Factors impactiong on progress towards elimination of transmission of schistosomiasis japonica in China

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Factors impactiong on progress towards elimination of transmission of schistosomiasis japonica in China
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Zhou, Yi-Biao
Liang, Song
Jiang, Qing-Wu
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Abstract:
Over the past decades China has made a great stride in controlling schistosomiasis, eliminating transmission of Schistosoma japonicum in 5 provinces and remarkably reducing transmission intensities in the rest of the seven endemic provinces. Recently, an integrated control strategy, which focuses on interventions on humans and bovines, has been implemented throughout endemic areas in China. This strategy assumes that a reduction in transmission of S. japonicum from humans and bovines to the intermediate Oncomelania snail host would eventually block the transmission of this parasite, and has yielded effective results in some endemic areas. Yet the transmission of S. japonicum is relatively complicated – in addition to humans and bovines, more than 40 species of mammalians can serve as potential zoonotic reservoirs. Here, we caution that some factors – potential roles of other mammalian reservoirs and human movement in sustaining the transmission, low sensitivity/specificity of current diagnostic tools for infections, praziquantel treatment failures, changes in environmental and socio-economic factors such as flooding in key endemic areas - may pose great obstacles towards transmission interruption of the parasite. Assessing potential roles of these factors in the transmission and implications for current control strategies aiming at transmission interruption is needed. Keywords: Schistosoma japonicum, Integrated control strategy, Transmission interruption
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Publication of this article was funded in part by the University of Florida Open-Access publishing Fund. In addition, requestors receiving funding through the UFOAP project are expected to submit a post-review, final draft of the article to UF's institutional repository, IR@UF, (www.uflib.ufl.edu/UFir) at the time of funding. The institutional Repository at the University of Florida community, with research, news, outreach, and educational materials.
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Zhou et al. Parasites & Vectors 2012, 5:275 http://www.parasitesandvectors.com/content/5/1/275; Pages 1-7
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doi:10.1186/1756-3305-5-275 Cite this article as: Zhou et al.: Factors impacting on progress towards elimination of transmission of schistosomiasis japonica in China. Parasites & Vectors 2012 5:275.

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title
p Factors impacting on progress towards elimination of transmission of schistosomiasis japonica in China
aug
au id A1 ca yes snm Zhoufnm Yi-Biaoinsr iid I1 I2 email z_yibiao@hotmail.com
A2 LiangSongI3 I4 songliang@ufl.edu
A3 JiangQing-Wujiangqw@fudan.edu.cn
insg
ins Department of Epidemiology, School of Public Health, Fudan University, 138 Yi Xue Yuan Road, Shanghai 200032, China
Key Laboratory of Public Health Safety, Ministry of Education (Fudan University), 138 Yi Xue Yuan Road, Shanghai 200032, China
Department of Environmental and Global Health, College of Public Health and Health Professions, University of Florida, Gainesville, FL, 32610, USA
Emerging Pathogens Institute, University of Florida, Gainesville, FL, 32610, USA
source Parasites & Vectors
issn 1756-3305
pubdate 2012
volume 5
issue 1
fpage 275
url http://www.parasitesandvectors.com/content/5/1/275
xrefbib pubidlist pubid idtype doi 10.1186/1756-3305-5-275pmpid 23206326
history rec date day 17month 10year 2012acc 27112012pub 3122012
cpyrt 2012collab Zhou et al.; licensee BioMed Central Ltd.note This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
kwdg
kwd
it Schistosoma japonicum
Integrated control strategy
Transmission interruption
abs
sec
st
Abstract
Over the past decades China has made a great stride in controlling schistosomiasis, eliminating transmission of Schistosoma japonicum in 5 provinces and remarkably reducing transmission intensities in the rest of the seven endemic provinces. Recently, an integrated control strategy, which focuses on interventions on humans and bovines, has been implemented throughout endemic areas in China. This strategy assumes that a reduction in transmission of S. japonicum from humans and bovines to the intermediate Oncomelania snail host would eventually block the transmission of this parasite, and has yielded effective results in some endemic areas. Yet the transmission of S. japonicum is relatively complicated – in addition to humans and bovines, more than 40 species of mammalians can serve as potential zoonotic reservoirs. Here, we caution that some factors – potential roles of other mammalian reservoirs and human movement in sustaining the transmission, low sensitivity/specificity of current diagnostic tools for infections, praziquantel treatment failures, changes in environmental and socio-economic factors such as flooding in key endemic areas may pose great obstacles towards transmission interruption of the parasite. Assessing potential roles of these factors in the transmission and implications for current control strategies aiming at transmission interruption is needed.
meta classifications classification elimination_para_inf subtype theme_series_title type BMC Elimination of parasitic infectionstheme_series_editor David Rollinsonbdy
Review
Background
Worldwide, Schistosoma infections remain a serious public health problem, infecting more than 200 million people in approximately 76 countries with a loss of 1·53 million disability-adjusted life years (DALYs) abbrgrp
abbr bid B1 1
B2 2
. Of the species of schistosomes infecting humans, Schistosoma japonicum, distributed in southern China, the Philippines, and parts of Indonesia, is the only schistosome species whose transmission is zoonotic
1
. China’s schistosomiasis control program was initiated in the mid-1950s, and has undergone three stages
B3 3
B4 4
B5 5
B6 6
B7 7
B8 8
. The first stage (from the mid-1950s to mid-1980s) focused on transmission control, and the control program included chemotherapy, snail control primarily by environmental management or the use of molluscicide, improving access to clean water and sanitary facilities
3
5
. By the end of the 1980s, schistosomiasis transmission was eliminated in four endemic provinces but the prevalence of disease remained high in the rest of eight endemic provinces
3
5
. The second stage (from the mid-1980s to the early 2000s) focused on morbidity control, and large-scale chemotherapy (due to the introduction of praziquantel) served as the backbone of The National Schistosomiasis Control Program, which was complemented with health education and continued snail control
3
4
5
6
7
8
. In the mid-1990s, schistosomiasis transmission was eliminated in one of the remaining eight endemic provinces
3
. Despite continued and intensified control efforts, controlling transmission of the disease in the remaining seven endemic provinces (Hubei, Hunan, Anhui, Jiangxi, Jiangsu Sichuan and Yunnan provinces) has been challenging, and, eliminating the transmission in these regions seems a daunting task
3
. A number of studies reported that bovines are the primary infection source of S. japonicum transmission in China
3
B9 9
B10 10
B11 11
B12 12
. Based on this, the third stage of control, also called integrated control, aiming at reducing the roles of bovines and humans as infection sources, has been implemented in China since 2005. With renewed emphasis on transmission control and ultimately transmission interruption, control programs at this stage consist of agricultural mechanization, fencing bovines (particularly water buffalos), chemotherapy on both humans and bovines, health education, provision of clean water and improved sanitation
3
. This national strategy has so far achieved promising results and two notable patterns have been observed in some endemic areas the prevalence of S. japonicum infection in humans was brought below 1%
3
B13 13
, whereas in other endemic regions with implementation of the same strategy, human infections were sustained at around 3%
3
B14 14
. More recently, there was a discussion on the generalizability of this national integrated strategy to control and eventually interrupt the transmission of S. japonicum, which was based on the studies in lake regions of China, and in hilly and mountainous regions of Sichuan and Yunnan the transmission ecology is quite different
B15 15
. Concern has been raised that, in addition to humans and bovines, there might be other factors that implicate the transmission but are neglected
14
B16 16
B17 17
. Here we summarize these factors based on a systematic review of published literature and focus on non-bovine animal hosts, human movements, low sensitivity/specificity of current diagnostic tools for schistosome infection, and praziquantel treatment failure and their implications for the current schistosomiasis control strategy in China. The following databases were used for identifying relevant articles: PubMed, Cochrane Library, Science Citation Index Expanded, China National Knowledge Infrastructure, Wanfang Database, VIP Database, and ProQuest. No restriction was applied to year of publication. All titles and abstracts were independently examined and screened by two reviewers to check their eligibility for inclusion in the review. An article was included in the tables of this paper if it met one of the following criteria included: (1) report on prevalence of infection of S. japonicum in non-bovine animal hosts in China; (2) report on prevalence of infection of S. japonicum in migrant populations in China. Upon inclusion, full papers were retrieved and reviewed by the same two reviewers.
Non-bovine animal hosts
S. japonicum, unlike S. mansoni and S. haematobium, is widely recognized as a zoonotic parasite. Over 40 species of wild and domesticated animals can serve as reservoir hosts for this parasite
9
. The zoonotic nature of S. japonicum complicates control efforts for the parasite. In China a number of non-human mammalian hosts, such as bovines, pigs, dogs, cats, goats/sheep, and rats, can serve as reservoir hosts and are of potential public health importance (Table tblr tid T1 1)
10
11
16
B18 18
B19 19
B20 20
B21 21
B22 22
B23 23
B24 24
B25 25
B26 26
. In addition to bovines, relatively high infection levels were also found in other mammalian hosts in some endemic areas (Table 1)
10
11
16
18
19
20
21
22
23
24
25
26
. High prevalences of S. japonicum infections in rats (59.8%) and in Oncomelania snails (0.4-3.1%) were reported in two islands located in the Yangtze River
19
. The two islands have only emerged in the last 40 years, humans do not inhabit these islands. High infections together with estimates of high transmission index (measured by excreted eggs per day) were also reported in dogs, cats, and rats in a hilly area of China where no infected bovines were found
16
. A similar pattern was also reported in Samar Province, the Philippines, where high prevalences and intensities of S. japonicum infection were also observed in dogs (14.9% prevalence) and rats (29.5% prevalence), suggesting that dogs could potentially be a very important reservoir host of S. japonicum in that region
B27 27
B28 28
. A modeling study indicated that rats may also play a role in human infections in Samar
27
. These findings suggested that the transmission of S. japonicum might occur in the absence of bovines. In addition, high genetic variation in S. japonicum was found in the marshland and lake endemic regions of China (where bovines are considered as an important source of infection) and two main genetic clusters were discovered, separating the strain in bovines and humans from that in goats, dogs, pigs and cats
18
. The result indicated that S. japonicum from bovines and humans might be different from that from other mammalian animals in lake and marshland areas of southern China. Also notable was that the prevalence of S. japonicum infection in pigs, dogs and cats increased when the bovines with high prevalence of infection were removed from the endemic area
16
. The strain from bovines and humans may be more prevalent than those from other mammalian animals in lake and marshland areas of southern China. When the predominant strain is completely or partly removed from endemic areas, the other strain may become predominant. Further studies are needed to address this question, for example, molecular epidemiological research should be performed to address whether the strains cross-infect humans and evaluate relative contribution of different animal reservoirs to sustain the transmission. Without improved knowledge on these issues, the reliance of human- and bovine-oriented control to achieve full control of infection sources might miss some other important sources of infection.
