Veterinary Parasitology 208 (2015) 254–258
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
Elimination of schistosomiasis japonica from formerly endemic areas in mountainous regions of southern China using a praziquantel regimen Hao Li a,1 , Guo-Dong Dong b,1 , Jin-Ming Liu a,∗ , Jian-Xing Gao c , Yao-Jun Shi a , Ying-Guo Zhang b , Ya-Mei Jin a , Ke Lu a , Guo-feng Cheng a , Jiao-Jiao Lin a,d a National Laboratory of Animal Schistosomiasis Control/Key Laboratory of Animal Parasitology, Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, P.R. China b Yunnan Center for Animal Disease Control and Prevention, Kunming 650051, Yunnan, P.R. China c Weishan County Center for Animal Disease Control and Prevention, Weishan 672400, Yunnan, P.R. China d Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou 225009, P.R. China
a r t i c l e
i n f o
Article history: Received 4 September 2014 Received in revised form 11 December 2014 Accepted 20 December 2014 Keywords: Schistosoma japonicum Domestic animal Mountainous area Drug-based intervention
a b s t r a c t Schistosomiasis japonica is a major public health problem in China. Domestic animals play a major role in the transmission of Schistosoma japonicum to humans. To better understand the epidemiology of schistosomiasis japonica in domestic animals in the mountainous areas of China, we performed a 5-year longitudinal study of schistosomiasis in cattle and horses in Yunnan Province from 2009 to 2013. We also performed a concurrent drug-based intervention study in three settlement groups in Yunnan Province aimed at developing an effective means of controlling transmission in this region. The prevalence of infection in cattle fluctuated between 1.67% and 3.05% from 2009 to 2011, and monthly treatments of schistosome-positive animals reduced the prevalence to 0% (P < 0.05) from 2012 to 2013. Prior to the intervention, we found that schistosomiasis was prevalent from May to October, with the highest prevalence observed in June (10.00%). We surveyed for environmental schistosome contamination, and 94.29% of the miracidia found were from cattle. Our study showed that it is possible to eliminate schistosomiasis in domestic animals in the mountainous regions of China by monthly treating cattle and horses from schistosome-positive households from May to October. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Human schistosomiasis is a chronic debilitating disease caused by blood-dwelling flukes of the genus Schistosoma (Gryseels et al., 2006), and it is common in many tropical and subtropical countries. Schistosomiasis japonicum
∗ Corresponding author. Tel.: +86 21 34293459; fax: +86 21 34293619. E-mail address: [email protected] (J.-M. Liu). 1 Contributed equally. http://dx.doi.org/10.1016/j.vetpar.2014.12.031 0304-4017/© 2014 Elsevier B.V. All rights reserved.
is one of the most common serious parasitic diseases in the People’s Republic of China (PRC), where it has remained a long-standing major public-health problem. This disease is endemic in the lake and marshland regions of the Jiangxi, Hunan, Jiangsu, Anhui, and Hubei provinces of southern China and the mountainous regions of the Sichuan and Yunnan provinces (McManus et al., 2010; Zhou et al., 2005). Based on ecological, environmental, genetic, and molecular factors, Davis et al. (1999) categorized areas of schistosomiasis transmission in the PRC into discrete ecosystems representing four transmission modes, which
H. Li et al. / Veterinary Parasitology 208 (2015) 254–258
included Poyang Lake (mode I), Dongting Lake (mode II), the Yangtze River islands of Anhui Province (mode II), the canals and water networks of Hubei Province (mode III), and the mountainous areas of the Sichuan and Yunnan provinces (mode IV). In addition to humans, Schistosoma japonicum is also known to infect over 40 species of animals (Chen, 1993), of which bovines are especially important for transmission to humans (Chitsulo et al., 2000; Wang et al., 2005; Gray et al., 2008). Due to the zoonotic nature of schistosomiasis japonica, controlling S. japonicum infections in domestic animals is critical to the elimination of human schistosomiasis. Many parasitologists have suggested that this disease cannot be eliminated in China using only praziquantel-based control methods. In 2004, a comprehensive schistosomiasis control campaign aimed at blocking the transmission of S. japonicum from cattle, buffalos, and humans to snails was initiated over a wide geographic area of China (Wang et al., 2009). In Yunnan Province, the prevalence of schistosomiasis japonica in humans and bovines had been reduced to less than 1% in 2009 (Hao et al., 2010), meeting the national criteria for transmission control. To better understand the epidemiology of schistosomiasis japonica in domestic animals in the mountainous areas of China, we performed a 5-year longitudinal study of schistosomiasis in cattle in Yunnan Province from 2009 to 2013. We also performed a concurrent drug-based intervention study in three settlement groups in Yunnan Province to develop an effective means of maintaining transmission control in this region of China. Within one year, schistosomiasis japonicum was eliminated in domestic animals in this region through monthly screening and the treatment of Schistosoma-positive animals. 