Skip to main content
Log in

Molecular characterization of canine filarioids in a previously non-endemic area of Rio de Janeiro State, Brazil

  • Helminthology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Dirofilaria immitis is the causative agent of canine heartworm disease, a severe health problem in dogs, especially in coastal areas of tropical and subtropical regions of the world. We employed molecular methods to investigate the occurrence of canine infection by filarioids in five municipalities of Baixada Fluminense (Magé, Duque de Caxias, Guapimirim, Nova Iguaçu, and São João de Meriti), a non-endemic area of Rio de Janeiro State, Southeast Brazil. A total of 110 canine blood samples collected from 2017 to 2018 and positive for microfilariae at the modified Knott’s test were screened by cPCR targeting DNA fragments of the 12S rDNA gene for filarial nematodes. Seventy-seven samples (70%) tested positive at the molecular analysis. Of these, 72 were identified as D. immitis and 5 (4.5%) as Acanthocheilonema reconditum. Dirofilaria repens was not detected in the studied municipalities of Baixada Fluminense. This is the first record of D. immitis and A. reconditum in the Baixada Fluminense region, Rio de Janeiro State, Brazil. The prevalence of D. immitis cases in the five municipalities suggests the establishment and maintenance of its enzootic cycle in the studied region, which indicate vulnerability to the occurrence of epidemic cycles and, possibly, human cases.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

The datasets used and/or analyzed during the present study are available from the corresponding author upon reasonable request. The nucleotide sequences of the dataset generated here are available on the Genbank website (https://www.ncbi.nlm.nih.gov/nucleotide/) with the accession numbers: MZ678855-MZ678931.

Code availability

Not applicable.

References

  • Acha PN, Szyfres B (2003) Filariasis zoonóticas. In: Organización Panamericana de la Salud. Zoonosis y enfermedades transmisibles comunes al hombre y a los animales: parasitosis 3.ª ed. Washington, D.C.: OPS, 2003. 3 vol. — (Publicación Científica y Técnica No. 580) p.284–91

  • Alberigi B, Oliveira AC, Vieira GSR, Fernandes PA, Labarthe N, Mendes-de-Almeida F (2020) Unusual feline Dirofilaria immitis infection: a case report. Braz J Vet Parasitol 29(3):e008420.7. https://doi.org/10.1590/S1984-29612020061

    Article  Google Scholar 

  • American Heartworm Society – AHS (2020). Guidelines for the diagnosis, prevention, and management of heartworm (Dirofilaria immitis) infection in dogs and cats. https://www.heartwormsociety.org/veterinary-resources/american-heartworm-society-guidelines. Accessed 08 jul 2021.

  • Araújo RB, Estradioto L, Coelho MS, Araújo VB, Kusano LDC, da Silva LLG (2019) Dirofilariose pulmonar - Um atípico diagnóstico de um nódulo pulmonar. Relatos Casos Cir 5(3):e2299. https://doi.org/10.30928/2527-2039e-20192299

    Article  Google Scholar 

  • Argôlo EGG, Reis T, Fontes DAT, Gonçalves EC, Giese EG, Melo FTV et al (2018) Canine filariasis in the Amazon: species diversity and epidemiology of these emergent and neglected zoonoses. PLoS ONE 13(7):e0200419

    Article  PubMed  PubMed Central  Google Scholar 

  • Bendas AJR, Mendes-de-Almeida F, Guerrero J, Labarthe N (2017) Update on Dirofilaria immitis epidemiology in South America and Mexico: literature review. Braz J Vet Res Anim Sci 54(4):319–2. https://www.revistas.usp.br/bjvras/article/view/132572. Accessed 30 Dec 2021

  • Bendas AJR, Branco AS, da Silva BRSA et al (2019) Mosquito abundance in a Dirofilaria immitis hotspot in the eastern state of Rio de Janeiro. Brazil Vet Parasitol Reg Stud Reports 18:100320. https://doi.org/10.1016/j.vprsr.2019.100320