table
Table 1
caption
b Reported prevalence of infection of
Schistosoma japonicum
among different non-human hosts in China
tgroup align left cols 12
colspec center colname c1 colnum 1 colwidth 1*
c2 2
c3 3
c4 4
c5 5
c6 6
c7 7
c8 8
c9 9
c10 10
c11 11
c12
thead valign top
row
entry
Author and date of publication
Environmental type
nameend namest rowsep
Definitive hosts
Bovine
Pig
Dog
Goat/sheep
Cat
Donkey
Horse
Mule
Rodent
Rabbit
tfoot
Note: = 2006; †=2007; ‡= Chenqiao village; § = Guanghui village.
tbody
Lu DB et al. (2010)
16
Marshland*
35·5
0·0
4·8
55·0
0·0
-
-
-
0·0
-
Marshland†
-
3·9
8·4
-
37·5
-
-
-
-
-
Hill*
0·0
0·0
18·9
-
2·6
-
-
-
26·5
-
Hill†
-
0·0
21·1
-
5·3
-
-
-
17·7
-
Wang TP et al. (2006)
18
Marshland‡
26·9
7·4
2·7
33·3
0·0
-
-
-
-
-
Marshland§
15·4
0·0
4·1
0·0
1·5
-
-
-
-
-
Xu GY et al. (1999)
19
Marshland
-
-
-
-
-
-
-
59·8
-
Wang TP et al. (1997)
20
Marshland
48·7
21·3
0·7
13·0
0·0
-
-
-
8·3
18·2
Sun LP et al. (1997)
21
Marshland
22·1
26·7
-
-
-
-
-
-
-
-
Xu FS et al. (1995)
22
Mountain
36·9
-
3·0
-
-
-
-
-
Su ZW et al. (1994)
23
Lake
35·7
60·0
75·0
-
-
-
-
-
-
-
Gu XG et al. (1993)
24
Mountain
36·9
-
3·0
-
-
-
-
-
0·9
-
Dai ZJ et al. (1991)
10
Mountain
42·3
6·7
7·5
8·5
-
-
13·5
-
-
-
Zheng J et al. (1990)
11
Mountain
17·3
13·2
8·2
4·2
0·0
4·3
3·4
3·2
1·4
-
Chen DJ et al. (1989)
25
Mountain
15·2
17·1
75·0
10·8
-
-
4·7
-
57·1
-
Yao BY et al. (1989)
26
Mountain
16·5
9·3
9·6
0·0
0·0
1·8
1·4
3·5
1·7
-
Human movement
The second potential obstacle in moving towards the elimination of schistosomiasis transmission relates to human movement. Along with China’s rapid economic development and urbanization over the past decades, the country has witnessed the largest human movement, in particular rural–urban migration in the human history (Table T2 2)
B29 29
B30 30
B31 31
B32 32
B33 33
B34 34
B35 35
B36 36
B37 37
. For example, the movement population of rural migrants moving to coastal cities is approximately 120 million
B38 38
. Meanwhile, large population movements are also occurring between cities, in particular from small cities to big cities
38
. It has long been recognized that human movement plays an important role in the epidemiology of many infectious diseases
38
B39 39
B40 40
. For example, some infectious diseases (e.g. leishmaniasis, Chagas disease, lymphatic filariasis, and schistosomiasis) have emerged or re-emerged in urban areas or previously controlled regions, which have been linked to human movements
38
B41 41
.
Table 2
Prevalence of infection of
Schistosoma japonicum
in different migrant populations
Author and date of publication
Movement type
Proportion of migration (%)
Prevalence (%)
Chen GX et al. (2011)
29
Migration from endemic areas to other areas
22·4-38·5
2·6-5·3
Wang ZC et al. (2008)
30
Migration from non-endemic areas to endemic areas
>5·3
12·5
morerows
He JC et al. (2008)
31
Migration from endemic areas to other areas
-
3·2
Migration from non-endemic areas to endemic areas
-
3·0
Zhang YQ et al. (2003)
32
Migration from endemic areas to other areas
29·9
26·0
Li YS et al. (2003)
33
Fishing population
-
68·9
Chen GX et al. (2001)
34
Migration from endemic areas to other areas
19·7
15·6
Zhang SQ et al. (1998)
35
Migration from endemic areas to other areas
19·8-32·4
2·1-13·9
Zheng J et al. (1999)
36
Fishing population
-
18·2-84·2
Boatman
-
54·2-69·4
Herdsman
-
41·2
Ross AG et al. (1997)
37
Fishing population
-
22·4
The occurrence of schistosome transmission in urban areas or re-emergence of the transmission in previously controlled areas were most probably through infected migrants and endemic foci was present in large cities such as in Bamako, Kampala, Changsha and Dar el Salam
38
41
. The impact of human migration on the transmission of schistosomiasis has been reported. For example, a report in Brazil indicated that migrants play an important role in the transmission of schistosomiasis, and the presence of mobile populations (e.g. migrants, returnees and tourists) in endemic regions can also impact significantly on the control effectiveness of schistosomiasis due to insufficient health services
B42 42
. Yet, this potential remains largely unknown in China. In addition to lack of information on the spatial and temporal patterns of population movements, little is available on the epidemiological impact of the movement patterns on transmission and maintenance of schistosomiasis in China. Hence, studies to understand how human movements (e.g. between endemic and endemic areas, endemic and non-endemic areas) impact the transmission and control are needed. In addition to human movement, livestock movement (e.g. through livestock trade or movement to new grazing fields) also occurs frequently in endemic regions in China
42
, and this raises another concern for the current national control strategy.
Diagnostic tests
While extensive control efforts in endemic areas have greatly suppressed the transmission levels, selective chemotherapy with praziquantel focusing on infected individuals becomes an important component of the national control program, and thus diagnosis of infection is a key step for determination of target populations for treatment, evaluation of morbidity, and assessment of control measures
B43 43
. With decreasing infection intensities due to extensive control efforts, widely used direct parasitological techniques (e.g. miracidium hatch test (MHT) and Kato-Katz thick smear (KK)) have become increasingly insensitive
43
. KK and MHT are the two widely field-applied direct parasitological methods in China. The sensitivity of KK method ranges generally from 40% to 70%, while for MHT it varies from 24% to 95%, depending primarily on the levels of infection intensities
43
. The sensitivities of these direct parasitological techniques decrease generally with decrease in infection levels of humans. The insensitivities of KK and MHT methods lead to missing diagnosis of infected cases in areas of low endemicity, and in post-treatment situations. Other widely field-applied diagnostic alternatives are indirect immunodiagnostic assays (i.e. detecting schistosome-specific antibodies), e.g. Circumoval precipitin test (COPT), Indirect hemagglutination assay (IHA), Enzyme-linked immunosorbent assay (ELISA) and Dipstick dye immunoassay (DDIA). These antibody detection assays have relatively high sensitivities, but generally low specificities. The specificity varies widely for each test 55% to 96% for COPT method, 35% to 94% for IHA method, 20% to 93% for ELISA method, and 33% to 97% for DDIA
43
. These antibody detection techniques cannot differentiate between current and past infections. Thus, the insensitivity or non-specificity of the currently field-applied diagnostic methods may result in difficulties in identifying true infected individuals for selective chemotherapy and assessing the effectiveness of interventions, collectively posing a significant obstacle in moving towards complete control of schistosomiasis. There are many other diagnostic methods such as clinical or ultrasonographic methods measuring the morbidity associated Schistosomiasis japonica, questionnaires, direct immunological tests detecting the schistosome-derived antigens, and the histological methods detecting schistosome eggs in tissue biopsies, but clinical or ultrasonographic methods, and questionnaires lack specificity in some areas such as China
43
. Although the circulating antigen detection assays have a relatively high specificity, they are not any better than the egg detection assays in terms of sensitivity in areas of low endemicity
B44 44
B45 45
B46 46
B47 47
. The histological diagnostic method with both high sensitivity and high specificity is neither simple nor convenient for population-based investigations. Recently, polymerase chain reaction (PCR) based techniques for detection of schistosome DNA in stool or sera and plasma have been developed, showing promise as a highly sensitive and specific assay for diagnosis of schistosome infection
B48 48
B49 49
B50 50
B51 51
B52 52
B53 53
B54 54
B55 55
.
Other neglected factors
Other neglected factors (e.g. praziquantel treatment failures, frequent flooding, and environmental and socio-economic changes) may also pose challenges to the current control program. The praziquantel treatment failures include treatment non-compliance and drug resistance. The chemotherapy with praziquantel has been implemented widely in endemic regions in China since the 1990s, especially during the 10-year World Bank Loan Project (WBLP)
B56 56
. The compliance rates of chemotherapy drop in many communities after repeated rounds of mass or selective treatment
B57 57
. Although currently there is no evidence of praziquantel resistance for S. japonicum, the resistance is found in other schistosoma species (e.g. S. mansoni)
56
. Frequent flooding along the Yangtze River and in the lake regions (e.g. Dongting Lake and Poyang Lake regions) have contributed to the spread of the intermediate host Oncomelania hupensis, and might counteract control efforts
4
. Environmental changes, caused by returning reclaimed land to the lake, construction and operation of Three Gorges dam, and the South-to-North water transfer project, might create new habitats for O. hupensis
4
B58 58
.
