• 1

    Eckert J, Deplazes P, 1999. Alveolar echinococcosis in human: The current situation in Central Europe and the need for countermeasures. Parasitol Today 15 :315–319.

    • Search Google Scholar
    • Export Citation
  • 2

    Wen H, Chai JJ, Wang JC, Wang SH, Wang XY, Feng XH, Zhou HX, 2002. Hydatid Control within a Continental System in P.R.China. Craig P, Pawlowski Z, eds. Cestode Zoonoses: Echinococcosis and Cysticercosis. NATO Science Series. Amsterdam: IOS Press, 355–366.

  • 3

    Vuitton DA, Zhou HX, Bresson-Hadni S, Wang Q, Piarroux M, Raoul F, Giraudoux P, 2003. Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127 :S87–S107.

    • Search Google Scholar
    • Export Citation
  • 4

    Qiu JM, Liu FJ, Schantz P, Ito A, Carol D, He JG, 1999. Epidemiological Survey of Hydatidosis in Tibetan Areas of Western Sichuan Province. Larrieu E, Romeo S, Mehapide C eds. XXXIII Archivos Internacionales de la Hidatidosis: 84.

  • 5

    Kern P, Ammon A, Kron M, Sinn G, Sander S, Petersen LR, Gaus W, Kern P, 2004. Risk factors for alveolar echinococcosis in humans. Emerg Infect Dis 10 :2088–2093.

    • Search Google Scholar
    • Export Citation
  • 6

    Craig PS, Giraudoux P, Shi D, Bartholomot B, Barnish G, Delattre P, Quere JP, Harraga S, Bao G, Wang Y, Lu F, Ito A, Vuitton DA, 2000. An epidemiological and ecological study of human alveolar echinococcosis transmission in south Gansu, China. Acta Trop 77 :167–177.

    • Search Google Scholar
    • Export Citation
  • 7

    Budke CM, Campos-Poncec M, Wang Q, Torgerson PR, 2005. A canine purgation study and risk factor analysis for echinococcosis in a high endemic region of the Tibetan plateau. Vet Parasitol 127 :43–49.

    • Search Google Scholar
    • Export Citation
  • 8

    Wang Q, Vuitton DA, Qiu JM, Giraudoux P, Xiao YF, Schantz PM, Raoul F, Li TY, Yang W, Craig P, 2004. Fenced pasture: a possible risk factor for human alveolar echinococcosis in Tibetan pastoralist communities of Sichuan, China. Acta Trop 90 :285–293.

    • Search Google Scholar
    • Export Citation
  • 9

    Wang Q, Qiu JM, Schantz P, He JG, Ito A, Liu F, 2001. Risk factors for development of human hydatidosis among people whose family is raising livestock in western Sichuan Province, China. Chin J Parasitic Dis Parasitol 19 :289–293.

    • Search Google Scholar
    • Export Citation
  • 10

    Ito A, Nakao M, Kutsumi H, Lightowlers MW, Itoh M, Sato S, 1993. Serodiagnosis of alveolar hydatid diseases by Western blotting. Trans R Soc Trop Med Hyg 87 :170–172.

    • Search Google Scholar
    • Export Citation
  • 11

    Bartholomot B, Vuitton D, Harraga D, Shi DZ, Giraudoux P, Barnish G, Wang YH, Macpherson CNL, Craig PS, 2002. Combined ultrasound and serologic screening for hepatic alveolar echinococcosis in central China. Am J Trop Med Hyg 66 :23–29.

    • Search Google Scholar
    • Export Citation
  • 12

    Schantz PM, Wang H, Qiu J, Liu FJ, Saito E, Emshoff A, Ito A, Roberts JM, Delker C, 2003. Echinococcosis on the Tibetan Plateau: prevalence and risk factors for cystic and alveolar echinococcosis in Tibetan populations in Qinghai Province, China. Parasitology 127 :S109–S120.

    • Search Google Scholar
    • Export Citation
  • 13

    Bresson-Hadni S, Vuitton DA, Bartholomot B, Heyd B, Godard D, Meyer JP, Hrusovsky S, Becker MC, Mantion G, Lenys D, Miguet JP, 2000. A twenty-year history of alveolar echinococcosis in humans: analysis of a series of 117 patients from eastern France. Eur J Gastroenterol 12 :327–336.

    • Search Google Scholar
    • Export Citation
  • 14

    Yang YR, Vuitton DA, Jones MK, Craig PS, McManus DP, 2005. Brain metastasis of alveolar echinococcosis in a hyperendemic focus of Echinococcus multilocularis infection. Trans R Soc Trop Med Hyg 99 :937–941.

    • Search Google Scholar
    • Export Citation
  • 15

    Lawson JR, Gemmell MA, 1985. The potential role of blowflies in the transmission of taeniid tapeworm eggs. Parasitology 91 :129–143.

  • 16

    Li G, Shi XQ, 1985. A case report of human AE in Heilongjiang. Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih 3 :8.

  • 17

    Yu SH, Xu LQ, Jiang ZX, Xu SH, Han JJ, Zhu YG, Chang J, Lin JX, Xu FN, 1994. Report on the first national wide survey of human parasites in China 1. Regional distribution of parasite species. Chin J Parasitic Dis Parasitol 12 :241–247.

