Emerging angiostrongyliasis in mainland China.

Our review of angiostrongyliasis in China found that the disease is emerging as a result of changes in food consumption habits and long-distance transportation of food. Enhanced understanding of angiostrongyliasis epidemiology, increased public awareness about the risks associated with eating raw food, and enhanced food safety measures are needed.

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Angiostrongylus cantonensis was first described as a parasite of the Norway rat (Rattus norvegicus) and the black rat (R. rattus) in Guangzhou (formerly Canton), People's Republic of China, in 1933. The first human case was reported from Taiwan in 1945. Transmission to humans is primarily by consumption of raw snails. Contaminated vegetables and paratenic hosts such as freshwater prawns, crabs, and frogs may also play a role in transmission (1).

The first case of human angiostrongyliasis in mainland China was diagnosed in 1984 (2). During the past decade, the number of cases has sharply increased (3). A large outbreak occurred in Beijing during 2006. The outbreak peaked during August and involved 160 persons, 100 of whom were hospitalized. This number of patients is similar to the total number of infections recorded in China over the past decade. Our aim was to briefly review angiostrongyliasis outbreaks in mainland China, update angiostrongyliasis epidemiology, and recommend measures to prevent and control angiostrongyliasis.

The Study

The first reported outbreak of angiostrongyliasis in China occurred in 1997 in the city of Wenzhou in the eastern coastal Zhejiang province; it affected 65 persons (4). Since 2000, 6 more outbreaks have been reported, along with numerous individual cases. A literature review found 334 recorded cases; only 4 cases were reported between 1984 and the 1997 outbreak in Wenzhou city. The 7 outbreaks summarized in Table 1 accounted for 86.5% of the total cases.

The Figure depicts the 9 provinces in China where angiostrongyliasis has been reported thus far. The youngest patient was 11 months of age, and the oldest was 70 years of age. In the recent Beijing outbreak, 99 of the 100 hospitalized patients were available for interview; 59 were male and 40 were female, age range was 13-57 years, median age was 36 years. The causative agent was confirmed for 16 (4.8%) of 334 cases. Four children died. Outbreak investigations found that 75.1% of all patients had eaten raw apple snails (Pomacea canaliculata) or raw giant African land snails (Achatina fulica).

A. cantonensis-endemic foci have been discovered in the provinces of Fujian, Guangxi, Hainan, Yunnan, and Zhejiang (Figure). Jinhua city in Zhejiang province is the parasite-endemic setting furthest north. Infected A. fulica were found in a farm (used for temporary cultivation and selling of snails) in Liaoning province in northeast China; however, the infected snails might have been imported from provinces located further south.

Thirty-two species of wild mollusk in China have been screened for A. cantonensis; 22 of these species (68.8%) harbored the parasite (Table 2). The highest rate and intensity of infections were recorded in A. fulica, followed by slugs (Vaginulus spp.) and P. canaliculata. Terrestrial snails and slugs showed higher rates and intensities of infections than freshwater mollusks. However, at least 1 freshwater snail, P. canaliculata, plays an important role in the epidemiology of angiostrongyliasis.

Of 15 wild rodent species captured in mainland China, 11 harbored A. cantonensis. The prevalence and intensity of infection were generally higher in R. norvegicus than in other rodents. Infections were also found among nonhuman primate, equine, and canine species (5,6). However, the prevalence in domestic animals and nonrodent wildlife remains to be fully investigated.

During surveys of 12 potential paratenic host species in China, A. cantonensis larvae were recovered from frogs (Hylarana guentheri, Rana limnocharis, and R. plancyi) and toads (Bufo melanostictus). In contrast to the situation on different Pacific islands (7,8), A. cantonensis has not yet been found in freshwater shrimp, fish, crabs, and planariae in mainland China.

The A. cantonensis-endemic area in China is rapidly expanding, and causes are multifactorial. First, A. fulica and P. canaliculata have invaded the southern part of China after being imported from East Africa in the 1930s and South America (through Taiwan) in the 1980s, respectively. While both snail species were imported as food, they also became established in the wild fauna and are now common in southern China. Second, vast habitats with suitable environmental conditions can be found in many parts of the country. Recent studies indicate suitable habitats not yet colonized; hence, further expansion of A. cantonensis-endemic settings is cause for concern (9). Finally, the low host specificity of A. cantonensis further supports the expansion of this parasite into new areas.

