The global status of Dirofilaria immitis in dogs: a systematic review and meta-analysis based on published articles

doi:10.1016/j.rvsc.2020.04.002

Research in Veterinary Science

Volume 131, August 2020, Pages 104-116

https://doi.org/10.1016/j.rvsc.2020.04.002 Get rights and content

Highlights

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The prevalence of D. immitis infection in dogs worldwide was 10.91%.
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Significant differences detected between the prevalence of D. immitis in dogs and country.

Abstract

Dirofilaria immitis is a parasitic filarial nematode responsible for heartworm disease in domestic as well as wild canines and felines and pulmonary or cutaneous infections in humans. This systematic review and meta-analysis aimed to evaluate the status of D. immitis in dogs based on available literature. Four English language databases (ISI Web of Science, Scopus, PubMed and Science Direct) containing data on D. immitis prevalence in dogs were thoroughly searched resulting in the inclusion of 193 studies. The findings revealed that the pooled and weighted prevalence of D. immitis infection in dog population based on published papers throughout the world was 10.91% (95% CI=10.18–11.65). In addition, subgroup analysis based on meta-regression revealed that a significant difference between the pooled and weighted prevalence of D. immitis in dogs and country (β =0.14, P=0.049). Given the relatively high prevalence of D. immitis infection in dogs and its adverse effects, it is suggested that to perform more research on the prevention and control of dirofilariasis infection in dogs worldwide.

Introduction

Dirofilariasis is a common disease between human and animals, caused by Dirofilaria immitis (D. immitis), a nematode that can be transmitted by insects and spread worldwide. Many domestic animals, especially dogs and cats play the role of main hosts for this parasite (Atkins, 2003). Human may be infected with the larval stage as an aberrant host, and several human cases have so far been detected in Iran, Japan and the United States (Ettinger and Feldman, 2005). Adult worm resides in the pulmonary artery of dogs which can produce blood-circulating microfilariae in dogs. On the other hand, the preadult worm is responsible for pulmonary dirofilariasis in humans since the worm cannot reach full maturity, (Taylor et al., 2016). The infective third-stage larvae can be transmitted to the vertebrate hosts, such as humans and animals through mosquito bite (Anopheles and Culex). Dirofilariasis in dogs can cause clinical symptoms, such as persistent cough, dyspnea, congestive heart failure, physical activity intolerance, intravascular hemolysis, hemoptysis, ascites, pulmonary thromboembolism, and loss of appetite and weight. In tropical and subtropical regions of the world, dirofilariasis is considered one of the most important zoonotic diseases transmitted between humans and carnivores (Vieira et al., 2014) and deadly in dogs if not treated (Taylor et al., 2016). The presence of dogs infected with microfilariae-producing adult worms determines the prevalence and transmission of D. immitis in dogs and cats. The prevalence tends to vary dramatically among different regions of the world on account of certain epidemiological factors, such as the distribution of the mosquito species (vector), mosquito fertility, mosquito population density, animal behavior, environmental temperature, living conditions, and the average age of the susceptible host (Anvari et al., 2019a; Omar et al., 2018; Taylor et al., 2016).

Over the past 20 years, the geographic range of canine heartworm infection has increased significantly. In addition, an increasing number of D. immitis infection cases in dogs has been reported in many countries (Hou et al., 2011). However, there still exists a gap in our knowledge concerning the status of this parasite throughout the world and across different continents.

With this background in mind, the present systematic review and meta-analysis aimed to update and broaden our knowledge on the status of Dirofilaria immitis infections in dogs based on published articles, provide and compile information on the status and distribution of Dirofilaria immitis infections in dogs around the world, assess the risk factors of heartworm infection, and establish the worldwide status of this parasite for the first time according to so far published studies.

Section snippets

Methods

This systematic literature review and meta-analysis is strictly subject to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline and its checklist (Moher et al., 2009).

Qualified studies

The search of four databases resulted in the inclusion of 2031 articles, 1446 articles of which were excluded due to duplication and 585 papers were screened after this exclusion. A total of 379 papers were excluded after a preliminary screening based on titles and abstracts and 206 studies were extracted. Thereafter, 17 articles were ruled out by considering the inclusion and exclusion criteria of the full texts of the articles. Finally, a number of 189 eligible papers (includes 193 dataset)

Discussion

Cardiopulmonary dirofilariasis is a worldwide distributed vector-borne transmitted disease caused by Dirofilaria immitis mainly affecting dogs and cats. Different species of culicid mosquitoes mainly belonging to Culex, Anopheles, and Aedes genera have been implicated in the transmission of this parasite. Since some of these mosquito species indiscriminately feed on both humans and animal reservoirs, D. immitis can be transmitted to humans residing in endemic areas, causing benign pulmonary

