Schistosomiasis in a Migrating Population in the Lake Region of China and Its Potential Impact on Control Operation

Acta Tropica 145 (2015) 88–92

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Schistosomiasis in a migrating population in the lake region of China and its potential impact on control operation

Chun-li Cao a,∗∗, Zi-ping Bao a, Shi-zhu Li a, Wang-yuan Wei b, Ping Yi b, Qing Yu a, Hong-qing Zhu a, Jing Xu a, Jia-gang Guo a, Zheng Feng a,∗ a National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, WHO Collaborating Center for Malaria, Schistosomiasis and Filariasis, The Key laboratory of Parasite and Vector Biology, Ministry of Health, China, 207 Rui Jin Er Road, Shanghai 200025, People’s Republic of China b Hunan Institute of Schistosomiasis Control, Hunan, People’s Republic of China article info abstract

Article history: Coverage of migrating people in schistosomiasis control program is a growing concern in China. Schis- Received 17 March 2014 tosomiasis caused by Schistosoma japonicum is still one of the major infectious diseases of public health Received in revised form 2 February 2015 importance in China though tremendous efforts have been made to control the transmission over the past Accepted 8 February 2015 decades. Along with the rapid social-economic development, migrant population has been remarkably Available online 18 February 2015 increasing across the country. The infected migrants may introduce a new souse of infection to endemic areas or the areas where the transmission had been controlled or interrupted but the intermediate host Keywords: Oncomelania snail is still present. Preliminary studies for surveillance on schistosomiasis prevalence in Schistosomiasis japonica Migrant population migrants were reported, but there is little basic information provided. We carried out an investigation on Knowledge of schistosomiasis the prevalence in immigrants, emigrants and permanent residents in three villages of Hunan province Impact factor located in the main endemic area of lake region, and analyzed the potential impact of migration on control China practice. In the study villages, the migrant population accounts for 53.6% of the total. Schistosoma infection was detected by modified Kato-Katz method and miracidium hatching test. Questionnaire survey was conducted comprising knowledge of disease and its transmission, water contact, personal protective measures, and whether examined and treated after water contact. The survey indicated that the migrants and permanent residents had similar life style, and the majority of them experienced water contact in agricultural work or routine life activities. However, the infection rate in immigrants was significantly higher than that in permanent residents. It was also found that the migrants had significantly less knowledge about the disease than the permanent residents, and took no personal protective measures. This is due to that the control program could not cover the migrants when they were absent at the time the program being implemented. The present study suggested that the surveillance and intervention for migrants, immigrants in particular, should be included and strengthened in schistosomiasis control program and a feasible scheme be developed. © 2015 The Author. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction where interruption of transmission has proven difficult (Zhou et al., 2007a,b; Gray et al., 2008). Schistosomiasis japonica, a zoonotic parasitic disease caused Along with the social-economic development, migrant popu- by Schistosoma japonicum, remains a public health problem and lation has been in continuous increase in the country (Guo and is listed among the top infectious diseases prioritized for control Yu, 2005). According to the nationwide census sampling survey in and elimination in China, despite tremendous efforts have been China in 2005, there were 147 million migrating population, among made over the past decades (Wang et al., 2008; Ross et al., 2013). them 61.3% were from rural areas, and 84.4% migrating from rural More than 82% of infected persons lived in lake and marshland to urban areas (Duan and Yang, 2009). About 30 million people regions (Dongting Lake and Poyang Lake) along the Yangtze River, moved from schistosomiasis endemic areas to cities and developed regions in the country (Zheng, 2003). During the migration, people may carry the parasite and/or snail vector to the new settlement ∗ introducing a risk of transmission (Gautret et al., 2012; Ostroff and Corresponding author. Tel.: +86 21 54653507; fax: +86 21 54653512. ∗∗ Co-corresponding author. Tel.: +86 21 54650863; fax: +86 21 54650863. Kozarsky, 1998; Bella et al., 1980). Importantly, the schistosomiasis E-mail addresses: [email protected] (C.-l. Cao), [email protected] (Z. Feng). patients among the migrants may miss treatment after left home http://dx.doi.org/10.1016/j.actatropica.2015.02.009 0001-706X/© 2015 The Author. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). C.-l. Cao et al. / Acta Tropica 145 (2015) 88–92 89 and become a new source of infection in the endemic areas or the The infected individuals among the immigrants and permanent areas where snails are present (Zhou et al., 2011; Chen et al., 2011). residents were treated by the local anti-schistosomiasis station Currently, studies were reported on the surveillance of schistoso- with praziquantel in October when the local intervention took miasis in migrant population in the areas where the transmission place. The infected emigrants were treated in January–February was controlled or interrupted (Zhou et al., 2007a,b; Huang et al., 2010, before outgoing for work again. The treatment was delivered 2008; Cai et al., 2007), but there is little basic information on the as described in the national manual (Bureau of Disease Control, prevalence in migrating population and its implication in control Ministry