prevalence
Trichinellosis shown in the first national survey [6]. Many animal species
Human trichinellosis in mainland China is caused by are infected with T. gondii in all mainland provinces
Trichinella spiralis and Trichinella nativa, and infection (Table 1). For example, as the definitive host for T. gondii,
occurs through the consumption of raw or undercooked cats have a prevalence of up to 79.4% [22]. Genotyping T.
meat [14–16]. The recent national serological survey con- gondii isolates from cats in Guangzhou, Guangdong Pro-
ducted by using ELISA (enzyme-linked immunosorbent vince identified two genotypes, which are different from the
assay) in ten endemic provinces estimated a mean preva- Type I, II and III lineages that predominate in North
lence of 3.3% [8] (Table 1). Human trichinellosis is extre- America and Europe [22].
mely serious in several provinces, in particular in Yunnan
and Inner Mongolia where it has a mean prevalence of Echinococcosis
8.3% and 6.3%, respectively [8]. In fact, trichinellosis is Echinococcosis, including cystic echinococcosis caused by
the cestode Echinococcus granulosus and alveolar echino-
Corresponding author: Zhu, X.-Q. (xingquanzh@scau.edu.cn). coccosis caused by Echinococcus multilocularis, is regarded
*
Authors contributed equally to this publication. as one of the most serious parasitic zoonoses in China
190 1471-4922/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.pt.2008.01.001 Available online 7 March 2008
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Review
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Table 1. The prevalence of major food-borne parasitic zoonoses (FBPZs) in mainland China
Disease Parasite Definitive host Intermediate host Prevalence, and people infected Prevalence in animal Refs
Trichinellosis Trichinella spiralis Humans and other Not applicable 3.3% in ten endemic provinces; Pig: 6.7% in Hubei, 4.3% in Henan provinces; [8,14–16]
T. nativa mammals 20 million Dog: 9.8%–44.8% in northeastern China
Cysticercosis Taenia solium Humans Humans and pigs 0.55%; 7 million Pig: 0.23% in Hubei, 3.3%–10.5% in Sichuan province [7,8,17,21]
Toxoplasmosis Toxoplasma gondii Felids Humans, other 7.9%; 100 million Pig: 32.8% in Yunnan province, 33.1% in Hebei; sheep: [8,22,65–67]
mammals and birds 6.2% in Yunnan, 13.3% in Hebei; dog: 13.2% in Beijing,
14.6% in Yunnan, 26.9% in Hebei; cat: 14.6% in Beijing,
79.4% in Guangzhou
Echinococcosis Echinococcus Dogs and wild Humans and other 0.38 million Dog: 39.9%; fox: 24.8%; sheep: 55.3%; yak: 55.3%; [8,25]
granulosus canids mammals Goats: 30.7%; pigs: 7.6% in Qinghai Province
E. multilocularis
Clonorchiasis Clonorchis sinensis Humans and other Water snails, 2.4% in 27 endemic provinces; Snail: up to 15%; [8,29,30]
mammals freshwater fish and 12.5 million Fish: up to 100%;
shrimps Cat: 45.5%; dog: up to 60.4%
Paragonimiasis Paragonimus Humans, cats, dogs Water snails and 1.7% in eight provinces; Stream crab: 9.5%–54.3% [8,33–35]
westermani and other crustaceans 29.7% children in the countryside
carnivores (Shangluo)
Angiostrongyliasis Angiostrongylus Rats Snails and slugs 400 reported cases Rat: 19.5% in Wenzhou, 6%–15.9% in Fujian Province [39–43]
cantonensis Snail: 69.4% in Wenzhou, 0%–35.6% in Fujian Province
Schistosomiasis Schistosoma Humans and other Oncomelania 0.73 million Cattle and buffalos: 4.4% in seven endemic provinces [51,52,54]
japonicum mammals hupensis
Cryptosporidiosis Cryptosporidium spp. Humans and many Not applicable 2.1% in children with diarrhea in 14 Dairy cow: 6.4% in Anhui, 32.7% in Qinghai; cattle: 35%, [55–58]
animals provinces; 10.4% in children with yak: 39.7% in Qinghai Province
diarrhea in Zhejiang Province
Giardiasis Giardia lamblia Human and other Not applicable 2.5%; 30 million Dog: 25.2% in Jilin Province [59,62]
mammals

Trends in Parasitology
Vol.24 No.4
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Review Trends in Parasitology Vol.24 No.4

[8,10]. Echinococcus shiquicus n. sp. [23] and a variant of E. [31]. Since 1980, a total of 3591 marine fish specimens off
multilocularis have been reported in China [24], but it is the Chinese coasts, representing 177 fish species, have
yet to be determined whether these new members of been surveyed for the prevalence of anisakid nematodes.
