Author:
- INTRODUCTION
- MATERIALS AND METHODS
- Sample features.
- Determination of the physicochemical and microbiological characteristics of the organic fertilizers.
- Histoplasma capsulatum culture.
- DNA extraction from H. capsulatum isolates in yeast phase.
- DNA extraction from organic fertilizer, soil, and bird dropping samples using the “FastDNA SPIN Kit for Soil.”
- Hc100 nested PCR assay for H. capsulatum.
- Agarose gel electrophoresis.
- Detection limit of the Hc100 nested PCR.
- Specificity of the Hc100 nested PCR.
- Search for H. capsulatum in organic fertilizers by Hc100 nested PCR.
- Sequencing of the products amplified by Hc100 nested PCR.
- Histoplasma capsulatum recovery in microbiological cultures from fertilizer and organic amendment samples that tested positive in the Hc100 nested PCR.
- Statistical analysis.
- RESULTS
- Standardization of the Hc100 nested PCR assay to assess the presence of H. capsulatum in organic fertilizers.
- Detection limit of H. capsulatum DNA amplified by Hc100 nested PCR.
- Specificity of the Hc100 nested PCR to amplify H. capsulatum DNA.
- Usefulness of the Hc100 nested PCR for the detection of H. capsulatum in soil, organic fertilizers, and poultry depositions.
- Persistence of H. capsulatum in the environment.
- Sequencing of the amplification products obtained by Hc100 nested PCR.
- Recovery of H. capsulatum in culture from Hc100 nested PCR positive samples.
- Correlation of physicochemical and microbiological characteristics of organic fertilizers with the presence of H. capsulatum genetic material by Hc100 nested PCR.
- DISCUSSION
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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1.
Kauffman CA, 2007. Histoplasmosis: a clinical and laboratory update. Clin Microbiol Rev 20: 115–132.
-
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Aidé MA, 2009. Continuing education course—mycoses. Chapter 4: histoplasmosis. J Bras Pneumol 35: 1145–1151.
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Porta A, Eletto A, Török Z, Franceschelli S, Glatz A, Vígh L, Maresca B, 2010. Changes in membrane fluid state and heat shock response cause attenuation of virulence. J Bacteriol 192: 1999–2005.
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4.
Garfoot AL, Rappleye CA, 2016. Histoplasma capsulatum surmounts obstacles to intracellular pathogenesis. FEBS J 283: 619–633.
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5.
Knox KS, Hage CA, 2010. Histoplasmosis. Proc Am Thorac Soc 7: 169–172.
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Gómez BL, 2011. Histoplasmosis: epidemiology in Latin America. Curr Fungal Infect Rep 5: 199–205.
-
7.
Nieto-Ríos JF, Serna-Higuita LM, Guzman-Luna CE, Ocampo-Kohn C, Aristizabal-Alzate A, Ramírez I, Velez-Echeverri C, Vanegas-Ruiz JJ, Zuleta JJ, Zuluaga-Valencia GA, 2014. Histoplasmosis in renal transplant patients in an endemic area at a reference hospital in Medellin, Colombia. Transplant Proc 46: 3004–3009.
-
8.
Emmons CW, 1949. Isolation of Histoplasma capsulatum from soil. Public Health Rep 64: 892–896.
-
9.
Emmons CW, 1950. Histoplasmosis: animal reservoirs and other sources in nature of pathogenic fungus, Histoplasma. Am J Public Health Nations Health 40: 436–440.
-
10.
Emmons CW, 1958. Association of bats with histoplasmosis. Public Health Rep 73: 590–595.
-
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Hoff GL, Bigler WJ, 1981. The role of bats in the propagation and spread of histoplasmosis: a review. J Wildl Dis 17: 191–196.
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Suárez-Alvarez RO, Pérez-Torres A, Taylor ML, 2010. Adherence patterns of Histoplasma capsulatum yeasts to bat tissue sections. Mycopathologia 170: 79–87.
