Volume 20, Number 11—November 2014
Increasing Prevalence and Intensity of Foodborne Clonorchiasis, Hengxian County, China, 1989–2011
During 1989–2011, three parasitic disease surveys were conducted in Hengxian County, China, where soil-transmitted helminthiases and foodborne clonorchiasis are endemic. We compared the data and found that the prevalence of helminthiases decreased and the prevalence and intensity of clonorchiasis increased over time, especially among men. Clonorchiasis control/intervention measures are urgently needed in this area.
Soil-transmitted helminthiases (STHs), parasitic diseases of humans, are caused by a group of intestinal nematodes, including roundworms (Ascaris lumbricoides), whipworms (Trichuris trichiura), and hookworms (Ancylostoma duodenale and Necator americanus) (1,2). Clonorchiasis, another parasitic disease of humans, is caused by ingestion of raw freshwater fish harboring infective Clonorchis sinensis metacercariae (3,4). STHs and clonorchiasis are endemic to China. STHs occur mainly in western and southern China, where environmental conditions are more favorable to helminths and social infrastructure is limited; clonorchiasis occurs predominantly in southeastern and northeastern China, where residents commonly eat raw fish. According to 2 national parasitic disease surveys conducted during 1988–1992 and 2001–2004, the prevalence of STHs in China decreased from 53.6% to 19.6% and prevalence of clonorchiasis increased from 0.3% to 0.6% between surveys (5,6).
Hengxian County (2010 population 860,000 persons), located in southern China, was one of the areas sampled in 1989 (survey 1) and 2002 (survey 2), and a third survey was conducted in the county in 2011. We used data from surveys 1–3 to determine epidemiologic changes in STHs and clonorchiasis over time in Hengxian County.
Survey 1 sampled 1 natural village from each of 5 different towns in Hengxian County. (Towns in China have several administrative villages, the basic level of administration, which often comprise >1 natural villages) Each sampled natural village had 500–600 residents, all of whom were eligible for survey participation. The same procedures were followed in survey 2, but only 3 towns were sampled. Survey 3 sampled 8 towns and 3 administrative villages within each town. Dozens of households were surveyed from each administrative village, and all household members >5 years of age were eligible for participation; ≈200 villagers were selected in each administrative village. In each survey, a single fecal sample from each participant was used to prepare a Kato-Katz thick smear to determine the presence of helminths and count C. sinensis eggs.
Prevalence was determined by sex and age groups. Participants were categorized as <4 years, 5–9 years, 10–14 years, 15–19 years, 20–29 years, 30–39 years, 40–49 years, 50–59 years, 60–69 years, or >70 years of age. Overall prevalence was standardized according to data from the 2010 census for Hengxian County. We defined infection intensity as the geometric mean number of eggs per gram of feces (EPG) in the egg-positive survey participants; lg(EPG + 1) transformation was used to calculate infection intensity in all survey participants. We used Student t test and analysis of variance to compare infection intensities between sexes and among surveys, respectively; Fisher least significant difference test was used to compare between individual surveys. Logarithmic correlation was used to explore the relationship between prevalence and infection intensity in age groups.
Survey 1 had 2,623 participants; surveys 2 and 3 had 1,748 and 3,437, respectively (Table 1). During surveys 1–3, the standardized prevalences were 19.7%, 30.5%, and 46.5%, respectively, for clonorchiasis and 86.3%, 25.1%, and 7.0%, respectively, for STHs. The corresponding standardized prevalences were 69.8%, 13.8%, and 0.5% for roundworm infections; 55.7%, 11.2%, and 1.4% for whipworm infections; and 24.3%, 6.3%, and 5.3% for hookworm infections.
During surveys 1–3, the standardized prevalences of clonorchiasis were 10.4%, 20.8%, and 29.2%, respectively, among females and 28.5%, 39.6%, and 62.9%, respectively, among males. The corresponding standardized prevalences of STHs were 86.2%, 29.5%, and 9.4% among females and 86.3%, 20.9%, and 4.7% among males. The corresponding standardized prevalences of roundworm, whipworm, and hookworm infections among males and females showed a decreasing trend similar to that for the total STHs.
In surveys 1–3, clonorchiasis prevalence increased fairly steadily by age group to middle age, after which, prevalence continued to increase with age in survey 1 and decreased with age in surveys 2 and 3 (Figure 1, panel A). STHs prevalence changed irregularly by age group in surveys 1 and 2 but increased gradually by age group in survey 3 (Figure 1, panel B). Prevalences of roundworm and whipworm infections usually peaked among children 5–14 years of age; hookworm infections peaked in middle-aged age groups in surveys 1 and 2 and in older age groups in survey 3.