Echinococcus are infective to humans. The results revealed that 47.1% of the fish specimens,
The recent nationwide ELISA survey estimated that representing 151 fish species (85.3%), are infected with
380 000 people are infected with echinococcosis and 50 anisakids [32], and several fish species have a prevalence of
million are at risk of infection [8] (Table 1). The endemic 100% [32]. In China, human infection with anisakids has
provinces include Inner Mongolia, Ningxia, Qinghai, Jilin, been reported in the media, but there have been no case
Henan, Sichuan, Guizhou, Yunnan, Shaanxi, Gansu, Tibet reports documented in scientific literature.
and Xinjiang; of these, Xinjiang, Sichuan, Qinghai, Gansu
and Tibet have the most severe problems [8]. The preva- Paragonimiasis and pagumogonimiasis
lence of Echinococcus in animals is still unacceptably high Human paragonimiasis is caused by the consumption of
in northwestern China [25] (Table 1). Genotyping hydatid raw or undercooked stream crabs that are infected with
cysts from humans and gravid tapeworms from dogs in Paragonimus westermani or drinking water contaminated
Xinjiang in northwestern China revealed that the E. gran- by metacercaria. This disease is prevalent in 24 provinces
ulosus G1 genotype is the major source of human cystic [8] [Table 1]. People in Shanghai and Chongqing have the
echinococcosis, although the G6 genotype also was present highest prevalences, at 5.1% and 4.1%, respectively [8].
[26]. Children in the endemic regions are at high risk of infection
with this parasite [33] [Table 1]. The prevalence of para-
Sparganosis gonimiasis in stream crabs is high [34,35] (Table 1). Cats,
Sparganosis is caused by larvae of the tapeworm Spirome- dogs and civet cats are considered to be the most important
tra spp. Humans become infected by: (i) drinking inade- reservoir hosts of Paragonimus spp. in the endemic regions
quately treated water contaminated by procercoid-infected [34] (Table 1). Human pagumogonimiasis is caused by
crustaceans; (ii) eating the raw or insufficiently heated Pagumogonimus skrjabini through the ingestion of meta-
meat of second intermediate or paratenic hosts, such as cercaria in crabs, and human cases have been reported in
frogs and snakes, that are infected with plerocercoids; and 14 provinces in mainland China [9,36].
(iii) placing poultices of frog or snake flesh on open wounds
or other lesions, in particular on the eyes. If the flesh is Echinostomiasis
infected with plerocercoids, these plerocercoids can Human echinostomiasis is caused by the ingestion of
actively penetrate into the treated lesion [10]. A total of metacercariae of digenean trematodes of the family Echi-
1000 cases of human sparganosis have been reported in nostomatidae in raw or undercooked mollusks, fish, crus-
22 provinces [10]. Frogs are the main source of human taceans and amphibians (tadpoles or frogs) from fresh or
infection; their plerocercoid prevalence ranges from 8.1% brackish water [3,37]. In mainland China, human infection
to 71.4% [27,28]. with echinostomiasis has been reported in at least eight
provinces, with an average prevalence of 0.015% [6], and an
Fish-, shellfish- and mollusk-borne parasitic zoonoses average prevalence of 5% was reported in some parts of the
Clonorchiasis Fujian and Guangdong provinces [36,37]. Animal infection
Clonorchiasis caused by the oriental liver fluke Clonorchis with echinostomes is common in some provinces of China;
sinensis is considered to be one of the major parasitic for example, in the southern part of Fujian Province, the
zoonoses in some parts of Asia [29]. Humans and other prevalence in dogs and cats is 39.7% and 9.5%, respectively
mammals become infected with C. sinensis when they [36].