2. Materials and methods 2.1. Study area Our study was conducted in three settlement groups, Shitoudi, Achahe, and Jiligu, in the Zhonghe administrative village (25.05 N, 100.18 E) in Yunnan Province (Weibaoshan Township, Weishan County). Zhonghe is located at an altitude of 2160 m above sea level, and has a mean annual temperature of 15.6 ◦ C. Zhonghe includes 14 settlement groups, and schistosomiasis japonicum has been endemic in three settlement groups (Shitoudi, Achahe, and Jiligu) of them since at least 1996. Zhonghe is geographically separated from other schistosomiasis japonicum-endemic areas in Weishan County by mountains. Cattle, goats, horses, and donkeys graze freely on the mountainsides, whereas most pigs are reared in stalls. The snail, Oncomelania hupensis, an intermediate host of S. japonicum, primarily inhabits the farmland and streams of Shitoudi, Achahe, and Jiligu. In 2007 and 2008, local health and veterinary officials reported that the prevalence of schistosomiasis was 0% and 3.84% in humans and 0.75% and 1.36% in cattle, respectively, in the Zhonghe area. Snail control efforts consisted primarily of the application of chemical molluscicides once yearly and modification of mud ditch with cement. From 2006 to 2008, all of the cattle in the three settlement groups were
255
screened for schistosomiasis in July or June of each year, and all of the Schistosoma-positive animals were immediately treated with single dose of praziquantel. From 2006 to 2008, all of the cattle, both Schistosoma-positive and Schistosoma-negative, were treated with a single dose of praziquantel in September or October. 2.2. Parasitological techniques and praziquantel treatment All cattle and horses in the study areas were screened for schistosomiasis in May or June 2009 and 2010 using a miracidia-detection technique. From October 2010 to 2013, all of cattle and horses, and some of pigs, sheep, and dogs that were randomly selected by their owners, were screened for schistosomiasis. Fecal sampling and the parasitological analysis were performed as described previously (Liu et al., 2012). The fecal sample sizes used in the analysis were 150, 150, 60, 30, and 30 g for cattle, horses, pigs, sheep, and dogs, respectively. The fecal samples were divided equally into three subsamples, and three independent hatching tests were performed for each fecal sample. The Schistosoma-positive animals were subject to treatment with a single dose of praziquantel (30 mg/kg) within 3 days. In September 2009 and October 2010, both Schistosoma-positive and Schistosoma-negative cattle, were treated with an additional single dose of praziquantel. From November 2010 to October 2011, all of the Schistosomapositive animals screened monthly were also treated with praziquantel within 3 days. In 2012 and 2013, although no Schistosoma-positive animals were found, all of the cattle and horses were treated with one dose of praziquantel in July. The praziquantel was administered orally. Pregnant animals were not treated. The baseline prevalence of schistosomiasis in cattle was based on the prevalences recorded in May or June from 2009 to 2011. The prevalence of schistosomiasis in cattle following the initiation of praziquantel treatment was recorded in April, June, August, and October of 2012 and June and August of 2013. 2.3. Seasonal dynamics of schistosomiasis From November 2010 to October 2011, all of the cattle and horses were monthly screened to determine the seasonal dynamics of schistosomiasis. We also monthly screened 21 goats, 18 pigs (grazed), and 7 dogs that were randomly selected by their owners in November 2010. 2.4. Survey of environmental contamination with schistosome eggs The survey was performed in June 2011. We selected four grazing-pasture areas in Shitoudi, each of which occupied 10,000 m2 , for the collection of fresh fecal samples (one dropping per sample for cattle and horse, and 50 g per sample for goats). Samples were classified based on their source, and weighed. The prevalence of S. japonicum in the fecal samples was determine based on one miracidial-hatching test per sample using 50 g samples for cattle, horses, and goats, respectively. For each
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Table 1 Prevalence of schistosomiasis in cattle from 2009 to 2013. Year 2009 2010 2011 2012 2013
Total no. 240 242 210 472 625
No. examined 240 197 210 472 625
No. infected 4 6 5# 0## 0##
Percent infected 1.67 3.05 2.38 0* 0*
Table 2 Incidence in cattle by location, age, and sex from November 2010 to October 2011. Characteristic
No. examined
No. infected
Incidence (%)
All
37
17.62
Location Shitoudi Achahe Jiligu
56 74 80
23 3 11
41.07* 4.05 13.75
Age (year) ≤2 2–3 >3
13 32 155
0 7 30
0.00 21.19 19.35
Sex Male Female
144 66
26 11
18.06 16.67
#
Included data recorded in May only. The data was the summery of four monitoring tests in 2012 and two monitoring tests in 2013. * P < 0.05, compared with that of 2009–2011. ##
host species, the relative environmental contamination index (RECI) was calculated based on the formula, RECI = (N × PR × MW × mpg)/ (N × PR × MW × mpg), where N is the number of samples, PR is the positive rate, MW is the mean sample weight in g, and mpg is the number of miracidia per g.
