Correlation between clonorchiasis incidences and climatic factors in Guangzhou, China
© Li et al.; licensee BioMed Central Ltd. 2014
Received: 20 August 2013
Accepted: 9 January 2014
Published: 15 January 2014
Human infection with Clonorchis sinensis is still a big public health problem in Guangzhou. To investigate the correlation between clonorchiasis and climatic factors, we analyzed the clonorchiasis reported cases and simultaneous meteorological data during 2006–2012 in Guangzhou City, China.
Annual incidence rate of clonorchiasis from 2006 to 2012 was 166.76, 191.55, 247.37, 213.82, 246.03, 274.71, and 239.63 (per 100 000), respectively. Each 1°C rise of temperature corresponded to an increase of 1.18% (95% CI 0.88% to 1.48%) in the monthly number of cases, and a one millimeter rise of rainfall corresponded to increase of 0.03% (95% CI 0.01% to 0.04%). Whereas each one percent rise of relative humidity corresponded to a decrease in the number of cases by 1.51% (95% CI -1.75% to -1.27%).
We reported incidence rates of clonorchiasis showed an increasing trend by years. Temperature and rainfall were positively associated with clonorchiasis incidence, while relative humidity was inversely associated with clonorchiasis incidence. Our study provided evidence that climatic factors affect the occurrence of clonorchiasis in Guangzhou city, China.
Clonorchiasis, also known as liver fluke disease, is a major foodborne parasitoses and caused by Clonorchis sinensis that parasitizes the human intrahepatic bile duct. Globally, clonorchiasis is mainly distributed in East Asia and Southeast Asia, including China, Korea, Vietnam, and the Philippines. It is estimated that more than 200 million people are at risk of infection, 15–20 million people are infected, and 1.5–2 million show symptoms or complications. Based on the second national survey on parasitic diseases between 2001 and 2004 in China, the overall Clonorchiasis sinensis infection rate of the surveyed population was 0.58%, and Guangdong was the most endemic province with estimated infection rate of 5.36%.
Since 1995 Guangzhou government (capital city of Guangdong providence) has legislated to include clonorchiasis into a local reportable disease inventory. This means that physicians who diagnose suspected or confirmed clonorchiasis cases must report these cases to Guangzhou Centers for Disease Control and Prevention (GZCDC) through the National Notifiable Disease Report System (NNDRS). Despite complementary interventions such as information, education and communication on safe food practices and others, which were implemented and improved by the health department, the incidence of clonorchiasis still showed a rapid increasing trend in Guangzhou. Of particular note, in 2012, a total of 3,075 cases were reported, which is nearly two times the number reported in 2006 (1,662 cases). Controlling the spread of clonorchiasis infection is becoming a matter of urgency in Guangzhou, public health authorities are concerned about its increased incidence.
In recent decades, weather variables have been widely studied for their potential as early warning tools to fend off climate-sensitive infectious diseases such as dengue fever, malaria, and respiratory tract infections. However, very little information is available for using meteorological variables to predict clonorchiasis infection. In this study, we used ecological methodology to investigate clonorchiasis epidemiological features in the subtropical city of Guangzhou for the period of 2006–2012, and compared those with the climate factors, in an effort to assess the relationship between meteorological variables and clonorchiasis, and to assist public health prevention and control measures.
Clonorchiasis cases were obtained from NNDRS. In China, all cases of clonorchiasis were diagnosed according to the unified diagnostic criteria issued by Chinese Ministry of Health (MOH). The confirmation of diagnosis relies on 1) detecting clonorchis eggs in stool samples (Triple Kato-Katz thick smears), and/or 2) detecting worm-specific antibodies in serum samples or worm-specific antigens in serum or stool samples (ELISA or real-time PCR). Simultaneous meteorological data, including daily average temperature (in degrees Centigrade), relative humidity (as a percentage), atmospheric pressure (in hPa), wind velocity (in meters per second), sunshine (in hours) and rainfall (in millimeter) were obtained from the documentation of the Guangzhou Meteorological Bureau (GZMB). The weather data were measured at a fixed-site station located in the center district of Guangzhou. Meteorological instruments included barometers, pressure readings, thermometers, anemometers, actinometers, psychrometers, evaporimeters, and weather vanes, etc. The measurements of temperature, relative humidity, atmospheric pressure and wind velocity were usually taken every three hours before the daily average being calculated. However, for the sunshine and rainfall, the daily total was used.