consume raw or undercooked freshwater fish and shrimp
infected by C. sinensis metacercariae [29]. The recent Angiostrongyliasis
national survey showed that human clonorchiasis is ende- Human angiostrongyliasis is caused by the larvae of rat
mic in 27 provinces (including municipal cities and lungworm Angiostrongylus cantonensis and leads to eosi-
autonomous regions) [8] (Table 1). The southern province nophilic meningitis. Humans become infected by ingesting
Guangdong has the largest number of infected people (5.5 freshwater and terrestrial snails and slugs [38,39]. The
million) because of the local custom of eating raw and first case of human angiostrongyliasis in mainland China
undercooked fish [8,29]. In China, 140 species of fresh- was reported in 1984 [38]. Since then, 400 human cases
water fish and four species of shrimp have been recognized have been reported (Table 1), including outbreaks of 65
as second intermediate hosts for C. sinensis [30]. The cases in Wenzhou City of Zhejiang Province in 1997 [39]; 30
prevalence of infected fish is still high in some provinces cases in Fuzhou, Fujian Province, in 2002 [39]; 28 cases in
(Table 1). Cats and dogs are the most important animal Yunnan Province between 2003–2005 [40]; and 131 cases
reservoirs for human infection and have high prevalence in in Beijing in 2006 [41]. Other sporadic cases occurred in the
some provinces [30] (Table 1). Heilongjiang, Liaoning, Jiangsu, Zhejiang, Fujian, Guang-
dong, Yunnan, Beijing and Tianjin provinces [39].
Anisakiasis Rats of 11 species are the definitive hosts for A. canto-
Human anisakiasis is caused by larvae of some genera of nensis and have prevalence up to 19.5% [42,43] (Table 1).
the family Anisakidae (such as Anisakis, Contracaecum The prevalence of A. cantonensis larvae in Ampullaria
and Pseudoterranova), and infection occurs through eating gigas, one of its intermediate hosts, is unacceptably high
raw or inadequately cooked fish infected with anisakids in some endemic areas [42,43] (Table 1).

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Plant- and water-borne parasitic zoonoses recorded in 14 provinces, with young children being more
Fasciolopsiasis susceptible to infection than adults [55] (Table 1). For
Fasciolopsiasis in pigs and humans is caused by Fascio- example, Cryptosporidium oocysts were found in 57 of 548
lopsis buski through ingestion of freshwater plants or children with diarrhea (10.4%) in Zhejiang Province [56].
water containing metacercariae of this trematode [2,44]. The prevalence of Cryptosporidium spp. in animals is high
The first national survey between 1988 and 1992 revealed in some provinces [57,58] (Table 1).
that fasciolopsiasis is distributed across 16 provinces and
affects a total of 9531 infected people [45]. Pig infection Giardiasis
with F. buski is common in the southern provinces of Giardiasis is caused by Giardia lamblia, which constitutes
China, and its prevalence is 7.5% in Hunan Province [46]. the most common cause of protozoan diarrhea worldwide.
Contaminated water is an important source of human
Fascioliasis infection, either through direct consumption or through
Human and animal fascioliasis is caused by infection with the use of contaminated water in food processing or prep-
Fasciola hepatica and Fasciola gigantica through ingestion aration [4].
of freshwater plants or water containing metacercariae of Human infection with G. lamblia has been documented
these trematodes [2]. In China, an intermediate Fasciola in every mainland province [59] (Table 1). The prevalence
between F. hepatica and F. gigantica has been identified is high (9.3%) in Xinjiang, where people used to drink
genetically [47]. untreated or poorly treated water. Giardia is more com-
A national survey between 1988 and 1992 revealed mon in children (<10 years old), and the prevalence varies
that 148 people were infected with F. hepatica and nine from 5.0% in children aged 5–9 years to 4.2% in children
people were infected with F. gigantica [45]. Animal in- aged 10–14 years [59]. Genotyping G. lamblia isolates of
fection with Fasciola spp. is common and causes signifi- human origin from China revealed that the Chinese G.