    • Search Google Scholar
    • Export Citation
  • 18

    Craig PS, Deshan L, MacPherson CN, Dazhong S, Reynolds D, Barnish G, Gottstein B, Zhirong W, 1992. A large focus of alveolar echinococcosis in central China. Lancet 340 :826–831.

    • Search Google Scholar
    • Export Citation
  • 19

    Giraudoux P, Delattre P, Takahashi K, Raoul F, Quere K-P, Craig P, Vuitton D, 2002. Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multiscale approaches? Craig P, Pawlowski Z, eds. Cestode Zoonoses: Echinococcosis and Cysticercosis. NATO Science Series, Amsterdam: IOS Press, 251–266.

  • 20

    Giraudoux P, Craig PS, Delattre P, Bao G, Bartholomot B, Harraga S, Quere JP, Raoul F, Wang Y, Shi D, Vuitton DA, 2003. Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127 (Suppl)127:S121–S131.

    • Search Google Scholar
    • Export Citation
  • 21

    Schantz PM, 1993. Echinococcus multilocularis in North America. Uchino J, Sato N, eds. Alveolar Echincoccosis of the Liver. Volume 30. Sapporo, Japan: Hokkaido University School of Medicine. Medical Library Series, 11–20.

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

SOCIOECONOMIC AND BEHAVIOR RISK FACTORS OF HUMAN ALVEOLAR ECHINOCOCCOSIS IN TIBETAN COMMUNITIES IN SICHUAN, PEOPLE’S REPUBLIC OF CHINA

View More View Less
  • 1 World Health Organization Collaborating Centre on Prevention and Treatment of Human Echinococcosis, Santé et Environnement Rural-Université de Franche-Comté (SERF) and Laboratoire de Biologie Environnementale (LBE) Unité sous contrat avec l’Institut National de la Recherche Agronomique (Usc INRA) Research Units, Université de Franche-Comté, Besançon, France; Sichuan Provincial Center for Disease Control and Prevention, Chengdu, Sichuan, People’s Republic of China; Division of Parasitic Diseases, National Center for Infectious Diseases, Centers For Disease Control and Prevention, Atlanta, Georgia; Cestode Zoonoses Research Group, Bioscience Research Institute and School of Environment and Life Sciences, University of Salford, Salford, United Kingdom

Data from two cross-sectional investigations on 7,138 subjects were used to explore risk factors of human alveolar echinococcosis (AE) in Tibetan communities. The overall human AE prevalence was 3.1% (223 of 7,138), females had a higher prevalence (3.6%, 132 of 3,713) than males (2.7%, 91 of 3,425; P = 0.011), and herdsmen had a higher prevalence (5.2%, 154 of 2,955) than farmers (1.8%, 12 of 661; P < 0.001) and urban populations (2.1%, 49 of 2,360; P < 0.001). Age in all populations, number of dogs kept, fox skin ownership in farmers, not preventing flies from landing on food in herdsmen, using open streams as drinking water sources, and playing with dogs in urban populations were statistically significant risk factors. The results suggest that AE is highly endemic in the eastern Tibetan plateau, in Sichuan Province, the role of the dog is important for human infection, and other factors associated with environmental contamination may vary according to structure and practices of communities.

INTRODUCTION

Human alveolar echinococcosis (AE), which is caused by the metacestode of the fox tapeworm Echinococcus multilocularis, is considered one of the most pathogenic and chronic parasitic zoonoses in the northern hemisphere.1 It is a major public health problem in western China.2,3 In Sichuan Province, China, AE mostly affects Tibetan communities and the prevalence was 1.9% in one study.4 Risk factors for human AE are not generally known precisely, but the role of foxes as contaminating definitive hosts is usually well recognized.3 A recent study in Europe on 40 cases and 120 controls showed that being a farmer, living in a dwelling close to the fields, going into forests for vocational reasons, growing leaf or root vegetables, chewing grass and eating unwashed strawberries were significant risk factors.5 A role for dogs in Gansu Province, China, in Alaska, and more recently in Europe has been suggested.5,6 Actual risk factors on the Tibetan plateau are unknown.

In Sichuan, surveys of definitive hosts for adult tapeworm infection showed E. multilocularis in 44.4% of Tibetan foxes (Vulpes ferrilata), in 12.1–25.0% of stray dogs,4 and in 12% of owned dogs purged using arecoline.7 In the pastoral areas of endemic Tibetan communities, E. multilocularis larval infection was observed in 25% of plateau voles (Microtus irene) and in small lagomorphs (6.7% of the black-lipped pika (Ochotona curzoniae), and 7.1% of Tibetan hares (Lepus oiostolus).4 Overgrazing of pastures was suggested to be a key factor promoting abundance of small mammals, which may promote AE transmission through dogs.8 In Tibetan communities, the population can be separated into pastoral, farming, and urban populations relative to their living area and occupation. The situation regarding the environment and behavior may also be very different for these three populations. We thus addressed the epidemiologic characteristics, especially specific risk factors, for each population in two counties of the Sichuan Tibetan plateau to better understand the mode of transmission of E. multilocularis in this area, which is also endemic for E. granulosus infection,9 and to identify specific control opportunities for these respective populations.

MATERIALS AND METHODS

Study area.

