Urine-Based Molecular Diagnostic Tests for Leishmaniasis Infection in Human and Canine Populations: A Meta-Analysis
Abstract
:1. Introduction
2. Results
2.1. Studies’ Characteristics
2.2. Analysis of Diagnostic Performance
3. Discussion
4. Materials and Methods
4.1. Literature Search Strategy
4.2. Study Selection Criteria
4.3. Data Extraction
4.4. Data Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Alvar, J.; Vélez, I.D.; Bern, C.; Herrero, M.; Desjeux, P.; Cano, J.; Jannin, J.; den Boer, M. Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 2012, 7, e35671. [Google Scholar] [CrossRef]
- Akhoundi, M.; Downing, T.; Votýpka, J.; Kuhls, K.; Lukeš, J.; Cannet, A.; Ravel, C.; Marty, P.; Delaunay, P.; Kasbari, M.; et al. Leishmania infections: Molecular targets and diagnosis. Mol. Asp. Med. 2017, 57, 1–29. [Google Scholar] [CrossRef] [PubMed]
- Burza, S.; Croft, S.L.; Boelaert, M. Leishmaniasis. Lancet 2018, 392, 951–970. [Google Scholar] [CrossRef]
- Akhoundi, M.; Kuhls, K.; Cannet, A.; Votýpka, J.; Marty, P.; Delaunay, P.; Sereno, D. A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies. PLoS Negl. Trop. Dis. 2016, 10, e0004349. [Google Scholar] [CrossRef] [PubMed]
- WHO, Facts Sheets, Leishmaniasis. Available online: https://www.who.int/news-room/fact-sheets/detail/leishmaniasis (accessed on 18 January 2021).
- Braliou, G.G.; Kontou, P.I.; Boleti, H.; Bagos, P.G. Susceptibility to leishmaniasis is affected by host SLC11A1 gene polymorphisms: A systematic review and meta-analysis. Parasitol. Res. 2019, 118, 2329–2342. [Google Scholar] [CrossRef] [PubMed]
- Gumy, A.; Louis, J.A.; Launois, P. The murine model of infection with Leishmania major and its importance for the deciphering of mechanisms underlying differences in Th cell differentiation in mice from different genetic backgrounds. Int J. Parasitol. 2004, 34, 433–444. [Google Scholar] [CrossRef] [PubMed]
- Roatt, B.M.; de Oliveira Cardoso, J.M.; De Brito, R.C.F.; Coura-Vital, W.; de Oliveira Aguiar-Soares, R.D.; Reis, A.B. Recent advances and new strategies on leishmaniasis treatment. Appl. Microbiol. Biotechnol. 2020, 104, 8965–8977. [Google Scholar] [CrossRef] [PubMed]
- Bezerra, G.S.N.; Barbosa, W.L.J.; Silva, E.D.D.; Leal, N.C.; Medeiros, Z.M. Urine as a promising sample for Leishmania DNA extraction in the diagnosis of visceral leishmaniasis—A review. Braz. J. Infect. Dis. 2019, 23, 111–120. [Google Scholar] [CrossRef] [PubMed]
- de Vries, H.J.; Reedijk, S.H.; Schallig, H.D. Cutaneous leishmaniasis: Recent developments in diagnosis and management. Am. J. Clin. Dermatol. 2015, 16, 99–109. [Google Scholar] [CrossRef] [Green Version]
- Adel, A.; Berkvens, D.; Abatih, E.; Soukehal, A.; Bianchini, J.; Saegerman, C. Evaluation of Immunofluorescence Antibody Test Used for the Diagnosis of Canine Leishmaniasis in the Mediterranean Basin: A Systematic Review and Meta-Analysis. PLoS ONE 2016, 11, e0161051. [Google Scholar] [CrossRef]
