Global prevalence of Borrelia burgdorferi and Anaplasma phagocytophilum coinfection in wild and domesticated animals: A systematic review and meta-analysis.
Abstract: Both Borrelia burgdorferi (Bb) and Anaplasma phagocytophilum (Ap) can infect humans and animals through tick-borne transmission, resulting in zoonosis. Under certain conditions, human infection can lead to Lyme disease (LD) and human granulocytosis (HGA), whereas infection in animals can cause various acute and non-specific symptoms. The combination of Bb and Ap has been reported to increase the disease severity in infected animals. In this systematic review and meta-analysis, we investigated the global diversity of Bb and Ap coinfection in animals and their prevalence and distribution regarding spatial and species ecoepidemiology. Unassigned: We queried PubMed, Web of Science, Embase, and the Cochrane Library for original studies on Bb and Ap coinfection. We assessed the rate of Bb and Ap in all included articles by single-group meta-analysis and subgroup analyses. We evaluated publication bias using a combination of funnel plots, Egger's tests, and Begg's tests, and conducted risk of bias assessment using the SYRCLE tool. Unassigned: Our search retrieved 40 articles, with eight involving 8419 infected animals meeting our inclusion criteria. The SYRCLE bias risk assessment indicated that most of the included studies were of high quality. Forest maps showed that the combined Bb and Ap infection rate in animals worldwide was 5.5% (95% confidence interval (CI) = 2.4-9.6). Subgroup analysis of forest maps showed that the coinfection rates were 8.2% (95% CI = 2.2-17.2) in North American, 0.2% (95% CI = 0.1-0.7) in European, and 1.2% (95% CI = 0.8-1.8) in Asian animals. Coinfection rates were 6.7% (95% CI = 2.7-12.2) in domestic and 0.0% (95% CI = 0.0-0.4) in wild animals. The coinfection rates were 9% (95% CI = 5.7-12.8) in domestic horses and 6% (95% CI = 1.9-12.2) in domestic dogs, whereas 7.5% (95% CI = 3-17.9) in wild squirrels and 0.2% (95% CI = 0.1-0.7) in wild mice. Funnel diagrams, Egger's tests, and Begg's tests showed no significant publication bias in the included studies. Unassigned: Spatial epidemiology showed that coinfection with Bb and Ap in animals worldwide was most prevalent in the southwestern region of North America, whereas species epidemiology showed that coinfection was most prevalent in domesticated horses, followed by wild squirrels and domesticated dogs, but was less common in wild mice. These data on the epidemiological status of Bb and Ap coinfection in animals may help guide the prevention and treatment of zoonosis.
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Research Overview
This study systematically analyzed the global occurrence and distribution of coinfection by Borrelia burgdorferi (Bb) and Anaplasma phagocytophilum (Ap) in both wild and domesticated animals.
It estimated the prevalence rates, explored geographic and species-related patterns, and assessed the quality of existing research on this coinfection.
Background
Borrelia burgdorferi (Bb) and Anaplasma phagocytophilum (Ap) are both pathogens transmitted by ticks that can infect humans and animals causing diseases like Lyme disease (LD) and human granulocytosis (HGA).
In animals, infections may lead to acute and non-specific symptoms, and coinfection with both Bb and Ap is believed to increase disease severity.
Understanding the prevalence and distribution patterns of these coinfections in animal populations is crucial for managing zoonotic risks.
Research Objectives
To assess the global prevalence of coinfection with Bb and Ap in wild and domesticated animals through a comprehensive review and meta-analysis of published studies.
To determine how coinfection rates differ by geographic region (North America, Europe, Asia) and animal species.
To evaluate the quality of available studies and check for potential publication biases in the data.
Methodology
Systematic literature searches were performed in major databases: PubMed, Web of Science, Embase, and the Cochrane Library.
Inclusion criteria selected original studies reporting on coinfection rates of Bb and Ap in animals.
