Human social conditions predict the risk of exposure to zoonotic parasites in companion animals in East and Southeast Asia

Asia has undergone rapid socioeconomic and urban transitions, increasing pet ownership in metropolitan areas. However, wealth and living standards are uneven, and disadvantaged communities bear a high burden of zoonotic and neglected parasitic diseases. While dogs and cats can carry fleas, ticks, and soil-transmitted helminths affecting human health, little is known about the prevalence, distribution, and predictors of exposure to zoonotic parasites in companion animals in Asian cities. The study hypothesizes that, in addition to animal characteristics and bioclimatic factors, human living standards can predict the risk of exposure to zoonotic parasites in pets sharing metropolitan areas with their owners. To test this, the authors surveyed endo- and ectoparasites and arthropod-borne pathogens in over 2300 client-owned dogs and cats across eight East and Southeast Asian countries, and used statistical modeling to identify predictors of exposure. The goal is to inform One Health-oriented, sustainable control strategies for urban companion animals in Asia.

Study design and sites: A multicenter cross-sectional study was conducted from June 2017 to July 2018 in metropolitan areas of eight East and Southeast Asian countries/territories (Mainland China, Taiwan, Indonesia, Malaysia, the Philippines, Singapore, Thailand, Vietnam). Monthly sampling targeted 10 client-owned dogs and 10 client-owned cats in Taiwan, Indonesia, Malaysia, the Philippines, Singapore, Thailand, and Vietnam, and 40 dogs and 40 cats in Mainland China, aiming for 2640 animals. Ethics approval was granted by the University of Bari (protocol no. 13/17); informed owner consent was obtained. Inclusion criteria: regular outdoor access and no recent antiparasitic treatment (~2 weeks). Data collection: For each animal, investigators recorded demographics and management (age class, sex, neuter status, environment rural/urban, household apartment vs house with garden) via questionnaire, followed by clinical exam, ectoparasite collection, blood sampling, and fecal collection. Standardized training (on-site and online) ensured protocol adherence. Parasite detection: Ectoparasites and vector-borne pathogens (VBPs) were detected as per Colella et al. 2020. Endoparasites were detected using fecal flotation (zinc sulfate or sodium chloride; specific gravity 1.200–1.350), sedimentation, and Baermann-Wetzel techniques within 24 h of collection. Hookworm-positive samples (Ancylostomatidae eggs/larvae) had aliquots preserved in 70% ethanol and tested by high-throughput multiplex qPCR at the University of Melbourne to identify species (e.g., Ancylostoma ceylanicum). Other endoparasites were identified morphologically to family/genus. Risk indicator variables: Four groups were compiled: (1) Animal characteristics (species, age class <5, 5–15, >15 years; sex; neuter status); (2) Husbandry (environment: rural vs urban; household: apartment vs house with garden); (3) Bioclimatic (city-level annual mean temperature BIO1 in °C; annual precipitation BIO12 in mm) from WorldClim; (4) Socioeconomic (city human population density from WorldPop; country pet-human population ratio calculated from Boehringer Ingelheim 2018 dog/cat census and World Bank 2019 population; country life expectancy at birth in 2017 from World Bank). Statistical analysis: Descriptive statistics characterized populations and infection rates. Associations among infection status (ectoparasites, endoparasites, VBPs, overall) and candidate indicators were explored using Cramér's V and multiple correspondence analysis (MCA). Mixed-effects logistic regression (lme4) modeled infection status with fixed effects (risk indicators) and random intercept for city. Model selection used forward/backward steps minimizing AIC; significance threshold 10%. Collinearity assessed via correlation matrix (temperature and precipitation strongly correlated). Predictive performance evaluated by ROC AUC. Sensitivity analyses tested parameter robustness to extreme values. Animals with missing data were excluded from multivariable analyses.