Discussion
Although bovines are largely responsible for transmission of S. japonicum in the lake and marshland regions of China, they are a major source of incomes for local farmers. The large marshland areas of Dongting Lake and Poyang Lake are a natural and ideal pasture for bovines and goats, and provide natural habitats for the intermediate snail host. It is difficult to remove all bovines from or completely fence pastures on the large marshland areas, since the farmers have herded bovines, especially water buffaloes, in the marshland areas for generations
17
. Even if all bovines were removed from or well fenced from the large marshland areas some time, it is also challenging to maintain the state of “without bovines” on the marshland areas for a long period of time because bovine movement also occurs frequently in the lakes and marshland regions due to livestock trade or new grazing fields
B59 59
. So, fencing pastures or removing bovines often conflicts with the traditional way of raising livestock (especially water buffalo) and farmers’ incomes, and this considerable conflict might reduce the control efforts of the ongoing integrated control strategy, as fencing pastures is one of the key technical measures of the control strategy
3
. Hence, this integrated control strategy should be implemented in the light of local conditions of endemic areas for mutual benefit and development. For example, the environmental management should be encouraged to be implemented in some snail-inhabited marshland areas suitable for agricultural or forestry practices (e.g., Cropping cole or wheat, planting trees for controlling snails), thus, the farmers not only might increase their incomes, but also bovines could be well fenced by these modified snail-inhabited marshland areas, and snails could be controlled by the environmental management.Although much is known about migration in China, the typology of population movement is complex and remains less well characterized
40
. There are at least two types of population movements related to schistosomiasis transmission in China (Table 2)
29
30
31
32
33
34
35
36
37
: a) fishermen, boatmen and herders who move around in rivers or lakes; b) People moving seasonally for paid work (e.g. 1) people from endemic areas moving into other endemic regions; 2) people from non-endemic areas moving to endemic areas; 3) from endemic areas to controlled areas; 4) from endemic areas to non-endemic areas but back to endemic areas). Tens of thousands of fishermen, boatmen and herders, with a high prevalence and intensity of S. japonicum infection, move around in Dongting Lake and Poyang Lake which are strongholds of schistosomiasis endemic areas in China (Table 2)
33
36
37
. These people frequently contact infected water, and their stools generally go into the water or snail habitats directly. It has been well-known that these migrant fishermen and bovines are responsible for a large proportion of the total contamination of the environment with Schistosoma eggs and are hence drivers in maintaining transmission of the disease in the lake and marshland areas of southern China
33
. The administration of chemotherapy or stool collection for these nomads is very difficult and little is known about the optimal treatment window for these nomads. Seasonal mobility for paid work has been very common in recent years in China, e.g. some rural young labourers from endemic areas leave their homes in the slack season (in farming), and return in the busy season (in farming), and other migrants only return to their home annually in the Chinese New Year. Some labourers from non-endemic regions enter endemic areas for agriculture in the busy season and leave in the slack season. In the current national control program of schistosomiasis, praziquantel-based chemotherapy is implemented generally only in endemic areas in autumn each year (i.e. slack season for farming), and the target population of chemotherapy is usually the local residents, not non-local people
3
14
. So, most of migrants infected with S. japonicum are missed for the treatment, and continue to be the infection sources. Hence, the target population and time of chemotherapy in the national control program of schistosomiasis should be adjusted in light of the patterns of population movement, for example, the target population of chemotherapy should include the non-local people infected with S. japonicum, and chemotherapy should also be implemented in the Chinese New Year when most of the infected migrants return to their home for the Spring Festival.It is unclear whether schistosomiasis transmission could be maintained by these neglected factors in the absence of bovines. To address this question further study is needed, and the long-term effectiveness of the comprehensive national strategy should be also further evaluated
9
. For example, some longitudinal studies should be carried out to determine or evaluate whether these neglected factors are important for S. japonicum transmission.
Conclusion
The current integrated strategy in China assumed that blocking the transmission of S. japonicum from human and cattle to snails would stem the transmission of this parasite
13
. Yet, the process of S. japonicum transmission is, in fact, relatively complicated, and might be abetted by other domesticated (e.g. dogs, cats, and goats) and wild (e.g. rats, and rabbits) animals, by population movement, and by social and hydrologic (e.g. flooding) links among some focal ‘hot spots’ of transmission. While we are working towards the transmission elimination of S. japonicum, these factors, which are currently neglected in the integrated strategy, need to be paid some attention by public health authorities.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
YBZ, SL and QWJ wrote the manuscript together, YBZ summarized the Tables and all authors have read and approved the final version of the manuscript.
bm
ack
Acknowledgements
This work is supported by National High Technology Research and Development Program of China (No. 2006AA02Z402), the National S & T Major Program (Grant No. 2012ZX10004-220 and 2008ZX10004-011), National Natural Science Foundation of China (No. 30590374), and Shanghai Leading Academic Discipline Project (Project No. B118).
refgrp Human schistosomiasisGryseelsBPolmanKClerinxJKestensLLancet20063681106lpage 111810.1016/S0140-6736(06)69440-3link fulltext 16997665Schistosomiasis elimination: lessons from the past guide the futureGrayDJMcManusDPLiYSWilliamsGMBergquistRRossAGLancet Infect Dis20101073373610.1016/S1473-3099(10)70099-220705513China's new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasisWangLDGuoJGWuXHChenHGWangTPZhuSPZhangZHSteinmannPYangGJWangSPWuZDWangLYHaoYBergquistRUtzingerJZhouXNTrop Med Int Health2009141475148310.1111/j.1365-3156.2009.02403.x19793080Schistosomiasis control: experiences and lessons from ChinaWangLDUtzingerJZhouXNLancet20083721793179510.1016/S0140-6736(08)61358-618930529Optimal combined approaches of field intervention for schistosomiasis control in ChinaLinDDHuGHZhangSJActa Trop20059624224710.1016/j.actatropica.2005.07.01816125658Morbidity control of schistosomiasis in ChinaJiangQWWangLYGuoJGChenMGZhouXNEngelsDActa Trop20028211512510.1016/S0001-706X(02)00006-212020884Achievements of schistosomiasis control in ChinaYuanHCJiangQWZhaoGMHeNMen Inst Oswaldo Cruz200297Suppl 1187189The public health significance and control of schistosomiasis then and nowZhouXNWangLYChenMGWuXHJiangQWChenXYZhengJUtzingerJActa Trop200520059697105Transmission dynamics of Schistosoma japonicum in the lakes and marshlands of ChinaGrayDJWilliamsGMLiYMcManusDPPLoS One20083e405810.1371/journal.pone.0004058pmcid 260525919115007Study on epidemic factors and regularity of schistosomiasis japonica in mountainous district of liangshan yi autouomous prefectureDaiZJYanJBChenDRXieZMXieDWLiaoTBSouthest Chin J Agri Sci19914115120in ChineseStudies on distribution characteristics of infection sources of schistosomiasis in mountainous regionsZhengJQianKYaoBYZhuHQChenSHZhangRChin J Schisto Control199022427in ChineseA baseline study of importance of bovines for human Schistosoma japonicum infections around Poyang Lake, China: villages studied and snail sampling strategyDavisGMWuPWChenHGLiuHYGuoJGLinDDLuSBWilliamsGSleighAFengZMcManusDPAm J Trop Med Hyg20026635937112164289A strategy to control transmission of Schistosoma japonicum in ChinaWangLDChenHGGuoJGZengXJHongXLXiongJJWuXHWangXHWangLYXiaGHaoYChinDPZhouXNN Engl J Med200936012112810.1056/NEJMoa080013519129526An integrated strategy for transmission control of Schistosoma japonicum in a marshland area of China: findings from a five-year longitudinal survey and mathematical modelingZhouYBLiangSChenGXReaCHeZGZhangZJWeiJGZhaoGMJiangQWAm J Trop Med Hyg201185838810.4269/ajtmh.2011.10-0574312234921734130Toward sustainable and comprehensive control of schistosomiasis in China: lessons from SichuanSetoEYWRemaisJVCarltonEJWangSLiangSBrindleyPJQiuDSpearRCWangLDWangTPChenHGDongXQWangLYHaoYBergquistRZhouXNPLoS Negl Trop Dis20115e137210.1371/journal.pntd.0001372320191622039563Contrasting reservoirs for Schistosoma japonicum between marshland and hilly regions in Anhui, China–a two-year longitudinal parasitological surveyLuDBWangTPRudgeJWDonnellyCAFangGRWebsterJPParasitology20101379911010.1017/S003118200999103X19723358Thought of schistosomiasis control strategy with emphasis on controlling sources of infection in lake and marshland endemic regionsHeHBChin J Schisto Control201123710713Does multiple hosts mean