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Stobierski MG, Hospedales CJ, Hall WN, Robinson-Dunn B, Hoch D, Sheill DA, 1996. Outbreak of histoplasmosis among employees in a paper factory–Michigan, 1993. J Clin Microbiol 34: 1220–1223.
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Detection of Histoplasma capsulatum in Organic Fertilizers by Hc100 Nested Polymerase Chain Reaction and Its Correlation with the Physicochemical and Microbiological Characteristics of the Samples
Luisa F. Gómez
Luisa F. Gómez
Medical Mycology Group, Microbiology and Parasitology Department, School of Medicine, Universidad de Antioquia, Medellín, Colombia;
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Isaura P. Torres
Isaura P. Torres
Cellular and Molecular Biology Group, Corporación para Investigaciones Biológicas (CIB), Universidad de Antioquia, Medellín, Colombia;
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María del Pilar Jiménez-A
María del Pilar Jiménez-A
Medical Mycology Group, Microbiology and Parasitology Department, School of Medicine, Universidad de Antioquia, Medellín, Colombia;
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Juan Gmo McEwen
Juan Gmo McEwen
Medical Mycology Group, Microbiology and Parasitology Department, School of Medicine, Universidad de Antioquia, Medellín, Colombia;
Cellular and Molecular Biology Group, Corporación para Investigaciones Biológicas (CIB), Universidad de Antioquia, Medellín, Colombia;
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Cellular and Molecular Biology Group, Corporación para Investigaciones Biológicas (CIB), Universidad de Antioquia, Medellín, Colombia;
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Catalina de Bedout
Catalina de Bedout
Medical and Experimental Mycology Group, Corporación para Investigaciones Biológicas (CIB), Medellín, Colombia;
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Carlos A. Peláez
Carlos A. Peláez
Grupo Interdisciplinario de Estudios Moleculares (GIEM), Institute of Chemistry, School of Exact and Natural Sciences, Universidad de Antioquia, Medellín, Colombia;
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José M. Acevedo
José M. Acevedo
Grupo Interdisciplinario de Estudios Moleculares (GIEM), Institute of Chemistry, School of Exact and Natural Sciences, Universidad de Antioquia, Medellín, Colombia;
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María L. Taylor
María L. Taylor
Fungal Immunology Laboratory, Universidad Nacional Autónoma de México (UNAM), Coyoacan, Mexico City, Mexico
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Myrtha Arango
Myrtha Arango
Medical Mycology Group, Microbiology and Parasitology Department, School of Medicine, Universidad de Antioquia, Medellín, Colombia;
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Histoplasma capsulatum is the causative agent of histoplasmosis and this fungus inhabits soils rich in phosphorus and nitrogen that are enriched with bird and bat manure. The replacement of organic matter in agroecosystems is necessary in the tropics, and the use of organic fertilizers has increased. Cases and outbreaks due to the presence of the fungus in these components have been reported. The Instituto Colombiano Agropecuario resolution 150 of 2003 contains the parameters set by the Colombian Technical Standard (NTC 5167) on the physicochemical and microbiological features of fertilizers, but it does not regulate the search for H. capsulatum. The aim of this study was to demonstrate H. capsulatum presence in organic fertilizers by nested polymerase chain reaction (PCR). A total of 239 samples were collected: 201 (84.1%) corresponded to organic fertilizers, 30 (12.5%) to bird excrement, and 8 (3.4%) to cave soils. The Hc100 nested PCR had a detection limit of 0.1 pg/µL and a specificity of 100%. A total of 25 (10.5%) samples were positive and validated by sequencing. Seven of the positive samples represented locations where H. capsulatum was previously detected, suggesting the persistence of the fungus. No significant correlations were detected between the physicochemical and microbiological parameters with the presence of H. capsulatum by nested PCR, indicating the fungus existence in organic fertilizers that complied with the NTC 5167. The Hc100 nested PCR targeting H. capsulatum standardized in this work will improve the evaluation of organic fertilizers and ensure the prevention of outbreaks and cases due to manufacturing, marketing, and use of fertilizers contaminated with H. capsulatum.