Surveys were conducted in two counties, Ganzi County and Shiqu County, of the Ganzi Tibetan Autonomous Prefecture, Sichuan, China in 1997, 2001, 2002, and 2003. The two counties are located at 97°20′–100°25′E and 36°19′–31°24′N. They share eastern, northern, and western borders with Qinghai Province and a southern border with the Tibet Autonomous Region. These areas are part of the Tibetan Plateau. Shiqu County has an area of 25,100 km2 and a mean elevation of 4,200 meters; grassland covers an area of 21,000 km2, of which 19,000 km2 can be used as grazing pasture. By the end of 1997, there was an estimated livestock population of 581,470, mainly yaks, sheep, goats, horses, and a small number of pigs. The human population of Shiqu County was approximately 63,400 and 96.8% were ethnic Tibetans; there were 49,100 herdsmen, representing 77.6% of the population. Ganzi County has an area of 7,350 km2 and a mean elevation of 3,410 meters; grassland covers an area of 5,370 km2. By the end of 1997, there was an estimated livestock population of 326,730 of the same species as in Shiqu County. The human population was 55,550 and 95% were Tibetan; there were approximately 19,000 herdsmen. The weather in both counties is affected by a highland monsoon climate. Winter is longer than summer and there are no days in the year without frost. The average temperature is −10°C. The humid season stretches from May to October, and the yearly rainfall ranges from 460 mm to 636 mm.

Data collection.

Township officials and village cadres passed messages through herdsmen to inform the inhabitants where they could get free medical examination for echinococcosis, which is known as gan bao nang chong in Tibetan and Chinese. Thus, volunteer, self-selected subjects went to one of the designated screening places. Before examination, informed consent was obtained from all adult subjects and from the parents of minors. The study was reviewed and approved by the Ethical Committee of Sichuan Institute of Parasitic Diseases, Sichuan Province, as well as those of collaborating investigators, according to regulations of the National Institutes of Health in the United States. After answering an epidemiologic questionnaire, each registered person was given an abdominal examination using a portable ultrasound machine. For people diagnosed by ultrasound with AE or suspected AE, a 5-mL venous blood sample was obtained for serologic confirmation using the E. multilocularis-specific Em18-blot test.10 Diagnosis was based on ultrasound characteristics recommended by the World Health Organization Informal Working Group Echinococcosis Ultrasound Classification Network that were used in previous mass screenings in China.11

Statistical analysis.

From the epidemiologic questionnaires, the following potential transmission risk factors were analyzed: age, sex, county of residence, nationality (ethnic group), education level, number of dogs kept, dogs kept by neighbors, fox skin products ownership, drinking water sources, nomadic life style, income, livestock raising, habit of washing hands before eating, drinking non-boiled water, preventing flies from landing on food, and playing with dogs.

Statistical analysis included a general description and analysis of the age and sex structure, as well as AE prevalence of the population under study globally and in each of the studied counties. A sex-stratified stepwise logistic regression taking age into account was then used to characterize AE prevalence differences among farming, pastoral, and urban populations. Single factor and multiple factor stepwise logistic regressions were used to identify risk factors for each of the three populations. Factors with P values < 0.15 were used for variable inclusion in multiple logistic regressions. Age and the number of dogs had one-year increments. All analyses were conducted using SPSS version 10 software (SPSS Inc., Chicago, IL).

RESULTS

A total of 7,138 subjects were screened in the two counties of the study and used for the analysis. Of the investigated population 86.4% (6,167 of 7,138) were Tibetans. All subjects who listed occupations as farmers and herdsmen were Tibetans. In the current analyses, all patients identified in previous surveys or diagnosed in hospitals were not included. Pastoral communities had 2,955 subjects screened, farming communities 661, urban communities 2,360, students 1,043 (mostly less than 15 years of age), and others 119 (for example people from other counties and with a short time of residence). The mean ± SD age of the population was 31.1 ± 16.4 years (n = 7,138). The mean ± SD age was 31.0 ± 16.5 years (n = 3,425) for males and 31.2 ± 16.3 years (n = 3,713) for females. The mean ± SD number of dogs kept by the adult screened subjects was 1.17 ± 1.13 in the three communities, with 1.44 ± 1.16, 1.04 ± 0.95, and 0.88 ± 1.05 in pastoral, farming, and urban communities, respectively.

Sex- and age-specific AE prevalence.

The overall AE prevalence for the population was 3.1% (223 of 7,138) with a prevalence in males of 2.7% (91 of 3,425) and a prevalence in females of 3.6% (132 of 3,713). There was a tendency of increasing AE prevalence with age in all groups except for students (Table 1). Overall AE prevalence in herdsmen was 5.2% (154 of 2,955); 4.8% (65 of 1,368) in males and 5.6% (89 of 1,587) in females. Overall AE prevalence in farmers was 1.8% (12 of 661); 1.1% (3 of 268) in males and 2.3% (9 of 393) in females. In the urban population, AE prevalence was 2.1% (49 of 2,360); 1.3% (16 of 1,235) in males and 2.9% (33 of 1,125) in females. In students, AE prevalence was 0.3% (3 of 1,043); 0.4% (2 of 483) in males and 0.2% (1 of 560) in females.

Multiple stepwise logistic regression that included age, sex, and community factors (urban community, farming community, and pastoral community) showed that prevalence in females (3.6%, 132 of 3,713) was significantly higher than in males (2.7%, 91 of 3,425; P = 0.011) and that herdsmen (5.2%, 154 of 2,955) had a higher prevalence than farmers (1.8%, 12 of 661; P < 0.001) and the urban population (2.1%, 49 of 2,360; P < 0.001). Using stratified logistic regression in which sex was a stratifying factor and that included age and community, the pastoral community was also identified as the population with the highest AE prevalence (Table 2).