*
P < 0.01, compared with those recorded in Achahe and in Jiligu.
3. Results
significantly higher than that of Achahe (4.05%, P < 0.01) or Jiligu (13.75%, P < 0.01; Table 2). The infected cattle were from 22 households (25% in 88 investigated households). The incidence of cattle in eight of the households was 76.92% (20/26). The reinfection rate was 8.82% (3/34). Approximately, 80% of all of the cattle in Shitoudi, Achahe, and Jiligu were used to plough fields, which included all of the infected cattle. The incidences in the cattle that were 2–3 year old and those that were older than 3 years of age were 21.19% and 19.35%, respectively. However, no cattle younger than 2 years of age were infected. No significant difference in prevalence was observed between males and females (Table 2).
3.1. Annual dynamics of schistosomiasis in cattle
3.3. Seasonal dynamics of schistosomiasis in cattle
In the three settlement groups studied, the total number of cattle ranged from 210 to 625. The prevalence of schistosomiasis at the various time points is shown in Table 1. From 2009 to 2011, the prevalence of schistosomiasis in cattle was 1.67–3.05%, with no significant difference between the various years. Following the mass treatment in September 2010 and the following monthly treatments of infected animals, the prevalence was reduced to 0% in 2012 (all of the animals were tested four times) and 2013 (all of the animals were tested twice), which were statistically significant reductions (P < 0.05), compared with the prevalences in 2009, 2010, and 2011. In addition, of the 82 horses and 46 goats screened in 2012 and the 37 horses, 35 pigs, 40 goats, and 10 dogs screened in 2013, none were infected with S. japonicum.
The monthly prevalence of schistosomiasis from November 2010 to October 2011 is shown in Fig. 1. No infected cattle were identified from November 2010 to April 2011. From May 2011 to October 2011, the prevalence ranged between 0.48% and 10.00%, with the highest prevalence (10.00%) occurring in June 2011, which was significantly higher than that observed in the remaining months from May 2011 to October 2011.
2.5. Statistical analysis All of the statistical analyses were performed using the SAS, version 9.2, statistical software package (SAS Institute, Cary, NC, USA). Chi-squared tests were used to examine the intergroup differences based on location, sex, and age group. The level of statistical significance was set at 0.05 or 0.01 for all of the evaluations performed.
3.2. Incidence of schistosomiasis from October 2010 to October 2011 A total of 300 domestic animals, which included 210 cattle, 41 horses, 21 goats, 18 pigs (grazed), and 10 dogs, were screen monthly for schistosomiasis. The incidence of schistosomiasis in the cattle was 17.62% (37/210), which was significantly higher (P < 0.05) than that in the horses (2.38%, 1/41). None of the goats, pigs and dogs was infected. The distribution of infections in cattle was not uniform, with the highest incidence (41.07%) in Shitoudi, which was
3.4. Survey of environmental contamination In June 2011, a total of 63 fecal samples were collected in the field, among which 42 (66.67%) were from cattle and 21 (33.33%) were from goats and horses. The schistosomepositive rates were 4.76% for cattle, 7.69% for goats, and 12.5% for horses. It was estimated that the total number of miracidia from all of the fecal samples was 456, of which cattle contributed 94.29% (Table 3). 4. Discussion Because of high rates of S. japonicum reinfection in both humans and bovines, a comprehensive control strategy has been implemented in most schistosomiasis endemic areas in China. The study of Wang et al. (2009) in the villages along the Poyang Lake in Jiangxi Province from 2005 to 2007 and that of Hong et al. (2013) in
H. Li et al. / Veterinary Parasitology 208 (2015) 254–258
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Fig. 1. Seasonal dynamics of schistosomiasis in cattle from November 2010 to October 2011. Table 3 Schistosome-positive rates, numbers of miracidia per g (mpg), and relative environmental contamination index (RECI) of schistosome-infected hosts. Host
No. examined
Sample weight (g)
No. positive
Percent positive
mpg
RECI (%)
Cattle Goats Horses
42 13 8
1120 50 821
2 1 1
4.76 7.69 12.5
0.09 0.08 0.01
94.29 1.87 3.84