multiple parasites? Population genetic structure of Schistosoma japonicum between definitive host speciesWangTPShrivastavaJJohansenMVZhangSQWangFFWebsterJPInt J Parasit200620063613171325Observation on natural focal disease of schistosomiasis in rattus norvegicus in NanjingXuGYTianJCChenGMYangHMQiuLHuHBJ Pract Parasit Dis1999746in ChineseThe infection sources of schistosomiasis japonica and their role in the transmission of this disease in marshland areas, Anhui provinceWangTPGuoJHWuWCZhangSQLuDBZhangGHParasit Prev Res199726138140in ChineseRole of different infection sources in the transmission of schistosomiasis japonica in marshland regionSunLPHongQBCaoQGuBLGaoZHGuoBYChin J Schisto Control199794445in ChineseRole of different infection sources in the transmission of schistosomiasis japonica in mountainous regionXuFSGuXGZhaoWXLiYXYinHZZhaoLGJ Pract Parasit Dis19953129in ChineseRole of several host in transmission of schistosomiasis japonica in lake regionSuZWHuCQFuYChenWHuanXBChin J Parasitol Parasit Dis1994124851in ChineseAnalysis on epidemiology of schisotosomiasis in mountainous terrace regions in Sichuan through a typical investigationGuXGZhaoWXXuFSQiuDCHanYChenGYChin J Schisto Control199358284in ChineseEpidemiological survey of schistosomiasis in high mountainous region in Eryuan county of Yunnan provinceChenDJGongZBChin J Schisto Control198911013in ChineseThe role of the animal host in the epidemiology of schistosomiasis in mountainous regionsYaoBYZhengJQianKChenSHZhuHQWuWPChin J Schisto Control1989113in ChineseMulti-host transmission dynamics of Schistosoma japonicum in Samar Province, the PhilippinesRileySCarabinHBeLislePJosephLTalloVBalolongEWillinghamALFernandezTJGonzalesROOlvedaRMcGarveySTPLoS Med20085e1810.1371/journal.pmed.0050018221155918215106Population genetics of schistosoma japonicum within the Philippines suggest high levels of transmission between humans and dogsRudgeJWCarabinHBalolongETalloVShrivastavaJLuDBBasáñezMGOlvedaRMcGarveySTWebsterJPPLoS Negl Trop Dis20082e34010.1371/journal.pntd.0000340258295219030225Investigation on prevalent trends and analysis of control period among floating population in schistosomiasis endemic areas of Guichi DistrictChenGXHeZGHanSMChin J Schisto Contro201123148153in ChineseSero-epidemiological survey on floating population immigrated from schistosomiasis free areas to Hyper-endemic marshland areaWangZCSunWSXiongYQTianJPZhangJZhangWParasit Infect Dis20086127130in ChineseInvestigation on schistosome infection among migrant workers from rural areasHeJCZhangSQWangTPChenGXCuiDYHeZGChin J Schisto Control200820114116in ChineseSurvey on schistosomiasis among farmers working outside native farmland in rural area of Qianjiang cityZhangYQZhangRQiLJZhangJShuRRHeQXParasit Infect Dis200316264in ChineseEpidemiological and morbidity assessment of Schistosoma japonicum infection in a migrant fisherman community, the Dongting Lake region, ChinaLiYSHeYKZengQRMcManusDPTrans R Soc Trop Med Hyg20039717718110.1016/S0035-9203(03)90112-X14584373Investigation of movement population infected with schistosome in the endemic areas of Guichi cityChenGXWangMSHanSMChin J Schisto Control200113102103in ChineseEpidemiological survey of movement population infected with schistosomiasis in marshland areaZhangSQLiQYWangTPZhangGHWuWDGeJHChin J Zoon1998148586in ChineseMovement population and schistosomiasis transmissionZhengJGuoJGZhuHQChin J Schisto Control199911125127in ChineseEpidemiologic features of Schistosoma japonicum among fishermen and other occupational groups in the Dongting Lake region (Hunan Province) of ChinaRossAGYueshengLSleighASYiLWilliamsGMWuWZWuWZXinsongLYongkangHMcManusDPAm J Trop Med Hyg1997573023089311640Urbanisation and infectious diseases in a globalised worldAlirolEGetazLStollBChappuisFLoutanLLancet Infect Dis20111113114110.1016/S1473-3099(10)70223-121272793Population movement: a key factor in the epidemiology of neglected tropical diseasesAagaard-HansenJNombelaNAlvarJTrop Med Int Health2010151281128810.1111/j.1365-3156.2010.02629.x20976871The classification of population mobility and impact on infectious diseasesRenFFFuHPLiuMLiangWNSoft Science of Health201024272276in ChineseSchistosome infection and control of migrant populationCaoCLGuoJGChin J Schisto Control201022388390in ChineseThe role of population movement in the epidemiology and control of schistosomiasis in Brazil: a preliminary typology of population movementKloosHCorrea-OliveiraRdos ReisDCRodriguesEWMonteiroLAGazzinelliAMem Inst Oswaldo Cruz201010557858610.1590/S0074-0276201000040003820721511A diagnostic challenge for schistosomiasis japonica in China: consequences on praziquental-based morbidity controlZhouYBZhengHMJiangQWParasit Vectors2011419410.1186/1756-3305-4-194319575721981948Collaborative study on evaluation of immunodiagnostic assays in Schistosomiasis japonica by treatment efficacy assessment Collaboration GroupGuanXShiYChin Med J19961096596649275331Rapid detection of a Schistosoma mansoni circulating antigen excreted in urine of infected individualsby using a monoclonal antibodyAttallahAMIsmailHEl MasrySARizkHHandousaAEl BendaryMTabllAEzzatFJ Clin Microbiol199937354357843069889217Detection of circulating anodic antigen by ELISA for seroepidemiology of schistosomiasis mansoniDe JongeNGryseelsBHilberathGWPoldermanAMDeeldeAMTrans R Soc Trop Med Hyg19888259159410.1016/0035-9203(88)90523-83151417Immunodiagnosis of schistosomiasis mansoni in a low endemic area in Surinam by determination of the circulating antigens CAA and CCAVan LieshoutLPandayUGde JongeNKrijgerFWOostburgBFPoldermanAMDeelderAMActa Trop199559929Diagnosis of Schistosoma haematobium by detection of specific DNA fragments from filtered urine samplesIbironkeOAPhillipsAEGarbaALamineSMShiffCAm J Trop Med Hyg201184998100110.4269/ajtmh.2011.10-0691311037521633040Evaluation of polymerase chain reaction as an additional tool for the diagnosis of low-intensity Schistosoma mansoni infectionOliveiraLMSantosHLGonçalvesMMBarretoMGPeraltaJMDiagn Microbiol Infect Dis20106841642110.1016/j.diagmicrobio.2010.07.01620884153Development and evaluation of a sensitive PCR-ELISA system for detection of schistosoma infection in fecesGomesLIDos Santos MarquesLHEnkMJde OliveiraMCCoelhoPMRabelloAPLoS Negl Trop Dis20104e66410.1371/journal.pntd.0000664285764020421918Sensitive and rapid detection of Schistosoma japonicum DNA by loop-mediated isothermal amplification (LAMP)XuJRongRZhangHQShiCJZhuXQXiaCMInt J Parasitol20104032733110.1016/j.ijpara.2009.08.01019735662Assessing the marginal error in diagnosis and cure of Schistosoma mansoni in areas of low endemicity using Percoll and PCR techniquesAllamAFKaderOZakiAShehabAYFaragHFTrop Med Int Health20091431632110.1111/j.1365-3156.2009.02225.x19278527Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasmaWichmannDPanningMQuackTKrammeSBurchardGDGreveldingCDrostenCPLoS Negl Trop Dis20093e42210.1371/journal.pntd.0000422266726019381285A new PCR-based approach for the specific amplification of DNA from different Schistosoma species applicable to human urine samplesSandovalNSiles-LucasMPérez-ArellanoJLCarranzaCPuenteSLópez-AbánJMuroAParasitology200613358158710.1017/S003118200600089816834820Detection by polymerase chain reaction of Schistosoma mansoni DNA in human serum and fecesPontesLADias-NetoERabelloAAm J Trop Med Hyg20026615716212135287Is there reduced susceptibility to praziquantel in Schistosoma japonicum? Evidence from ChinaWangWDaiJRLiHJShenXHLiangYSParasitology20101371905191210.1017/S003118201000120420810006Compliance analysis of the residents with mass medical treatment in areas highly endemic for schistosomiasisGuoJGHuGHXiongYLChin J Parasitol Parasit Dis2000185859in ChineseThe South-to-North Water Diversion Project: effect of the water diversion pattern on transmission of Oncomelania hupensis, the intermediate host of Schistosoma japonicum in ChinaLiangYSWangWLiHJShenXHXuYLDaiJRParasit Vectors201255210.1186/1756-3305-5-52332584122433070Relationship of the livestock trade to schistosomiasis transmission in mountainous areaZhengJGuoJGWangXFZhuHQChin J Parasitol Parasit Dis200018146148in Chinese


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Over the past decades China has made a great stride in controlling schistosomiasis, eliminating transmission of Schistosoma japonicum in 5 provinces and remarkably reducing transmission intensities in the rest of the seven endemic provinces. Recently, an integrated control strategy, which focuses on interventions on humans and bovines, has been implemented throughout endemic areas in China. This strategy assumes that a reduction in transmission of S. japonicum from humans and bovines to the intermediate Oncomelania snail host would eventually block the transmission of this parasite, and has yielded effective results in some endemic areas. Yet the transmission of S. japonicum is relatively complicated – in addition to humans and bovines, more than 40 species of mammalians can serve as potential zoonotic reservoirs. Here, we caution that some factors – potential roles of other mammalian reservoirs and human movement in sustaining the transmission, low sensitivity/specificity of current diagnostic tools for infections, praziquantel treatment failures, changes in environmental and socio-economic factors such as flooding in key endemic areas may pose great obstacles towards transmission interruption of the parasite. Assessing potential roles of these factors in the transmission and implications for current control strategies aiming at transmission interruption is needed.