Risk factors for pastoral, farming, and urban communities.

Significant risk factors for pastoral communities are shown in Table 3. After multiple factors stepwise logistic regression analysis, only age (odds ratio [OR] = 1.036, 95% confidence interval [CI] = 1.027–1.046, P < 0.001) and not preventing flies from landing on food (OR = 8.598, 95% CI = 3.182–23.484, P < 0.001) were statistically significant.

Significant risk factors for farming communities are shown in Table 4. After multiple factors stepwise logistic regression, only Shiqu County as an area of residence (OR = 5.167, 95% CI = 1.521–17.561, P = 0.009) and age (OR = 1.078, 95% CI = 1.033–1.125, P = 0.001) were statistically significant risk factors. However, when the county of residence was excluded from the analysis, the number of dogs kept was statistically significant by forward stepwise multiple logistic regression (OR = 1.722, 95% CI = 1.072–2.739, P = 0.022) and ownership of fox skin was a statistically significant risk factor by backward stepwise multiple logistic regression (OR = 6.583, 95% CI = 1.407–30.805, P = 0.017) (Table 4). Farmers living in Shiqu County owned more fox skin products (P < 0.001) and kept more dogs than farmers living in Ganzi County (P < 0.001) (Table 5). Therefore, co-linearity might exist between county of residence and fox skin ownership, as well as between county of residence and number of dogs kept.

Significant risk factors for urban communities are shown in Table 6. After multiple factors stepwise logistic regression, female sex (OR = 2.345, 95% CI = 1.242–4.427, P = 0.009), increasing age (OR = 1.031, 95% CI = 1.012–1.051, P = 0.001), streams as a drinking water source (OR = 0.267, 95% CI = 0.136–0.920, P < 0.001), well water (OR = 0.354, 95% CI = 0.119–0.600, P = 0.033), and playing with dogs (always versus never; OR = 4.550, 95% CI = 1.611–12.846, P < 0.004 and occasionally versus never; OR = 2.826, 95% CI = 1.146–6.970, P = 0.024) were statistically significant risk factors.

DISCUSSION

This study included more than 7,000 subjects screened for human AE, with 223 patients identified, and thus constitutes the largest study of AE risk factors in a human community ever performed. The study confirmed that pastoral communities and females in this Tibetan area were at highest risk for AE, and showed that differences in prevalence among counties might be due to behavioral factors, in addition to well-recognized environmental factors that determine E. multilocularis infection in intermediate and definitive animal hosts.

Nomadic pastoral communities on the Tibetan plateau are at high risk of E. multilocularis infection. The prevalence of AE in herdsmen was as high as 8.5% in another study,8 and contacts with dogs were suggested to be an important risk factor.9,12 Local Buddhist practices often result in large numbers of stray dogs in villages. Our field observations found that the environment, especially in the immediate area surrounding herdsmen houses, was highly contaminated by dog feces. Women of the community care for dogs, and this could be a part of the explanation for the higher risk found in women. Such a higher risk in adult females was also found in rural communities of Gansu province.6 Additional risks for Tibetan women could also be related to the specific use of yak feces cakes as the main fuel in the pastoral communities both in rural and urban communities. The screened women reported that dogs sometimes defecated directly on the pile of yak feces. Collecting yak feces and putting yak feces cakes into the stove, which is usually done by women, could thus result in contact with dog feces and/or contaminating parasitic eggs directly.

A role for immune suppression during pregnancy cannot be ruled out. Aggravation of previously stable AE during or immediately after pregnancy has been reported by the clinicians who followed-up AE patients.13 Recently such a deleterious effect of pregnancy with occurrence of brain metastasis in Chinese women in Ningxia has been observed.14 Both environmental/behavioral and immunologic explanations are consistent with the sex ratio favoring females only in adult cases in our study and in Gansu Province.6,11 Increased risk with age in both sexes has been found in epidemiologic studies of AE and can be explained by the long latent period of infection that may delay the diagnosis of the disease for several years, and even decades, after infection.3

In pastoral communities, dogs tied to doorways during the day and released at night are used to watch houses and tents and to drive wolves away from livestock. Young dogs roam around inside and outside houses and tents. In these pastoral communities, only preventing flies from landing on food was found to be a statistically significant protection against the disease; other assumed important factors such as keeping dogs, playing with dogs, owning fox skin products, water sources, and washing hands before eating were not statistically significant independent factors. The possible reason might be that the environment was so highly contaminated that only hygiene behavior related to direct food contamination could be beneficial. We observed significant differences depending on water source and dog owning in urban populations whose environment, style of life, and behavior are much more diverse. Our household visits showed that families of herdsmen who prevent flies from landing on food also had other types of behavior to improve the hygienic status in the houses. In such families, food was stored in cupboards that not only prevented contact with flies, but also prevented dogs from having contact with food. We also observed that young dogs had access to places where food was stored in some households. However, other combinations of variables might be significant, and the fly factor may be a surrogate for some causal undetected variables because of the transport of E. multilocularis eggs by flies. Until now, only E. granulosus eggs were convincingly shown to be transported by flies,15 but nothing is known about this mode of contamination of food regarding E. multilocularis.