The predominant freshwater and land snail species found in Chinese markets are P. canaliculata, A. fulica, Cipangopaludina chinensis, and Bellamya aeruginosa. The first 2 account for most A. cantonensis infections in mainland China. In Taiwan, C. chinensis plays an important role in the epidemiology of angiostrongyliasis (10). Recently, B. aeruginosa was found to harbor natural infections with A. cantonensis; several infections have been linked to this species (11,12). Consumption of freshwater shrimp and crabs has increased over consumption of snails. Although only few A. cantonensis infections could be traced to shrimp and crabs and none yet in China, their infection potential merits attention.

Conclusions

The booming economy and rapid infrastructure development in China have affected food production and trade. For example, these developments enabled the countrywide marketing of aquaculture products and snails produced in the southern provinces, which might also be responsible for the emergence of foodborne trematodiasis (13). After the recent angiostrongyliasis outbreak in Beijing, the source of infection was traced to P. canaliculata originating from Guangxi province in southwest China. Socioeconomic changes have also increased the popularity of specific consumption habits across China. Although the residents of the southeastern coastal areas have a long history of eating raw food, including snails and seafood, similar dishes have recently become popular among the urban middle and upper classes in inland China.

[FIGURE OMITTED]

After the 2006 outbreak in Beijing, different measures have been proposed for preventing and controlling angiostrongyliasis. First, food safety and transportation must be improved to avoid human infections and the further spread of intermediate host snails to areas in which the disease is not endemic. In snail farms, rigorous control of rats should be implemented. Collection and marketing of wild snails should be limited. Second, hygiene and food preparation techniques in restaurants should be improved to prevent cross-contamination of other food items. Third, these efforts should be accompanied by sound information in communication and education campaigns to raise public awareness. The basic message, that consumption of raw or undercooked snails is a key risk factor for the transmission of a serious disease, can be easily conveyed and is readily understood by the public. After the first outbreak in Wenzhou city in 1997, a comprehensive health education campaign about safe food consumption habits and the most prominent symptoms associated with angiostrongyliasis was launched in Zhejiang province. Few cases were reported thereafter.

Awareness of angiostrongyliasis needs to be improved for consumers and health professionals. Education campaigns should inform consumers about the risk of contracting angiostrongyliasis, e.g., by eating raw snails, and professional knowledge among healthcare providers should be improved to ensure timely detection of infections and adequate medical response.

Acknowledgments

We thank Li-Ying Wang for her support with data collection; Xian-Hong Wang, Kun Yang, Shi-Zhu Li, and He-Xiang Liu for assistance with data analysis; and Jurg Utzinger for revising this manuscript. We are also grateful to the anonymous referees for a set of useful comments on an earlier version of this manuscript.

This work was supported by grants from the National Natural Science Foundation of China (No. 30590373), the Ministry of Science and Technology of China (No. 2005DKA21104), and the Ministry of Health (No. 2006-133).

Mr Lv works at the National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, in Shanghai. He is engaged in research on the epidemiology of angiostrongyliasis in China and the compatibility of A. cantonensis with different host snails.

References

(1.) Alicata JE. The discovery of Angiostrongylus cantonensis as a cause of human eosinophilic meningitis. Parasitol Today. 1991;7:151-3.

(2.) He JZ, Zhu SH, Yang SQ, Yu BW, Chen YS, Hu QX, et al. First discovery and evidence of Angiostrongylus cantonensis in the cerebrospinal fluid from a case of the population of mainland China. J Guangzhou Med Coll. 1984;12:l-4.

(3.) Chen XG, Li H, Lun ZR. Angiostrongyliasis, mainland China. Emerg Infect Dis. 2005; 11: 1645-7.

(4.) Zheng RY, Jin R, Lin BC, Pan CW, Xue DY. Probing and demonstrating etiological factors for the outbreak of angiostrongyliasis cantonensis in Wenzhou. Sh J Prev Med. 2001; 13:105-7.

(5.) Duffy MS, Miller CL, Kinsella JM, Lahunta AD. Parastrongylus cantonensis in a nonhuman primate, Florida. Emerg Infect Dis. 2004;10:2207-10.