of Health, China, 2000). practice (Guo and Yu, 2005; Cao and Guo, 2006). To provide essen- tial information for optimizing control strategy covering migrants, 2.4. Questionnaire survey we investigated the schistosomiasis prevalence status in migrant population and its potential impact on the control operation in the The questionnaire survey was conducted for cognition of sch- lake region of schistosomiasis endemic area of China in September istosomiasis knowledge and personal behavior as described (Cao 2009–February 2010. et al., 2008; Chen et al., 2008). Three sets of questions were designed for the participants: (1) basic demographic informa- 2. Method tion including the gender, age, education (illiterate, elementary school, middle school or higher) and occupation (farmer, fishery 2.1. Migrating and permanent residents and aquatic work, business and others), and the current staying status in the village for defining the groups of immigrant, emi- In this study, the villagers who have administratively registered grant and permanent residents; (2) knowledge of schistosomiasis and possessed house property in the study villages for more than comprising whether knowing: how people contract the disease 10 years are defined as the permanent residents, while the native (infection route), harm of the disease, and the transmission through villagers temporally left home for work in other places for more feces of infected people and livestock, the snail is the mediate than 3 months as the emigrants. host, the best way to prevent from infection is to avoid contact- The immigrants are those have migrated from other places into ing infested water, and the drug for treatment; (3) water contact the study villages for work for 6 months or longer. According to the pertaining weather experiencing water contact during the trans- administrative rule, one person can only register at one permanent mission season (April–October) for agricultural work or routine home residence, and the migrants only need to have a local record life, taking personal protective measure, and receiving examination in the new places where they temporally stay for a period of time. and treatment after water contact. The proportion of knowledge cognition and personal protection in the three defined groups 2.2. Study subjects and sites of participants were estimated and compared. The investigators were trained for the survey protocol before the questionnaire Three villages were selected in the endemic area in Yueyang commenced. City, Dongting lake region, Hunan Province of China. The selected villages were Jinshan village/Yueyang county, Changjiang vil- 2.5. Data analysis lage/Junshan district and Pulao village/Yueyanglou district, where >30% of the total population were migrants, and the ecological envi- The participants were grouped as immigrant, emigrant and per- ronment were similar. manent residents, and the data were processed accordingly. On a village base, all migrants and permanent residents, who All survey data were input using Excel (2007) and analyzed with were present at the time of project survey, at age 6–65, were SPSS 13.0. For the group comparison, the chi-square test was used enrolled, of them 808 migrants and 699 permanent residents and the significance at P < 0.05 was estimated. participated in the project, excluding those were sick, failed in collecting fecal sample or absent. The resident enrollment was carried out based on the administrative information and confirmed by 3. Result house-to-house questionnaire to define three groups (permanent villagers, immigrants and emigrants). 3.1. Demographic characters of study population The questionnaire and parasitological examination for the permanent residents and immigrants was conducted in September– A total of 1602 residents were enrolled. Of 860 migrants enrolled October 2009, after the transmission season and before the local (618 emigrants, 190 immigrants) in the villages, 808 participated intervention, while for the emigrants, the survey was carried out in the study with a survey coverage 94.0%. Among them, the gender in January–February 2010, when they returned home for family ratio of male to female was 0.98: 1, with a majority at the age of ∼ ∼ reunion during the Chinese lunar New Year holiday season. 20 and 30 . Most of the migrants (91.6%) experienced education The approval for this study protocol was obtained from the at middle school or higher. More than three fourths of the migrants Review Board of National Institute of Parasitic Diseases, Chinese (74.3%) engaged in farming and fishery (Table 1). The number of Center for Disease Control and Prevention. Informed consent was migrants accounted for 53.6% of the total participates. obtained from all adult participants or guardians verbally. Of 742 permanent residents enrolled, 699 participated in the survey reaching a coverage rate 94.2%. The ratio of male to female ∼ ∼ 2.3. Parasitological examination was 1: 0.94, with the majority at the age group of 40 and 50 . About two-thirds of permanent residents (62.9%) were educated One fresh fecal sample was collected from each examinee and at middle school or higher. The majority of permanent residents examined using modified Kato-Katz method (reading 3 slices per (88.4%) involved in farming and fishery along the lake. sample), and the egg pre-concentrated miracidium hatching test A total of 1507 residents participated in the project. (3 hatchings per sample) as described in the Manual of Schisto- somiasis Control and Prevention, Ministry of Health, China 2000 3.2. Schistosomiasis prevalence (Bureau of Disease Control, Ministry of Health, China, 2000). The egg-positive found by either Kato-Katz method or hatching test The prevalence was estimated by using modified Kato-Katz was regarded as the individual infected. method and miracidium hatching test for schistosome egg. The 90 C.-l. Cao et al. / Acta Tropica 145 (2015) 88–92