Farmers in Shiqu County had a higher risk of AE than farmers in Ganzi County. Our analyses suggested that the difference may be the result of ownership of fox skin and the number of dogs kept. There was co-linearity between the county of residence and both of these risk factors. The P value of the factor county of residence increased from 0.051 in single factor analysis to 0.009 in multiple factor regression. When the county of residence factor was excluded, the number of dogs kept was significant by forward stepwise multiple regression and ownership of fox skin products was significant by backward stepwise multiple regression. This is the first time in China that epidemiologic analysis suggests that the fox might play a significant role in AE transmission to humans. However, geographic factors might interact with behavioral factors to produce such a difference between counties because ownership of fox products might be a consequence of higher number of foxes in the area related to environmental causes.

In addition to contamination through the E. multilocularis cycle, contamination through dogs imported from other pastoral communities cannot be ruled out. When we conducted household visits, the transfer of dogs between communities, even between provinces, was common. For example, two pastoral settlements in Yiniu Township, Shiqu County reported that most of their dogs died in 2002. Almost all of the dogs they had in 2003 came from other settlements. A businessman in Arizha Township, Shiqu County reported that his dogs were regularly sold to people in Heilongjiang Province. This province is known to have AE in humans; however, no final or intermediate host infection has been reported.2,3,16,17 Thus, transfer of infected dogs might contribute to infections in farmers.

Active transmission has been recorded in farmers of Han communities in South Gansu.2,18 This may be the result of deforestation leading to the extension of favorable habitats for small mammalian intermediate hosts.19,20 However, the process by which such a newly favorable environment is contaminated with E. multilocularis remains unclear. In the United States, a shipment of foxes and coyotes was confiscated in South Carolina by federal and state wildlife authorities in 1989. Echinococcus multilocularis was identified in 3 of 44 red foxes that had been transported illegally from eastern Indiana and western Ohio and were to be released into fox-hunting enclosures in southeastern states. Subsequent investigation showed that translocation of foxes from areas where E. multilocularis is currently enzootic into southeastern states is common.21 Thus, the dog trade may be an important way for the parasite to spread in areas where it is not present. This possibility should be taken into account in China if control measures are planned at the national level.

Table 1

Age- and sex-specific infection rates of the surveyed population*

Age (years)
< 1111–2021–3031–4041–50> 50χ2 and P values
* –= no data.
Total0.5% (4/740)0.8% (11/1,422)1.9% (30/1,573)3.5% (53/1,522)4.4% (42/952)8.8% (83/940)157.2
< 0.001
    Male0.5% (2/366)0.6% (4/692)1.3% (10/744)2.8% (20/721)3.4% (15/443)8.7% (40/459)88.9
< 0.001
    Female0.5% (2/371)1.0% (7/729)2.4% (20/826)4.1% (33/799)5.3% (27/508)9.0% (43/480)73.5
< 0.001
Herdsmen1.3% (4/310)1.1% (5/445)2.8% (19/676)6.3% (39/621)7.0% (28/401)11.6% (59/509)78.7
    < 0.001
    Male1.4% (2/148)1.0% (2/120)1.7% (5/300)5.6% (16/286)4.8% (8/168)12.5% (32/256)51.2
< 0.001
    Female1.3% (2/159)1.3% (3/235)3.7% (14/375)6.9% (23/334)8.6% (20/232)10.7% (27/252)33.9
< 0.001
Farmers0% (0/22)1.5% (1/65)0% (0/138)1.3% (2/154)1.3% (2/153)5.4% (7/129)12.9
0.025
    Male0% (0/11)0% (0/30)0% (0/57)0% (0/65)0% (0/52)5.7% (3/53)12.3
0.031
    Female0% (0/11)2.9% (1/35)0% (0/81)2.2% (2/89)2.0% (2/101)5.3% (4/76)5.3
0.386
Town population0% (0/141)1.3% (2/150)1.4% (10/690)1.7% (12/707)2.1% (8/381)2.3% (17/293)25.3
    < 0.001
    Male0% (0/71)0% (0/109)1.1% (4/353)1.2% (4/343)1.4% (3/211)3.4% (5/148)7.5
0.184
    Female0% (0/70)4.9% (2/41)1.8% (6/336)2.2% (8/363)2.9% (5/170)8.3% (12/145)19.4
0.002
Students0% (0/258)0.4 (3/761)0% (0/24)1.117
0.572
    Male0% (0/132)0.6% (2/341)0% (0/10)0.836
0.658
    Female0% (0/126)0.2% (1/420)0% (0/14)0.334
0.846
Table 2

Sex-stratified analyses including age and living place using stepwise multiple logistic regressions (2,850 male cases and 3,086 female cases included)*

Male populationParameter estimateStandard errorWaldPOdds ratio (95% CI)
Age0.0490.00752.503< 0.0011.050 (1.036, 1.065)
Farmers vs. herdsmen−1.5860.5977.0570.0080.205 (0.064, 0.660)
Urban vs. herdsmen−1.2810.28520.182< 0.0010.278 (0.159, 0.486)
Farmers vs. Urban−0.3050.6350.2300.632
Intercept−4.9490.341211.155< 0.0010.007 (0.004, 0.014)
Female populationParameter estimateStandard errorWaldPOdds ratio (95% CI)
* CI = not applicable; – = not applicable.
Age0.0380.00550.811< 0.0011.039 (1.029, 1.049)
Farmers vs. herdsmen−1.1140.3579.7660.0020.328 (0.163, 0.661)
Urban vs. herdsmen−0.7010.20911.2090.0010.496 (0.329, 0.747)
Farmers vs. Urban−0.4130.3831.1650.280
Intercept−4.2680.256276.953< 0.0010.014 (0.008, 0.023)
Table 3

