Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T13:03:30.898Z Has data issue: false hasContentIssue false

Visceral leishmaniasis in a recent transmission region: 27.4% infectivity rate among seronegative dogs

Published online by Cambridge University Press:  26 January 2022

Carolina Novato Gondim*
Affiliation:
Department of Health Sciences, Faculty of Health Sciences, Federal University of Lavras, Lavras, Minas Gerais, Brazil
Sidney de Almeida Ferreira
Affiliation:
Department of Health Sciences, Faculty of Health Sciences, Federal University of Lavras, Lavras, Minas Gerais, Brazil
Beatriz Ketelin Sousa Vasconcelos
Affiliation:
Department of Veterinary Medicine, Faculty of Zootechnics and Veterinary Medicine, Federal University of Lavras, Lavras, Minas Gerais, Brazil
Flademir Wouters
Affiliation:
Department of Veterinary Medicine, Faculty of Zootechnics and Veterinary Medicine, Federal University of Lavras, Lavras, Minas Gerais, Brazil
Ricardo Toshio Fujiwara
Affiliation:
Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
Joseane Camilla de Castro
Affiliation:
Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
Joziana Muniz de Paiva Barçante
Affiliation:
Department of Health Sciences, Faculty of Health Sciences, Federal University of Lavras, Lavras, Minas Gerais, Brazil
*
Author for correspondence: Carolina Novato Gondim, E-mail: carolina.gondim@ufla.br

