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Risk Factors for and Seroprevalence of Tickborne Zoonotic Diseases Among Livestock Owners, Kazakhstan Jennifer R

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Risk Factors for and Seroprevalence of Tickborne Zoonotic Diseases Among Livestock Owners, Kazakhstan Jennifer R RESEARCH Risk Factors for and Seroprevalence of Tickborne Zoonotic Diseases among Livestock Owners, Kazakhstan Jennifer R. Head, Yekaterina Bumburidi, Gulfaira Mirzabekova, Kumysbek Rakhimov, Marat Dzhumankulov, Stephanie J. Salyer, Barbara Knust, Dmitriy Berezovskiy, Mariyakul Kulatayeva, Serik Zhetibaev, Trevor Shoemaker, William L. Nicholson, Daphne Moffett infectious aerosols, consumption of contaminated Crimean-Congo hemorrhagic fever (CCHF), Q fever, and animal products, or a bite from a vector, such as a tick Lyme disease are endemic to southern Kazakhstan, but population-based serosurveys are lacking. We assessed (2). Global incidence of tickborne diseases is increas- risk factors and seroprevalence of these zoonoses and ing and expected to continue rising (3). Given chang- conducted surveys for CCHF-related knowledge, atti- es in ecologic factors, such as climate and land use, tudes, and practices in the Zhambyl region of Kazakh- tickborne diseases have emerged in new areas dur- stan. Weighted seroprevalence for CCHF among all par- ing the past 3 decades, and the incidence of endemic ticipants was 1.2%, increasing to 3.4% in villages with a tickborne pathogens has increased (4). Vectorborne known history of CCHF circulation. Weighted seropreva- infections were responsible for ≈28.8% of emerging lence was 2.4% for Lyme disease and 1.3% for Q fever. infectious diseases during 1990–2000 (5). We found evidence of CCHF virus circulation in areas not Crimean-Congo hemorrhagic fever (CCHF), Q known to harbor the virus. We noted that activities that fever, and Lyme disease are widespread zoonotic put persons at high risk for zoonotic or tickborne disease diseases that cause a range of illness and death in also were risk factors for seropositivity. However, recog- nition of the role of livestock in disease transmission and humans. CCHF, caused by Crimean-Congo hemor- use of personal protective equipment when performing rhagic fever virus (CCHFV), an RNA virus of the high-risk activities were low among participants. family Nairoviridae, is highly fatal (6). The virus is maintained through an enzootic cycle involving oonoses account for 61% of human infectious mammals, ticks, and humans, and is transmitted to Zdiseases and 75% of emerging pathogens (1). humans through contact with viremic livestock or in- Zoonotic diseases pass from animals to humans fected ticks. CCHF is endemic to Africa, Asia, eastern through direct contact with animals, inhalation of and southern Europe, and central Asia (7). Q fever is caused by the bacterium Coxiella burnetii, which in- fects many vertebrates, but ruminant livestock are Author affiliations: Association of Schools and Programs for thought to be its primary reservoir. Transmission to Public Health, Washington, DC, USA (J.R. Head); Public Health humans most commonly occurs from inhalation of Institute, San Francisco, California, USA (J.R. Head); Centers for dust contaminated with urine, feces, milk, or birth Disease Control and Prevention, Atlanta, Georgia, USA products from infected animals (8). Q fever has been (J.R. Head, S.J. Salyer, B. Knust, T. Shoemaker, W.L. Nicholson); identified in most countries (8). Severe cases can re- Centers for Disease Control and Prevention, Almaty, Kazakhstan sult in pneumonia or hepatitis in humans, and ≈5% of (Y. Bumburidi, D. Berezovskiy, D. Moffett); Zhambyl Oblast infections become chronic (9). Lyme disease is caused Public Health Protection Department, Taraz, Kazakhstan by Borrelia burgdorferi, a bacterium transmitted to hu- (G. Mirzabekova, K. Rakhimov); Zhambyl Oblast Health mans through the bite of Ixodes ticks. Untreated Lyme Department, Taraz (M. Dzhumankulov); Zhambyl Oblast infection can disseminate and spread to the joints, Sanitary Epidemiology Expertise Center, Taraz (M. Kulatayeva, heart, and nervous system. Lyme disease is the most S. Zhetibaev) commonly reported arthropodborne disease in North DOI: https://doi.org/10.3201/eid2601.190220 America and is prevalent throughout central Europe, 70 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 1, January 2020 Seroprevalence of Tickborne Zoonotic Diseases, Kazakhstan particularly Germany, Austria, and Slovenia (10,11). Sample Size Lyme disease is the sixth most commonly reported Sample selection was based on concern about CCHF notifiable infectious disease in the United States as a nationally reportable disease. We conducted sur- (https://www.cdc.gov/lyme). In addition, incidence veys in households in which sheep and cattle sero- of Lyme disease and the range of tick vectors have surveys simultaneously were conducted; sample size been increasing in Europe and Asia (10,11), where calculations were based on expected seroprevalence Lyme disease is found in western Russia, Mongolia, of sheep and cattle. We calculated a target sample size northeast China, and Japan. of 561 households with sheep and 473 households CCHF, Q fever, and Lyme disease are endemic