First provincial survey of Angiostrongylus cantonensis in Guangdong Province, China
Corresponding Author Zhuo-Hui Deng, Center for Disease Control and Prevention of Guangdong Province, 176 Xingang Xi Road, Guangzhou 510300, China. Tel.: + 86 20 34452685; Fax: +86 20 34452685; E-mail: firstname.lastname@example.org
The rat lungworm Angiostrongylus cantonensis is a zoonotic nematode with a wide distribution. We report the first provincial survey of the prevalence of A. cantonensis infection among wild rodents and snails in Guangdong Province, China. A total of 2929 Pomacea canaliculata and 1354 Achatina fulica were collected from fields in 22 survey sites with a larval infection rates ranging from 0–26.6% to 0–45.4%. In addition, 114 Cipangopaludina sp and 252 Bellamya sp were bought from markets; larvae were found only in Bellamya snails from two survey sites with an infection rate of 1.4% (1/70) and 3.3% (3/91), respectively. Four hundred and ninety-one rodents were captured in nine sites (Rattus norvegicus, R. flavipectus, Suncus murinus, Mus musculus, Bandicota indica, R. losea and R. rattus). Adult worms were found in R. norvegicus, R. flavipectus and Bandicota indica. Our survey revealed a wide distribution of A. cantonensis and its intermediate hosts P. canaliculata and A. fulica in Guangdong. The prevalence of A. cantonensis in wild snails and rats poses a substantial risk for angiostrongyliasis in humans.
Le vers du poumon du rat Angiostrongylus cantonensis est un nématode zoonotique avec une large distribution. Nous rapportons la première surveillance provinciale de la prévalence de l’infection par A. cantonensis chez les rongeurs sauvages et les escargots dans la province du Guangdong, en Chine. Au total 2929 espèces Pomacea canaliculata et 1354 Achatina fulica ont été collectées dans des champs sur 22 sites d’enquête avec un taux d’infection par les larves variant de 0 à 26,6% et de 0 à 45,4%. En outre, 114 Cipangopaludina sp et 252 Bellamya sp ont été achetés sur les marchés; des larves ont été trouvées seulement chez les escargots Bellamya provenant de 2 sites de l’enquête avec un taux d’infection de 1,4% (1/70) et de 3,3% (3/91), respectivement. 491 rongeurs (Rattus norvegicus, R. flavipectus, Suncus murinus, Mus musculus, Bandicota indica, R. losea et R. rattus) ont été capturés sur 9 sites. Les vers adultes ont été retrouvés chez R. norvegicus, R. flavipectus et Bandicota indica. Notre sondage a révélé une large distribution de A. cantonensis et ses hôtes intermédiaires P. canaliculata et A. fulica dans le Guangdong. La prévalence de A. cantonensis chez les escargots et rats sauvages constitue un risque substantiel de l’angiostrongylose pour les humains.
El gusano del pulmón de la rata, Angiostrongylus cantonensis, es un nemátodo zoonótico con una amplia distribución. Reportamos el primer estudio provincial sobre la prevalencia de la infección por A. cantonensis entre roedores silvestres y caracoles en la Provincia de Guangdong, China. Se recolectó un total de 2929 Pomacea canaliculata y 1354 Achatina fulica del campo en 22 emplazamientos de estudio con tasas de infección por larvas con rangos de 0-26.6% a 0-45.4%. Adicionalmente, se compraron en mercados 114 Cipangopaludina sp y 252 Bellamya sp; se hallaron larvas solo en caracoles Bellamya de 2 emplazamientos de estudio, con una tasa de infección de 1.4% (1/70) y 3.3% (3/91), respectivamente. Se capturaron 491 roedores en 9 emplazamientos (Rattus norvegicus, R. flavipectus, Suncus murinus, Mus musculus, Bandicota indica, R. losea y R. rattus). Se encontraron gusanos adultos en R. norvegicus, R. flavipectus y Bandicota indica. Nuestro estudio reveló una amplia distribución de A. cantonensis y su hospedero intermediario P. canaliculata y A. fulica en Guangdong. La prevalencia de A. cantonensis en caracoles silvestres y ratas posee un riesgo sustancial de angioestrongiliasis en humanos.
Angiostrongylus cantonensis, a zoonotic parasite, occurs in Southeast Asia, Australia, the Caribbean, the Pacific Islands, South and North America (Pien & Pien 1999; Caldeira et al. 2007) and infects various terrestrial and freshwater snail species as intermediate hosts, including Achatina fulica and Pomacea canaliculata. Rodents, including Rattus norvegicus and Rattus rattus, are its natural definitive hosts in some Asian countries (Lv et al. 2009a), North America (Diaz 2008), Africa (Foronda et al. 2010) and Australia (Bhaibulaya 1968). Humans acquire infection primarily via consumption of raw snails harbouring third-stage larvae in Asia (Lv et al. 2010). Angiostrongyliasis is emerging in mainland China as a result of changes in food consumption habits and long-distance transportation of food (Lv et al. 2008).