Descriptive statistics (e.g. rate, proportion, mean and median) were used to describe the basic features of clonorchiasis confirmed cases in the study. A negative binomial multivariable regression was used to explore the relationship between meteorological variables and clonorchiasis. Negative binomial distribution is a Poisson distribution with an extra-dispersion term, the extra dispersion term acts as a random effect that subjects the Poisson means to additional variation that has a gamma distribution. Given the data were over-dispersed, we chose negative binomial distribution model rather than Poison model. The cases were clonorchiasis occurrence. Data were presented as the prevalence of clonorchiasis per 100,000 inhabitants grouped by month of onset. The meteorological variables were calculated by monthly average or aggregate. A preliminary analysis was conducted through Pearson’s correlation coefficient (‘r’) matrix within meteorological variables. Two separate negative binomial regression models were carried out: the first included average temperatures but no atmospheric pressure, while the second considered atmospheric pressure but no temperature. Both models included additionally relative humidity, wind velocity, sunshine, rainfall, and year as independent variables. In the final model, those variables with a P value of <0.05 in the preliminary model were included. To quantify the effects of meteorological variables, we computed the influences (eβ - 1), which correspond to the percent increase. The residual was checked using Pearson goodness of fit. The analyses were carried out with SAS (V.8.01, SAS Institute, Cary, New Jersey, USA).
Summary statistics for monthly clonorchiasis confirmed cases and weather conditions in Guangzhou, China, 2006-2012
Average temperature (°C)
Average atmospheric pressure (hPa)
Average relative humidity (%)
Average wind velocity (m/s)
Aggregate rainfall (mm)
Aggregate sunshine (h)
Clonorchiasis confirmed cases
Pearson’s correlation coefficient (‘r’) matrix of meteorological variables in Guangzhou, China, 2006-2012
-0.59 (p < 0.001)
-0.86 (p < 0.001)
0.32 (p < 0.001)
-0.58 (p < 0.001)
0.52 (p < 0.001)
0.53 (p < 0.001)
-0.28 (p = 0.01)
-0.43 (p < 0.001)
0.40 (p < 0.001)
-0.16 (p = 0.15)
-0.10 (p = 0.36)
0.20 (p = 0.06)
-0.28 (p = 0.01)
-0.12 (p = 0.29)
0.06 (p = 0.99)
Negative binomial regression model of meteorological factors associated with risk of clonorchiasis incidence*
(e β - 1) = percent increase (%)
95% CI for percent increase (%)
Average relative humidity
Average wind velocity
Average atmospheric pressure
Average relative humidity
Average wind velocity
Average relative humidity
We found the incidence of clonorchiasis showed an increasing trend by years in Guangzhou, this is consistent with the finding from northern cities of China. Numerous studies revealed that occurrence of cholelithiasis is related to the unhealthy habits of residents who like to have raw fish or half-raw fish. However, our study also demonstrated that more cases were observed in males, farmers, ages 45–64 years and rural residents. These findings indicated that the infection of clonorchiasis may be associated with special labor activities. In Guangzhou, it is very common for people to use human feces as fertilizer, this cultivation and breeding practice may increase the risk of clonorchiasis infection because the feces may be highly saturated with Clonorchis sinensis eggs. Furthermore, there is evidence that human beings can become infected via the accidental ingestion of Clonorchis sinensis metacercariae via their hands, contaminated as a consequence of not washing after catching freshwater fish. Therefore, integrated strategies and measures should be implemented to control clonorchiasis in these endemic areas.
The increasing evidence for rapid global climate change has highlighted the need for investigations examining the relationship between weather variability and infectious diseases. However, the impact of weather fluctuations on clonorchiasis is still not well understood. Our current study, which was conducted in Guangzhou, demonstrated that climate factors had a significant influence on clonorchiasis infection. We found high temperature presented higher risk of clonorchiasis infection. This finding is in agreement with Liang’s findings, which showed that when temperature was elevated from 24.3 to 37.2 degrees C, the infection rate of clonorchiasis in the snails Parafossarulus striatulus and Alocinma longicornis increased from 12.5% to 18.0%. A possible explanation for this may be due to the fact that temperatures are important causes of variability in egg hatching, as well as the activities of intermediate host. For example, a natural field investigation of Sichuan providence, China, indicated that rate of red bean snails infection with Clonorchis sinensis miracidia was noticeable high in the warm season (May-October) whereas almost zero in the cold season (November-March). The high temperature was believed to contribute significantly to high activities of snails.
To the best of our knowledge, the relationship between relative humidity and clonorchiasis has not been reported. The result of current study showed that the relative humidity of air was negatively correlated with incidence of clonorchiasis. No literatures have been published yet revealing the underlying mechanism. A very similar report was also documented in Thailand which indicated that of 6,000 examinees, the largest number of human infections with Opisthorchis viverrini occurred in dry season. However, when viewing the observation on schistosomes, most published studies reached the opposite conclusion. For example, a study of Pakistan reported that Pearson’s correlation between snails’ infection with schistosome cercariae and relative humidity was significantly (P < 0.05) positive. Although the authors did not give an explanation for this, it is true that egg hatching of schistosomes needs a moist environment. Therefore, the finding of the current study requires replication, especially in different areas with different weather patterns. More efforts, which focus on the mechanism of climate factors affecting the parasite infection, also need to be undertaken in future.