- Sample: 2381 client-owned animals (1229 dogs, 1152 cats). Majority <5 years (65.8%); 85.8% lived in urban areas; 66% in houses with gardens; 35.8% neutered. - Overall infection: 44.9% [42.9%; 47.0%] had ≥1 parasite. - By parasite class (all animals): ectoparasites 31.4% [29.6%; 33.3%]; VBPs 13.1% [11.7%; 14.5%]; endoparasites 13.5% [12.1%; 14.9%]. - Dogs vs cats (selected estimates): ticks 22.3% in dogs vs 3.73% in cats; fleas 14.8% dogs vs 19.6% cats; mites 3.01% dogs vs 13.3% cats; VBPs 23.8% dogs vs 0.93% cats; endoparasites 12.9% dogs vs 14.1% cats; hookworms 9.38% dogs vs 6.70% cats; Toxocaridae 2.60% dogs vs 4.18% cats. - Geographic variation (overall infected): highest in Yogyakarta, Indonesia 94.4% [86.2%; 98.4%], Nueva Ecija, Philippines 81.4% [75.8%; 86.2%], Bogor, Indonesia 73.7% [63.9%; 82.1%]; lowest in Shanghai, China 14.2% [10.0%; 19.2%], Nanning 20.7% [15.8%; 26.3%], Nanjing 27.5% [22.0%; 33.6%]. - Hookworm species (qPCR among hookworm-positive): in dogs: A. caninum/A. tubaeforme 52.6%, A. ceylanicum 26.3%, A. braziliense 15.8%, Uncinaria stenocephala 5.3%; in cats: A. caninum/A. tubaeforme 38.9%, A. ceylanicum 38.9%, A. braziliense 17.1%, U. stenocephala 5.1%. A. braziliense detected in Taiwan and Thailand (cats) and Taiwan and Vietnam (dogs). - Mixed-effects regression (overall parasites): higher odds in <5 years (OR 1.35 [1.07; 1.71]) and >15 years (OR 4.10 [1.50; 11.2]) vs 5–15 years; neutered animals had lower odds (OR 0.61 [0.48; 0.77]); urban residence lowered odds vs rural (OR 0.36 [0.26; 0.50]); higher annual mean temperature increased odds per 1°C (OR 1.14 [1.08; 1.21]); higher national human life expectancy reduced odds per year (OR 0.86 [0.78; 0.95]). Pet-human ratio and population density were not explanatory. - VBPs: dogs >> cats (OR 34.1 [17.7; 65.8]); house with garden associated with higher odds (OR 2.49 [1.54; 4.03]); higher temperature or precipitation increased odds; higher human life expectancy decreased odds (OR 0.86 [0.76; 0.98]). - Ectoparasites: neutered animals had lower odds (OR 0.53 [0.41; 0.69]); urban residence lowered odds (OR 0.28 [0.21; 0.39]); higher precipitation/temperature increased odds. Dogs were more likely to have ticks (OR 11.6 [7.83; 17.3]), while cats were more likely to have fleas (dogs vs cats OR 0.53 [0.39; 0.73]). Flea and tick infestations were less abundant in countries with higher life expectancy. - Endoparasites overall: age was the key predictor; animals <5 years had higher odds (OR 2.12 [1.43; 3.15]) vs 5–15 years. Hookworms were more frequent in dogs (OR 1.65 [1.17; 2.33]) and in young and older animals. - Model performance (AUC): overall parasites 0.783; VBPs 0.659; ectoparasites 0.819; endoparasites 0.738.

The study demonstrates that human social conditions, proxied by national life expectancy, and access to veterinary care, proxied by neutering status, are strongly associated with reduced exposure of companion animals to zoonotic parasites in urban East and Southeast Asia. These findings support the hypothesis that living standards and anthropogenic factors influence parasite transmission risks in pets that share environments with humans. Elevated risks were observed at the extremes of pet age (<5 and >15 years), and dogs were significantly more exposed to VBPs and ticks, while cats were more affected by fleas. Environmental and climatic drivers (higher temperature and precipitation) increased the risk of ectoparasites and VBPs, whereas urban environments generally reduced overall parasite exposure compared to rural settings. The detection of zoonotic hookworms, including A. ceylanicum and A. braziliense, underscores meaningful One Health risks, with pets acting as reservoirs for human infections in the region. The results emphasize the importance of incorporating socio-economic context, veterinary access, and climate factors into tailored control strategies and surveillance programs, and they highlight biosecurity implications for pet movement between endemic and non-endemic regions.

This multicountry survey provides a comprehensive view of parasite occurrence and key predictors of exposure in client-owned dogs and cats in metropolitan East and Southeast Asia. It identifies higher human life expectancy and neutering status as strong protective factors, while younger and older pet age, rural environments, and warmer/wetter climates increase risk. The findings advocate for One Health-aligned, targeted prevention and control strategies that integrate public education, enhanced access to veterinary services (including neutering and parasite prevention), and consideration of local climatic and management contexts. Future research should evaluate within-country socio-economic disparities, apply more sensitive diagnostics for protistan parasites, longitudinally monitor intervention impacts, and model climate change effects on vector and parasite dynamics.

- Study population mainly comprised urban, client-owned animals with access to veterinary care, potentially underrepresenting pets from poorer or rural communities with higher parasitism. - Exclusion of animals with recent antiparasitic treatment (<2 weeks) may have biased prevalence estimates by omitting some parasite-free animals. - Conventional fecal diagnostic methods likely underestimated protistan parasites such as Giardia relative to molecular or antigen-based assays. - Variation in technician expertise across sites could contribute to differences in coprodiagnostic sensitivity, despite training efforts. - Socioeconomic variables were analyzed at country level (e.g., life expectancy), not at the individual owner level; within-country heterogeneity was not captured. - Animals with missing data were excluded from multivariable analyses, which may introduce selection bias. - Strong collinearity between temperature and precipitation limited simultaneous interpretation of their effects in regression models.