Author Notes
Authors’ addresses: Luisa F. Gómez, Juan G. McEwen, Myrtha Arango and María del Pilar Jiménez-A, Department of Microbiology and parasitology, School of Medicine, Universidad de Antioquia, Medellin, Antioquia, Colombia, E-mails: luisa.gomezl@udea.edu.co, mcewen@une.net.co, and myrthaarango@yahoo.com, and delpilar.jimenez@udea.edu.co. Isaura P. Torres, School of Medicine, Universidad CES, Medellin, Antioquia, Colombia, E-mail: isaurap10@gmail.com. Catalina de Bedout, Medical and Experimental Mycology Group, Corporación para Investigaciones Biológicas (CIB), Medellin, Colombia, E-mail: catybedout@gmail.com. Carlos A Peláez and Jose M Acevedo, Molecular Studies Interdisciplinary Group, Chemistry Institute, Natural and Exact Sciences, Universidad de Antioquia, Medellín, Colombia, E-mails: carlos.pelaez@udea.edu.co and joseacevedor@yahoo.es. María L. Taylor, Fungal Immunology Laboratory, Universidad Nacional Autonoma de Mexico, Coyoacan, Distrito Federal, Mexico, E-mail: luciataylor@yahoo.com.mx.
- INTRODUCTION
- MATERIALS AND METHODS
- Sample features.
- Determination of the physicochemical and microbiological characteristics of the organic fertilizers.
- Histoplasma capsulatum culture.
- DNA extraction from H. capsulatum isolates in yeast phase.
- DNA extraction from organic fertilizer, soil, and bird dropping samples using the “FastDNA SPIN Kit for Soil.”
- Hc100 nested PCR assay for H. capsulatum.
- Agarose gel electrophoresis.
- Detection limit of the Hc100 nested PCR.
- Specificity of the Hc100 nested PCR.
- Search for H. capsulatum in organic fertilizers by Hc100 nested PCR.
- Sequencing of the products amplified by Hc100 nested PCR.
- Histoplasma capsulatum recovery in microbiological cultures from fertilizer and organic amendment samples that tested positive in the Hc100 nested PCR.
- Statistical analysis.
- RESULTS
- Standardization of the Hc100 nested PCR assay to assess the presence of H. capsulatum in organic fertilizers.
- Detection limit of H. capsulatum DNA amplified by Hc100 nested PCR.
- Specificity of the Hc100 nested PCR to amplify H. capsulatum DNA.
- Usefulness of the Hc100 nested PCR for the detection of H. capsulatum in soil, organic fertilizers, and poultry depositions.
- Persistence of H. capsulatum in the environment.
- Sequencing of the amplification products obtained by Hc100 nested PCR.
- Recovery of H. capsulatum in culture from Hc100 nested PCR positive samples.
- Correlation of physicochemical and microbiological characteristics of organic fertilizers with the presence of H. capsulatum genetic material by Hc100 nested PCR.
- DISCUSSION
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Kauffman CA, 2007. Histoplasmosis: a clinical and laboratory update. Clin Microbiol Rev 20: 115–132.
-
2.
Aidé MA, 2009. Continuing education course—mycoses. Chapter 4: histoplasmosis. J Bras Pneumol 35: 1145–1151.
-
3.
Porta A, Eletto A, Török Z, Franceschelli S, Glatz A, Vígh L, Maresca B, 2010. Changes in membrane fluid state and heat shock response cause attenuation of virulence. J Bacteriol 192: 1999–2005.
-
4.
Garfoot AL, Rappleye CA, 2016. Histoplasma capsulatum surmounts obstacles to intracellular pathogenesis. FEBS J 283: 619–633.