Some limitations must be acknowledged. First of all, we used the clonorchiasis data from NNDRS, which do not capture all cases in the community. This under-reporting of infectious can occur anywhere in the report chain, from the initial decision of patient to not seek health care to failure to record a case in the disease registry, due to the mildness or lack of symptoms. Secondly, the incubation period of 30 days for every case cannot be determined exactly. We thus chose to use monthly aggregated data of clonorchiasis and monthly average or aggregate meteorological data, the direction of these approximations are likely to be random, suggesting that our risk estimates are reliable. Thirdly, owing to this investigation being an ecological study, although we emphasized the impact of climate, we could not exclude potential confounding factors. For example, the diagnosis bias, our study did not identify clonorchiasis co-infection with intestinal flukes. It is reported that the co-infection with clonorchiasis and minute intestinal flukes (MIF) is very common in some area of China. On the other hand, considering the increase of clonorchiasis reports over the years, we added the “year” as a variable in the model to control the yearly variance. Even though, reporting bias may also exist due to the data we used from NNDRS. In addition, other factors such as socio-economic factors, sanitation service levels, and personal hygiene awareness etc., need to be addressed in further studies.
In conclusion, despite these limitations, we reported that the incidence of clonorchiasis showed an increasing trend by years in Guangzhou. A rise of temperature and rainfall may increase the risk of clonorchiasis infection, whereas an increase in relative humidity may reduce the risk of clonorchiasis infection. Our study provided evidence that climatic factors affect the occurrence and transmission of clonorchiasis, which may be useful for developing an early warning system.
The authors are all epidemiologists in Guangzhou center for disease control and prevention (GZCDC). The authors regularly conduct the surveillance on infectious disease, filed investigation on outbreak, emergent management on public health crisis, and research on risk factor and transmission of diseases.
This work was supported by the Research Fund from the Health Bureau of Guangzhou (grant number 201102A212006, 20121A010015), Science and Technology Bureau of Guangzhou (grant number 2012Y2-00020), Guangdong Science and Technology Program (grant number 2012B040304002), The Project For Key Medicine Discipline Construction Of Guangzhou Municipality (grant number 2013-2015-07).
All enrollees who participated in the study are appreciated. We wish to give special thanks to the public unit coordinators and nurses in hospitals in Guangzhou.
- Xu Y, Chen W, Bian M, Wang X, Sun J, Sun H, Jia F, Liang C, Li X, Zhou X, Huang Y, Yu X: Molecular characterization and immune modulation properties of Clonorchis sinensis-derived RNASET2. Parasit Vectors. 2013, 6: 360-10.1186/1756-3305-6-360.PubMed CentralView ArticlePubMedGoogle Scholar
- Rim HJ: Clonorchiasis: an update. J Helminthol. 2005, 79: 269-281. 10.1079/JOH2005300.View ArticlePubMedGoogle Scholar
- Xue-Ming L, Ying-Dan C, Yi O, Hong-Man Z, Rui L, Weil M: Overview of human clonorchiasis sinensis in China. Southeast Asian J Trop Med Public Health. 2011, 42: 248-254.PubMedGoogle Scholar
- Liu X, Li LS, Feng Y, Li H: [A national survey on current status of the important parasitic diseases in human population] (in Chinese). Chin J Parasitol Parasit Dis. 2005, 23: 332-340.Google Scholar
- Wu W, Qian X, Huang Y, Hong Q: A review of the control of clonorchiasis sinensis and Taenia solium taeniasis/cysticercosis in China. Parasitol Res. 2012, 111: 1879-1884. 10.1007/s00436-012-3152-y.View ArticlePubMedGoogle Scholar
- Li T: Varicella emergency vaccination seemed instrumental in declining chickenpox incidence in Guangzhou, Southern China. Rev Inst Med Trop Sao Paulo. 2013, 55: 217-10.1590/S0036-46652013000300016.View ArticleGoogle Scholar
- Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, Fang YY: Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis. 2005, 5: 31-41. 10.1016/S1473-3099(04)01252-6.View ArticlePubMedGoogle Scholar