the 12 villages in Gong’an County of Hubei Province from 2009 to 2011 showed that the integrated control strategy was highly effective in controlling the transmission of S. japonicum in marshland regions of China. However, some of these interventions could not be completed in the mountainous area of Yunnan Province. Although snail control efforts (chemical molluscicides and habitat modification), health education, annual treatment of schistosome-positive animals, and annual mass treatment were undertaken in our study area, the prevalence of schistosomiasis in cattle varied from 0.65% to 3.05% from 2007 to 2010, indicating that a more effective strategy was urgently needed in these areas. Although many parasitologists have concluded that schistosomiasis cannot be eliminated from China using praziquantel-based control methods only, our results showed that S. japonicum can be eliminated from domestic animals in the mountainous regions of China using praziquantel alone. In our study area, we performed monthly praziquantel treatments of schistosome-positive animals in 2011 and two preventive praziquantel treatments in 2012 and 2013. Multiple rounds of screening showed that the prevalence of schistosomiasis in cattle was 0% during 2012 and 2013, which was significantly lower (P < 0.05), compared with those from 2009 to 2011. Both human prevalence and infection rate of Oncomelania hupensis in our study area stayed at 0% during 2012 and 2013 (data from the local health institute, not shown). Zhu et al. (2011) reported substantial decreases in the incidences of human (75%) and bovine (100%) schistosomiasis in Shian (Sichuan Province), which might be attributable to the annual human and bovine praziquantel treatments for schistosome-positive individuals. The studies in the Anhui (Wang et al., 2006), Hunan (Liu et al., 2012), and Jiangxi (Liu et al., 2013) provinces concluded that a single annual treatment strategy did not effectively control S. japonicum transmission. In our current study in Yunnan
Province, we also found that a single annual mass treatment was not effective for the long-term control of bovine schistosomiasis. Thus, we undertook the development of new praziquantel treatment regimen. Our previous study suggested that the use of two mass treatments in late March or early April and November, combined with an additional treatment of schistosomepositive animals in July or June, might be effective for schistosomiasis control in the Dongting Lake region of Hunan Province and the Poyang Lake region of Jiangxi Province (Liu et al., 2012, 2013). However, the epidemiological characteristics of schistosomiasis japonica in domestic animals in the mountainous areas of Yunnan Province differed from those in the Hunan and Jiangxi provinces. Our survey of field-collected feces indicated that 94.29% of the environmental contamination was from cattle. Schistosomiasis in cattle occurred primarily from May to October, with the highest prevalence occurring in June. Households had 3–5 cattle, most of which were used to plough fields. The distribution of infections in cattle was not uniform, and most infected cattle were from a subgroup of households. Therefore, we conclude that schistosomiasis in the similar mountainous areas can be eliminated using monthly mass treatments for cattle and horses from schistosome-positive households from May to October. Conflict of interest statement The authors declare that they have no competing interests with regard to the publication of this research report. Acknowledgments This project was supported by research grants awarded by the Special Fund for Agroscientific Research in the Public Interest (grant nos. 200903036 and 201303037). We sincerely thank the veterinary professionals and agricultural
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workers in Weishan County for their kind assistance with the field work. References Chen, M.G., 1993. Schistosoma japonicum and S. japonicum-like infections: epidemiology, clinical and pathological aspects. In: Jordan, P., Webbe, G., Sturrock, R.F. (Eds.), Human Schistosomiasis. CAB International, Oxon, pp. 241–244. Chitsulo, L., Engels, D., Montresor, A., Savioli, L., 2000. The global status of schistosomiasis and its control. Acta Trop. 77, 41–51. Davis, G.M., Wilke, T., Zhang, Y., Xu, X.J., Qiu, C.P., Spolsky, C., Qiu, D.C., Li, Y.S., Xia, M.Y., Feng, Z., 1999. Snail-schistosoma, paragonimus interactions in China: population ecology, genetic diversity, coevolution and emerging diseases. Malacologia 41, 355–377. Gryseels, B., Polman, K., Clerinx, J., Kestens, L., 2006. Human schistosomiasis. Lancet 368, 1106–1118. Gray, D.J., Williams, G.M., Li, Y.S., McManus, D.P., 2008. Transmission dynamics of Schistosoma japonicum in the lakes and marshlands of China. PLoS One 3, e4058. Hao, Y., Zheng, H., Zhu, R., Guo, J., Wang, L., Chen, Z., Zhou, X., 2010. Schistosmiasis situation in People’s Republic of China in 2009. Chin. J. Schisto. Control 22, 521–527 (in Chinese). Hong, X.C., Xu, X.J., Xi Chen, X., Li, Y.S., Yu, C., Yuan, H., Chen, Y., Li, Y.Y., Qiu, R.D., Liu, J., Yi, Z.C., Ren, P., He, G.H.H.B., 2013. Assessing the effect of an integrated control strategy for Schistosomiasis japonica emphasizing bovines in a Marshland Area of Hubei Province, China: a cluster randomized trial. PLoS Negl. Trop. Dis. 7, e2122. Liu, J., Zhu, C., Shi, Y., Li, H., Wang, L., Qin, S., Kang, S., Huang, Y., Jin, Y., Lin, J., 2012. Surveillance of Schistosoma japonicum infection in domestic