Abstract

American visceral leishmaniasis (VL) is a parasitic disease whose main domestic reservoir in the urban environment is dog and is considered one of the most important zoonoses in the context of public health. Serological tests are typically used for the diagnostic screening of the disease. This study aimed to analyse the performance of different methodologies used in the diagnosis of VL in dogs sampled from a recent transmission area. The sample consisted of 52 dogs separated into groups based on the absence and presence of clinical signs of VL. The following serological techniques were carried out: the DPP® rapid test (RT), the ALERE® RT and an RT and immunoenzymatic assay with a recently developed protein (rKDDR-plus). In addition, molecular techniques were carried out with conjunctival swabs, and bone marrow aspirate samples and parasitological samples were obtained directly from bone marrow aspirates. It was concluded that 27.4% of seronegative dogs were infected, but the serological tests, used as screening tests, showed unsatisfactory sensitivity results (average: 51.2%) for dogs without clinical signs. It was suggested that polymerase chain reaction with conjunctival swabbing be used as a screening test for dogs without clinical signs, as this is a non-invasive collection technique with high-sensitivity values.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Borja, LS, Coelho, LB, De Jesus, MS, De Queiroz, ATL, Celedon, PAF, Zachin, NIT, Silva, ED, Ferreira, AGP, Krieger, MA, Veras, PST and Fraga, DBM (2018) High accuracy of an ELISA test based in a flagela antigen of Leishmania in serodiagnosis of canine visceral leishmaniasis with potential to improve the control measures in Brazil – a phase II study. PLoS Neglected Tropical Diseases 12, e0006871.CrossRefGoogle Scholar
Brazil (2014) Ministry of Health. Secretariat of Health Surveillance. Department of Epidemiological Surveillance. Manual for surveillance and control of visceral leishmaniasis. 1 ed., 5. Reprint – Brasília: Ministry of Health, 120 p.Google Scholar
Brazil (2016a) Ministry of Health. Oswaldo Cruz Foundation. TR DPP® Canine Visceral Leishmaniasis: User manual and technical guidelines. Bio-Manguinhos, Rio de Janeiro.Google Scholar
Brazil (2016b) Ministry of Health. Health Surveillance Secretariat. General Coordination for the Development of Epidemiology in Services. Health Surveillance Guide, 1. Updated edition. – Brasília: Ministry of Health, 773 p. Retrieved from Ministry of Health website http://portalarquivos.saude.gov.br/images/pdf/2016/novembro/18/Guia-LV-2016.pdf (accessed 24 February 2019).Google Scholar
Cardoso, MS, Bento, GA, De Almeida, LV, De Castro, JC, Reis-Cunha, JL, Barbosa, VA, De Souza, CF, Brasil, RP, Valdivia, HO and Bartholomeu, DC (2019) Detection of multiple circulating Leishmania species in Lutzomyia longipalpis in the city of Governador Valadares, southeastern Brazil. PLoS One 14, e0211831.CrossRefGoogle ScholarPubMed
Coura-Vital, W, Ker, HG, Roatt, BM, Aguiar-Soares, RDO, Leal, GGA, Moreira, ND, Oliveira, LAM, Machado, EMM, Maria Morais, MHF, Corrêa-Oliveira, R, Carneiro, M and Reis, AB (2014) Evaluation of change in canine diagnosis protocol adopted by the visceral leishmaniasis control program in Brazil and a new protocol for diagnosis. PLoS One 9, e91009.CrossRefGoogle Scholar
Courtenay, O, Quinnell, RJ, Garcez, LM, Shaw, JJ and Dye, C (2002) Infectiousness in a cohort of Brazilian dogs: why culling fails to control visceral leishmaniasis in areas of high transmission. The Journal of Infectious Diseases 186, 13141320.CrossRefGoogle Scholar
Courtenay, O, Carson, C, Calvo-Bado, L, Garcez, LM and Quinnell, RJ (2014) Heterogeneities in Leishmania infantum infection: using skin parasite burdens to identify highly infectious dogs. PLoS Neglected Tropical Diseases 8, e2583.CrossRefGoogle ScholarPubMed
Dantas-Torres, F (2007) The role of dogs as reservoirs of Leishmania parasites with emphasis on Leishmania (Leishmania) infantum and Leishmania (Viannia) braziliensis. Veterinary Parasitology 149, 139146.CrossRefGoogle ScholarPubMed
Dhom-Lemos, L, Viana, AG, Cunha, JLR, Cardoso, MS, Mendes, TAO, Pinheiro, GRG, Siqueira, WF, Lobo, FP, Teles, LF, Bueno, LL, Guimarães-Carvalho, SF, Bartholomeu, DC and Fujiwara, RT (2019) Leishmania infantum recombinant kinesin degenerated derived repeat (rKDDR): a novel potential antigen for serodiagnosis of visceral leishmaniasis. PLoS One 14, e0211719.CrossRefGoogle ScholarPubMed
Ferreira, AS, Leite, RS, Ituassu, LT, Almeida, GG, Souza, DM, Fujiwara, RT, De Andrade, ASR and Melo, MN (2012) Canine skin and conjunctival swab samples for the detection and quantification of Leishmania infantum DNA in an endemic urban area in Brazil. PLoS Neglected Tropical Diseases 6, e1596.CrossRefGoogle Scholar
Franco, LJ and Passos, ADC (2005) Fundamentals of Epidemiology. Barueri, SP, Brazil: Publisher Manole, pp. 151164.Google Scholar
Grimaldi, GJ, Teva, A, Ferreira, AL, Santos, CB, Pinto, IS, Azevedo, CT and Falqueto, A (2012) Evaluation of a novel chromatographic immunoassay based on Dual-Path Platform technology (DPP® CVL rapid test) for the serodiagnosis of canine visceral leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 106, 5459.CrossRefGoogle ScholarPubMed
