First molecular detection of Dirofilaria immitis (Spirurida: Onchocercidae) infection in dogs from Northern Algeria

doi:10.1016/j.cimid.2017.04.001

Comparative Immunology, Microbiology and Infectious Diseases

Volume 51, April 2017, Pages 66-68

https://doi.org/10.1016/j.cimid.2017.04.001 Get rights and content

Highlights

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Dirofilarial nematodes were investigated by molecular tools in dogs from Northern Algeria.
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Dirofilaria immitis DNA was detected in 1.4% of dogs.
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This is the first molecular report of D. immitis in northern Algeria.

Abstract

Dirofilaria immitis and Dirofilaria repens are mosquito-borne filarioid nematodes that affect dogs and other domestic and wild carnivores, causing heartworm disease and subcutaneous dirofilariosis, respectively. In Algeria, the data about the epidemiology of these infections is largely unknown. The present study was designed to establish the occurrence of D. immitis and D. repens in dogs in Algeria using molecular tools.

In 2014 and 2015, a total of 209 dogs over one year of age of different breed and sex, living in Northern Algeria, were examined and blood samples were collected from each dog. The presence of D. immitis and D. repens in these samples was detected by real-time PCR followed by standard PCR and sequencing. Overall, the blood of 209 dogs from two departments was collected and only 3 (1.4%) of the blood samples were found positive for D. immitis DNA. Sequencing of the corresponding amplicon displayed a 99.8% identity to D. immitis, confirming the presence of this mosquito-borne nematode in Algeria. Furthermore, all tested samples were negative for D. repens.

Section snippets

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

DT, BD and PP designed the study. DT, HD and BD collected samples and clinical data. DT performed the experiments, carried out data analysis and interpretation and wrote the first draft of the manuscript. BD and PP participated in the critically revised the manuscript. All authors read and approved the final manuscript.

Acknowledgments

This study was supported by the AMIDEX project (No. ANR-11-IDEX-0001-02) funded by the “Investissements d’Avenir,” a French Government program managed by the French National Research Agency (ANR) and the Foundation Méditerranée Infection (www.mediterranee-infection.com). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors thank Dr. Abdelghani Loudahi and Dr. Kahina Razali for their help in the field study.