- Islam, M.Z.; Itoh, M.; Mirza, R.; Ahmed, I.; Ekram, A.R.; Sarder, A.H.; Shamsuzzaman, S.M.; Hashiguchi, Y.; Kimura, E. Direct agglutination test with urine samples for the diagnosis of visceral leishmaniasis. Am. J. Trop. Med. Hyg. 2004, 70, 78–82. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Islam, M.Z.; Itoh, M.; Takagi, H.; Islam, A.U.; Ekram, A.R.; Rahman, A.; Takesue, A.; Hashiguchi, Y.; Kimura, E. Enzyme-linked immunosorbent assay to detect urinary antibody against recombinant rKRP42 antigen made from Leishmania donovani for the diagnosis of visceral leishmaniasis. Am. J. Trop. Med. Hyg. 2008, 79, 599–604. [Google Scholar] [CrossRef] [PubMed]
- Ghatei, M.A.; Hatam, G.R.; Hossini, M.H.; Sarkari, B. Performance of latex agglutination test (KAtex) in diagnosis of visceral leishmaniasis in Iran. Iran. J. Immunol. 2009, 6, 202–207. [Google Scholar]
- Ejazi, S.A.; Bhattacharya, P.; Bakhteyar, M.A.; Mumtaz, A.A.; Pandey, K.; Das, V.N.; Das, P.; Rahaman, M.; Goswami, R.P.; Ali, N. Noninvasive Diagnosis of Visceral Leishmaniasis: Development and Evaluation of Two Urine-Based Immunoassays for Detection of Leishmania donovani Infection in India. PLoS Negl. Trop. Dis. 2016, 10, e0005035. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Asfaram, S.; Hosseini Teshnizi, S.; Fakhar, M.; Banimostafavi, E.S.; Soosaraei, M. Is urine a reliable clinical sample for the diagnosis of human visceral leishmaniasis? A systematic review and meta-analysis. Parasitol. Int. 2018, 67, 575–583. [Google Scholar] [CrossRef] [PubMed]
- Sakkas, H.; Gartzonika, C.; Levidiotou, S. Laboratory diagnosis of human visceral leishmaniasis. J. Vector Borne Dis. 2016, 53, 8–16. [Google Scholar]
- Pessoa, E.S.R.; Mendonça Trajano-Silva, L.A.; Lopes da Silva, M.A.; da Cunha Gonçalves-de-Albuquerque, S.; de Goes, T.C.; Silva de Morais, R.C.; Lopes de Melo, F.; de Paiva-Cavalcanti, M. Evaluation of urine for Leishmania infantum DNA detection by real-time quantitative PCR. J. Microbiol. Methods 2016, 131, 34–41. [Google Scholar] [CrossRef]
- Ferreira Sde, A.; Almeida, G.G.; Silva Sde, O.; Vogas, G.P.; Fujiwara, R.T.; de Andrade, A.S.; Melo, M.N. Nasal, oral and ear swabs for canine visceral leishmaniasis diagnosis: New practical approaches for detection of Leishmania infantum DNA. PLoS Negl. Trop. Dis. 2013, 7, e2150. [Google Scholar] [CrossRef] [Green Version]
- Sambrook, J.; Fritsch, E.F.; Maniatis, T. Molecular Cloning: A Laboratory Manual; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 1989. [Google Scholar]
- Mirzaei, A.; Ahmadipour, F.; Cannet, A.; Marty, P.; Delaunay, P.; Perrin, P.; Dorkeld, F.; Sereno, D.; Akhoundi, M. Immunodetection and molecular determination of visceral and cutaneous Leishmania infection using patients’ urine. Infect. Genet. Evol. 2018, 63, 257–268. [Google Scholar] [CrossRef]