Lachaud, L, Marchergui-Hammami, S, Chabbert, E, Dereure, J, Dedet, JP and Bastien, P (2002) Comparison of six PCR methods using peripheral blood for detection of canine visceral leishmaniasis. Journal of Clinical Microbiology 40, 210215.CrossRefGoogle ScholarPubMed
Landis, JR and Koch, GG (1977) The measurement of observer agreement for categorical data. Biometrics 33, 159174.CrossRefGoogle ScholarPubMed
Laurenti, MD, Rossi, CN, Da Matta, VLR, Tomokane, TY, Corbett, CEP, Secundino, NFC, Pimenta, PFP and Marcondes, M (2013) Asymptomatic dogs are highly competent to transmit Leishmania (Leishmania) infantum/chagasi to the natural vector. Veterinary Parasitology 196, 296300.CrossRefGoogle Scholar
Laurenti, MD, Santana Leandro, MV, Tomokane, TY, De Lucca, HRL, Aschar, M, Souza, CSF, Silva, RM, Marcondes, M and Da Matta, VLR (2014) Comparative evaluation of the DPP® CVL rapid test for canine serodiagnosis in area of visceral leishmaniasis. Veterinary Parasitology 205, 444450.CrossRefGoogle ScholarPubMed
Lavras (2019) City Hall. Environmental and epidemiological surveillance. Canine Visceral Leishmaniasis Surveys.Google Scholar
Lombardo, G, Pennisi, MG, Lupo, T, Migliazzo, A, Caprì, A and Solano-Gallego, L (2012) Detection of Leishmania infantum DNA by real-time PCR in canine oral and conjunctival swabs and comparison with other diagnostic techniques. Veterinary Parasitology 184, 1017.CrossRefGoogle ScholarPubMed
Lopes, EG, Sevá, AP, Ferreira, F, Nunes, CM, Keid, LB, Hiramoto, RM, Ferreira, HL, Oliveira, TMFS, Bigotto, MFD, Galvis-Ovallos, F, Galati, EAB and Soares, RM (2017) Serological and molecular diagnostic tests for canine visceral leishmaniasis in Brazilian endemic area: one out of five seronegative dogs are infected. Epidemiology and Infection 145, 24362444.CrossRefGoogle ScholarPubMed
Lukes, J, Mauricio, IL, Schönian, G, Dujardin, JC, Soteriadou, K, Dedet, JP, Kuhls, K, Tintaya, KWQ, Jirku, M, Chocholová, E, Haralambous, C, Pratlong, F, Oborník, M, Horák, A, Ayala, FJ and Miles, MA (2007) Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proceedings of the National Academy of Sciences of the USA 104, 93759380.CrossRefGoogle ScholarPubMed
Moreno, J and Alvar, J (2002) Canine leishmaniasis: epidemiological risk and the experimental model. Trends in Parasitology 8, 399495.CrossRefGoogle Scholar
Peixoto, HM, De Oliveira, MRF and Romero, GAS (2015) Serological diagnosis of canine visceral leishmaniasis in Brazil: systematic review and meta-analysis. Tropical Medicine and International Health 20, 334352.CrossRefGoogle ScholarPubMed
Quaresma, PFS, Murta, SMF, Ferreira, EC, Da Rocha-Lima, ACVM, Xavier, AAP and Gontijo, CMF (2009) Molecular diagnosis of canine visceral leishmaniasis: identification of Leishmania species by PCR-RFLP and quantification of parasite DNA by real-time PCR. Acta Tropica 111, 289294.CrossRefGoogle ScholarPubMed
Quinnell, RJ, Courtenay, O, Davidson, S, Garcez, L, Lambson, B, Ramos, P, Shaw, JJ, Shaw, MA and Dye, C (2001) Detection of Leishmania infantum by PCR, serology and immune response in a cohort study of Brazilian dogs. Parasitology 122, 253261.CrossRefGoogle Scholar
Ribeiro, RR, Michalick, MSM, Da Silva, ME, Dos Santos, CCP, Frézard, FJG and Da Silva, SM (2018) Canine leishmaniasis: an overview of the current status and strategies for control. BioMed Research International 2018, 112.CrossRefGoogle ScholarPubMed
Siqueira, WF, Viana, AG, Reis Cunha, JL, Rosa, LM, Bueno, LL, Bartholomeu, DC, Cardoso, MS and Fujiwara, RT (2021) The increased presence of repetitive motifs in the KDDR-plus recombinant protein, a kinesin-derived antigen from Leishmania infantum, improves the diagnostic performance of serological tests for human and canine visceral leishmaniasis. PLoS Neglected Tropical Diseases 15, e0009759.CrossRefGoogle ScholarPubMed
Solano-Gallego, L, Morell, P, Arboix, M, Alberola, J and Ferrer, L (2001) Prevalence of Leishmania infantum infection in dogs living in an area of canine leishmaniasis endemicity using PCR on several tissues and serology. Journal of Clinical Microbiology 39, 560563.CrossRefGoogle Scholar
Souza Filho, JA, Barbosa, JR, Figueiredo, FB, Mendes, AAV, Da Silva, SR, Coelho, GLLM and Marcelino, AP (2016) Performance of ALERE™ immunochromathographic test for the diagnosis of canine visceral leishmaniasis, Veterinary Parasitology 225, 114116, ISSN 0304-4017.CrossRefGoogle Scholar
Teixeira, AIP, Silva, DM, Vital, T, Nitz, N, De Carvalho, BC, Hecht, M, Oliveira, D, Oliveira, E, Rabello, A and Romero, GAS (2019) Improving the reference standard for the diagnosis of canine visceral leishmaniasis: a challenge for current and future tests. Memórias do Instituto Oswaldo Cruz 114, e180452, 1–9.CrossRefGoogle Scholar
Tolezano, JE, Uliana, SRB, Taniguchi, HH, Araújo, MFL, Barbosa, JAR, Barbosa, JER, Floeter-Winter, LM and Shaw, JJ (2007) The first records of Leishmania (Leishmania) amazonensis in dogs (Canis familiaris) diagnosed clinically as having canine visceral leishmaniasis from Araçatuba county, São Paulo state Brazil. Veterinary Parasitology 149, 280284.CrossRefGoogle ScholarPubMed
World Health Organization (2018) Leishmaniasis. Updated on: 14/03/18. Retrieved from website http://www.who.int/es/news-room/fact-sheets/detail/leishmaniasis (accessed 07 July 2018).CrossRefGoogle Scholar