Single and multiple factor analysis using stepwise logistic regression for pastoral communities*

Risk factorsAE prevalencePOdds ration (95% confidence interval)
* – = not applicable for results of single factor logistic regressions. AE = alveolar echinococcosis.
P < 0.05 using multiple factors logistic regressions.
‡ In Chinese Yuans (RMB) per year (exchange rate 2005: 8.1 Yuan = 1 US $).
County
    Ganzi3.2% (14/440)Reference
    Shiqu5.6% (140/2,522)0.0421.788 (1.023, 3.127)
Age< 0.0011.041 (1.031, 1.050)†
Education
    None6.2% (139/2,239)Reference
    Primary school3.2% (13/403)0.0200.504 (0.282, 0.898)
    Middle school0.7% (2/279)0.0020.109 (0.027, 0.443)
    College and above0% (0/24)0.549
Water sources
    Stream6.9% (88/1,271)Reference
    River5.0% (40/794)0.085
    Well2.4% (11/458)0.0010.331 (0.175, −0.625)
    Pond0% (0/14)0.545
    Tap water4.4% (12/271)0.133
Income‡
    < 2,0006.3% (83/1,313)Reference
    2,000–< 5,0005.8% (61/1,051)0.601
    5,000–10,0003.2% (8/249)0.060
    > 10,0000.5% (1/186)0.0120.081 (0.011, 0.579)
Livestock raising
    No3.7% (20/545)Reference
    Yes5.9% (130/2,214)0.0441.637 (1.013, 2.647)
Hand washing before eating
    No6.4% (129/2,007)Reference
    Always3.2% (14/435)0.0110.484 (0.276, 0.849)
    Sometimes2.2% (8/358)0.0030.333 (0.162, 0.686)
Drinking non-boiled water
    No6.7% (66/983)Reference
    Sometimes4.8% (47/498)0.071
    Always4.5% (38/842)0.0440.657 (0.436, 0.990)
Preventing flies from landing on food
    Yes0.7% (4/557)Reference
    No6.6% (147/2,242)< 0.0019.685 (3.574, 26.245)†
    Always5.6% (45/804)0.0082.977 (1.330, 6.664)
Playing with dogs
    Sometimes6.1% (99/1,632)0.0033.262 (1.503, 7.078)
    Never1.9% (7/359)Reference
Table 4

Single and multiple factor analysis using stepwise logistic regression for farmers’ communities*

Risk factorsAE prevalencePOdds ratio (95% confidence interval)
* – = not applicable for results of single factor logistic regressions. AE = alveolar echinococcosis.
P < 0.05 using multiple factors logistic regressions.
County
    Ganzi1.3% (7/537)Reference
    Shiqu40% (5/124)0.051
Age0.0011.076 (1.031, 1.123)†
No. of dogs kept0.0241.636 (1.066, 2.511)†
    None0.6% (2/347)Reference
Fox skin products
    Bought or donated3.6% (10/280)0.0176.389 (1.388, 29.402)†
    Self hunting0% (0/8)0.886
Drinking non-boiled water
    No4.5% (5/112)Reference
    Sometimes1.7% (3/176)0.181
    Always1.1% (4/349)0.0400.248 (0.065, 0.941)
Table 5

Number of dogs kept and ownership of fox skin products in Ganzi and Shiqu farmers’ communities

GanziShiqu
MeanNSDMeanNSDFP
Dog ownership
    Number of dogs per household0.975370.791.341241.4215.3< 0.001
GanziShiqu
No. of fox skinsBought or donatedSelf huntingNo of fox skinsBought or donatedSelf huntingχ2P
Ownership of fox skin
    Proportion of households61.6% (331/537)37.1% (199/537)1.3% (7/537)16.3% (16/98)82.7% (81/98)1.0% (1/98)70.3< 0.001
Table 6

Single and multiple factor analysis using stepwise logistic regression for urban communities*