    Article  PubMed  Google Scholar 

  • Benzaquen M, Brajon D, Delord M, Yin N, Bittar F, Toga I et al (2015) Cutaneous and pulmonary dirofilariasis due to Dirofilaria repens. Brit Jour Dermat 173:788–879

    Article  CAS  Google Scholar 

  • Cabrera ED, Carréton E, Morchón R, Falcón-Cordón Y, Falcón-Cordón S, Simón F, Montolya-Alonso JÁ (2018) The Canary Islands as a modelo of risk of pulmonar dirofilariasis in a hyperendemic area. Paras Research 117:933–936. https://doi.org/10.1007/s00436-018-57774-1

    Article  Google Scholar 

  • Campos JRM, Barbas CSV, Filomeno LTB, Fernandez A, Minamoto H, Barbas Filho JV et al (1997) Human pulmonar dirofilariasis. Chest 112:729–733

    Article  Google Scholar 

  • Casiraghi M, Bain O, Guerrero R, Martin C, Pocacqua V, Gardner SL et al (2004) Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. Int J Parasitol 34:191–203

    Article  PubMed  Google Scholar 

  • Cavallazi RS, Cavallazi AC, Souza IV (2002) Dirofilariose pulmonar humana: relato de sete casos. Jornal Pneum 28:100–102

    Article  Google Scholar 

  • Costa RC, Couto-Lima D, Serrão ML, Labarthe N (2004) An update survey of the prevalence of Canine Dirofilariasis in a focus area of the city of Rio de Janeiro. Brazil Rev Bras Parasitol Vet 13(1):23–28

    Google Scholar 

  • Dantas-Torres F, Otranto D (2013) Dirofilariosis in the Americas: a more virulent Dirofilaria immitis? Parasit Vectors Oct 2 6(1):288. https://doi.org/10.1016/j.vprsr.2019.100320

    Article  Google Scholar 

  • Dantas-Torres F, Otranto D (2020) Overview on Dirofilaria immitis in the Americas, with notes on other filarial worms infecting dogs. Vet Parasitol 282:109113. https://doi.org/10.1016/j.vetpar.2020.109113

    Article  PubMed  Google Scholar 

  • Doutrário AB, Valim NC, Dellaspora EAPB, Gaspar GG, Puga FG, Fabro AT et al (2019) Human pulmonar dirofilariasis with secondary myocarditis. Jour Braz Soc Trop Med 52:e20180461

    Article  Google Scholar 

  • Garcez LM, Souza NF, Mota EF, Dickson LAJ, Abreu WU, Cavalcanti VFN et al (2006) Focos de dirofilariose canina na Ilha de Marajó: um fator de risco para a saúde humana. Rev Soc Bras Med Trop 39(4):333–336

    Article  PubMed  Google Scholar 

  • Genchi C, Rinaldi L, Mortarino M, Genchi M, Cringoli G (2009) Climate and Dirofilaria infection in Europe. Vet Parasitol 4:286–292

    Article  Google Scholar 

  • Gioia G, Lecova L, Genchi M, Ferri E, Genchi C, Mortarino M (2010) Highly sensitive multiplex PCR for simultaneous detection and discrimination of Dirofilaria immitis and Dirofilaria repens in canine peripheral blood. Vet Parasitol 172:160–163

    Article  CAS  PubMed  Google Scholar 

  • Klinge MES, Robayo PC, Barreto CAM (2011) Dirofilaria immitis: una zoonosis presente en el mundo. Rev Med Vet 22:57–68

    Article  Google Scholar 

  • Knight DH (1987) Heartworm infection. Veterinary Clinics of North America. Small Animals Practice, USA 17:1463–1518

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33(7):1870–4. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoseini M, Jalousian F, Hoseini SH, Gerami Sadeghian A (2020) A cross sectional study on Dirofilaria immitis and Acanthocheilonema reconditum in sheepdogs in a western region in Iran. Veterinary research forum: an international quarterly journal 11(2):185–190. https://doi.org/10.30466/vrf.2018.78930.2046

    Article  Google Scholar 

  • Huynh T, Thean J, Maini R (2001) Dipetalonema reconditum in the human eye. Br J Ophthalmol 85:1384–1393. https://doi.org/10.1136/bjo.85.11.1384

    Article  PubMed Central  Google Scholar 

  • IBGE (2010) Instituto Brasileiro de Geografia e Estatística. Baixada Fluminense. https://cidades.ibge.gov.br/brasil. Acessed 08 jul 2021.