Table 1 Demographic characteristics of study population.

Character Migrant Permanent resident

Emigrant No. (%) Immigrant No. (%) Sub-total No. (%) No. (%)

Total 618 (100) 190 (100) 808 (100) 699 (100) Sex Male 302 (48.9) 97 (51.1) 399 (49.4) 361 (51.6) Female 316 (51.1) 93 (48.9) 409 (50.6) 338 (48.4) Age (years) 6–19 107 (17.3) 16 (8.4) 123 (15.2) 14 (2.0) 20–29 234 (37.9) 57 (30.0) 291 (36.0) 84 (12.0) 30–39 136 (22.0) 62 (32.6) 198 (24.5) 133 (19.0) 40–49 127 (20.6) 33 (17.4) 160 (19.8) 228 (32.6) 50–59 11 (1.8) 21 (11.1) 32 (4.0) 162 (23.2) 60–65 3 (0.5) 1 (0.5) 4 (0.5) 78 (11.2) Education Illiterate 5 (0.8) 2 (1.1) 7 (0.9) 65 (9.3) Elementary school 39 (6.3) 22 (11.6) 61(7.5) 194 (27.8) Middle school or higher 574 (92.9) 166 (87.4) 740 (91.6) 440 (62.9) Occupation Farmer 438 (70.9) 154 (81.1) 592 (73.3) 377 (53.9) Fishery and aquatic work 0 8 (4.2) 8 (1.0) 241 (34.5) Business and others 180 (29.1) 28 (14.7) 208 (25.7) 81 (11.6)

Table 2 3.3. Knowledge of schistosomiasis Schistosome infection in migrants and permanent residents found by fecal examination. To assess residents’ knowledge cognition of schistosomiasis, six Groups No. examined No. positive Positive rate (%) questions were listed in the questionnaire regarding to the knowl- Migrant (n = 808) edge of the infection route, harm of the disease, transmission, Emigrant 618 27 4.4 mediate host snail, best preventive way, and the drug for treat- Immigrant 190 15 7.9 ment. A cognition proportion was estimated for each participant Permanent resident (n = 699) 699 26 3.7 group. It was found that the awareness level in the immigrants and emigrants for all questions were significantly lower than that in the permanent residents (P < 0.05). Between the immigrant and emigrant, except knowing the snail mediate host (P = 0.226), the egg positive rate (7.9%) in the immigrants was found to be signifi- immigrants were significantly less aware of other five knowledge cantly higher than in the permanent residents (3.7%) (2 = 5.920, questions than emigrants (P < 0.05) (Table 3). P = 0.015). However, in comparison of the positive rate among Further examining the awareness of disease knowledge in 27 the other groups, no significant difference was found between egg positive emigrants and 15 egg positive immigrants, it is inter- the groups of migrants and permanent residents (2 = 1.9012, estingly noted that except for knowing the infection route and the P = 0.1679), emigrants and immigrants (2 = 3.666, P = 0.056), treatment drug, the infected immigrants were less aware of the and emigrants and permanent residents (2 = 0.358, P = 0.550) transmission source and the best way of prevention than infected (Table 2). emigrants (P < 0.05) (Table 4).

Table 3 Awareness of schistosomiasis knowledge in migrants and permanent residents.