- da Costa Lima, M.S.J.; Hartkopf, A.C.L.; de Souza Tsujisaki, R.A.; Oshiro, E.T.; Shapiro, J.T.; de Fatima Cepa Matos, M.; Cavalheiros Dorval, M.E. Isolation and molecular characterization of Leishmania infantum in urine from patients with visceral leishmaniasis in Brazil. Acta Trop. 2018, 178, 248–251. [Google Scholar] [CrossRef] [Green Version]
- Silva, M.A.; Medeiros, Z.; Soares, C.R.; Silva, E.D.; Miranda-Filho, D.B.; Melo, F.L. A comparison of four DNA extraction protocols for the analysis of urine from patients with visceral leishmaniasis. Rev. Soc. Bras. Med. Trop. 2014, 47, 193–197. [Google Scholar] [CrossRef]
- Hernández, L.; Montoya, A.; Checa, R.; Dado, D.; Gálvez, R.; Otranto, D.; Latrofa, M.S.; Baneth, G.; Miró, G. Course of experimental infection of canine leishmaniosis: Follow-up and utility of noninvasive diagnostic techniques. Vet. Parasitol. 2015, 207, 149–155. [Google Scholar] [CrossRef]
- Phumee, A.; Kraivichian, K.; Chusri, S.; Noppakun, N.; Vibhagool, A.; Sanprasert, V.; Tampanya, V.; Wilde, H.; Siriyasatien, P. Detection of Leishmania siamensis DNA in saliva by polymerase chain reaction. Am. J. Trop Med. Hyg 2013, 89, 899–905. [Google Scholar] [CrossRef] [Green Version]
- Veland, N.; Espinosa, D.; Valencia, B.M.; Ramos, A.P.; Calderon, F.; Arevalo, J.; Low, D.E.; Llanos-Cuentas, A.; Boggild, A.K. Polymerase chain reaction detection of Leishmania kDNA from the urine of Peruvian patients with cutaneous and mucocutaneous leishmaniasis. Am. J. Trop. Med. Hyg. 2011, 84, 556–561. [Google Scholar] [CrossRef] [Green Version]
- Fisa, R.; Riera, C.; López-Chejade, P.; Molina, I.; Gállego, M.; Falcó, V.; Ribera, E.; Portús, M. Leishmania infantum DNA detection in urine from patients with visceral leishmaniasis and after treatment control. Am. J. Trop. Med. Hyg. 2008, 78, 741–744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Motazedian, M.; Fakhar, M.; Motazedian, M.H.; Hatam, G.; Mikaeili, F. A urine-based polymerase chain reaction method for the diagnosis of visceral leishmaniasis in immunocompetent patients. Diagn. Microbiol. Infect. Dis. 2008, 60, 151–154. [Google Scholar] [CrossRef]
- Manna, L.; Reale, S.; Picillo, E.; Vitale, F.; Gravino, A.E. Urine sampling for real-time polymerase chain reaction based diagnosis of canine leishmaniasis. J. Vet. Diagn. Investig. 2008, 20, 64–67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Solano-Gallego, L.; Rodriguez-Cortes, A.; Trotta, M.; Zampieron, C.; Razia, L.; Furlanello, T.; Caldin, M.; Roura, X.; Alberola, J. Detection of Leishmania infantum DNA by fret-based real-time PCR in urine from dogs with natural clinical leishmaniosis. Vet. Parasitol. 2007, 147, 315–319. [Google Scholar] [CrossRef]
- Franceschi, A.; Merildi, V.; Guidi, G.; Mancianti, F. Occurrence of Leishmania DNA in urines of dogs naturally infected with leishmaniasis. Vet. Res. Commun. 2007, 31, 335–341. [Google Scholar] [CrossRef] [PubMed]