(6.) Mason KV. Canine neural angiostrongylosis: the clinical and therapeutic features of 55 natural cases. Aust Vet J. 1987;64:201-3.

(7.) Alto W. Human infections with Angiostrongylus cantonensis. Pac Health Dialog. 2001;8:176-82.

(8.) Yoshimura K, Sugaya H, Ishida K. The role of eosinophils in Angiostrongylus cantonensis infection. Parasitol Today. 1994;10:231-3.

(9.) Lv S, Zhou XN, Zhang Y, Liu HX, Zhu D, Yin WG, et al. The effect of temperature on the development of Angiostrongylus cantonensis (Chen, 1935) in Pomacea canaliculata (Lamarck, 1822). Parasitol Res. 2006;99:583-7.

(10.) Chen ER. Current status of food-borne parasitic zoonoses in Taiwan. Southeast Asian J Trop Med Public Health. 1991;22(Suppl):62-4.

(11.) Lin JX, Zhou XN, Li LS, Zhang Y, Cheng YZ, Zhang RY, et al. Bellamya aeruginosa acts as the intermediate host for Angiostrongylus cantonensis. Chin J Zoonoses. 2005;21:24-6.

(12.) Li LS, Zhou XN, Lin JX, Zhang Y, Chen YZ, Zhang RY, et al. Discovery of six new host species of Angiostrongylus cantonensis and investigation of the epidemic foci in Fujian province. Chin J Zoonoses. 2006;22:533-7.

(13.) Keiser J, Utzinger J. Emerging foodborne trematodiasis. Emerg Infect Dis. 2005;11:1507-14.

Shan Lv, * Yi Zhang, * Peter Steinmann, ([dagger]) and Xiao-Nong Zhou *

* Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China; and ([dagger]) Swiss Tropical Institute, Basel, Switzerland

Address for correspondence: Xiao-Nong Zhon, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, 200025, People's Republic of China; email: ipdzhouxn@ sh163.net

All material published in Emerging Infectious Diseases is in the public domain and may be used and reprinted without special permission; proper citation, however, is required.

Table 1. Reported angiostrongyliasis outbreaks in mainland China
since 1997

Year   Location (city, province)   No. infections

1997       Wenzhou, Zhejiang             65
2002        Changle, Fujian               8
2002        Fuzhou, Fujian                9
2002        Fuzhou, Fujian               13
2004        Kunming, Yunnan              25
2005        Kunming, Yunnan               9
2006       Beijing, Beijing             160

Year          Source of infection                Reference *

1997    Pomacea canaliculata ([dagger])     Zheng RY et al., 2001
2002       P. canaliculata ([dagger])        Lin JX et al., 2003
2002       P. canaliculata ([dagger])       Yang FZ et al., 2004
2002   Achatina fulica ([double dagger])     Wu CH et al., 2004
2004       P. canaliculata ([dagger])        Han JH et al., 2005
2005       P. canaliculata ([dagger])        Wei LP et al., 2005
2006       P. canaliculata ([dagger])           Not available

* Full reference details are available from the corresponding author
upon request.

([dagger]) (Common name, apple snail.

([double dagger]) Common name, giant African land snail.

Table 2. Known intermediate hosts of Angiostrongylus cantonensis in
mainland China

                                                   First observation of
                         First investigation,      positive specimens,
Species                         y, place                 y, place

