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.

S oil-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.

The Study
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.
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 middleaged age groups in surveys 1 and 2 and in older age groups in survey 3.

Conclusions
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 (13).   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.