with cattle. We based the sample size on an α of 0.05, to the southern Kazakhstan region of Zhambyl, but power of 80%, a design effect of 2, and an expected their true burden is largely unknown because few se- response rate of 90%. We assumed CCHF seropreva- rologic surveys have been conducted in Kazakhstan lence of 24% in sheep and 19% in cattle, on the basis of and central Asia. The Zhambyl region covers >55,000 a meta-analysis of previous serosurveys (15). km2 and has a population of ≈1.2 million. The region is characterized by diverse ecology, containing both Participant Selection desert steppes and mountainous pastures, and eleva- We stratified the 363 villages in the region by known tions of 213–4,115 m. The region has 363 villages and (CCHF-endemic) or unknown (non–CCHF-endemic) 4 cities. Livelihoods are largely pastoral or agricultur- recent circulation of CCHF. We defined recent circu- al, and common occupations involve a high degree of lation as 1 confirmed human case reported in hospi- animal contact, placing humans at increased risk for tal-based surveillance from Zhambyl Oblast Health zoonotic infections. Department (Taraz, Kazakhstan) or 1 CCHF-positive Among the 3 diseases, only CCHF is a reportable tick confirmed in the previous 5 years and reported disease in Kazakhstan. During 2000–2013, the Zham- in annual tick surveillance data from the Ministry of byl region had 73 reported human CCHF cases, the Agriculture of Kazakhstan. We identified 66 (18.2%) second highest case-count among regions in Kazakh- villages that met the definition for having known, re- stan (12). However, data on human prevalence of cent CCHF circulation. CCHF in Kazakhstan are limited to reported clinical We selected 15 villages from each stratum; probabil- cases, even though studies show >80% of infections ity of selection was proportional to the number of sheep are subclinical (13). Although Q fever was detected and cattle in the village. We obtained livestock counts in Kazakhstan in the 1950s, the lack of surveillance or from reports by village veterinarians to the Ministry of serologic studies obscure our understanding of Q fe- Agriculture. Elevation of the 30 villages was 220–2,590 ver or Lyme disease incidence in the population (14). m (mean 781 m, median 488 m). Mean elevation was 513 Quantifying seroprevalence of these diseases in hu- m for villages with known CCHF circulation and 1,049 mans can help identify areas of pathogen circulation m for villages without known circulation. and areas where humans could be infected. Local veterinarians provided information on live- For this study, we aimed to determine the sero- stock-owning households in each village. To verify, prevalence of antibodies against CCHFV, C. burnetii, data collectors conducted a census of 5 villages and and B. burgdorferi in humans who interact with live- mapped households containing sheep or cattle. The stock in the Zhambyl region. In addition, we sought to veterinarian registry was accurate except for 2 in- assess the population’s knowledge of risk factors for stances in which the household recently had sold ani- disease transmission and how frequently they engage mals. Survey teams randomly selected 35 households in activities that increase or reduce risk for infection. from these registries and 1 adult per household for study participation. Methods In June 2017, we conducted a knowledge, attitudes, KAP/Risk Factor Survey and practices and risk factor survey (KAP/risk factor We adapted our KAP/risk factor survey from one survey), along with serosurveys for CCHF, Q fever, conducted in Georgia during a 2014 CCHF outbreak and Lyme disease, in 30 rural villages in the Zhambyl (16). We translated the survey into Russian and Ka- region. Participants could enroll in the KAP/risk fac- zakh, the 2 most common languages in the region. tor survey, the serosurvey, or both. Eligible partici- Survey teams pilot tested the questionnaire in an eli- pants were >18 years of age, residents of the village gible village not selected for the study. for >2 months, and residents of a household contain- The survey team administered the questionnaire ing a sheep or cow of >1 year of age. verbally at each respondent’s residence. Survey Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 1, January 2020 71 RESEARCH questions covered demographics; occupations; his- Ethics Review tory of animal and tick interactions; illness in the Each participant provided written, informed consent. previous 4 months or fever and hemorrhaging; and No personal identifying information was collected. knowledge of CCHF transmission routes, symp- The Institutional Review Board in Almaty, Kazakh- toms, and risk factors. The survey did not contain stan, through the Committee for Public Health Protec- questions specific for Lyme disease or Q fever. tion, approved the study. The protocol was reviewed according to the US Centers for Disease Control and Serosurvey Prevention human subjects review procedures, which After answering the questionnaire, respondents were determined the agency was not engaged in the study asked to go to their local health clinic to provide a because the Zhambyl Departments of Health and Ag- blood sample on the same day.
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