ruminants in the Dongting Lake region, Hunan province, China. PLoS One 7, e31876. Liu, J.M., Yu, H., Shi, Y.J., Li, H., He, L., Li, J.X., Dong, C.H., Xie, Q., Jin, Y.M., Lu, K., Lin, J.J., 2013. Seasonal dynamics of Schistosoma japonicum infection in buffaloes in the Poyang Lake region and suggestions on local treatment schemes. Vet. Parasitol. 198, 219–222. McManus, D.P., Gray, D.J., Li, Y.S., Feng, Z., Williams, G.M., Stewart, D., ReyLadino, J., Ross, A.G., 2010. Schistosomiasis in the Peoples’ Republic of China: the era of the Three Gorges Dam. Clin. Microbial. Rev. 23, 442–466. Wang, L.D., Guo, J.G., Wu, X.H., Chen, H.G., Wang, T.P., Zhu, S.P., Zhang, Z.H., Steinmann, P., Yang, G.J., Wang, S.P., Wu, Z.D., Wang, L.Y., Hao, Y., Bergquist, R., Utzinger, J., Zhou, X.N., 2009. China’s new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Trop. Med. Int. Health 14, 1475–1483. Wang, T., Zhang, S., Wu, W., Zhang, G., Lu, D., Ornbjerg, N., Johansen, M.V., 2006. Treatment and reinfection of water buffaloes and cattle infected with Schistosoma japonicum in Yangtze River Valley, Anhui province. China. J. Parasitol. 92, 1088–1091. Wang, T.P., Vang Johansen, M., Zhang, S.Q., Wang, F.F., Wu, W.D., Zhang, G.H., Pan, X.P., Ju, Y., Ørnbjerg, N., 2005. Transmission of Schistosoma japonicum by humans and domestic animals in the Yangtze River valley, Anhui province, China. Acta Trop. 96, 198–204. Zhou, X.N., Wang, L.Y., Chen, M.G., Wu, X., Jiang, H., Chen, W.Q., Zheng, X.Y., Utzinger, J.J., 2005. The public health significance and control of schistosomiasis in China—then and now. Acta Trop. 96, 97–105. Zhu, R., Gray, D.J., Thrift, A.P., Williams, G.M., Zhang, Y., Qiu, D.C., Zheng, F., Li, Y.S., Guo, J.G., Zhu, H.Q., Wu, W.P., Li, R.S., McManus, D.P., 2011. A 5-year longitudinal study of schistosomiasis transmission in Shian village, the Anning River Valley, Sichuan Province, the Peoples’ Republic of China. Parasit. Vectors 4, 43.
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
Elimination of schistosomiasis japonica from formerly endemic areas in mountainous regions of southern China using a praziquantel regimen Hao Li a,1 , Guo-Dong Dong b,1 , Jin-Ming Liu a,∗ , Jian-Xing Gao c , Yao-Jun Shi a , Ying-Guo Zhang b , Ya-Mei Jin a , Ke Lu a , Guo-feng Cheng a , Jiao-Jiao Lin a,d a National Laboratory of Animal Schistosomiasis Control/Key Laboratory of Animal Parasitology, Ministry of Agriculture, Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, P.R. China b Yunnan Center for Animal Disease Control and Prevention, Kunming 650051, Yunnan, P.R. China c Weishan County Center for Animal Disease Control and Prevention, Weishan 672400, Yunnan, P.R. China d Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou 225009, P.R. China
a r t i c l e
i n f o
Article history: Received 4 September 2014 Received in revised form 11 December 2014 Accepted 20 December 2014 Keywords: Schistosoma japonicum Domestic animal Mountainous area Drug-based intervention
a b s t r a c t Schistosomiasis japonica is a major public health problem in China. Domestic animals play a major role in the transmission of Schistosoma japonicum to humans. To better understand the epidemiology of schistosomiasis japonica in domestic animals in the mountainous areas of China, we performed a 5-year longitudinal study of schistosomiasis in cattle and horses in Yunnan Province from 2009 to 2013. We also performed a concurrent drug-based intervention study in three settlement groups in Yunnan Province aimed at developing an effective means of controlling transmission in this region. The prevalence of infection in cattle fluctuated between 1.67% and 3.05% from 2009 to 2011, and monthly treatments of schistosome-positive animals reduced the prevalence to 0% (P < 0.05) from 2012 to 2013. Prior to the intervention, we found that schistosomiasis was prevalent from May to October, with the highest prevalence observed in June (10.00%). We surveyed for environmental schistosome contamination, and 94.29% of the miracidia found were from cattle. Our study showed that it is possible to eliminate schistosomiasis in domestic animals in the mountainous regions of China by monthly treating cattle and horses from schistosome-positive households from May to October. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Human schistosomiasis is a chronic debilitating disease caused by blood-dwelling flukes of the genus Schistosoma (Gryseels et al., 2006), and it is common in many tropical and subtropical countries. Schistosomiasis japonicum
∗ Corresponding author. Tel.: +86 21 34293459; fax: +86 21 34293619. E-mail address: [email protected] (J.-M. Liu). 1 Contributed equally. http://dx.doi.org/10.1016/j.vetpar.2014.12.031 0304-4017/© 2014 Elsevier B.V. All rights reserved.