Knowledge Migrant (n = 808) Permanentc (n = 699)

Emigranta No. (%) Immigrantb No. (%) Sub-total No. (%) No. (%)

Know the infection route 429 (69.4) 115 (60.5) 544 (67.3) 681 (97.4) Know the harm of schistosomiasis 355 (57.4) 83 (43.7) 438 (54.2) 650 (93.0) Know the transmission through feces of infected people or livestock 332 (53.7) 73 (38.4) 405 (50.1) 603 (86.3) Know the snail is the mediate host 327 (52.9) 91 (47.9) 418 (51.7) 662 (94.7) Know the best prevention is to avoid contacting infested water 427 (69.1) 109 (57.4) 536 (66.3) 673 (96.3) Know the drug for treatment 214 (34.6) 87 (45.8) 301 (37.3) 585 (83.7)

a Emigrant n = 618. b Immigrant, n = 190. c Permanent residents.

Table 4 Comparison of knowledge of schistosomiasis in egg positive emigrants and immigrants.

Knowledge Emigrant (n = 27) Prop. (%)* Immigrant (n = 15) Prop. (%)* 2* P*

Know the infection route 19 70.4 7 46.7 2.297 0.130 Know the harm of schistosomiasis 22 81.5 5 33.3 9.737 0.002 Know the transmission through feces of infected people or livestock 23 85.2 6 40.0 9.212 0.002 Know the snail is the mediate host 17 63.0 3 20.0 7.136 0.008 Know the best prevention is to avoid contacting infested water 21 77.8 5 33.3 8.077 0.004 Know the drug for treatment 11 40.7 2 13.3 3.389 0.066

* Proportion. C.-l. Cao et al. / Acta Tropica 145 (2015) 88–92 91

Table 5 Water contact and protective measures of permanent residents and migrants.

Water contact Permanent (n = 605)a Migrant (n = 754) Proportion (%)

No. Proportion (%) Immigrantb No. Emigrantc No.

Exposure to water contact during Apr.–Oct. 598 98.8 163 578 98.3 Pattern of contact Agriculture work 484 80.0 171 578 99.3 Routine life 115 19.0 166 557 95.9 Take personal protective measures 475 78.5 0 0 0 Receive exam and treat after water contact 596 98.5 9 0 1.2

a Permanent residents. b Immigrant n = 171. c Emigrant n = 583.

3.4. Water contact history of exposure to transmission. We defined the emigrants for the native villagers who temporally left home for work in other Table 5 presents the survey results of water contact during the places for more than 3 months, and the immigrants for those peo- transmission season (April to October). All participants were ques- ple who have migrated from other places into the study villages for tioned in regard to contact patterns comprising (1) agricultural work for 6 months or longer. Considering the transmission season work (farming, fishing, and shipping), and (2) routing life activ- lasts for 6–7 months of a year, if the immigrants only work in the ity (washing clothes or general things). The participants were also study villages for 3 months, their staying time may not overlap the asked whether taking personal protective measures (wearing rub- transmission season. Therefore, we set 6 months as a classification ber shoes or using skin protection lotion), and whether received criterion for the immigrants. fecal examination and treatment after water contact. It was shown Actually, the sub-group of migrants represents a location- and that 98% permanent residents and migrants experienced water time-dependent migrating status. The immigrant and emigrant we contact during the transmission season for both agricultural work defined in the study sites would be classified in reverse as emigrant and routine life activities. However, the survey revealed that 78.5% or immigrant elsewhere they migrated to or from, e.g., an emigrant permanent residents took personal protective measures, but none from the study village would be regarded as an immigrant in the of the migrants did. Notably, 98.5% permanent residents received place emigrated to for work. Hence, the result of this study may local examination and treatment after water contact, but only 2.5% imply a broader sense in understanding the correlation of migration (9/171) immigrants and none of emigrants (0/583) obtained the and schistosomiasis control activities. service. The results of this study demonstrated that schistosomiasis prevalence rate in the immigrants was twice as high as in the per- 4. Discussion manent residents. Two factors contributing to the difference were noted. First, we found that 98.5% permanent residents received In Hunan province, agriculture is one of the major productions, examination and treatment, but only few immigrants and none where abundant resource of Dongting Lake, the second largest lake of emigrants did. The intervention is on a regular base set by the in China, advances the agriculture, fishery and water carriage. It is national control program including examination, treatment, health also a densely populated region with a high prevalence of schisto- education, sanitation, and snail control (Bureau of Disease Control, somiasis in the past years. There is a large population going out for Ministry of Health, China, 2000; Wang et al., 2009). The local anti- work, and at the same time, a sizable number of people coming-in schistosomiasis stations in endemic area perform the examination for agricultural and aquatic work. for villagers and deliver treatment to the egg positives in October to To extend intervention measures to migrating people in schisto- November (after transmission season) annually, requesting a cov- somiasis control program is an increasing challenge. The migration erage rate >90%. The health education is performed as an integrant has an irregular dynamic flowing character. The migrants may component of intervention, and extended to the transmission sea- return home once or twice a year, most of them return home for son to popularize with slogans or alert billboards along the risk family reunion during the Chinese lunar New Year holiday season. waterside etc. All residents including the migrants present dur- Some of them may come home to assist family’s farm work in har- ing the intervention and education time would equally have the vest season. The number of migrant and the duration of their stay in chances and access receiving the services. In the study villages, all a new place is depending on their livelihood, family needs or spe- participants were exposed to the same environment, and in fact, cial occasions and varies from time to time and place to place, thus >96% participants experienced water contact during the transmis- cannot fit in the regular intervention time schedule in the endemic sion season. Some migrants might be infected either after moved in, area they moved to or from. or elsewhere before moved in, but evidently the migrants had not According to the nationwide census sampling survey in China been covered by the intervention round last year when they were mainland in 2005, migrating population was defined as the people out of reach. The present work demonstrated that a possible leak in who are present at a residence in a township working for living at the current intervention program may leave migrants unattended the surveying time, but have administratively registered outside of resulting in a higher prevalence the township. In 2005, there were 147 million migrating population Secondly, the result showed that the migrants gained signif- in China mainland, among them 61.3% were from rural areas, and icantly lower knowledge score than the permanent residents, 84.4% migrating from rural to urban areas (Duan and Yang, 2009). and took no personal protective measures. Furthermore, the As described by Teng (2010), the person who left home to other immigrants were less aware of the disease knowledge than the places for work for more than 3 months was defined as migrant in emigrants. Similar to the parasitological intervention scenario, the general. However, in the present work, as the transmission is con- migrants might be out of the coverage of health education while cerned, the migrants were further classified into two subgroups they were on moving. In addition, the immigrants coming from in terms of migrating status because they might have different non-endemic area to endemic area were vulnerable to the infection 92 C.-l. Cao et al. / Acta Tropica 145 (2015) 88–92