In C. sinensis egg–positive participants, the geometric mean numbers of EPG were 367.3 EPG, 833.3 EPG, and 942.9 EPG in surveys 1–3, respectively (F = 36.2, p<0.001) (Table 2). Differences were significant between survey 1 and surveys 2 and 3 (p<0.001) but not between survey 2 and survey 3 (p = 0.210). In surveys 1–3, geometric mean numbers of EPG were 241.7 EPG, 364.9 EPG, and 405.1 EPG, respectively, among females (F = 3.3, p<0.05) and 419.8 EPG, 1,199.7 EPG, and 1,363.2 EPG, respectively, among males (F = 43.6, p<0.001). Among all participants, the geometric mean numbers of EPG were 1.6 EPG, 6.3 EPG, and 38.2 EPG during surveys 1–3, respectively (F = 522.9, p<0.001); differences between surveys were all significant (p<0.001). In surveys 1–3, geometric mean numbers of EPG were 0.6 EPG, 2.2 EPG, and 6.8 EPG, respectively, among females (F = 137.6, p<0.001) and 3.1 EPG, 13.5 EPG, and 171.5 EPG, respectively, among males (F = 474.4, p<0.001). Among egg-positive participants and all participants, infection intensities were all significantly lower among females than males, and infection intensities increased as ages increased, reaching a peak in middle-aged persons and then decreasing in older persons (Figure 2).
In surveys 1–3, clonorchiasis prevalence in different age groups was significantly correlated with the corresponding infection intensity in terms of the geometric mean number of EPG after logarithmic transformation (p<0.01). Determination coefficients (R2) were 0.709, 0.891, and 0.748 in surveys 1–3, respectively, when only egg-positive participants were included in the analysis; corresponding R2 were 0.901, 0.980, and 0.997, respectively, for all participants.
Analysis of data from 3 parasitic disease surveys conducted in Hengxian County over the last 22 years showed substantial decreases in the trend of STHs prevalence and substantial increases in the patterns of clonorchiasis prevalence and infection intensity. These findings indicate a transitioning pattern of the most prominent parasitic disease changing from STHs to clonorchiasis. Distribution patterns of prevalence and infection intensity among sex and age groups showed that men have been most affected by increases in C. sinensis transmission and infection. Thus, control measures and health education programs are urgently needed, especially among men, to reduce C. sinensis disease and transmission.
National STHs surveillance showed a similar decreasing trend (7). This trend may partly be explained by massive health education programs and chemotherapy for STHs, which were implemented in schools in China after the first national parasitic disease survey (8). In addition, over the last 30 years, rapid economic development has occurred in China, resulting in increased availability of safe water and establishment of sanitary lavatories for improved hygiene (9). Furthermore, the increased use of chemical fertilizer has reduced the use of human feces as fertilizer (a source of helminth transmission) (10). However, economic development has also promoted development of aquaculture and made it economically possible for more residents to include freshwater fish in their diets, a source of C. sinensis metacercariae when consumed raw (11).
Clonorchiasis is a neglected parasitic disease in China: no nationwide intervention or control programs have been implemented to reduce the caseload (12). A third national survey is expected to be conducted beginning in 2014, which will provide updated data regarding the national status of clonorchiasis and an impetus for public health control/intervention and education programs. A national clonorchiasis surveillance system should also be established to gather up-to-date information and inform public health policymakers.
Mr Qian works as an assistant professor at the National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention. His research focuses on the epidemiology of clonorchiasis, including the disease burden, intervention strategies, and evaluation of new diagnosis methods and drugs.
We thank the staff in the National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Guangxi Center for Disease Control and Prevention, and Hengxian Center for Disease Control and Prevention for organization of this study in the field and for sample collection and examination.
This project was funded through a capacity-building initiative for Ecohealth Research on Emerging Infectious Disease in Southeast Asia, which was supported by IDRC (International Development Research Centre), the Canadian International Development Agency, and AusAID (Australian Agency for International Development) in partnership with the Global Health Research Initiative (grant no. 105509-00001002-023); and through a National S&T Major Program grant (no. 2008ZX10004-011).
- de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol. 2003;19:547–51.
- Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367:1521–32.
- Sripa B, Kaewkes S, Intapan PM, Maleewong W, Brindley PJ. Food-borne trematodiases in Southeast Asia: epidemiology, pathology, clinical manifestation and control. Adv Parasitol. 2010;72:305–50 .
- Qian MB, Chen YD, Liang S, Yang GJ, Zhou XN. The global epidemiology of clonorchiasis and its relation with cholangiocarcinoma. Infect Dis Poverty. 2012;1:4.
- Chen YD, Tang LH, Xu LQ. Current status of soil-transmitted nematode infection in China. Biomed Environ Sci. 2008;21:173–9 .
- Chen YD, Zhou CH, Xu LQ. Analysis of the results of two nationwide surveys on Clonorchis sinensis infection in China. Biomed Environ Sci. 2012;25:163–6 .
- Zang W, Zhang XQ, Chen YD. Analysis on the epidemiological situation of soil-transmitted nematodiasis at monitoring spots from 2006 to 2010 [in Chinese]. International Journal of Medical Parasitic Diseases. 2013;40:144–8.
- Ministry of Health and National Education Commission. Program of comprehensive control on intestinal helminth infections in schools [in Chinese]. Chinese Journal of School Health. 1992;13:78–9.
- Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, Utzinger J. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med. 2012;9:e1001162 .
- Department of Comprehensive Statistics of National Bureau of Statistics. China compendium of statistics 1949–2008. Beijing: China Statistics Press; 2009.
- Keiser J, Utzinger J. Emerging foodborne trematodiasis. Emerg Infect Dis. 2005;11:1507–14 .
- Qian MB, Chen YD. Yan Fei. Time to tackle clonorchiasis in China. Infect Dis Poverty. 2013;2:4