A single-group meta-analysis was conducted to estimate pooled coinfection prevalence across studies.
Subgroup analyses explored prevalence differences by continent and host animal categories (domesticated vs. wild animals, and specific species such as horses, dogs, squirrels, and mice).
Study quality was assessed using the SYRCLE risk of bias tool designed for animal studies.
Funnel plots, Egger’s tests, and Begg’s tests were applied to identify possible publication bias.
Key Findings
40 articles were initially retrieved; 8 articles including data on 8419 infected animals met all inclusion criteria.
The SYRCLE tool indicated that most included studies were of high methodological quality.
The global combined coinfection rate of Bb and Ap in animals was estimated at 5.5% (95% CI: 2.4–9.6%).
Geographically:
North America showed the highest coinfection rate at 8.2% (95% CI: 2.2–17.2%).
Europe had a low rate of 0.2% (95% CI: 0.1–0.7%).
Asia showed a moderate rate of 1.2% (95% CI: 0.8–1.8%).
By animal type:
Domestic animals had a coinfection rate of 6.7% (95% CI: 2.7–12.2%).
Wild animals had negligible coinfection prevalence at 0.0% (95% CI: 0.0–0.4%).
Among specific species:
Domestic horses exhibited the highest coinfection rate at 9% (95% CI: 5.7–12.8%).
Domestic dogs showed a 6% rate (95% CI: 1.9–12.2%).
Wild squirrels had a coinfection rate of 7.5% (95% CI: 3–17.9%).
Wild mice had a low rate of 0.2% (95% CI: 0.1–0.7%).
No significant publication bias was detected in funnel plots or statistical tests.
Spatial epidemiology highlighted the southwestern region of North America as the hotspot for Bb and Ap coinfection in animals.
Implications and Conclusions
The study reveals important patterns in the ecology and epidemiology of Bb and Ap coinfection across multiple continents and a range of animal hosts.
The higher prevalence in domesticated animals, particularly horses and dogs, suggests these animals may serve as important indicators or reservoirs for zoonotic transmission risks.
Low coinfection rates in wild animals like mice imply species-specific differences in exposure or susceptibility.
Geographical hotspots identified can guide targeted surveillance, prevention, and control efforts for tick-borne zoonotic diseases.
The findings provide valuable epidemiological data that can inform veterinary and public health strategies aimed at mitigating the burden of Lyme disease, human granulocytosis, and related animal illnesses linked to tick-borne coinfections.
Cite This Article
APA
Ma W, Gao L, Wu X, Zhong L, Huang X, Yang R, Wu H, Zhu L, Ma W, Peng L, Li B, Song J, Luo S, Bao F, Liu A.
(2024).
Global prevalence of Borrelia burgdorferi and Anaplasma phagocytophilum coinfection in wild and domesticated animals: A systematic review and meta-analysis.
J Glob Health, 14, 04231.
https://doi.org/10.7189/jogh.14.04231
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Gao, Li
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Wu, Xinya
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Zhong, Lei
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Huang, Xun
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Yang, Rui
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Wu, Hanxin
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Zhu, Liangyu
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Ma, Weijiang
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Peng, Li
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Li, Bingxue
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Yunnan Provincial Key Laboratory of Public Health and Biosafety, School of Public Health, Kunming Medical University, China.
Song, Jieqin
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Luo, Suyi
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Bao, Fukai
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Yunnan Provincial Key Laboratory of Public Health and Biosafety, School of Public Health, Kunming Medical University, China.
Liu, Aihua
Yunnan Province Key Laboratory of Children's Major Diseases Research, Department of Pathogen Biology and Immunology, School of Basic Medical Sciences, Kunming Medical University, China.
Yunnan Provincial Key Laboratory of Public Health and Biosafety, School of Public Health, Kunming Medical University, China.
Disclosure of interest: The authors completed the ICMJE Disclosure of Interest Form (available upon request from the corresponding author) and disclose no relevant interest.
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