cant economic losses. For example, in Tongren, Guizhou lamblia isolates represent Group 2, Group 3, and the
Province, the prevalence of cattle with F. hepatica and F. mixture of Groups 1 and 3 [60,61]. Giardia is commonly
gigantica is 68.9% and 37.6%, respectively [48]. A survey found in the feces of pets, livestock and wild animals, but
in an abattoir in Nanning, Guangxi Zhuang Autonomous generally it is not considered to cause significant animal
Region, revealed that 50.5% of examined cattle and disease [4]. Prevalence of Giardia in dogs in Jilin Province
53.9% of examined buffalos are infected with F. gigantica is high [62] (Table 1).
[49].
Other FBPZs
Schistosomiasis In addition to the major FBPZs mentioned above,
Human schistosomiasis caused by the trematode Schisto- there are some other parasites that cause emerging
soma japonicum was once a devastating disease in China. FBPZs. These include Mammomonogamus laryngeus,
It is still considered the most important parasitic zoonosis Babesia sp., Gnathostoma spinigerum, Armillifer spp.,
and has been listed as one of China’s three most important Heterophyes heterophyes, Cyclospora cayetanensis, Enta-
communicable diseases to control and prevent from moeba histolytica and Balantidium coli [6–10]. These
spreading, together with HIV/AIDS and tuberculosis parasites also should be taken into consideration when
[50–52]. Humans become infected with S. japonicum by implementing strategies and measures for controlling
drinking water containing cercariae or through skin con- FBPZs.
tact with cercariae in the water [2]. In the mid-1950s,
schistosomiasis was endemic in 12 southern provinces, Problems in the control of FBPZs in China
with 12 million people being infected, and killed millions China has undergone major socioeconomic development in
of people [50–53]. After continued efforts for effective con- the past two decades, and one of her achievements is her
trol for 50 years, schistosomiasis has been eliminated in tremendous progress in the control of major human para-
five of the 12 previously endemic provinces and the preva- sitic diseases transmitted mainly via soil, such as hook-
lence of schistosomiasis has dropped significantly in the worms, Ascaris lumbricoides and Trichuris trichiura [8].
remaining seven endemic provinces since 2005 [52] For instance, the total number of people infected with soil-
(Table 1). transmitted parasites has decreased significantly from
In China, 40 species of mammals are the natural hosts 5360 million in 1990 to 1290 million in 2004 [8]. However,
for S. japonicum. Buffalos and cattle have high prevalence compared with the first national survey carried out be-
among animals and are the main reservoir hosts for human tween 1988 and 1992, there has been a significant increase
infection [54] (Table 1). in the total number of people suffering from FBPZs such as
clonorchiasis, trichinellosis, paragonimiasis and angios-
Cryptosporidiosis trongyliasis [6,8]. Some emerging FBPZs are causing sig-
Cryptosporidium spp. represents one of the most common nificant public health problems [8–10]. The most striking
enteric protozoan parasites of vertebrates and causes example is clonorchiasis, for which the average national
diarrhea in humans and domestic animals [12]. Cryptos- prevalence has increased by 75% when compared with the
poridiosis is transmitted to humans either when they results of the first national survey. In particular, the
drink water with oocysts or when they eat raw vegetables prevalence has increased by 182% in the province of
or plants containing infective stages of Cryptosporidium Guangdong, 162% in the province of Guangxi and 630%
[12]. Human cases of cryptosporidiosis have been in the province of Jilin [8]. In the west region of China, the

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prevalences of trichinellosis and toxoplasmosis are 69.4% Box 1. Strategies and measures that can be taken to control
and 45.2% higher, respectively, than in the east region. FBPZs in China
Several factors are considered to contribute to the
increase of FBPZ prevalence in mainland China: (i) Political commitment and increase of financial support and
dedicated personnel by the central and local governments. This
(i) the habit of eating raw or undercooked fish and
is the key element for the effective control of FBPZs. For
meat, and the pursuit of eating exotic and example, when the World Bank Loan Project ended in 2001,
delicate foods such as sushi (in which raw fish there was a corresponding drop in funding to control schisto-
is the main component) and cisheng (sliced raw somiasis, which in turn caused the increase of human cases of
fish); schistosomiasis in 2003.