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REVIEWOpenAccessFactorsimpactingonprogresstowards eliminationoftransmissionofschistosomiasis japonicainChinaYi-BiaoZhou1,2*,SongLiang3,4andQing-WuJiang1,2*AbstractOverthepastdecadesChinahasmadeagreatstrideincontrollingschistosomiasis,eliminatingtransmissionof Schistosomajaponicum in5provincesandremarkablyreducingtransmissionintensitiesintherestoftheseven endemicprovinces.Recently,anintegratedcontrolstrategy,whichfocusesoninterventionsonhumansand bovines,hasbeenimplementedthroughoutendemicareasinChina.Thisstrategyassumesthatareductionin transmissionof S.japonicum fromhumansandbovinestotheintermediate Oncomelania snailhostwould eventuallyblockthetransmissionofthisparasite,andhasyieldedeffectiveresultsinsomeendemicareas.Yetthe transmissionof S.japonicum isrelativelycomplicated – inadditiontohumansandbovines,morethan40speciesof mammalianscanserveaspotentialzoonoticreservoirs.Here,wecautionthatsomefactors – potentialrolesof othermammalianreservoirsandhumanmovementinsustainingthetransmission,lowsensitivity/specificityof currentdiagnostictoolsforinfections,praziquanteltreatmentfailures,changesinenvironmentaland socio-economicfactorssuchasfloodinginkeyendemicareas-mayposegreatobstaclestowardstransmission interruptionoftheparasite.Assessingpotentialrolesofthesefactorsinthetransmissionandimplicationsfor currentcontrolstrategiesaimingattransmissioninterruptionisneeded. Keywords: Schistosomajaponicum ,Integratedcontrolstrategy,TransmissioninterruptionReviewBackgroundWorldwide, Schistosoma infectionsremainaseriouspublic healthproblem,infectingmorethan200millionpeoplein approximately76countrieswithalossof153million disability-adjustedlifeyears(DALYs)[1,2].Ofthespecies ofschistosomesinfectinghumans, Schistosomajaponicum, distributedinsouthernChina,thePhilippines,andparts ofIndonesia,istheonlyschistosomespecieswhosetransmissioniszoonotic[1].China ’ sschistosomiasiscontrol programwasinitiatedinthemid-1950s,andhasundergonethreestages[3-8].Thefirststage(fromthemid1950stomid-1980s)focusedontransmissioncontrol,and thecontrolprogramincludedchemotherapy,snailcontrol primarilybyenvironmentalmanagementortheuseof molluscicide,improvingaccesstocleanwaterandsanitary facilities[3,5].Bytheendofthe1980s,schistosomiasis transmissionwaseliminatedinfourendemicprovinces buttheprevalenceofdiseaseremainedhighintherestof eightendemicprovinces[3,5].Thesecondstage(fromthe mid-1980stotheearly2000s)focusedonmorbiditycontrol,andlarge-scalechemotherapy(duetotheintroductionofpraziquantel)servedasthebackboneofThe NationalSchistosomiasisControlProgram,whichwas complementedwithhealtheducationandcontinuedsnail control[3-8].Inthemid-1990s,schistosomiasistransmissionwaseliminatedinoneoftheremainingeightendemic provinces[3].Despitecontinuedandintensifiedcontrol efforts,controllingtransmissionofthediseaseinthe remainingsevenendemicprovinces(Hubei,Hunan, Anhui,Jiangxi,JiangsuSichuanandYunnanprovinces) hasbeenchallenging,and,eliminatingthetransmissionin theseregionsseemsadauntingtask[3].Anumberof studiesreportedthatbovinesaretheprimaryinfection sourceof S.japonicum transmissioninChina[3,9-12]. *Correspondence: z_yibiao@hotmail.com ; jiangqw@fudan.edu.cn1DepartmentofEpidemiology,SchoolofPublicHealth,FudanUniversity,138 YiXueYuanRoad,Shanghai200032,China2KeyLaboratoryofPublicHealthSafety,MinistryofEducation(Fudan University),138YiXueYuanRoad,Shanghai200032,China Fulllistofauthorinformationisavailableattheendofthearticle 2012Zhouetal.;licenseeBioMedCentralLtd.ThisisanOpenAccessarticledistributedunderthetermsoftheCreative CommonsAttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse,distribution,and reproductioninanymedium,providedtheoriginalworkisproperlycited.Zhou etal.Parasites&Vectors 2012, 5 :275 http://www.parasitesandvectors.com/content/5/1/275

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Basedonthis,thethirdstageofcontrol,alsocalledintegratedcontrol,aimingatreducingtherolesofbovinesand humansasinfectionsources,hasbeenimplementedin Chinasince2005.Withrenewedemphasisontransmissioncontrolandultimatelytransmissioninterruption, controlprogramsatthisstageconsistofagricultural mechanization,fencingbovines(particularlywaterbuffalos),chemotherapyonbothhumansandbovines,health education,provisionofcleanwaterandimprovedsanitation [3].Thisnationalstrategyhassofarachievedpromising resultsandtwonotablepatternshavebeenobserved-in someendemicareastheprevalenceof S.japonicum infectioninhumanswasbroughtbelow1%[3,13],whereasin otherendemicregionswithimplementationofthesame strategy,humaninfectionsweresustainedataround3% [3,14].Morerecently,therewasadiscussiononthe generalizabilityofthisnationalintegratedstrategytocontrolandeventuallyinterruptthetransmissionof S.japonicum ,whichwasbasedonthestudiesinlakeregionsof China,andinhillyandmountainousregionsofSichuan andYunnanthetransmissionecologyisquitedifferent [15].Concernhasbeenraisedthat,inadditiontohumans andbovines,theremightbeotherfactorsthatimplicate thetransmissionbutareneglected[14,16,17].Herewe summarizethesefactorsbasedonasystematicreviewof publishedliteratureandfocusonnon-bovineanimal hosts,humanmovements,lowsensitivity/specificityof currentdiagnostictoolsforschistosomeinfection,and praziquanteltreatmentfailureandtheirimplicationsfor thecurrentschistosomiasiscontrolstrategyinChina.The followingdatabaseswereusedforidentifyingrelevantarticles:PubMed,CochraneLibrary,ScienceCitationIndex Expanded,ChinaNationalKnowledgeInfrastructure, WanfangDatabase,VIPDatabase,andProQuest.Norestrictionwasappliedtoyearofpublication.Alltitlesand abstractswereindependentlyexaminedandscreenedby tworeviewerstochecktheireligibilityforinclusioninthe review.Anarticlewasincludedinthetablesofthispaper ifitmetoneofthefollowingcriteriaincluded:(1)report onprevalenceofinfectionof S.japonicum innon-bovine animalhostsinChina;(2)reportonprevalenceofinfectionof S.japonicum inmigrantpopulationsinChina. Uponinclusion,fullpaperswereretrievedandreviewed bythesametworeviewers.Non-bovineanimalhostsS.japonicum ,unlike S.mansoni and S.haematobium ,is widelyrecognizedasazoonoticparasite.Over40species ofwildanddomesticatedanimalscanserveasreservoir hostsforthisparasite[9].Thezoonoticnatureof S. japonicum complicatescontroleffortsfortheparasite. InChinaanumberofnon-humanmammalianhosts, suchasbovines,pigs,dogs,cats,goats/sheep,andrats, canserveasreservoirhostsandareofpotentialpublic healthimportance(Table1)[10,11,16,18-26].Inaddition tobovines,relativelyhighinfectionlevelswerealso foundinothermammalianhostsinsomeendemicareas (Table1)[10,11,16,18-26].Highprevalencesof S.japonicum infectionsinrats(59.8%)andin Oncomelania snails (0.4-3.1%)werereportedintwoislandslocatedinthe Table1Reportedprevalenceofinfectionof Schistosomajaponicum amongdifferentnon-humanhostsinChinaAuthoranddateof publication Environmental type Definitivehosts BovinePigDogGoat/sheepCatDonkeyHorseMuleRodentRabbit LuDB etal .(2010)[ 16 ]Marshland*355004855000---00Marshland † -3984-375----Hill*0000189-26---265Hill † -00211-53---177WangTP etal .(2006)[ 18 ]Marshland ‡ 269742733300----Marshland§15400410015----XuGY etal .(1999)[ 19 ]Marshland-------598WangTP etal .(1997)[ 20 ]Marshland4872130713000---83182 SunLP etal .(1997)[ 21 ]Marshland221267-------XuFS etal .(1995)[ 22 ]Mountain369-30----SuZW etal .(1994)[ 23 ]Lake357600750------GuXG etal .(1993)[ 24 ]Mountain369-30-----09DaiZJ etal .(1991)[ 10 ]Mountain423677585--135--ZhengJ etal .(1990)[ 11 ]Mountain17313282420043343214ChenDJ etal .(1989)[ 25 ]Mountain152171750108--47-571YaoBY etal .(1989)[ 26 ]Mountain1659396000018143517-Note:*=2006; † =2007; ‡ =Chenqiaovillage;§=Guanghuivillage.Zhou etal.Parasites&Vectors 2012, 5 :275 Page2of7 http://www.parasitesandvectors.com/content/5/1/275