Guangdong Province, bounded by the South China Sea, is the southern gateway of China. It has a land area of 178 000 km2 and a coastline of 3368 km. The subtropical monsoon climate has an average annual temperature between 19 and 24 °C. The greater part of the province has a mean annual precipitation of about 1300–2500 mm. In 2009, there were 96 million registered permanent residents and 30 million migrant labourers who lived in the province for at least 6 months of the year. The number of migrant labourers is the highest in China, and their eating habits are very diverse.
There was an outbreak among migrant labourers in Guangdong in 2007 during which six migrant labourers developed symptoms of meningitis after consumption of P. canaliculata. (Zhuo-Hui Deng, Shan Lv, Jin-Yan Lin, Rong-Xing Lin, Fu-Quan Pei, personal communication). Because of the low host specificity of A. cantonensis, it is difficult to control this parasite (Lv et al. 2009b). Therefore, it is important to investigate the prevalence of the parasite in snails and rodents to understand the source of the zoonotic infections associated with them. There are numerous reports about A. cantonensis infection among snails and rodents in different parts of the world (Pipitgool et al. 1997; John et al. 2002; Claveria et al. 2005). However, the information concerning infections of snails and rodents in Guangdong Province, China, is very limited (Zhang et al. 2008; Lv et al. 2009b). In this study, we report the first provincial survey results of the prevalence of A. cantonensis infection among wild rodents and snails in Guangdong Province from 2006 to 2008.
According to the national survey methods in China, 16 survey sites were selected from 2006 to 2007. The potential range of P. canaliculata in China was predicted using a degree-day model based on temperature data obtained from 149 observing stations across China. A grid with a spatial resolution of 40 × 40 km was laid over the predicted area, and approximately 5% of the grid cells were randomly selected for sample collection (Lv et al. 2009b). For further study, another five sites were selected in 2008 including coastal and mountain areas by Center for Disease Control and Prevention of Guangdong Province (GDCDC). One site was investigated during the angiostrongyliasis outbreak in 2007 (Zhuo-Hui Deng, Shan Lv, Jin-Yan Lin, Rong-Xing Lin, Fu-Quan Pei, personal communication). In total, 22 survey sites were selected. Markets were selected by asking local CDC staff to identify one large market that sells snails. P. canaliculata and A. fulica collected from fields in each survey site, and other species of freshwater or terrestrial snails obtained in markets were examined for the third-stage larvae by tissue grinding or lung examination (Lv et al. 2009b). Rodents were captured in the fields in survey sites. The research protocol was designed to euthanize the animals and was reviewed by the Academic Board of GDCDC. Rodent’s hearts and lungs were dissected to obtain adult worms and their faeces was also collected for the detection of first-stage larvae by water precipitation (Lv et al. 2009a).
A large number of P. canaliculata was found at all sites, and A. fulica was found at most sites (Table 1). In our survey, 2929 P. canaliculata and 1354 A. fulica were collected with larval infection rate that ranged from 0–26.6% to 0–45.4%, respectively. One hundred and fourteen Cipangopaludina sp. and 252 Bellamya sp. were bought from markets in nine sites. Larvae were found only in Bellamya snails from two sites with infection rates of 1.4% (1/70) and 3.3% (3/91).