Risk factorsAE prevalencePOdds ration (95% confidence interval)
* – = not applicable for results of single factor logistic regressions. AE = alveolar echinococcosis.
P < 0.05 using multiple factors logistic regressions.
‡ In Chinese Yuans (RMB) per year (exchange rate 2005: 8.1 Yuan = 1 US $).
County
    Ganzi1.0% (13/1,307)Reference
    Shiqu3.4% (36/1,055)< 0.0013.516 (1.855, 6.664)
Sex
    Male1.3% (16/1,235)Reference
    Female2.9% (33/1,125)0.0072.302 (1.260, 4.206)†
Age< 0.0011.046 (1.027, 1.065)†
Ethnic group
    Tibetan2.7% (46/1,720)0.0035.853 (1.814, 18.884)
    Han0.5% (3/642)Reference
Education
    None4.8% (28/589)Reference
    Primary school1.7% (5/293)0.0310.348 (0.133, 0.910)
    Middle school1.1% (15/1,314)< 0.0010.231 (0.123, 0.437)
    College and above0.6% (1/156)0.0450.130 (0.018, 0.958)
No. of dogs kept< 0.0011.429 (1.172, 1.742)
    None1.3% (12/935)Reference
Fox skin products
    Bought or donated2.7% (37/1,377)0.0252.124 (1.102, 4.095)
    Self hunting0% (0/10)0.805
Water sources
    Stream5.7% (18/314)Reference
    River3.5% (12/339)0.185
    Well1.7% (6/355)0.0080.283 (0.111, 0.721)†
    Pond4.8% (1/21)0.853
    Tap water0.9% (12/1,304)< 0.0010.153 (0.073, 0.321)†
Income‡
    < 2,0003.4% (20/591)Reference
    2,000–< 5,0002.2% (19/883)0.152
    5,000–10,0001.1% (8/702)0.0080.329 (0.144, 0.753)
    > 10,0001.4% (2/148)0.209
Livestock raising
    No1.2% (20/1,601)Reference
    Yes3.7% (26/705)< 0.0013.027 (1.678, 5.459)
Hand washing before eating
    No4.0% (28/702)Reference
    Always1.0% (10/1,040)< 0.0010.234 (0.113, 0.484)
    Sometimes1.9% (11/587)0.0310.460 (0.227, 0.932)
Preventing flies from landing on food
    Yes1.2% (18/1,463)Reference
    No3.6% (31/865)< 0.0012.984 (1.659, 5.367)
    Always4.8% (12/148)< 0.0016.943 (2.808, 17.166)†
Playing with dogs
    Sometimes3.0% (29/967)< 0.0014.222 (1.921, 9.275)†
    Never0.7% (8/1,102)Reference

*

Address correspondence to Dominique A. Vuitton, World Health Organization Collaborating Centre on Prevention and Treatment of Human Echinococcosis, SERF Research Unit, Université de Franche-Comté, 25030 Besançon, France. E-mail: dominique.vuitton@univ-fcomte.fr

Authors’ addresses: Qian Wang, World Health Organization Collaborating Centre on Prevention and Treatment of Human Echinococcosis; SERF and LBE Usc INRA Research Units, Université de Franche-Comté, 25030 Besançon, France and Sichuan Provincial Center for Disease Control and Prevention, 10, University Road, Chengdu Sichuan 610041, People’s Republic of China, Telephone: 86-28-8544-5580, Fax: 86-28-8543-8409, E-mail: wangqian67@yahoo.com.cn. Jiamin Qiu and Wen Yang, Institute for Parasitic Diseases Prevention and Control, Sichuan Provincial Center for Disease Control and Prevention, Chengdu, Sichuan, People’s Republic of China, Telephone: 86-28-8544-5580, Fax: 86-28-8543-8409, E-mails: qjm@mail.sc.cninfo.net.cn and wweennyang@tom.com. Peter M. Schantz, Division of Parasitic Diseases, National Center for Infectious Diseases, Centers For Disease Control and Prevention, Atlanta, GA 30333, Telephone: 770-488-7767, Fax: 770-488-7761, E-mail: pms1@cdc.gov. Francis Raoul, Patrick Giraudoux, and Dominique A. Vuitton, World Health Organization Collaborating Centre on Prevention and Treatment of Human Echinococcosis, SERF Research Unit, Université de Franche-Comté, 25030 Besançon, France, Telephone: 33-03-81-66-57-36, Fax: 33-03-81-66-57-97, E-mails: francis.raoul@univ-fcomte.fr, patrick.giraudoux@univ-fcomte.fr, and dominique.vuitton@univ-fcomte.fr. Philip S. Craig, Cestode Zoonoses Research Group, Bioscience Research Institute and School of Environment and Life Sciences, University of Salford, Salford MS4WT, UK, Telephone: 44-0161-295-5488, Fax: 44-0161-295-5210, E-mail: p.s.craig@salford.ac.uk.

Financial support: The research was supported by the Thrasher Foundation, the National Institutes of Health, the National Science Foundation (Ecology of Transmission of Infectious Diseases Program), and the Sichuan Provincial Health Department. Qian Wang was supported by a PhD grant from the French Embassy, French Ministry of Foreign Affairs, in Beijing, People’s Republic of China.

REFERENCES

  • 1

    Eckert J, Deplazes P, 1999. Alveolar echinococcosis in human: The current situation in Central Europe and the need for countermeasures. Parasitol Today 15 :315–319.

    • Search Google Scholar
    • Export Citation
  • 2

    Wen H, Chai JJ, Wang JC, Wang SH, Wang XY, Feng XH, Zhou HX, 2002. Hydatid Control within a Continental System in P.R.China. Craig P, Pawlowski Z, eds. Cestode Zoonoses: Echinococcosis and Cysticercosis. NATO Science Series. Amsterdam: IOS Press, 355–366.

  • 3

    Vuitton DA, Zhou HX, Bresson-Hadni S, Wang Q, Piarroux M, Raoul F, Giraudoux P, 2003. Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127 :S87–S107.

    • Search Google Scholar
    • Export Citation
  • 4

    Qiu JM, Liu FJ, Schantz P, Ito A, Carol D, He JG, 1999. Epidemiological Survey of Hydatidosis in Tibetan Areas of Western Sichuan Province. Larrieu E, Romeo S, Mehapide C eds. XXXIII Archivos Internacionales de la Hidatidosis: 84.