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YangtzeRiver[19].Thetwoislandshaveonlyemerged inthelast40years,humansdonotinhabittheseislands. Highinfectionstogetherwithestimatesofhightransmissionindex(measuredbyexcretedeggsperday)were alsoreportedindogs,cats,andratsinahillyareaof Chinawherenoinfectedbovineswerefound[16].A similarpatternwasalsoreportedinSamarProvince,the Philippines,wherehighprevalencesandintensitiesof S. japonicum infectionwerealsoobservedindogs(14.9% prevalence)andrats(29.5%prevalence),suggestingthat dogscouldpotentiallybeaveryimportantreservoirhost of S.japonicum inthatregion[27,28].Amodelingstudy indicatedthatratsmayalsoplayaroleinhumaninfectionsinSamar[27].Thesefindingssuggestedthatthe transmissionof S.japonicum mightoccurintheabsence ofbovines.Inaddition,highgeneticvariationin S.japonicum wasfoundinthemarshlandandlakeendemic regionsofChina(wherebovinesareconsideredasan importantsourceofinfection)andtwomaingenetic clusterswerediscovered,separatingthestraininbovines andhumansfromthatingoats,dogs,pigsandcats[18]. Theresultindicatedthat S.japonicum frombovinesand humansmightbedifferentfromthatfromothermammaliananimalsinlakeandmarshlandareasofsouthern China.Alsonotablewasthattheprevalenceof S.japonicum infectioninpigs,dogsandcatsincreasedwhenthe bovineswithhighprevalenceofinfectionwereremoved fromtheendemicarea[16].Thestrainfrombovinesand humansmaybemoreprevalentthanthosefromother mammaliananimalsinlakeandmarshlandareasof southernChina.Whenthepredominantstrainiscompletelyorpartlyremovedfromendemicareas,theother strainmaybecomepredominant.Furtherstudiesare neededtoaddressthisquestion,forexample,molecular epidemiologicalresearchshouldbeperformedtoaddress whetherthestrainscross-infecthumansandevaluate relativecontributionofdifferentanimalreservoirsto sustainthetransmission.Withoutimprovedknowledge ontheseissues,therelianceofhuman-andbovineorientedcontroltoachievefullcontrolofinfection sourcesmightmisssomeotherimportantsourcesof infection.HumanmovementThesecondpotentialobstacleinmovingtowardsthe eliminationofschistosomiasistransmissionrelatesto humanmovement.AlongwithChina ’ srapideconomic developmentandurbanizationoverthepastdecades, thecountryhaswitnessedthelargesthumanmovement, inparticularrural – urbanmigrationinthehumanhistory(Table2)[29-37].Forexample,themovement populationofruralmigrantsmovingtocoastalcitiesis approximately120million[38].Meanwhile,largepopulationmovementsarealsooccurringbetweencities,in particularfromsmallcitiestobigcities[38].Ithaslong beenrecognizedthathumanmovementplaysanimportantroleintheepidemiologyofmanyinfectiousdiseases [38-40].Forexample,someinfectiousdiseases(e.g. leishmaniasis,Chagasdisease,lymphaticfilariasis,and schistosomiasis)haveemergedorre-emergedinurban areasorpreviouslycontrolledregions,whichhavebeen linkedtohumanmovements[38,41]. Theoccurrenceofschistosometransmissioninurban areasorre-emergenceofthetransmissioninpreviously controlledareasweremostprobablythroughinfected migrantsandendemicfociwaspresentinlargecities suchasinBamako,Kampala,ChangshaandDarel Salam[38,41].Theimpactofhumanmigrationonthe transmissionofschistosomiasishasbeenreported.For example,areportinBrazilindicatedthatmigrantsplay animportantroleinthetransmissionofschistosomiasis, andthepresenceofmobilepopulations(e.g.migrants, returneesandtourists)inendemicregionscanalsoimpactsignificantlyonthecontroleffectivenessof Table2Prevalenceofinfectionof Schistosomajaponicum indifferentmigrantpopulationsAuthoranddateofpublicationMovementtypeProportionofmigration(%)Prevalence(%) ChenGX etal .(2011)[ 29 ]Migrationfromendemicareastootherareas224-38526-53 WangZC etal .(2008)[ 30 ]Migrationfromnon-endemicareastoendemicareas>53125 HeJC etal .(2008)[ 31 ]Migrationfromendemicareastootherareas-32 Migrationfromnon-endemicareastoendemicareas-30 ZhangYQ etal .(2003)[ 32 ]Migrationfromendemicareastootherareas299260 LiYS etal .(2003)[ 33 ]Fishingpopulation-689 ChenGX etal .(2001)[ 34 ]Migrationfromendemicareastootherareas197156 ZhangSQ etal .(1998)[ 35 ]Migrationfromendemicareastootherareas198-32421-139 ZhengJ etal .(1999)[ 36 ]Fishingpopulation-182-842 Boatman-542-694 Herdsman-412 RossAG etal .(1997)[ 37 ]Fishingpopulation-224 Zhou etal.Parasites&Vectors 2012, 5 :275 Page3of7 http://www.parasitesandvectors.com/content/5/1/275

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schistosomiasisduetoinsufficienthealthservices[42]. Yet,thispotentialremainslargelyunknowninChina.In additiontolackofinformationonthespatialandtemporalpatternsofpopulationmovements,littleisavailableontheepidemiologicalimpactofthemovement patternsontransmissionandmaintenanceofschistosomiasisinChina.Hence,studiestounderstandhow humanmovements(e.g.betweenendemicandendemic areas,endemicandnon-endemicareas)impactthe transmissionandcontrolareneeded.Inadditionto humanmovement,livestockmovement(e.g.through livestocktradeormovementtonewgrazingfields)also occursfrequentlyinendemicregionsinChina[42],and thisraisesanotherconcernforthecurrentnationalcontrolstrategy.DiagnostictestsWhileextensivecontroleffortsinendemicareashave greatlysuppressedthetransmissionlevels,selective chemotherapywithpraziquantelfocusingoninfected individualsbecomesanimportantcomponentofthenationalcontrolprogram,andthusdiagnosisofinfectionis akeystepfordeterminationoftargetpopulationsfor treatment,evaluationofmorbidity,andassessmentof controlmeasures[43].Withdecreasinginfectionintensitiesduetoextensivecontrolefforts,widelyuseddirect parasitologicaltechniques(e.g.miracidiumhatchtest (MHT)andKato-Katzthicksmear(KK))havebecome increasinglyinsensitive[43].KKandMHTarethetwo widelyfield-applieddirectparasitologicalmethodsin China.ThesensitivityofKKmethodrangesgenerally from40%to70%,whileforMHTitvariesfrom24%to 95%,dependingprimarilyonthelevelsofinfectionintensities[43].Thesensitivitiesofthesedirectparasitologicaltechniquesdecreasegenerallywithdecreasein infectionlevelsofhumans.TheinsensitivitiesofKKand MHTmethodsleadtomissingdiagnosisofinfected casesinareasoflowendemicity,andinpost-treatment situations.Otherwidelyfield-applieddiagnosticalternativesareindirectimmunodiagnosticassays(i.e.detecting schistosome-specificantibodies),e.g.Circumovalprecipitintest(COPT),Indirecthemagglutinationassay (IHA),Enzyme-linkedimmunosorbentassay(ELISA) andDipstickdyeimmunoassay(DDIA).Theseantibody detectionassayshaverelativelyhighsensitivities,but generallylowspecificities.Thespecificityvarieswidely foreachtest-55%to96%forCOPTmethod,35%to 94%forIHAmethod,20%to93%forELISAmethod, and33%to97%forDDIA[43].Theseantibodydetectiontechniquescannotdifferentiatebetweencurrentand pastinfections.Thus,theinsensitivityornon-specificity ofthecurrentlyfield-applieddiagnosticmethodsmay resultindifficultiesinidentifyingtrueinfectedindividualsforselectivechemotherapyandassessingthe effectivenessofinterventions,collectivelyposingasignificantobstacleinmovingtowardscompletecontrolof schistosomiasis.TherearemanyotherdiagnosticmethodssuchasclinicalorultrasonographicmethodsmeasuringthemorbidityassociatedSchistosomiasisjaponica, questionnaires,directimmunologicaltestsdetectingthe schistosome-derivedantigens,andthehistologicalmethodsdetectingschistosomeeggsintissuebiopsies,but clinicalorultrasonographicmethods,andquestionnaires lackspecificityinsomeareassuchasChina[43].Althoughthecirculatingantigendetectionassayshavea relativelyhighspecificity,theyarenotanybetterthan theeggdetectionassaysintermsofsensitivityinareas oflowendemicity[44-47].Thehistologicaldiagnostic methodwithbothhighsensitivityandhighspecificityis neithersimplenorconvenientforpopulation-based investigations.Recently,polymerasechainreaction (PCR)basedtechniquesfordetectionofschistosome DNAinstoolorseraandplasmahavebeendeveloped, showingpromiseasahighlysensitiveandspecificassay fordiagnosisofschistosomeinfection[48-55].OtherneglectedfactorsOtherneglectedfactors(e.g.praziquanteltreatmentfailures,frequentflooding,andenvironmentalandsocioeconomicchanges)mayalsoposechallengestothe currentcontrolprogram.Thepraziquanteltreatment failuresincludetreatmentnon-complianceanddrugresistance.Thechemotherapywithpraziquantelhasbeen implementedwidelyinendemicregionsinChinasince the1990s,especiallyduringthe10-yearWorldBank LoanProject(WBLP)[56].Thecomplianceratesof chemotherapydropinmanycommunitiesafterrepeated roundsofmassorselectivetreatment[57].Although currentlythereisnoevidenceofpraziquantelresistance for S.japonicum ,theresistanceisfoundinotherschistosomaspecies(e.g. S.mansoni )[56].Frequentflooding alongtheYangtzeRiverandinthelakeregions(e.g. DongtingLakeandPoyangLakeregions)havecontributedtothespreadoftheintermediatehost Oncomelania hupensis ,andmightcounteractcontrolefforts[4].Environmentalchanges,causedbyreturningreclaimedland tothelake,constructionandoperationofThreeGorges dam,andtheSouth-to-Northwatertransferproject, mightcreatenewhabitatsfor O.hupensis [4,58] .DiscussionAlthoughbovinesarelargelyresponsiblefortransmissionof S.japonicum inthelakeandmarshlandregions ofChina theyareamajorsourceofincomesforlocal farmers.ThelargemarshlandareasofDongtingLake andPoyangLakeareanaturalandidealpasturefor bovinesandgoats,andprovidenaturalhabitatsforthe intermediatesnailhost.ItisdifficulttoremoveallZhou etal.Parasites&Vectors 2012, 5 :275 Page4of7 http://www.parasitesandvectors.com/content/5/1/275