Table 1. Infection of Pomacea canaliculata and Achatina fulica with Angiostrongylus cantonensis, Guangdong Province, China, 2006–2008
|East GD*||Haifeng||219||11.8 (18/152)||211||20.8 (27/130)||16.0 (45/282)|
|Nanao||235||17.6 (29/165)||51||0 (0/51)||13.4 (29/216)|
|Lufeng||112||0 (0/110)||108||12.0 (13/105)||6.1 (13/215)|
|Chenghai||126||0.8 (1/126)||57||10.5 (6/57)||3.8 (7/183)|
|Chaozhou||200||2.0 (2/100)||100||4.0 (4/100)||3.0 (6/200)|
|West GD||Zhanjiang||129||1.8 (2/109)||145||14.4 (19/132)||8.7 (21/241)|
|Huazhou||111||6.3 (7/111)||109||8.3 (9/109)||7.3 (16/220)|
|Xuwen||113||2.2 (2/90)||52||9.6 (5/52)||4.9 (7/142)|
|Leizhou||200||0.6 (1/174)||41||4.9 (2/41)||1.4 (3/215)|
|North GD||Meixian||149||12.4 (16/129)||106||23.6 (25/106)||17.5 (41/235)|
|Wenyuan||285||12.3 (16/130)||0|| (0/0)||12.3 (16/130)|
|Luoding||110||2.0 (2/100)||116||13.2 (14/106)||7.8 (16/206)|
|Deqing||134||4.6 (5/109)||50||12.0 (6/50)||6.9 (11/159)|
|Yingde||191||0 (0/191)||20||25.0 (5/20)||2.4 (5/211)|
|Guangning||189||2.1 (4/189)||–||–||2.1 (4/189)|
|Heping||241||1.2 (2/171)||0||(0/0)||1.2 (2/171)|
|Qujiang||93||1.1 (1/93)||0||(0/0)||1.1 (1/93)|
|Pearl River Delta||Dongguan||128||26.6 (34/128)||97||45.4 (44/97)||34.7 (78/225)|
|Nanshan||104||2.2 (2/92)||57||31.6 (18/57)||13.4 (20/149)|
|Kaiping||145||3.6 (4/110)||128||15.3 (19/124)||9.8 (23/234)|
|Zhongshan||438||8.7 (24/275)||1||0 (0/1)||8.7 (24/276)|
|Huadu||102||0 (0/75)||16||43.8 (7/16)||7.7 (7/91)|
We captured 491 at nine sites: Rattus norvegicus, R. flavipectus, Suncus murinus, Mus musculus, Bandicota indica, R. losea and R. rattus (Table 2). Adult worms were found in R. norvegicus, R. flavipectus and B. indica. The infection rate of R. norvegicus ranged from 0 to 60%. For R. flavipectus and B. indica, the infection rate was 10.0% (3/30) and 16.7% (1/6), respectively. Two hundred and eighteen female adult worms and 234 male adult worms were found in 56 rats. Thirty-four rodent faecal samples were collected at seven sites; 44.1% contained larvae.
Table 2. Infection with Angiostrongylus cantonensis in definitive hosts in Guangdong Province, China, 2006–2008
|Qingxin||60.0 (12/20)||–||–||–||–||–||–||60.0 (12/20)|
|Heping||50.0 (1/2)||–||–||–||–||–||–||50.0 (1/2)|
|Zhanjiang||18.6 (18/97)||0 (0/26)||0 (0/6)||0 (0/37)||16.7 (1/6)||0 (0/1)||0 (0/1)||10.9 (19/174)|
|Kaiping||17.3 (14/81)||–||–||–||–||–||–||17.3 (14/81)|
|Lufeng||17.2 (5/29)||–||–||10.0 (3/30)||–||–||–||13.6 (8/59)|
|Leizhou||9.1 (1/11)||0 (0/55)||–||0 (0/48)||0 (0/4)||0 (0/4)||–||0.8 (1/122)|
|Zhongshan||7.7 (1/13)||0 (0/1)||–||0 (0/1)||–||–||–||6.7 (1/15)|
|Huadu||0 (0/8)||0 (0/1)||–||0 (0/2)||–||0 (0/3)||–||0 (0/14)|
|Deqing||0 (0/2)||0 (0/2)||–||–||–||–||–||0 (0/4)|
These results indicate that P. canaliculata and A. fulica are the principal intermediate hosts for A. cantonensis in Guangdong. The prevalence of the terrestrial snail A. fulica was far higher than that of the freshwater snail P. canaliculata. However, because of its high reproductive ability and wide distribution, P. canaliculata plays a more important role than that of A. fulica in the epidemiology of angiostrongyliasis (Lv et al. 2009b). Between 1997 and 2006, seven angiostrongyliasis outbreaks were reported in mainland China, of which six were attributed to P. canaliculata (Lv et al. 2008).
This report of endoparasitic infection in wild rats and snails demonstrates that foci of A. cantonensis are widely distributed in Guangdong Province with natural infection found in its intermediate and definitive hosts. Awareness of angiostrongyliasis needs to be improved for the public, especially migrant labourers, because of their diverse eating habits and history of A. cantonensis infections (Lv et al. 2009b), and for health professionals so that they consider the diagnosis. Educational campaigns should inform the public about the risk of eating raw or undercooked snails, and professional knowledge among healthcare providers should be improved to ensure timely detection of infections and adequate medical response. A hospital-based sentinel surveillance system should be established to more completely identify cases and outbreaks, and food safety inspection staff should educate restaurant owners to serve well-cooked snail dishes.
We thank the staff from different level CDCs for their dedicated work during this survey. This work was supported by Guangdong Medical Science and Technology Research Fund (No. A2007063).