Achatina fulica                1979-1982,          1979-1980, Guangzhou
  ([dagger])                   Guangzhou
  ([double dagger])
Pomacea canaliculata          1988, Hekou             1997, Cangnan
  ([section])
  ([parallel])
Camaena cicatricosa            1979-1982,          1979-1982, Guangzhou
  ([double dagger])            Guangzhou
Vaginulus sp. (#)              1980-1982,          1980-1982, Guangzhou
                               Guangzhou
Phiolomycus                    1979-1982,          1979-1982, Guangzhou
  bilineatus (#)               Guangzhou
Deroceras leave (#)         2005, Lianjiang/      2005, Lianjiang/Nan'an
                                 Nan'an
Vaginulus yuxjsjs             1988, Hekou              1988, Hekou
  sp. nov #
Ariophantidae spp.            1988, Hekou              1988, Hekou
  ([double dagger])
Macrochlamys loana (#)      2005, Lianjiang/      2005, Lianjiang/Nan'an
                                 Nan'an
Limax flavus (#)            2005, Lianjiang/      2005, Lianjiang/Nan'an
                                 Nan'an
Bradybaena brevispira          1979-1982,          1979-1980, Guangzhou
  ([double dagger])            Guangzhou
Meghimatium bilinestum      2005, Lianjiang/      2005, Lianjiang/Nan'an
  ([double dagger])              Nan'an
Trichochloritis            1986-1990, Zhuhai        1986-1990, Zhuhai
  rufopila ([double
  dagger])
Trichochloritis            1986-1990, Zhuhai        1986-1991, Zhuhai
hungerfordianus
  ([double dagger])
Vaginulus alte (#)            1988, Hekou              1988, Hekou
Bellamya                 2005, Lianjiang/Nan'an   2005, Lianjiang/Nan'an
  spp. ([parallel])
Bellamya aeruginosa      2004, Minhou/Lianjiang   2004, Minhou/Lianjiang
  ([parallel])
Bradybaena similaris           1980-1982,          1980-1982, Guangzhou
  ([double dagger])            Guangzhou
Bradybaena ravida        2005, Lianjiang/Nan'an   2005, Lianjiang/Nan'an
  ([double dagger])
Plectotropis appanata    2005, Lianjiang/Nan'an   2005, Lianjiang/Nan'an
  ([double dagger])
Bellamya quadrata           1986-1990. Panvu         1986-1990. Panvu
  ([parallel])

                            Highest recorded           Reference *
Species                   prevalence, %, place

Achatina fulica             96.8, Zhongshan       Ding BL et al., 1982
  ([dagger])                                      Liang HK et al., 1984
  ([double dagger])                               Liang HK et al., 1992
                                                  Zhang HM et al., 1996
Pomacea canaliculata         69.4, Cangnan         Li FH et al., 1989
  ([section])                                      Pan CW et al., 2002
  ([parallel])                                     Li YS et al., 2001
Camaena cicatricosa         50.0, Zhongshan       Ding BL et al., 1982
  ([double dagger])                               Liang HK et al., 1984
                                                  Liang HK et al., 1992
Vaginulus sp. (#)           49.2, Guangzhou       Ding BL et al., 1982
Phiolomycus                  100, Guangzhou       Ding BL et al., 1982
  bilineatus (#)                                  Liang HK et al., 1984
Deroceras leave (#)      23.8, Lianjiang/Nan'an    Li LS et al., 2006
Vaginulus yuxjsjs             21.0, Hekou          Li FH et al., 1989
  sp. nov #
Ariophantidae spp.            12.0, Hekou          Li FH et al., 1989
  ([double dagger])
Macrochlamys loana (#)   11.2, Lianjiang/Nan'an    Li LS et al., 2006
Limax flavus (#)         10.1, Lianjiang/Nan'an    Li LS et al., 2006
Bradybaena brevispira         8.3, Nanhai         Liang HK et al., 1984
  ([double dagger])                               Liang HK et al., 1992
                                                   Pan CW et al., 2002
Meghimatium bilinestum   5.9, Lianjiang/Nan'an     Li LS et al., 2006
  ([double dagger])
Trichochloritis               5.8, Zhuhai         Liang HK et al., 1992
  rufopila ([double
  dagger])
Trichochloritis               5.7, Zhuhai         Liang HK et al., 1992
hungerfordianus
  ([double dagger])
Vaginulus alte (#)             4.2, Hekou          Li FH et al., 1989
Bellamya                 4.1, Lianjiang/Nan'an     Li LS et al., 2006
  spp. ([parallel])
Bellamya aeruginosa           3.8, Minhou          Lin JX et al., 2005
  ([parallel])
Bradybaena similaris         3.2, Guangzhou       Ding BL et al., 1982
  ([double dagger])
Bradybaena ravida        3.1, Lianjiang/Nan'an     Li LS et al., 2006
  ([double dagger])
Plectotropis appanata    2.6, Lianjiang/Nan'an     Li LS et al., 2006
  ([double dagger])
Bellamya quadrata              2.5, Panvu         Liang HK et al., 1992
  ([parallel])

* Full reference details are available from the corresponding author
upon request.

([dagger]) Common name, giant African land snail.

([double dagger]) Land snail.

([section])  Common name, apple snail.

([parallel]) Freshwater snail.

(#) Slug.