  • Ionică AM, Matei IA, D’Amico G et al (2017) (2017) Filarioid infections in wild carnivores: a multispecies survey in Romania. Parasit Vectors 10(1):332. https://doi.org/10.1186/s13071-017-2269-3

    Article  PubMed  PubMed Central  Google Scholar 

  • John M, Mathew SM, Sebastian V, Biswas J, Raman M (2012) Multiple live subconjunctival dipetalonema: report of a case. Indian J Ophthalmol 60(3):228–229. https://doi.org/10.4103/0301-4738.95881

    Article  PubMed  PubMed Central  Google Scholar 

  • Labarthe N, Serrão ML, Melo YF, de Oliveira SJ, Lourenço-de-Oliveira R (1998) Potential Vectors of Dirofilaria immitis (Leidy, 1856) in Itacoatiara, Oceanic Region of Niterói Municipality, State of Rio de Janeiro. Brazil Mem Inst Oswaldo Cruz 93(4):425–432. https://doi.org/10.1590/s0074-02761998000400001

    Article  CAS  PubMed  Google Scholar 

  • Labarthe N, de Campos PM, Barbarini O, McKee W, Coimbra CA, Hoskins J (2003) Serologic prevalence of Dirofilaria immitis, Ehrlichia canis, and Borrelia burgdorferi infections in Brazil. Vet Ther 4(1):67–75 (PMID: 12756637)

    PubMed  Google Scholar 

  • Labarthe N, Guerrero J (2005) Epidemiology of heartwormn: what is happening in South América and México. Vet Paras 133:149–156

    Article  Google Scholar 

  • Labarthe NV, Paiva JP, Reifur L, Mendes-de-almeida F, Merlo A, Pinto CJC et al (2014) Updated canine infection rates for Dirofilaria immitis in areas of Brazil previously identified as having a high incidence of heartworm-infected dogs. Parasites Vectors 7(493):2–8

    Google Scholar 

  • Latrofa MS, Weigl S, Dantas-Torres F, Annoscia G, Traversa D, Brianti E (2012) A multiplex PCR for the simultaneous detection of species of filarioids infesting dogs. Acta Trop 122:150–154

    Article  CAS  PubMed  Google Scholar 

  • Lentz H, Freitas JFT (1937) Dirofilariose subcutânea dos cães no Brasil. Mem Inst Oswaldo Cruz 32:443–448

    Article  Google Scholar 

  • Maggi RG, Krämer F (2019) A review on the occurrence of companion vector-borne disease in pet animals in Latin America. Parasites Vectors 12:145

    Article  PubMed  PubMed Central  Google Scholar 

  • Mendes-de-Almeida F, Alves LC, Fernandes PA, Leivas RM, Labarthe N (2021) Infection with Dirofilaria immitis and Other Infections in Cats and Dogs from Rio de Janeiro, Brazil: The Need for Prophylactic Enforcement. Acta Parasitologica https://doi.org/10.1007/s11686-021-00345-z.

  • Moraes MFD, da Silva MX, Magalhães-Matos PC, de Albuquerque ACA, Tebaldi JH, Mathias LA et al (2017) Filarial nematodes with zoonotic potential in ring-tailed coatis (Nasua nasua Linnaeus, 1766, Carnivora: Procyonidae) and domestic dogs from Iguaçu National Park, Brazil. Vet Parasitol Reg Stud Reports 8:1–9

    PubMed  Google Scholar 

  • Napoli E, Gaglio G, Falsone L, Giannetto S, Dantas-Torres F, Otranto D et al (2014) New insights into the biology and ecology of Acanthocheilonema reconditum (spirurida: onchocercidae). Parasit Vectors 7(Suppl 1):O29. https://doi.org/10.1186/1756-3305-7-S1-O29