is one of the most common serious parasitic diseases in the People’s Republic of China (PRC), where it has remained a long-standing major public-health problem. This disease is endemic in the lake and marshland regions of the Jiangxi, Hunan, Jiangsu, Anhui, and Hubei provinces of southern China and the mountainous regions of the Sichuan and Yunnan provinces (McManus et al., 2010; Zhou et al., 2005). Based on ecological, environmental, genetic, and molecular factors, Davis et al. (1999) categorized areas of schistosomiasis transmission in the PRC into discrete ecosystems representing four transmission modes, which
H. Li et al. / Veterinary Parasitology 208 (2015) 254–258
included Poyang Lake (mode I), Dongting Lake (mode II), the Yangtze River islands of Anhui Province (mode II), the canals and water networks of Hubei Province (mode III), and the mountainous areas of the Sichuan and Yunnan provinces (mode IV). In addition to humans, Schistosoma japonicum is also known to infect over 40 species of animals (Chen, 1993), of which bovines are especially important for transmission to humans (Chitsulo et al., 2000; Wang et al., 2005; Gray et al., 2008). Due to the zoonotic nature of schistosomiasis japonica, controlling S. japonicum infections in domestic animals is critical to the elimination of human schistosomiasis. Many parasitologists have suggested that this disease cannot be eliminated in China using only praziquantel-based control methods. In 2004, a comprehensive schistosomiasis control campaign aimed at blocking the transmission of S. japonicum from cattle, buffalos, and humans to snails was initiated over a wide geographic area of China (Wang et al., 2009). In Yunnan Province, the prevalence of schistosomiasis japonica in humans and bovines had been reduced to less than 1% in 2009 (Hao et al., 2010), meeting the national criteria for transmission control. To better understand the epidemiology of schistosomiasis japonica in domestic animals in the mountainous areas of China, we performed a 5-year longitudinal study of schistosomiasis in cattle in Yunnan Province from 2009 to 2013. We also performed a concurrent drug-based intervention study in three settlement groups in Yunnan Province to develop an effective means of maintaining transmission control in this region of China. Within one year, schistosomiasis japonicum was eliminated in domestic animals in this region through monthly screening and the treatment of Schistosoma-positive animals. 2. Materials and methods 2.1. Study area Our study was conducted in three settlement groups, Shitoudi, Achahe, and Jiligu, in the Zhonghe administrative village (25.05 N, 100.18 E) in Yunnan Province (Weibaoshan Township, Weishan County). Zhonghe is located at an altitude of 2160 m above sea level, and has a mean annual temperature of 15.6 ◦ C. Zhonghe includes 14 settlement groups, and schistosomiasis japonicum has been endemic in three settlement groups (Shitoudi, Achahe, and Jiligu) of them since at least 1996. Zhonghe is geographically separated from other schistosomiasis japonicum-endemic areas in Weishan County by mountains. Cattle, goats, horses, and donkeys graze freely on the mountainsides, whereas most pigs are reared in stalls. The snail, Oncomelania hupensis, an intermediate host of S. japonicum, primarily inhabits the farmland and streams of Shitoudi, Achahe, and Jiligu. In 2007 and 2008, local health and veterinary officials reported that the prevalence of schistosomiasis was 0% and 3.84% in humans and 0.75% and 1.36% in cattle, respectively, in the Zhonghe area. Snail control efforts consisted primarily of the application of chemical molluscicides once yearly and modification of mud ditch with cement. From 2006 to 2008, all of the cattle in the three settlement groups were
255
screened for schistosomiasis in July or June of each year, and all of the Schistosoma-positive animals were immediately treated with single dose of praziquantel. From 2006 to 2008, all of the cattle, both Schistosoma-positive and Schistosoma-negative, were treated with a single dose of praziquantel in September or October. 2.2. Parasitological techniques and praziquantel treatment All cattle and horses in the study areas were screened for schistosomiasis in May or June 2009 and 2010 using a miracidia-detection technique. From October 2010 to 2013, all of cattle and horses, and some of pigs, sheep, and dogs that were randomly selected by their owners, were screened for schistosomiasis. Fecal sampling and the parasitological analysis were performed as described previously (Liu et al., 2012). The fecal sample sizes used in the analysis were 150, 150, 60, 30, and 30 g for cattle, horses, pigs, sheep, and dogs, respectively. The fecal samples were divided equally into three subsamples, and three independent hatching tests were performed for each fecal sample. The Schistosoma-positive animals were subject to treatment with a single dose of praziquantel (30 mg/kg) within 3 days. In September 2009 and October 2010, both Schistosoma-positive and Schistosoma-negative cattle, were treated with an additional single dose of praziquantel. From November 2010 to October 2011, all of the Schistosomapositive animals screened monthly were also treated with praziquantel within 3 days. In 2012 and 2013, although no Schistosoma-positive animals were found, all of the cattle and horses were treated with one dose of praziquantel in July. The praziquantel was administered orally. Pregnant animals were not treated. The baseline prevalence of schistosomiasis in cattle was based on the prevalences recorded in May or June from 2009 to 2011. The prevalence of schistosomiasis in cattle following the initiation of praziquantel treatment was recorded in April, June, August, and October of 2012 and June and August of 2013. 