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bovinesfromorcompletelyfencepasturesonthelarge marshlandareas,sincethefarmershaveherdedbovines, especiallywaterbuffaloes,inthemarshlandareasfor generations[17].Evenifallbovineswereremovedfrom orwellfencedfromthelargemarshlandareassome time,itisalsochallengingtomaintainthestateof “ withoutbovines ” onthemarshlandareasforalongperiodof timebecausebovinemovementalsooccursfrequentlyin thelakesandmarshlandregionsduetolivestocktrade ornewgrazingfields[59].So,fencingpasturesorremovingbovinesoftenconflictswiththetraditionalway ofraisinglivestock(especiallywaterbuffalo)andfarmers ’ incomes,andthisconsiderableconflictmightreduce thecontroleffortsoftheongoingintegratedcontrol strategy,asfencingpasturesisoneofthekeytechnical measuresofthecontrolstrategy[3].Hence,thisintegratedcontrolstrategyshouldbeimplementedinthe lightoflocalconditionsofendemicareasformutual benefitanddevelopment.Forexample,theenvironmentalmanagementshouldbeencouragedtobeimplementedinsomesnail-inhabitedmarshlandareassuitablefor agriculturalorforestrypractices(e.g.,Croppingcoleor wheat,plantingtreesforcontrollingsnails),thus,the farmersnotonlymightincreasetheirincomes,butalso bovinescouldbewellfencedbythesemodifiedsnailinhabitedmarshlandareas,andsnailscouldbecontrolledbytheenvironmentalmanagement. AlthoughmuchisknownaboutmigrationinChina, thetypologyofpopulationmovementiscomplexand remainslesswellcharacterized[40].Thereareatleast twotypesofpopulationmovementsrelatedtoschistosomiasistransmissioninChina(Table2)[29-37]:a)fishermen,boatmenandherderswhomovearoundinrivers orlakes;b)Peoplemovingseasonallyforpaidwork(e.g. 1)peoplefromendemicareasmovingintootherendemicregions;2)peoplefromnon-endemicareasmovingtoendemicareas;3)fromendemicareasto controlledareas;4)fromendemicareastonon-endemic areasbutbacktoendemicareas).Tensofthousandsof fishermen,boatmenandherders,withahighprevalence andintensityof S.japonicum infection,movearoundin DongtingLakeandPoyangLakewhicharestrongholds ofschistosomiasisendemicareasinChina(Table2) [33,36,37].Thesepeoplefrequentlycontactinfected water,andtheirstoolsgenerallygointothewateror snailhabitatsdirectly.Ithasbeenwell-knownthatthese migrantfishermenandbovinesareresponsiblefora largeproportionofthetotalcontaminationoftheenvironmentwith Schistosoma eggsandarehencedriversin maintainingtransmissionofthediseaseinthelakeand marshlandareasofsouthernChina[33].Theadministrationofchemotherapyorstoolcollectionforthese nomadsisverydifficultandlittleisknownabouttheoptimaltreatmentwindowforthesenomads.Seasonal mobilityforpaidworkhasbeenverycommoninrecent yearsinChina,e.g.someruralyounglabourersfromendemicareasleavetheirhomesintheslackseason(in farming),andreturninthebusyseason(infarming), andothermigrantsonlyreturntotheirhomeannually intheChineseNewYear.Somelabourersfromnonendemicregionsenterendemicareasforagriculturein thebusyseasonandleaveintheslackseason.Inthe currentnationalcontrolprogramofschistosomiasis, praziquantel-basedchemotherapyisimplementedgenerallyonlyinendemicareasinautumneachyear(i.e.slack seasonforfarming),andthetargetpopulationofchemotherapyisusuallythelocalresidents,notnon-local people[3,14].So,mostofmigrantsinfectedwith S.japonicum aremissedforthetreatment,andcontinuetobe theinfectionsources.Hence,thetargetpopulationand timeofchemotherapyinthenationalcontrolprogram ofschistosomiasisshouldbeadjustedinlightofthepatternsofpopulationmovement,forexample,thetarget populationofchemotherapyshouldincludethenonlocalpeopleinfectedwith S.japonicum ,andchemotherapyshouldalsobeimplementedintheChineseNew Yearwhenmostoftheinfectedmigrantsreturntotheir homefortheSpringFestival. Itisunclearwhetherschistosomiasistransmission couldbemaintainedbytheseneglectedfactorsinthe absenceofbovines.Toaddressthisquestionfurther studyisneeded,andthelong-termeffectivenessofthe comprehensivenationalstrategyshouldbealsofurther evaluated[9].Forexample,somelongitudinalstudies shouldbecarriedouttodetermineorevaluatewhether theseneglectedfactorsareimportantfor S.japonicum transmission.ConclusionThecurrentintegratedstrategyinChinaassumedthat blockingthetransmissionof S.japonicum fromhuman andcattletosnailswouldstemthetransmissionofthis parasite[13].Yet,theprocessof S.japonicum transmissionis,infact,relativelycomplicated,andmightbeabettedbyotherdomesticated(e.g.dogs,cats,andgoats) andwild(e.g.rats,andrabbits)animals,bypopulation movement,andbysocialandhydrologic(e.g.flooding) linksamongsomefocal ‘ hotspots ’ oftransmission. Whileweareworkingtowardsthetransmissioneliminationof S.japonicum ,thesefactors,whicharecurrently neglectedintheintegratedstrategy,needtobepaid someattentionbypublichealthauthorities.Competinginterests Theauthorsdeclarethattheyhavenocompetinginterests. Authors ’ contributions YBZ,SLandQWJwrotethemanuscripttogether,YBZsummarizedthe Tablesandallauthorshavereadandapprovedthefinalversionofthe manuscript.Zhou etal.Parasites&Vectors 2012, 5 :275 Page5of7 http://www.parasitesandvectors.com/content/5/1/275

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Acknowledgements ThisworkissupportedbyNationalHighTechnologyResearchand DevelopmentProgramofChina(No.2006AA02Z402),theNationalS&T MajorProgram(GrantNo.2012ZX10004-220and2008ZX10004-011),National NaturalScienceFoundationofChina(No.30590374),andShanghaiLeading AcademicDisciplineProject(ProjectNo.B118). Authordetails1DepartmentofEpidemiology,SchoolofPublicHealth,FudanUniversity,138 YiXueYuanRoad,Shanghai200032,China.2KeyLaboratoryofPublicHealth Safety,MinistryofEducation(FudanUniversity),138YiXueYuanRoad, Shanghai200032,China.3DepartmentofEnvironmentalandGlobalHealth, CollegeofPublicHealthandHealthProfessions,UniversityofFlorida, Gainesville,FL32610,USA.4EmergingPathogensInstitute,Universityof Florida,Gainesville,FL32610,USA. Received:17October2012Accepted:27November2012 Published:3December2012 References1.GryseelsB,PolmanK,ClerinxJ,KestensL: Humanschistosomiasis. Lancet 2006, 368: 1106 – 1118. 2.GrayDJ,McManusDP,LiYS,WilliamsGM,BergquistR,RossAG: Schistosomiasiselimination:lessonsfromthepastguidethefuture. LancetInfectDis 2010, 10: 733 – 736. 3.WangLD,GuoJG,WuXH,ChenHG,WangTP,ZhuSP,ZhangZH, SteinmannP,YangGJ,WangSP,WuZD,WangLY,HaoY,BergquistR, UtzingerJ,ZhouXN: China'snewstrategytoblock Schistosoma japonicum transmission:experiencesandimpactbeyondschistosomiasis. TropMedIntHealth 2009, 14: 1475 – 1483. 4.WangLD,UtzingerJ,ZhouXN: Schistosomiasiscontrol:experiencesand lessonsfromChina. Lancet 2008, 372: 1793 – 1795. 5.LinDD,HuGH,ZhangSJ: Optimalcombinedapproachesoffield interventionforschistosomiasiscontrolinChina. ActaTrop 2005, 96: 242 – 247. 6.JiangQW,WangLY,GuoJG,ChenMG,ZhouXN,EngelsD: Morbidity controlofschistosomiasisinChina. ActaTrop 2002, 82: 115 – 125. 7.YuanHC,JiangQW,ZhaoGM,HeN: Achievementsofschistosomiasis controlinChina. MenInstOswaldoCruz 2002, 97 (Suppl1):187 – 189. 8.ZhouXN,WangLY,ChenMG,WuXH,JiangQW,ChenXY,ZhengJ, UtzingerJ: Thepublichealthsignificanceandcontrolof schistosomiasis-thenandnow. ActaTrop 2005, 2005 (96):97 – 105. 9.GrayDJ,WilliamsGM,LiY,McManusDP: Transmissiondynamicsof Schistosomajaponicum inthelakesandmarshlandsofChina. PLoSOne 2008, 3: e4058. 10.DaiZJ,YanJB,ChenDR,XieZM,XieDW,LiaoTB: Studyonepidemic factorsandregularityofschistosomiasisjaponicainmountainousdistrict ofliangshanyiautouomousprefecture. SouthestChinJAgriSci 1991, 4: 115 – 120.inChinese. 11.ZhengJ,QianK,YaoBY,ZhuHQ,ChenSH,ZhangR: Studieson distributioncharacteristicsofinfectionsourcesofschistosomiasisin mountainousregions. ChinJSchistoControl 1990, 2: 24 – 27.inChinese. 12.DavisGM,WuPW,ChenHG,LiuHY,GuoJG,LinDD,LuSB,WilliamsG,SleighA,FengZ,McManusDP: Abaselinestudyofimportanceofbovines forhumanSchistosomajaponicuminfectionsaroundPoyangLake, China:villagesstudiedandsnailsamplingstrategy. AmJTropMedHyg 2002, 66: 359 – 371. 13.WangLD,ChenHG,GuoJG,ZengXJ,HongXL,XiongJJ,WuXH,WangXH, WangLY,XiaG,HaoY,ChinDP,ZhouXN: Astrategytocontrol transmissionofSchistosomajaponicuminChina. NEnglJMed 2009, 360: 121 – 128. 14.ZhouYB,LiangS,ChenGX,ReaC,HeZG,ZhangZJ,WeiJG,ZhaoGM, JiangQW: Anintegratedstrategyfortransmissioncontrolof Schistosoma japonicum inamarshlandareaofChina:findingsfromafive-year longitudinalsurveyandmathematicalmodeling. AmJTropMedHyg 2011, 85: 83 – 88. 15.SetoEYW,RemaisJV,CarltonEJ,WangS,LiangS,BrindleyPJ,QiuD,Spear RC,WangLD,WangTP,ChenHG,DongXQ,WangLY,HaoY,BergquistR, ZhouXN: Towardsustainableandcomprehensivecontrolof schistosomiasisinChina:lessonsfromSichuan. PLoSNeglTropDis 2011, 5: e1372. 16.LuDB,WangTP,RudgeJW,DonnellyCA,FangGR,WebsterJP: Contrasting reservoirsforSchistosomajaponicumbetweenmarshlandandhilly regionsinAnhui,China – atwo-yearlongitudinalparasitologicalsurvey. Parasitology 2010, 137: 99 – 110. 