(Cao et al., 2010; Li and Yu, 1991). Therefore, less prevention knowl- Cao, C.L., Guo, J.G., 2006. The evaluation of Schistosomiasis surveillance to migrant edge may also be a factor attributable to the higher prevalence in population. Chin. J. Prev. Med. 40, 223–224. Cao, C.L., Chen, H.Y., Chen, L., Xiong, Z.W., Fan, Y.B., Fu, R.L., Fu, G.L., Wan, X.X., migrant population. Liu, Q., Cai, X.P., Wu, X.H., Guo, J.G., Hu, G.H., 2008. Pretest of Questionbase for On the other hand, the migration of infected persons may induce knowledge and behavior of Schistosomiasis control. Chin J. Schisto. Control. 20, two potential risks. 443–445. Cao, C.L., Chen, L., Wan, X.X., Liu, Q., Cai, X.P., Zhong, B., Qiu, D.C., Wu, X.H., Zhou, If the migrating patients were not treated timely, chronic or X.N., Guo, J.G., 2010. 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A strategy to control transmission of Schistosoma japonicum in China. N. Engl. J. Med. 360, 121–128. We would like to thank the staff of Yue Yang County Station of Yang, J.L., Li, H.J., Qi, Y.L., Li, X.B., Mao, G.L., 2007. Investigation on advanced Schis- Schistosomiasis Control, Hunan Province, China, He Zhong, Wang tosomiasis in hilly and mountainous regions. Chin. J. Schisto. Control. 19, 427. Yihong and Huang XiaoSue for their efforts in the field survey. This Zhou, X.N., Guo, J.G., Wu, X.H., Jiang, Q.W., Zheng, J., Dang, H., Wang, X.H., Xu, J., work was supported by the National Institute of Parasitic Diseases, Zhu, H.Q., Wu, G.L., Li, Y.S., Xu, X.J., Chen, H.G., Wang, T.P., Zhu, Y.C., Qiu, D.C., Dong, X.Q., Zhao, G.M., Zhang, S.J., Zhao, N.Q., Xia, G., Wang, L.Y., Zhang, S.Q., Lin, Chinese Center for Disease Control and Prevention. D.D., Chen, M.G., Hao, Y., 2007a. Epidemiology of Schistosomiasis in the People’s Republic of China, 2004. Emerg. Infect. Dis. 13, 1470–1476. 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