Conclusion

The results of the current review determined a relatively significant prevalence of dirofilariasis in dog population worldwide. In addition, a significant difference was detected between prevalence of D. immitis and geographical region. Hence, it is recommended that a routine and reliable screening test be conducted onD. immitis infection among dogs in endemic regions. Moreover, veterinarians should pay more attention to this zoonotic disease and take appropriate measures to prevent it, such as

Acknowledgements

The authors would like to thank all members of the parasitology department at the medical school of Mazandaran University of Medical Sciences. Also, authors are grateful to Dr. Seyed Abdollah Hosseini for his helpful comments. This study was approved by the deputy of research and ethics committee, Mazandaran University of Medical Sciences, Sari, Iran (Grant No: 5468; Code of Ethics: IR.MAZUMS.REC.1398.5468).

Authors' contributions

DA, SG, AD, and SS conceived and designed the study, and SG critically revised the manuscript. DA, EN, HZH and MRN searched the literature; DA and EN extracted the data. DA wrote the manuscript. DA and MM performed the statistical analysis. All authors have read and approved the final version of manuscript.

Declaration of Competing Interest Statement

The authors have no conflicts of interest to declare.

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¹: Contributed equally.

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The global status of Dirofilaria immitis in dogs: a systematic review and meta-analysis based on published articles

Highlights

Abstract

Introduction

Section snippets

Methods

Qualified studies

Discussion

Conclusion

Acknowledgements

Authors' contributions

Declaration of Competing Interest Statement

Mol. Biochem. Parasitol.

Microb. Pathog.

Vet. Parasitol.

Vet. Parasitol.

Asian. Pac. J. Trop. Dis.

Mexico. Vet. Parasitol.

Vet. Clin. Small Anim. Pract.

Vet. Parasitol.

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Vet. J.

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Vet. Parasitol.

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China. Vet. Parasitol.

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Thailand. Agric. Nat. Resour.

Vet. Parasitol.

Germany. Vet. Parasitol.

The prevalence of Dirofilaria immitis in dogs with different breed, ages and sex

Vet. Fak. Derg.

Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi infection in stray dogs from sanliurfa in Turkey

Vet. Res.

A field survey on parasites and antibodies against selected pathogens in owned dogs in Lilongwe

Malawi. J. S. Afr. Vet. Assoc.

Prevalence of dirofilariasis in shepherd and stray dogs in iranshahr, southeast of Iran

J. Parasit. Dis.

Survey of Dirofilaria immitis in dogs from Sivas Province in the Central Anatolia Region of Turkey

Turk. J. Vet. Anim. Sci.

Comparison of results of three commercial heartworm antigen test kits in dogs with low heartworm burdens

J. Am. Vet. Med. Assoc.

Serological and molecular prevalence of selected canine vector borne pathogens in blood donor candidates, clinically healthy volunteers, and stray dogs in North Carolina

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Parasitological, Serological and Molecular Study of Dirofilaria immitis in Domestic Dogs, Southeastern Iran

Iran. J. Parasitol.

Vector-Borne Infections in Tornado-Displaced and Owner-Relinquished Dogs in Oklahoma, USA

Vector Borne Zoonotic Dis.

Serological and molecular prevalence of Borrelia burgdorferi, Anaplasma phagocytophilum, and Ehrlichia species in dogs from Minnesota

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Biological control of mosquito vectors: Past, present, and future

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Prevalence of haemoparasites in pet, working and stray dogs of Assam and North-East India: A hospital based study

Vet. World

Seroprevalence of vector borne parasites in naturally exposed dogs of Assam, India

Vet. World

The prevalence of Dirofilaria immitis in dogs in Sydney

Aust. Vet. J.

The prevalence of Dirofilaria immitis and other parasites in urban pound dogs in north-eastern Victoria

Aust. Vet. J.

The epidemiology of Dirofilaria immitis infection in outpatient dogs at Chiang Mai University Small Animal Hospital, Thailand

Southeast Asian J. Trop. Med. Public Health

Seroprevalence of canine dirofilariosis, granulocytic anaplasmosis and lyme borreliosis of public health importance in dogs from India’s North East

Vet. World

Prevalence and molecular epidemiological data on Dirofilaria immitis in dogs from Northeastern States of India

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Occult dirofilariosis in dogs of north eastern region in India

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A serological survey of Dirofilaria immitis infection in pet dogs of Busan, Korea, and effects of chemoprophylaxis

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The prevalence and abundance of helminth parasites in stray dogs from the city of Queretaro in central Mexico

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Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp. and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal - a national serological study

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