- Oliveira, M.J.; Silva Júnior, G.B.; Abreu, K.L.; Rocha, N.A.; Garcia, A.V.; Franco, L.F.; Mota, R.M.; Libório, A.B.; Daher, E.F. Risk factors for acute kidney injury in visceral leishmaniasis (Kala-Azar). Am. J. Trop. Med. Hyg. 2010, 82, 449–453. [Google Scholar] [CrossRef] [Green Version]
- Pace, D. Leishmaniasis. J. Infect. 2014, 69 (Suppl. 1), S10–S18. [Google Scholar] [CrossRef] [PubMed]
- Ortalli, M.; Lorrai, D.; Gaibani, P.; Rossini, G.; Vocale, C.; Re, M.C.; Varani, S. Serodiagnosis of Visceral Leishmaniasis in Northeastern Italy: Evaluation of Seven Serological Tests. Microorganisms 2020, 8, 1847. [Google Scholar] [CrossRef]
- Su, Y.H.; Wang, M.; Brenner, D.E.; Ng, A.; Melkonyan, H.; Umansky, S.; Syngal, S.; Block, T.M. Human urine contains small, 150 to 250 nucleotide-sized, soluble DNA derived from the circulation and may be useful in the detection of colorectal cancer. J. Mol. Diagn. 2004, 6, 101–107. [Google Scholar] [CrossRef] [Green Version]
- Bergallo, M.; Costa, C.; Gribaudo, G.; Tarallo, S.; Baro, S.; Negro Ponzi, A.; Cavallo, R. Evaluation of six methods for extraction and purification of viral DNA from urine and serum samples. New Microbiol. 2006, 29, 111–119. [Google Scholar]
- Brinkman, J.A.; Rahmani, M.Z.; Jones, W.E.; Chaturvedi, A.K.; Hagensee, M.E. Optimization of PCR based detection of human papillomavirus DNA from urine specimens. J. Clin. Virol. 2004, 29, 230–240. [Google Scholar] [CrossRef]
- Augustus, E.; Van Casteren, K.; Sorber, L.; van Dam, P.; Roeyen, G.; Peeters, M.; Vorsters, A.; Wouters, A.; Raskin, J.; Rolfo, C.; et al. The art of obtaining a high yield of cell-free DNA from urine. PLoS ONE 2020, 15, e0231058. [Google Scholar] [CrossRef] [Green Version]
- Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 2009, 6, e1000097. [Google Scholar] [CrossRef] [Green Version]
- Forero, D.A.; Lopez-Leon, S.; González-Giraldo, Y.; Bagos, P.G. Ten simple rules for carrying out and writing meta-analyses. PLoS Comput. Biol. 2019, 15, e1006922. [Google Scholar] [CrossRef]
- Hopewell, S.; McDonald, S.; Clarke, M.; Egger, M. Grey literature in meta-analyses of randomized trials of health care interventions. Cochrane Database Syst. Rev. 2007. [Google Scholar] [CrossRef]
- Stroup, D.F.; Berlin, J.A.; Morton, S.C.; Olkin, I.; Williamson, G.D.; Rennie, D.; Moher, D.; Becker, B.J.; Sipe, T.A.; Thacker, S.B. Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000, 283, 2008–2012. [Google Scholar] [CrossRef]
- Pan, Z.; Trikalinos, T.A.; Kavvoura, F.K.; Lau, J.; Ioannidis, J.P. Local literature bias in genetic epidemiology: An empirical evaluation of the Chinese literature. PLoS Med. 2005, 2, e334. [Google Scholar] [CrossRef]