    Article  PubMed Central  Google Scholar 

  • Newton MD, Wight LM (1956) The occurrence of a dog filarioid other than Dirofilaria immitis in the United States. Jour of Parasitol 42:246–258

    Article  CAS  Google Scholar 

  • WHO Expert Committee on Parasitic Zoonoses & World Health Organization (1979) Zoonosis parasitarias : informe de un Comité de Expertos de la OMS, con la participación de la FAO. Organización Mundial de la Salud Informe técnico 637: p 105–06. https://apps.who.int/iris/handle/10665/41290. Accessed 30 Dec 2021

  • Otranto D, Diniz DG, Dantas-Torres F et al (2011) Human intraocular filariasis caused by Dirofilaria sp. nematode, Brazil. Emerg Infect Dis 17(5):863–866. https://doi.org/10.3201/eid1705.100916

  • Pacifico L, Ferrari N, Romeo C, Buono F, Varuzza P, Sgroi G et al (2021) Haematological and biochemical abnormalities in hunting dogs infected with Acanthocheilonema reconditum, associated risk factors, and a European overview. Parasitol Res 120(6):2109–2124. https://doi.org/10.1007/s00436-021-07179-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Pampiglione S, Rivasi F, Gustinelli A (2009) Dirofilarial human cases in the old world, attributed to Dirofilaria immitis: a critical analysis. Histopathology 54:192–204

    Article  PubMed  Google Scholar 

  • Rocha PR, David HMSL (2015) Determination or determinants? A debate based on the Theory on the Social Production of Health. Rev Esc Enferm USP 49(1):129–135. https://doi.org/10.1590/S0080-623420150000100017

    Article  PubMed  Google Scholar 

  • Rodrigues-Silva R, Moura H, Dreyer G, Rey L (1995) Human pulmonar dirofilariasis: a review. Rev Inst Med Trop 37(6):523–530

    Article  CAS  Google Scholar 

  • Rodrigues-Silva R, Guerra RJA, Almeida FB, Machado-Silva JR, Paiva DD (2004) Dirofilaríase pulmonar humana no Estado do Rio de Janeiro, Brasil: relato de um caso. Rev Soc Bras Med Trop 37:56–59

    Article  PubMed  Google Scholar 

  • Silva MSG, Leles D, Sudré AP, Millar PR, Uchôa F, Brener B (2019) Prevalência e caracterização molecular de Dirofilaria immitis (Filarioidea: Onchocercidae) em cães de zonas endêmicas do estado do Rio de Janeiro. Brasil J Parasitol 105(2):387–390

    Article  CAS  Google Scholar 

  • Silva RC, Langoni H (2009) Dirofilariose. Zoonose emergente negligenciada. Revisão Bibliográfica. Cienc Rur 39:5:1614–23.

  • Simón F, Gonzaléz-Miguel J, Diosdado A, Goméz PJ, Morchón R, Kartashev (2017) The complexity of zoonotic filariasis episystem and its consequences: a multidisciplinary view. BioMed Research International ID6436130; https://doi.org/10.1155/2017/6436130

  • Simsek S, Ciftci AT (2016) Serological and molecular detection of Dirofilaria species in stray dogs and investigation of Wolbachia DNA by PCR in Turkey. J Arthropod Borne Dis 10(4):445–453

    PubMed  PubMed Central  Google Scholar 

  • Soares HS, Camargo LM, Gennari SM, Labruna MB (2014) Survey of canine tick-borne diseases in Lábrea, Brazilian Amazon: ‘accidental’ findings of Dirofilaria immitis infection. Rev Bras Parasitol Vet 23(4):473–480. https://doi.org/10.1590/S1984-29612014093

    Article  PubMed  Google Scholar 

  • Theis JH (2005) Public health aspects of dirofilariasis in the United States. Vet Parasitol 133:157–180