17.HeHB: Thoughtofschistosomiasiscontrolstrategywithemphasison controllingsourcesofinfectioninlakeandmarshlandendemicregions. ChinJSchistoControl 2011, 23: 710 – 713. 18.WangTP,ShrivastavaJ,JohansenMV,ZhangSQ,WangFF,WebsterJP: Doesmultiplehostsmeanmultipleparasites?Populationgenetic structureof Schistosomajaponicum betweendefinitivehostspecies. IntJParasit 2006, 2006 (36):1317 – 1325. 19.XuGY,TianJC,ChenGM,YangHM,QiuL,HuHB: Observationonnatural focaldiseaseofschistosomiasisinrattusnorvegicusinNanjing. JPractParasitDis 1999, 7: 4 – 6.inChinese. 20.WangTP,GuoJH,WuWC,ZhangSQ,LuDB,ZhangGH: Theinfection sourcesofschistosomiasisjaponicaandtheirroleinthetransmissionof thisdiseaseinmarshlandareas,Anhuiprovince. ParasitPrevRes 1997, 26: 138 – 140.inChinese. 21.SunLP,HongQB,CaoQ,GuBL,GaoZH,GuoBY: Roleofdifferent infectionsourcesinthetransmissionofschistosomiasisjaponicain marshlandregion. ChinJSchistoControl 1997, 9: 44 – 45.inChinese. 22.XuFS,GuXG,ZhaoWX,LiYX,YinHZ,ZhaoLG:Roleofdifferentinfection sourcesinthetransmissionofschistosomiasisjaponicainmountainous region. JPractParasitDis 1995, 3: 129.inChinese. 23.SuZW,HuCQ,FuY,ChenW,HuanXB: Roleofseveralhostin transmissionofschistosomiasisjaponicainlakeregion. ChinJParasitol ParasitDis 1994, 12: 48 – 51.inChinese. 24.GuXG,ZhaoWX,XuFS,QiuDC,HanY,ChenGY: Analysison epidemiologyofschisotosomiasisinmountainousterraceregionsin Sichuanthroughatypicalinvestigation. ChinJSchistoControl 1993, 5: 82 – 84.inChinese. 25.ChenDJ,GongZB: Epidemiologicalsurveyofschistosomiasisinhigh mountainousregioninEryuancountyofYunnanprovince. ChinJSchisto Control 1989, 1: 10 – 13.inChinese. 26.YaoBY,ZhengJ,QianK,ChenSH,ZhuHQ,WuWP: Theroleoftheanimal hostintheepidemiologyofschistosomiasisinmountainousregions. ChinJSchistoControl 1989, 1: 1 – 3.inChinese. 27.RileyS,CarabinH,BeLisleP,JosephL,TalloV,BalolongE,WillinghamAL, FernandezTJ,GonzalesRO,OlvedaR,McGarveyST: Multi-hosttransmission dynamicsof Schistosomajaponicum inSamarProvince,thePhilippines. PLoSMed 2008, 5: e18. 28.RudgeJW,CarabinH,BalolongE,TalloV,ShrivastavaJ,LuDB,BasezMG, OlvedaR,McGarveyST,WebsterJP: Populationgeneticsofschistosoma japonicumwithinthePhilippinessuggesthighlevelsoftransmission betweenhumansanddogs. PLoSNeglTropDis 2008, 2: e340. 29.ChenGX,HeZG,HanSM: Investigationonprevalenttrendsandanalysis ofcontrolperiodamongfloatingpopulationinschistosomiasisendemic areasofGuichiDistrict. ChinJSchistoContro 2011, 23: 148 – 153. inChinese. 30.WangZC,SunWS,XiongYQ,TianJP,ZhangJ,ZhangW: Seroepidemiologicalsurveyonfloatingpopulationimmigratedfrom schistosomiasisfreeareastoHyper-endemicmarshlandarea. ParasitInfectDis 2008, 6: 127 – 130.inChinese. 31.HeJC,ZhangSQ,WangTP,ChenGX,CuiDY,HeZG: Investigationon schistosomeinfectionamongmigrantworkersfromruralareas. ChinJSchistoControl 2008, 20: 114 – 116.inChinese. 32.ZhangYQ,ZhangR,QiLJ,ZhangJ,ShuRR,HeQX: Surveyon schistosomiasisamongfarmersworkingoutsidenativefarmlandinrural areaofQianjiangcity. ParasitInfectDis 2003, 1: 62 – 64.inChinese. 33.LiYS,HeYK,ZengQR,McManusDP: Epidemiologicalandmorbidityassessmentof Schistosomajaponicum infectioninamigrantfisherman community,theDongtingLakeregion,China. TransRSocTropMedHyg 2003, 97: 177 – 181. 34.ChenGX,WangMS,HanSM: Investigationofmovementpopulation infectedwithschistosomeintheendemicareasofGuichicity. ChinJSchistoControl 2001, 13: 102 – 103.inChinese. 35.ZhangSQ,LiQY,WangTP,ZhangGH,WuWD,GeJH: Epidemiological surveyofmovementpopulationinfectedwithschistosomiasisin marshlandarea. ChinJZoon 1998, 14: 85 – 86.inChinese. 36.ZhengJ,GuoJG,ZhuHQ: Movementpopulationandschistosomiasis transmission. ChinJSchistoControl 1999, 11: 125 – 127.inChinese.Zhou etal.Parasites&Vectors 2012, 5 :275 Page6of7 http://www.parasitesandvectors.com/content/5/1/275

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37.RossAG,YueshengL,SleighAS,YiL,WilliamsGM,WuWZ,WuWZ,Xinsong L,YongkangH,McManusDP: EpidemiologicfeaturesofSchistosoma japonicumamongfishermenandotheroccupationalgroupsinthe DongtingLakeregion(HunanProvince)ofChina. AmJTropMedHyg 1997, 57: 302 – 308. 38.AlirolE,GetazL,StollB,ChappuisF,LoutanL: Urbanisationandinfectious diseasesinaglobalisedworld. LancetInfectDis 2011, 11: 131 – 141. 39.Aagaard-HansenJ,NombelaN,AlvarJ: Populationmovement:akeyfactor intheepidemiologyofneglectedtropicaldiseases. TropMedIntHealth 2010, 15: 1281 – 1288. 40.RenFF,FuHP,LiuM,LiangWN: Theclassificationofpopulationmobility andimpactoninfectiousdiseases. SoftScienceofHealth 2010, 24: 272 – 276. inChinese. 41.CaoCL,GuoJG: Schistosomeinfectionandcontrolofmigrant population. ChinJSchistoControl 2010, 22: 388 – 390.inChinese. 42.KloosH,Correa-OliveiraR,dosReisDC,RodriguesEW,MonteiroLA, GazzinelliA: Theroleofpopulationmovementintheepidemiologyand controlofschistosomiasisinBrazil:apreliminarytypologyofpopulation movement. MemInstOswaldoCruz 2010, 105: 578 – 586. 43.ZhouYB,ZhengHM,JiangQW: Adiagnosticchallengeforschistosomiasis japonicainChina:consequencesonpraziquental-basedmorbidity control. ParasitVectors 2011, 4: 194. 44.GuanX,ShiY: Collaborativestudyonevaluationofimmunodiagnostic assaysinSchistosomiasisjaponicabytreatmentefficacyassessment CollaborationGroup. ChinMedJ 1996, 109: 659 – 664. 45.AttallahAM,IsmailH,ElMasrySA,RizkH,HandousaA,ElBendaryM,Tabll A,EzzatF: RapiddetectionofaSchistosomamansonicirculatingantigen excretedinurineofinfectedindividualsbyusingamonoclonalantibody. JClinMicrobiol 1999, 37: 354 – 357. 46.DeJongeN,GryseelsB,HilberathGW,PoldermanAM,DeeldeAM: DetectionofcirculatinganodicantigenbyELISAforseroepidemiology ofschistosomiasismansoni. TransRSocTropMedHyg 1988, 82: 591 – 594. 47.VanLieshoutL,PandayUG,deJongeN,KrijgerFW,OostburgBF, PoldermanAM,DeelderAM: Immunodiagnosisofschistosomiasis mansoniinalowendemicareainSurinambydeterminationofthe circulatingantigensCAAandCCA. ActaTrop 1995, 59: 9 –29. 48.IbironkeOA,PhillipsAE,GarbaA,LamineSM,ShiffC: Diagnosisof SchistosomahaematobiumbydetectionofspecificDNAfragmentsfrom filteredurinesamples. AmJTropMedHyg 2011, 84: 998 – 1001. 49.OliveiraLM,SantosHL,GonalvesMM,BarretoMG,PeraltaJM: Evaluation ofpolymerasechainreactionasanadditionaltoolforthediagnosisof low-intensitySchistosomamansoniinfection. DiagnMicrobiolInfectDis 2010, 68: 416 – 421. 50.GomesLI,DosSantosMarquesLH,EnkMJ,deOliveiraMC,CoelhoPM, RabelloA: DevelopmentandevaluationofasensitivePCR-ELISAsystem fordetectionofschistosomainfectioninfeces. PLoSNeglTropDis 2010, 4: e664. 51.XuJ,RongR,ZhangHQ,ShiCJ,ZhuXQ,XiaCM: Sensitiveandrapid detectionofSchistosomajaponicumDNAbyloop-mediatedisothermal amplification(LAMP). IntJParasitol 2010, 40: 327 – 331. 52.AllamAF,KaderO,ZakiA,ShehabAY,FaragHF: Assessingthemarginal errorindiagnosisandcureofSchistosomamansoniinareasoflow endemicityusingPercollandPCRtechniques. TropMedIntHealth 2009, 14: 316 – 321. 53.WichmannD,PanningM,QuackT,KrammeS,BurchardGD,GreveldingC, DrostenC: Diagnosingschistosomiasisbydetectionofcell-freeparasite DNAinhumanplasma. PLoSNeglTropDis 2009, 3: e422. 54.SandovalN,Siles-LucasM,Prez-ArellanoJL,CarranzaC,PuenteS,LpezAbnJ,MuroA: AnewPCR-basedapproachforthespecificamplification ofDNAfromdifferentSchistosomaspeciesapplicabletohumanurine samples. Parasitology 2006, 133: 581 – 587. 55.PontesLA,Dias-NetoE,RabelloA: Detectionbypolymerasechainreaction ofSchistosomamansoniDNAinhumanserumandfeces. AmJTropMed Hyg 2002, 66: 157 – 162. 56.WangW,DaiJR,LiHJ,ShenXH,LiangYS: Istherereducedsusceptibility topraziquantelinSchistosomajaponicum?EvidencefromChina. Parasitology 2010, 137: 1905 – 1912. 57.GuoJG,HuGH,XiongYL: Complianceanalysisoftheresidentswithmass medicaltreatmentinareashighlyendemicforschistosomiasis. ChinJParasitolParasitDis 2000, 18: 58 – 59.inChinese. 58.LiangYS,WangW,LiHJ,ShenXH,XuYL,DaiJR: TheSouth-to-North WaterDiversionProject:effectofthewaterdiversionpatternon transmissionofOncomelaniahupensis,theintermediatehostof SchistosomajaponicuminChina. ParasitVectors 2012, 5: 52.59.ZhengJ,GuoJG,WangXF,ZhuHQ: Relationshipofthelivestocktradeto schistosomiasistransmissioninmountainousarea. ChinJParasitolParasit Dis 2000, 18: 146 – 148.inChinese.doi:10.1186/1756-3305-5-275 Citethisarticleas: Zhou etal. : Factorsimpactingonprogresstowards eliminationoftransmissionofschistosomiasisjaponicainChina. Parasites&Vectors 2012 5 :275. Submit your next manuscript to BioMed Central and take full advantage of: € Convenient online submission € Thorough peer review € No space constraints or color “gure charges € Immediate publication on acceptance € Inclusion in PubMed, CAS, Scopus and Google Scholar € Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit Zhou etal.Parasites&Vectors 2012, 5 :275 Page7of7 http://www.parasitesandvectors.com/content/5/1/275