- Whiting, P.F.; Rutjes, A.W.; Westwood, M.E.; Mallett, S.; Deeks, J.J.; Reitsma, J.B.; Leeflang, M.M.; Sterne, J.A.; Bossuyt, P.M. QUADAS-2: A revised tool for the quality assessment of diagnostic accuracy studies. Ann. Intern. Med. 2011, 155, 529–536. [Google Scholar] [CrossRef]
- Van Houwelingen, H.C.; Zwinderman, K.H.; Stijnen, T. A bivariate approach to meta-analysis. Stat. Med. 1993, 12, 2273–2284. [Google Scholar] [CrossRef]
- Arends, L.R.; Hamza, T.H.; van Houwelingen, J.C.; Heijenbrok-Kal, M.H.; Hunink, M.G.; Stijnen, T. Bivariate random effects meta-analysis of ROC curves. Med. Decis. Mak. 2008, 28, 621–638. [Google Scholar] [CrossRef]
- Harbord, R.M.; Deeks, J.J.; Egger, M.; Whiting, P.; Sterne, J.A. A unification of models for meta-analysis of diagnostic accuracy studies. Biostatistics 2007, 8, 239–251. [Google Scholar] [CrossRef] [Green Version]
- Rutter, C.M.; Gatsonis, C.A. A hierarchical regression approach to meta-analysis of diagnostic test accuracy evaluations. Stat. Med. 2001, 20, 2865–2884. [Google Scholar] [CrossRef]
- White, I.R. Multivariate Random-effects Meta-regression: Updates to Mvmeta. Stata J. 2011, 11, 255–270. [Google Scholar] [CrossRef] [Green Version]
Author | Year | Country | Species | Comorbidity | Method of PCR | Amplified Locus | Form of Leishmaniasis | Leishmaniasis Ascertainment | DNA Extraction Method | Cases/Controls | Sensitivity | Specificity | TP/FN/TN/FP |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Mirzaei [21] | 2018 | Iran | Human | NA | qPCR | ITS2-region of ribosomal DNA | CL | 1. Blood-PCR 2. Serum-Westrn blot | Kit (QIAamp DNA Mini Kit QIAGEN) | 23/3 | 0.869 | 1 | 20/3/3/0 |
Mirzaei [21] | 2018 | Iran | Human | NA | qPCR | ITS2-region of ribosomal DNA | VL | 1. Blood-PCR 2. Serum-Westrn blot | Kit (QIAamp DNA Mini Kit QIAGEN) | 14/3 | 0.928 | 1 | 13/1/3/0 |
Da Costa Lima Junior [22] | 2018 | Brazil | Human | NA | PCR/ RFLP | ITS1-region of ribosomal DNA | VL | 1. ΒM aspirate, PB-PCR 2. Culture from LN, BM, spleen aspirates -Parasite counts 3.BM–Ab test ELISA, rk39-ICT | Phenol-chloroform | 30/50 | 0.366 | 1 | 11/9/50/0 |
Pessoa-E-Silva [18] | 2016 | Brazil | Human | AIDS | qPCR | L. infantum kDNA minicircle | VL | 1.Blood–qPCR 2. Blood, oral fluid-Ab test rK39–ICT | Kit (QIAamp DNA Mini Kit -QIAGEN RW Germany) | 8/50 | 0.500 | 1 | 4/4/10/0 |
Almerice Lopes da Silva [23] | 2014 | Brazil | Human | NA | PCR | L. infantum kDNA minicircle | VL | 1. BM, PB-PCR | Phenol–chloroform | 11/NA | 0.727 | NA | 8/3/-/- |
Hernández [24] | 2014 | Spain | Canine | NA | qPCR | L. infantum kDNA minicircle | CL | 1. BM, PB-Nested PCR, qPCR 2. Cultures from skin lesions, spleen, liver, BM, LN aspirates—Parasite counts 4. Serum–Ab test IFAT, ELISA | Kit (e QuiAamp DNA Micro kit QIAGEN) | 8/NA | 0.750 | NA | 6/2/-/- |
Phumee [25] | 2013 | Thailand | Human | HIV/DMII | PCR | ITS1- gene of L. siamensis | CL | 1. BM, blood, buffy coat tissue, saliva-PCR 2. Culture from blood, skin biopsy, BM-Parasite counts | Kit (Invisorb Spin Tissue Mini Kit) | 5/4 | 0.600 | 1 | 3/2/4/0 |