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Dirofilaria immitis and Di. repens are periodically reported from dogs in sub-Saharan African countries: the prevalence of Dirofilaria spp. was 17.5% in Tunisia in 2014 (Rjeibi et al., 2017), 1.4% in Algeria in 2014–2015 (Tahir et al., 2017), 5.92% in Tanzania in 2015 (Mukendi et al., 2016), and 31% in Mozambique in 1996 (Schwan and Durand, 2002). Historically, there have been reports of Di.
Neglected tropical diseases pose a threat to domestic animal health, as domestic animals can serve as reservoirs for certain zoonotic parasitic infections, including Guinea worm (Dracunculus medinensis) and lymphatic filariasis. Surveillance for these parasites in domestic animals is needed to understand infection prevalence and transmission cycles, with the goal of instituting appropriate interventions. The goal of this research was to report our finding of Brugia sp. infection in dogs from Chad, Africa, and to characterize the genetics and epidemiology of the parasite. During a recent Chadian canine pathogen surveillance project, we identified Brugia sp. infections in a total of 46 out of 428 dogs (10.7%) sampled at three time points in 2019–2020. We found high levels of sequence similarity to B. malayi and B. pahangi based on amplification of 18S rRNA, 5.8S rRNA, and ITS-2 regions. Phylogenetic analysis of 18S rRNA gene sequences placed the Chadian Brugia sp. in a clade with other Brugia spp. but grouped it separately from both B. malayi and B. pahangi. Analysis of Hha I sequences showed the greatest similarity with B. patei, a parasite previously reported from dogs, cats, and wildlife hosts in Kenya. Epidemiologic analysis using generalized linear regression modeling found significantly higher odds of Brugia sp. detection among dogs in villages in southern Chad compared to those in the northern region. Further, within the northern region, there were higher odds of detection in the dry season, compared to the wet season, which is consistent with the ecology of a presumably mosquito-borne parasite. The same 428 dogs were tested for Dirofilaria immitis antigen using a commercial assay (IDEXX SNAP 4Dx) at the earliest time point of the study, with 119 dogs testing positive. However, no association was noted between Brugia infection and a dog being positive for Di. immitis antigen, with only seven of the 119 Di. immitis antigen-positive dogs being Brugia-positive. This is the first report of Brugia sp. in domestic dogs in Chad and additional research is needed to definitively identify the species present, elucidate transmission, and understand potential risks to canine and human health.
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This infection is the causal agent of Chagas disease in humans (screening of the parasite carried out by serology and PCR) [63]. Numerous studies have also been conducted on canine filariasis due to Dirofilaria immitis and D. repens [64–67]. These are zoonotic parasitoses the range of which is now on the increase in Europe.
At the University Hospital Institute Méditerranée Infection (IHU, Marseille, France), for almost thirty years, veterinarians have been carrying out epidemiological investigations, together with doctors, on animals living near human cases of zoonoses, on the one hand, and on the other hand, transverse and longitudinal epidemiological surveillance studies on animals which are reservoirs, vectors or sentinels of potentially zoonotic infections,. This article presents the methods adopted and the results obtained from these studies. They have been the subject of 76 peer-reviewed publications relating to wild animals (37 publications) and/or domestic animals (48 publications). These studies were often carried out in the field with veterinarians from the French army's health service (39 publications). They were at the origin of the detection of some thirty zoonotic pathogens in the laboratories of the IHU (64 publications) and/or other French laboratories (18 publications). Our approach is an original embodiment of the “One Health” concept.
The global status of Dirofilaria immitis in dogs: a systematic review and meta-analysis based on published articles
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However, the necropsy is not approved and accepted on the basis of the ethical principles in scientific studies on animals (Fraser, 1999; Touitou et al., 2004, 2006). Therefore, molecular methods, such as antigen detection are more acceptable owing to high sensitivity and specificity of blood samples (Tahir et al., 2017b; Torres-Chable et al., 2018; Anvari et al., 2019b). According to meta-analysis, knott's test, and PCR are the next priorities.
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.
The prevalence of Dirofilaria immitis and D. repens in the Old World
2020, Veterinary Parasitology
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Dirofilaria immitis and D. repens are endemic throughout Europe and southern eastern regions of Asia and reported with increasing frequency in Africa. Nevertheless, the increased awareness of veterinary practitioners, even in countries where the prevalence is low, has led to a decrease D. immitis prevalence in dogs, especially in previously endemic/hyper-endemic areas. Prevalence has significantly increased, however, in areas where heartworm has apparently spread more recently, such as Central and North Eastern Europe. Furthermore, autochthonous cases have been observed in Siberia. Low seroprevalence has been reported in Croatia, while in Romania it has reached 14%. In Greece, the prevalence ranges between 0.7% and 25% whilst in Turkey is 0-18%. Data for canine dirofilariosis in Africa is scarce, and most are case reports. Overall, the dominant species is Achanthocheilonema dracunculoides, although both D. immitis and D. repens have been reported from some countries. In the Far East, the prevalence ranges from 2% to 15% in northeastern of China. In Hong Kong a novel species has been found in dogs and humans (Candidatus Dirofilaria hongkongensis). In India, the prevalence ranges from 4.7%-29.5% in Northeastern states.
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Feline heartworm infection has been diagnosed in every European country when diagnosed either by the Knott test or by serology for circulating antibodies and antigens of the parasite. However, prevalence is much lower than in dogs.
In spite of the continuing spreading of heartworm infection, D. repens is the main concern in Europe, mostly for physicians, while the infection is nearly always asymptomatic in dogs. The infection is spreading from Portugal to the Southeastern regions of Finland and Siberia, and in some areas its prevalence overlaps that of D. immitis. Many reasons make more difficult the control of D. repens than D. immitis: the frequent lack of clinical symptoms of suspicion, the specific diagnosis being possible only by blood examination and the inefficacy of some macrocyclic lactones.
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South Europe is considered an enzootic area for Dirofilaria spp. and particularly Spain (Montoya-Alonso et al., 2017), Portugal (Alho et al., 2018), France (Pantchev et al., 2009), Italy (Genchi et al., 2011) and Greece (Diakou et al., 2016), where the parasites' distribution covers a considerable area of the countries. There are reports of D. immitis infection also in other Mediterranean countries (Rjeibi et al., 2016; Khatat et al., 2017; Tahir et al., 2017) and Balkans (Rapti and Rehbein, 2010; Ionicǎ et al., 2015; Pantchev et al., 2015; Mrljak et al., 2017), while the parasite progressively spreads over Europe (Morchón et al., 2012), establishing new enzootic areas in formerly heartworm-free regions (Traversa et al., 2010). Simultaneously, D. repens shows a more aggressive spreading pattern with the northernmost areas reporting autochthonous cases being Northern Russia, Finland and Estonia (Jokelainen et al., 2016; Pietikäinen et al., 2017).
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Comparative Immunology, Microbiology and Infectious Diseases

Highlights

Abstract

Section snippets

Competing interests

Authors’ contributions

Acknowledgments

References (11)

A duplex real-time polymerase chain reaction assay for the detection of and differentiation between Dirofilaria immitis and Dirofilaria repens in dogs and mosquitoes

Vet. Parasitol.

Molecular survey of Dirofilaria immitis and Dirofilaria repens by new real-time TaqMan(R) PCR assay in dogs and mosquitoes (Diptera: Culicidae) in Corsica (France)

Vet. Parasitol.

Highly sensitive multiplex PCR for simultaneous detection and discrimination of Dirofilaria immitis and Dirofilaria repens in canine peripheral blood

Vet. Parasitol.

Rapid differentiation of Dirofilaria immitis and Dirofilaria repens in canine peripheral blood by real-time PCR coupled to high resolution melting analysis

Vet. Parasitol.

Human and animal dirofilariasis: the emergence of a zoonotic mosaic

Clin. Microbiol. Rev.

Cited by (12)

Characterization of the genetics and epidemiology of Brugia sp. in domestic dogs in Chad, Africa

Detection of zoonotic pathogens in animals performed at the University Hospital Institute Méditerranée Infection (Marseille – France)

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

The prevalence of Dirofilaria immitis and D. repens in the Old World

Filarial infections in dogs in Cyprus, an apparently heartworm free island

Filarial worms: A systematic review and meta-analysis of diversity in animals from Iran with emphasis on human cases