  • 5

    Kern P, Ammon A, Kron M, Sinn G, Sander S, Petersen LR, Gaus W, Kern P, 2004. Risk factors for alveolar echinococcosis in humans. Emerg Infect Dis 10 :2088–2093.

    • Search Google Scholar
    • Export Citation
  • 6

    Craig PS, Giraudoux P, Shi D, Bartholomot B, Barnish G, Delattre P, Quere JP, Harraga S, Bao G, Wang Y, Lu F, Ito A, Vuitton DA, 2000. An epidemiological and ecological study of human alveolar echinococcosis transmission in south Gansu, China. Acta Trop 77 :167–177.

    • Search Google Scholar
    • Export Citation
  • 7

    Budke CM, Campos-Poncec M, Wang Q, Torgerson PR, 2005. A canine purgation study and risk factor analysis for echinococcosis in a high endemic region of the Tibetan plateau. Vet Parasitol 127 :43–49.

    • Search Google Scholar
    • Export Citation
  • 8

    Wang Q, Vuitton DA, Qiu JM, Giraudoux P, Xiao YF, Schantz PM, Raoul F, Li TY, Yang W, Craig P, 2004. Fenced pasture: a possible risk factor for human alveolar echinococcosis in Tibetan pastoralist communities of Sichuan, China. Acta Trop 90 :285–293.

    • Search Google Scholar
    • Export Citation
  • 9

    Wang Q, Qiu JM, Schantz P, He JG, Ito A, Liu F, 2001. Risk factors for development of human hydatidosis among people whose family is raising livestock in western Sichuan Province, China. Chin J Parasitic Dis Parasitol 19 :289–293.

    • Search Google Scholar
    • Export Citation
  • 10

    Ito A, Nakao M, Kutsumi H, Lightowlers MW, Itoh M, Sato S, 1993. Serodiagnosis of alveolar hydatid diseases by Western blotting. Trans R Soc Trop Med Hyg 87 :170–172.

    • Search Google Scholar
    • Export Citation
  • 11

    Bartholomot B, Vuitton D, Harraga D, Shi DZ, Giraudoux P, Barnish G, Wang YH, Macpherson CNL, Craig PS, 2002. Combined ultrasound and serologic screening for hepatic alveolar echinococcosis in central China. Am J Trop Med Hyg 66 :23–29.

    • Search Google Scholar
    • Export Citation
  • 12

    Schantz PM, Wang H, Qiu J, Liu FJ, Saito E, Emshoff A, Ito A, Roberts JM, Delker C, 2003. Echinococcosis on the Tibetan Plateau: prevalence and risk factors for cystic and alveolar echinococcosis in Tibetan populations in Qinghai Province, China. Parasitology 127 :S109–S120.

    • Search Google Scholar
    • Export Citation
  • 13

    Bresson-Hadni S, Vuitton DA, Bartholomot B, Heyd B, Godard D, Meyer JP, Hrusovsky S, Becker MC, Mantion G, Lenys D, Miguet JP, 2000. A twenty-year history of alveolar echinococcosis in humans: analysis of a series of 117 patients from eastern France. Eur J Gastroenterol 12 :327–336.

    • Search Google Scholar
    • Export Citation
  • 14

    Yang YR, Vuitton DA, Jones MK, Craig PS, McManus DP, 2005. Brain metastasis of alveolar echinococcosis in a hyperendemic focus of Echinococcus multilocularis infection. Trans R Soc Trop Med Hyg 99 :937–941.

    • Search Google Scholar
    • Export Citation
  • 15

    Lawson JR, Gemmell MA, 1985. The potential role of blowflies in the transmission of taeniid tapeworm eggs. Parasitology 91 :129–143.

  • 16

    Li G, Shi XQ, 1985. A case report of human AE in Heilongjiang. Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih 3 :8.

  • 17

    Yu SH, Xu LQ, Jiang ZX, Xu SH, Han JJ, Zhu YG, Chang J, Lin JX, Xu FN, 1994. Report on the first national wide survey of human parasites in China 1. Regional distribution of parasite species. Chin J Parasitic Dis Parasitol 12 :241–247.

    • Search Google Scholar
    • Export Citation
  • 18

    Craig PS, Deshan L, MacPherson CN, Dazhong S, Reynolds D, Barnish G, Gottstein B, Zhirong W, 1992. A large focus of alveolar echinococcosis in central China. Lancet 340 :826–831.

    • Search Google Scholar
    • Export Citation
  • 19

    Giraudoux P, Delattre P, Takahashi K, Raoul F, Quere K-P, Craig P, Vuitton D, 2002. Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multiscale approaches? Craig P, Pawlowski Z, eds. Cestode Zoonoses: Echinococcosis and Cysticercosis. NATO Science Series, Amsterdam: IOS Press, 251–266.

  • 20

    Giraudoux P, Craig PS, Delattre P, Bao G, Bartholomot B, Harraga S, Quere JP, Raoul F, Wang Y, Shi D, Vuitton DA, 2003. Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127 (Suppl)127:S121–S131.

    • Search Google Scholar
    • Export Citation
  • 21

    Schantz PM, 1993. Echinococcus multilocularis in North America. Uchino J, Sato N, eds. Alveolar Echincoccosis of the Liver. Volume 30. Sapporo, Japan: Hokkaido University School of Medicine. Medical Library Series, 11–20.

Save