(ii) Regular epidemiological survey of FBPZs in humans and
(ii) the increase in income and living standard that animals, and the establishment of national and local informa-
offers more opportunities for people to eat in tion networks dedicated to FBPZs. This will provide the
restaurants, providing more chances for infection foundation (i.e. base-line information) for the design and
with FBPZs; implementation of control strategies and measures.
(iii) the relatively slow development in the detection and (iii) Enhancement of fundamental research relating to the effective
control of FBPZs, such as the elucidation of parasite life cycles
quarantine of meat and fish for zoonotic pathogens, and transmission, genetic variation, immune response and
which cannot match with the rapid development of protective immunity, epidemiology and diagnostic and control
livestock and fishery industries; and techniques. The Chinese Central Government has demonstrated
(iv) the insufficiency of comprehensive and inclusive its commitment to enhance fundamental research into the FBPZ
problem by funding a project for basic research relating to the
control strategies for several important FBPZs.
control of schistosomiasis and malaria through the National
The major difficulties and problems we are confronting Basic Research Program of China (i.e. the 973 program) in 2007.
in the control of FBPZs include: (iv) Enhancement of food safety by implementing stricter quaran-
(i) the insufficiency of comprehensive and authoritative tine techniques and detection methods for FBPZ-causing
data on the prevalence and epidemiology of FBPZs in pathogens at the production, processing, distribution and
buying stages. This measure can ensure that food of animal
animal hosts and the slack in validation and
origins on the market is safe. Significant advances have been
standardization of detection and diagnostic tech- made in the development of rapid detection and quarantine
niques for FBPZs in humans and animals, which has techniques for FBPZ pathogens.
resulted in difficulties when comparing similar (v) Enhancement of collaboration with the World Health Organiza-
prevalence data obtained by different institutions tion, the Food and Agriculture Organization of the United Nations
(FAO), the Office International Des Epizooties, the World Bank
in the same provinces; and other countries. For example, the FAO has established a
(ii) the insufficiency of financial supports for both global network of professionals directly involved in food-borne
research and control from central and local govern- zoonotic diseases including cysticercosis and echinococcosis,
ments, which has resulted in the slow increase in which provides a basic framework for the spread of information
fundamental research relating to the control of related to the diagnosis, prevention and control of major zoonotic
diseases [63]. Significant progress has been made in interna-
FBPZs; tional cooperation on the control of schistosomiasis, cysticerco-
(iii) the decrease in the number of personnel dedicated to sis and echinococcosis in China [53,64].
the control of FBPZs and the high turnover rate of (vi) Educational campaigns utilizing various media, in particular TV
research staff; and and radio, to promote awareness of the significance of and
control strategies for FBPZs. The change of people’s unhealthy
(iv) the lack of coordination between the control of FBPZs
eating habits is crucial to the successful control of FBPZs in
in humans and in animals. some parts of China, particularly for some ethnic groups.

Perspectives for effective control of FBPZs in China


Effective control of FBPZs is a tough task in China, a measures with support from the Chinese central and
country with more than 1.3 billion people of 56 nation- local governments.
alities. China’s economical development is uneven; the
west part of China is generally less developed than the Acknowledgements
other parts of China, and hence China is implementing This work is supported, in part, by grants from the National Basic
Research Program of China (Grant Nos. 2007CB513104 and
the strategy of the ‘Western Development Project’. The
2007CB116301), the Program for Changjiang Scholars and Innovative
control of FBPZs requires the consideration of several Research Team in University (Grant No. IRT0723), the National Natural
factors, including the thorough understanding of para- Science Foundation of China (Grant No. 30671578), the Key Research
sites’ life cycles, biology, transmission and epidemiology Programs in Natural Sciences for Institutions of Higher Education in
as well as the hygiene habits of the population, climate Guangdong Province (Grant No. 06Z004) and the Scientific and
Technological Programs of Guangdong Province (Grant No.
conditions and the culture and customs of different
2005B20201003) to X.Q.Z.
nationalities. Finally, an educational campaign and
executive measures need to be implemented. Given that References
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