Veland [26] | 2011 | Per-u | Human | NA | PCR/RFLP | L. Viannia kDNA minicircle | CL | 1. Skin scraping aspirate-PCR 2. Culture from skin lesions-Parasite counts | Phenol–chloroform | 86/22 | 0.210 | 1 | 18/68/22/0 |
Fisa [27] | 2008 | Spain | Human | AIDS in controls | Nested PCR | L. infantum genomic DNA | VL | 1. Blood-PCR 2. Blood-ADU by KAtex 3. Culture from BM aspirates-Parasite counts | Kit (High Pure PCR Template Roche Molecular Biochemicals, Mannheim, Germany) | 28/59 | 0.882 | 1 | 15/2/59/0 |
Motazedian [28] | 2008 | Iran | Human | NA | PCR | L. infantum kDNA minicircle | VL | 1. BM, LN, spleen, PB, serum aspirates-PCR 2. Culture from LN, BM, spleen aspirate—Parasite counts | Phenol–chloroform | 30/30 | 0.660 | 1 | 29/1/30/0 |
Manna [29] | 2008 | Italy | Canine | NA | qPCR | L. infantum, kDNA minicircle | CL | 1. Serum–Antibodies test IFAT 2. LN aspirate–PCR | Kit (QIAamp blood QIAGEN Santa Ciarita, CA) | 41/3 | 1.00 | 1 | 41/0/3/0 |
Solano-Gallego [30] | 2007 | Spain | Canine | NA | qPCR | L. infantum kDNA minicircle | VL | 1. PB, BM, LN-PCR 2. Spleen aspirate, LN-Westrn blot, ELISA | Kit (High Pure PCR Templat Roche Applied Science) | 43/10 | 0.465 | 1 | 20/23/10/0 |
Franceschi [31] | 2007 | Italy | Canine | NA | PCR | L. infantum kDNA minicircle | VL | 1. LN-IFAT 2. LN-Parasite counts 3. Clinical signs | Kit (Accuprep Genomic DNA Extraction Kit Bioneer Korea) | 40/NA | 0.250 | NA | 10/30/-/- |
DNA Extraction Method | Nucleic Acid Test | Locus Amplified | Studies/Patients/Controls | Sensitivity (95% CI) | Specificity (95% CI) |
---|---|---|---|---|---|
kit/phenol | qPCR/PCR | genomic/L.in-kmini | 13/367/234 | 0.692 (0.501, 0.883) | 1 (0.927, 1.000) |
kit/phenol | PCR | genomic/L.in-kmini | 7/230/165 | 0.574 (0.326, 0.822) | 1 (0.956, 1.000) |
kit/phenol | qPCR | genomic/L.in-kmini | 6/137/69 | 0.793 (0.592, 0.993) | 1 (0.816, 1.000) |
kit | qPCR/PCR | genomic/L.in-kmini | 9/210/132 | 0.728 (0.535, 0.917) | 1 (0.880, 1.000) |
phenol | qPCR/PCR | genomic/L.in-kmini | 4/157/102 | 0.585 (0.234, 0.936) | 1 (0.961, 1.000) |
kit | PCR | genomic/L.in-kmini | 3/73/63 | 0.588 (0.0816, 1.000) | 1 (0.843, 1.000) |
phenol | PCR | genomic/L.in-kmini | 4/157/102 | 0.585 (0.234, 0.936) | 1 (0.961, 1.000) |
kit | qPCR | genomic/L.in-kmini | 6/137/69 | 0.793 (0.592, 0.993) | 1 (0.816, 1.000) |
kit/phenol | qPCR/PCR | genomic | 6/186/141 | 0.671 (0.379, 0.963) | 1 (0.920, 1.000) |
kit/phenol | qPCR/PCR | L.in-kmini | 7/181/93 | 0.699 (0.473, 0.925) | 1 (0.896, 1.000) |
kit | qPCR/PCR | genomic | 4/70/69 | 0.851 (0.746, 0.956) | 1 (0.861, 1.000) |
kit | qPCR/PCR | L.in-kmini | 5/140/63 | 0.589 (0.311, 0.866) | 1 (0.847, 1.000) |
kit | qPCR/PCR | genomic/L.in-kmini | 9/210/132 | 0.726 (0.535, 0.917) | 1 (0.880, 1.000) |