- Li T, Yang Z, Luo L, Wang M: Dengue fever epidemiological status and relationship with meteorological variables in Guangzhou, Southern China, 2007–2012. Biomed Environ Sci. 2013, in pressGoogle Scholar
- Li T, Yang Z, Wang M: Temperature, relative humidity and sunshine may be the effective predictors for occurrence of malaria in Guangzhou, southern China, 2006–2012. Parasit Vectors. 2013, 6: 155-10.1186/1756-3305-6-155.PubMed CentralView ArticlePubMedGoogle Scholar
- Li T, Yang Z, Wang M: Diurnal temperature range may be the risk factor for respiratory tract infections among the elderly in Guangzhou, China. Int J Biometeorol. 2013, in press, PMID:23687823Google Scholar
- 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: 163-166.PubMedGoogle Scholar
- Qian MB, Chen YD, Fang YY, Tan T, Zhu TJ, Zhou CH, Wang GF, Xu LQ, Zhou XN: Epidemiological profile of Clonorchis sinensis infection in one community, Guangdong, People’s Republic of China. Parasit Vectors. 2013, 6: 194-10.1186/1756-3305-6-194.PubMed CentralView ArticlePubMedGoogle Scholar
- Animal Diversity Web: Clonorchis sinensis. (http://animaldiversity.ummz.umich.edu/accounts/Clonorchis_sinensis/) Accessed 7 December 2013
- Cross JH: Changing patterns of some trematode infections in Asia. Arzneimittelforschung. 1984, 34: 1224-1226.PubMedGoogle Scholar
- Wei JB, Qu ZQ, Feng C: Comprehensive evaluation of clonorchiasis epidemiological factors by probability accumulation test in Guangan, Sichuan Province (in Chinese). Chin J Parasit Dis Contr. 1997, 10: 259-263.Google Scholar
- Liang C, Hu XC, Lv ZY, Wu ZD, Yu XB, Xu J, Zheng HQ: Experimental establishment of life cycle of Clonorchis sinensis (in chinese). Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 2009, 27: 148-150.PubMedGoogle Scholar
- Ye XP, Fu YL, Wu ZX, Anderson RM, Agnew A: The effects of temperature, light and water upon the hatching of the ova of Schistosoma japonicum. Southeast Asian J Trop Med Public Health. 1997, 28: 575-580.PubMedGoogle Scholar
- Prasopdee S, Kulsuntiwong J, Piratae S, Khampoosa P, Thammasiri C, Suwannatrai A, Laha T, Grams R, Loukas A, Tesana S: Temperature dependence of Opisthorchis viverrini infection in first intermediate host snail, Bithynia siamensis goniomphalos. Acta Trop. 2013, (in press)Google Scholar
- CAO Zhiguo: Prevalent status of clonorchiasis and its control in China (in Chinese). China Tropical Medicine. 2007, 8: 1455-1457.Google Scholar
- Yang J, Zhao Z, Li Y, Krewski D, Wen SW: A multi-level analysis of risk factors for Schistosoma japonicum infection in China. Int J Infect Dis. 2009, 13: e407-e412. 10.1016/j.ijid.2009.02.005.View ArticlePubMedGoogle Scholar
- Xu XJ, Wei FH, Yang XX, Dai YH, Yu GY, Chen LY, Su ZM: Possible effects of the Three Gorges dam on the transmission of Schistosoma japonicum on the Jiang Han plain, China. Ann Trop Med Parasitol. 2000, 94: 333-341.PubMedGoogle Scholar
- Xu XJ, Yang XX, Dai YH, Yu GY, Chen LY, Su ZM: Impact of environmental change and schistosomiasis transmission in the middle reaches of the Yangtze River following the Three Gorges construction project. Southeast Asian J Trop Med Public Health. 1999, 30: 549-555.PubMedGoogle Scholar
- Li G, He X, Saidu K: Epidemiology and control of clonorchiasis sinensis in China. Southeast Asian J Trop Med Public Health. 2001, 32: 8-11.Google Scholar
- Wykoff DE, Harinasuta C, Juttijudata P, Winn MM: Opisthorchis viverrini in Thailand-the life cycle and comparison with O. felineus. J Parasitol. 1965, 51: 207-214. 10.2307/3276083.View ArticlePubMedGoogle Scholar
- Niaz S, Akhtar T, Hasanat A, Qureshi AW: Prevalence of snails and Schistosome cercariae and correlation with meteorological factors in Punjab, Pakistan. Iran J Vet Res. 2013, 14: 161-164.Google Scholar
- Lin LJ, Wen LY: Role of Oncomelania hupensis in transmission of schistosomiasis japonica (in Chinese). Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi. 2013, 25: 83-85.PubMedGoogle Scholar
- Jeon HK, Lee D, Park H, Min DY, Rim HJ, Zhang H, Yang Y, Li X, Eom KS: Human infections with liver and minute intestinal flukes in Guangxi, China: analysis by DNA sequencing, ultrasonography, and immunoaffinity chromatography. Korean J Parasitol. 2012, 50: 391-394. 10.3347/kjp.2012.50.4.391.PubMed CentralView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. 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.