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680. https://doi.org/10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres FD, Figueredo LA (2007) Heterodoxus spiniger (Enderlein, 1909) on domestic dogs (Canis familiaris, L. 1758) from the city of Recife, Pernambuco State, Brazil. Braz J Vet Res Anim Sci 44:77–80

    Article  Google Scholar 

  • Vieira VMA. Potencial zoonótico por Dirofilaria immitis (Leidy,1856) Raillet & Henry, 1911 na Baixada Fluminense do Rio de Janeiro. Dissertação [Mestrado em Medicina Tropical]. Fundação Oswaldo Cruz – Fiocruz; 2019. https://www.arca.fiocruz.br/handle/icict/37288. Accessed 30 Dec 2021

Download references

Acknowledgements

The authors would like to thank to Dr. Jonimar Pereira Paiva (in memoriam) (Universidade Federal Rural do Rio de Janeiro, Brazil) for providing heartworm specimens for positive control in the molecular assays, to Dr. Erik R. Wild for English review and comments, and to Genomic Platform DNA Sequencing (PDTIS/ FIOCRUZ, Rio de Janeiro, Brazil) for sequencing support.

Funding

This study was conducted with the support of Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—funding code 001) and Plano de Objetivos e Metas (POM) of the Laboratório de Inovações em Terapias, Ensino e Bioprodutos – LITEB and Laboratório de Referência Nacional em Vetores das Riquetsioses (LIRN), Instituto Oswaldo Cruz, Fiocruz.

Author information

Authors and Affiliations

Authors

Contributions

Designed the study: Viviane Marques de Andrade Vieira, Nicole Oliveira Moura Martiniano, Gilberto Salles Gazêta, Antonio Henrique Almeida de Moraes Neto; collected and analyzed clinical data from the animals: Viviane Marques de Andrade Vieira, Priscila Pinho da Silva, Norma Labarthe, Erica Tex Paulino, Gilberto Salles Gazêta, Antonio Henrique Almeida de Moraes Neto; performed the screening blood analysis: Priscila do Amaral Fernandes, Viviane Marques de Andrade Vieira; performed the molecular and phylogenetic analyses: Viviane Marques de Andrade Vieira, Nicole Oliveira Moura Martiniano; interpreted the results and wrote the article: Viviane Marques de Andrade Vieira, Nicole Oliveira Moura Martiniano, Gilberto Salles Gazêta, Antonio Henrique Almeida de Moraes Neto, Erica Tex Paulino; reviewed and edited the final version of the manuscript: Viviane Marques de Andrade Vieira, Nicole Oliveira Moura Martiniano, Gilberto Salles Gazêta, Antonio Henrique Almeida de Moraes Neto; supervise: Gilberto Salles Gazêta, Antonio Henrique Almeida de Moraes Neto.

Corresponding author

Correspondence to Antonio Henrique Almeida de Moraes Neto.

Ethics declarations

Ethics approval

The study was approved by the Animal Use Ethics Committee of the Oswaldo Cruz Institute/Oswaldo Cruz Foundation (CEUA-IOC-L009/2020) and by the Oswaldo Cruz Institute/Oswaldo Cruz Foundation Human Research Ethics Committee (CEP CAAE: 30759620.1.0000.5248).

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

Norma Labarthe is a consultant for Boehringer Ingelheim, Idexx, and Zoetis in Brazil. Viviane Marques de Andrade Vieira, Nicole Oliveira Moura Martiniano, Priscila do Amaral Fernandes, Priscila Pinho da Silva, Érica Tex Paulino, Gilberto Salles Gazêta and Antonio Henrique Almeida de Moraes Neto declare that they have no competing interests.

Additional information

Section Editor: Domenico Otranto.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Andrade Vieira, V.M., Martiniano, N.O.M., da Silva, P.P. et al. Molecular characterization of canine filarioids in a previously non-endemic area of Rio de Janeiro State, Brazil. Parasitol Res 121, 925–932 (2022). https://doi.org/10.1007/s00436-022-07433-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-022-07433-7

Keywords

Navigation