phenol | PCR | genomic/L.in-kmini | 4/157/102 | 0.585 (0.234, 0.936) | 1 (0.961, 1.000) |
phenol | PCR | genomic | 2/116/72 | 0.273 (0.111, 0.435) | 1 (0.957, 1.000) |
kit | qPCR | genomic | 2/37/6 | 0.888 (0.785, 0.992) | 1 (0.646, 1.000) |
kit | qPCR | L.in-kmini | 4/100/63 | 0.710 (0.417, 1.000) | 1 (0.832, 1.000) |
Form of Leishmaniasis | Species | Geographical Region | Studies/Patients/Controls | Sensitivity (95% CI) | Specificity (95% CI) |
---|---|---|---|---|---|
VL | human/canine | all regions | 8/204/202 | 0.649 (0.449, 0.849) | 1 (0.945, 1.000) |
CL | human/canine | all regions | 5/163/32 | 0.751 (0.386, 1.000) | 1 (0.856, 1.000 |
VL/CL | human | all regions | 9/235/221 | 0.712 (0.489, 0.934) | 1 (0.933, 0.999) |
VL/CL | canine | all regions | 4/132/13 | 0.631 (0.296, 0.967) | 1 (0.814, 1.000) |
VL/CL | human/canine | Europe–Middle East | 8/227/108 | 0.817 (0.639, 0.995) | 1 (0.904, 1.000) |
VL/CL | human/canine | Non-Europe–Middle East | 5/140/126 | 0.437 (0.220, 0.653) | 1 (0.923, 1.000) |
VL | human | all regions | 6/121/192 | 0.775 (0.557, 0.994) | 1 (0.948, 1.000) |
CL | human | all regions | 3/114/29 | 0.573 (0.007, 1.000) | 1 (0.823, 1.000) |
VL | human/canine | Europe–Middle East | 5/155/102 | 0.748 (0.479, 1.000) | 1 (0.926, 1.000) |
VL | human/canine | Non-Europe–Middle East | 3/49/100 | 0.514 (0.260, 0.768) | 1 (0.931, 1.000) |
CL | human/canine | Europe–Middle East | 3/72/6 | 0.889 (0.748, 1.000) | 1 (0.646, 1.000) |
CL | human/canine | Non-Europe–Middle East | 2/91/26 | 0.352 (0.068, 0.772) | 1 (0.856, 1.000) |
VL/CL | human | Europe–Middle East | 4/95/95 | 0.906 (0.838, 0.975) | 1 (0.911, 1.000) |
VL/CL | human | Non-Europe–Middle East | 5/146/126 | 0.437 (0.220, 0.653) | 1 (0.923, 1.000) |
VL/CL | canine | Europe–Middle East | 4/132/13 | 0.631 (0.296, 0.967) | 1 (0.814, 1.000) |
VL | human | Europe–Middle East | 3/72/92 | 0.923 (0.854, 0.997) | 1 (0.935, 1.000) |
VL | human | Non-Europe–Middle East | 3/49/100 | 0.5138 (0.260, 0.768) | 1 (0.931, 1.000) |
CL | human | Non-Europe–Middle East | 2/91/26 | 0.352 (0.068, 0.772) | 1 (0.856, 1.000) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pappa, S.A.; Kontou, P.I.; Bagos, P.G.; Braliou, G.G. Urine-Based Molecular Diagnostic Tests for Leishmaniasis Infection in Human and Canine Populations: A Meta-Analysis. Pathogens 2021, 10, 269. https://doi.org/10.3390/pathogens10030269
Pappa SA, Kontou PI, Bagos PG, Braliou GG. Urine-Based Molecular Diagnostic Tests for Leishmaniasis Infection in Human and Canine Populations: A Meta-Analysis. Pathogens. 2021; 10(3):269. https://doi.org/10.3390/pathogens10030269
Chicago/Turabian StylePappa, Styliani A., Panagiota I. Kontou, Pantelis G. Bagos, and Georgia G. Braliou. 2021. "Urine-Based Molecular Diagnostic Tests for Leishmaniasis Infection in Human and Canine Populations: A Meta-Analysis" Pathogens 10, no. 3: 269. https://doi.org/10.3390/pathogens10030269