2.3. Seasonal dynamics of schistosomiasis From November 2010 to October 2011, all of the cattle and horses were monthly screened to determine the seasonal dynamics of schistosomiasis. We also monthly screened 21 goats, 18 pigs (grazed), and 7 dogs that were randomly selected by their owners in November 2010. 2.4. Survey of environmental contamination with schistosome eggs The survey was performed in June 2011. We selected four grazing-pasture areas in Shitoudi, each of which occupied 10,000 m2 , for the collection of fresh fecal samples (one dropping per sample for cattle and horse, and 50 g per sample for goats). Samples were classified based on their source, and weighed. The prevalence of S. japonicum in the fecal samples was determine based on one miracidial-hatching test per sample using 50 g samples for cattle, horses, and goats, respectively. For each
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Table 1 Prevalence of schistosomiasis in cattle from 2009 to 2013. Year 2009 2010 2011 2012 2013
Total no. 240 242 210 472 625
No. examined 240 197 210 472 625
No. infected 4 6 5# 0## 0##
Percent infected 1.67 3.05 2.38 0* 0*
Table 2 Incidence in cattle by location, age, and sex from November 2010 to October 2011. Characteristic
No. examined
No. infected
Incidence (%)
All
37
17.62
Location Shitoudi Achahe Jiligu
56 74 80
23 3 11
41.07* 4.05 13.75
Age (year) ≤2 2–3 >3
13 32 155
0 7 30
0.00 21.19 19.35
Sex Male Female
144 66
26 11
18.06 16.67
#
Included data recorded in May only. The data was the summery of four monitoring tests in 2012 and two monitoring tests in 2013. * P < 0.05, compared with that of 2009–2011. ##
host species, the relative environmental contamination index (RECI) was calculated based on the formula, RECI = (N × PR × MW × mpg)/ (N × PR × MW × mpg), where N is the number of samples, PR is the positive rate, MW is the mean sample weight in g, and mpg is the number of miracidia per g.
*
P < 0.01, compared with those recorded in Achahe and in Jiligu.
3. Results
significantly higher than that of Achahe (4.05%, P < 0.01) or Jiligu (13.75%, P < 0.01; Table 2). The infected cattle were from 22 households (25% in 88 investigated households). The incidence of cattle in eight of the households was 76.92% (20/26). The reinfection rate was 8.82% (3/34). Approximately, 80% of all of the cattle in Shitoudi, Achahe, and Jiligu were used to plough fields, which included all of the infected cattle. The incidences in the cattle that were 2–3 year old and those that were older than 3 years of age were 21.19% and 19.35%, respectively. However, no cattle younger than 2 years of age were infected. No significant difference in prevalence was observed between males and females (Table 2).
3.1. Annual dynamics of schistosomiasis in cattle
3.3. Seasonal dynamics of schistosomiasis in cattle
In the three settlement groups studied, the total number of cattle ranged from 210 to 625. The prevalence of schistosomiasis at the various time points is shown in Table 1. From 2009 to 2011, the prevalence of schistosomiasis in cattle was 1.67–3.05%, with no significant difference between the various years. Following the mass treatment in September 2010 and the following monthly treatments of infected animals, the prevalence was reduced to 0% in 2012 (all of the animals were tested four times) and 2013 (all of the animals were tested twice), which were statistically significant reductions (P < 0.05), compared with the prevalences in 2009, 2010, and 2011. In addition, of the 82 horses and 46 goats screened in 2012 and the 37 horses, 35 pigs, 40 goats, and 10 dogs screened in 2013, none were infected with S. japonicum.
The monthly prevalence of schistosomiasis from November 2010 to October 2011 is shown in Fig. 1. No infected cattle were identified from November 2010 to April 2011. From May 2011 to October 2011, the prevalence ranged between 0.48% and 10.00%, with the highest prevalence (10.00%) occurring in June 2011, which was significantly higher than that observed in the remaining months from May 2011 to October 2011.
2.5. Statistical analysis All of the statistical analyses were performed using the SAS, version 9.2, statistical software package (SAS Institute, Cary, NC, USA). Chi-squared tests were used to examine the intergroup differences based on location, sex, and age group. The level of statistical significance was set at 0.05 or 0.01 for all of the evaluations performed.
3.2. Incidence of schistosomiasis from October 2010 to October 2011 A total of 300 domestic animals, which included 210 cattle, 41 horses, 21 goats, 18 pigs (grazed), and 10 dogs, were screen monthly for schistosomiasis. The incidence of schistosomiasis in the cattle was 17.62% (37/210), which was significantly higher (P < 0.05) than that in the horses (2.38%, 1/41). None of the goats, pigs and dogs was infected. The distribution of infections in cattle was not uniform, with the highest incidence (41.07%) in Shitoudi, which was
3.4. Survey of environmental contamination In June 2011, a total of 63 fecal samples were collected in the field, among which 42 (66.67%) were from cattle and 21 (33.33%) were from goats and horses. The schistosomepositive rates were 4.76% for cattle, 7.69% for goats, and 12.5% for horses. It was estimated that the total number of miracidia from all of the fecal samples was 456, of which cattle contributed 94.29% (Table 3). 4. Discussion Because of high rates of S. japonicum reinfection in both humans and bovines, a comprehensive control strategy has been implemented in most schistosomiasis endemic areas in China. The study of Wang et al. (2009) in the villages along the Poyang Lake in Jiangxi Province from 2005 to 2007 and that of Hong et al. (2013) in
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Fig. 1. Seasonal dynamics of schistosomiasis in cattle from November 2010 to October 2011. Table 3 Schistosome-positive rates, numbers of miracidia per g (mpg), and relative environmental contamination index (RECI) of schistosome-infected hosts. Host
No. examined
Sample weight (g)
No. positive
Percent positive
mpg
RECI (%)
Cattle Goats Horses
42 13 8
1120 50 821
2 1 1
4.76 7.69 12.5
0.09 0.08 0.01
94.29 1.87 3.84
the 12 villages in Gong’an County of Hubei Province from 2009 to 2011 showed that the integrated control strategy was highly effective in controlling the transmission of S. japonicum in marshland regions of China. However, some of these interventions could not be completed in the mountainous area of Yunnan Province. Although snail control efforts (chemical molluscicides and habitat modification), health education, annual treatment of schistosome-positive animals, and annual mass treatment were undertaken in our study area, the prevalence of schistosomiasis in cattle varied from 0.65% to 3.05% from 2007 to 2010, indicating that a more effective strategy was urgently needed in these areas. Although many parasitologists have concluded that schistosomiasis cannot be eliminated from China using praziquantel-based control methods only, our results showed that S. japonicum can be eliminated from domestic animals in the mountainous regions of China using praziquantel alone. In our study area, we performed monthly praziquantel treatments of schistosome-positive animals in 2011 and two preventive praziquantel treatments in 2012 and 2013. Multiple rounds of screening showed that the prevalence of schistosomiasis in cattle was 0% during 2012 and 2013, which was significantly lower (P < 0.05), compared with those from 2009 to 2011. Both human prevalence and infection rate of Oncomelania hupensis in our study area stayed at 0% during 2012 and 2013 (data from the local health institute, not shown). Zhu et al. (2011) reported substantial decreases in the incidences of human (75%) and bovine (100%) schistosomiasis in Shian (Sichuan Province), which might be attributable to the annual human and bovine praziquantel treatments for schistosome-positive individuals. The studies in the Anhui (Wang et al., 2006), Hunan (Liu et al., 2012), and Jiangxi (Liu et al., 2013) provinces concluded that a single annual treatment strategy did not effectively control S. japonicum transmission. In our current study in Yunnan
Province, we also found that a single annual mass treatment was not effective for the long-term control of bovine schistosomiasis. Thus, we undertook the development of new praziquantel treatment regimen. Our previous study suggested that the use of two mass treatments in late March or early April and November, combined with an additional treatment of schistosomepositive animals in July or June, might be effective for schistosomiasis control in the Dongting Lake region of Hunan Province and the Poyang Lake region of Jiangxi Province (Liu et al., 2012, 2013). However, the epidemiological characteristics of schistosomiasis japonica in domestic animals in the mountainous areas of Yunnan Province differed from those in the Hunan and Jiangxi provinces. Our survey of field-collected feces indicated that 94.29% of the environmental contamination was from cattle. Schistosomiasis in cattle occurred primarily from May to October, with the highest prevalence occurring in June. Households had 3–5 cattle, most of which were used to plough fields. The distribution of infections in cattle was not uniform, and most infected cattle were from a subgroup of households. Therefore, we conclude that schistosomiasis in the similar mountainous areas can be eliminated using monthly mass treatments for cattle and horses from schistosome-positive households from May to October. Conflict of interest statement The authors declare that they have no competing interests with regard to the publication of this research report. Acknowledgments This project was supported by research grants awarded by the Special Fund for Agroscientific Research in the Public Interest (grant nos. 200903036 and 201303037). We sincerely thank the veterinary professionals and agricultural
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