-
5.
Knox KS, Hage CA, 2010. Histoplasmosis. Proc Am Thorac Soc 7: 169–172.
-
6.
Gómez BL, 2011. Histoplasmosis: epidemiology in Latin America. Curr Fungal Infect Rep 5: 199–205.
-
7.
Nieto-Ríos JF, Serna-Higuita LM, Guzman-Luna CE, Ocampo-Kohn C, Aristizabal-Alzate A, Ramírez I, Velez-Echeverri C, Vanegas-Ruiz JJ, Zuleta JJ, Zuluaga-Valencia GA, 2014. Histoplasmosis in renal transplant patients in an endemic area at a reference hospital in Medellin, Colombia. Transplant Proc 46: 3004–3009.
-
8.
Emmons CW, 1949. Isolation of Histoplasma capsulatum from soil. Public Health Rep 64: 892–896.
-
9.
Emmons CW, 1950. Histoplasmosis: animal reservoirs and other sources in nature of pathogenic fungus, Histoplasma. Am J Public Health Nations Health 40: 436–440.
-
10.
Emmons CW, 1958. Association of bats with histoplasmosis. Public Health Rep 73: 590–595.
-
11.
Hoff GL, Bigler WJ, 1981. The role of bats in the propagation and spread of histoplasmosis: a review. J Wildl Dis 17: 191–196.
-
12.
Manolakos JJ, Cooray M, Patel A, Haider S, 2013. Bats, fever and adenopathy–what is the link? Can J Infect Dis Med Microbiol 24: 35–37.
-
13.
Suárez-Alvarez RO, Pérez-Torres A, Taylor ML, 2010. Adherence patterns of Histoplasma capsulatum yeasts to bat tissue sections. Mycopathologia 170: 79–87.
-
14.
Stobierski MG, Hospedales CJ, Hall WN, Robinson-Dunn B, Hoch D, Sheill DA, 1996. Outbreak of histoplasmosis among employees in a paper factory–Michigan, 1993. J Clin Microbiol 34: 1220–1223.
-
15.
Lockwood GF, Garrison RG, 1968. The possibel role of uric acid in the ecology of Histoplasma capsulatum. Mycopathol Mycol Appl 35: 377–388.
-
16.
Brandsberg JW, 1968. Fungi found in association with Histoplasma capsulatum in a naturally contaminated site in Clarksburg, Maryland, USA. Sabouraudia 6: 246–254.
-
17.
Huhn GD et al. 2005. Two outbreaks of occupationally acquired histoplasmosis: more than workers at risk. Environ Health Perspect 113: 585–589.
-
18.
Muñoz B, Martínez MA, Palma G, Ramírez A, Frías MG, Reyes MR, Taylor ML, Higuera AL, Corcho A, Manjarrez ME, 2010. Molecular characterization of Histoplasma capsulatum isolated from an outbreak in treasure hunters Histoplasma capsulatum in treasure hunters. BMC Infect Dis 10: 264.
-
19.
Ashford DA, Hajjeh RA, Kelley MF, Kaufman L, Hutwagner L, McNeil MM, 1999. Outbreak of histoplasmosis among cavers attending the National Speleological Society Annual Convention, Texas, 1994. Am J Trop Med Hyg 60: 899–903.
-
20.
Restrepo A, Robledo M, Ospina S, Restrepo M, Correa A, 1968. Distribution of paracoccidioidin sensitivity in Colombia. Am J Trop Med Hyg 17: 25–37.
-
21.
Carmona Fonseca J, 1971. Análisis estadístico y ecológico-epidemiológico de la sensibilidad a la histoplasmina en Colombia 1950–1968. Antioquia Med 21: 109–154.
-
22.
Arango M, Castañeda E, Agudelo CI, De Bedout C, Agudelo CA, Tobón A, Linares M, Valencia Y, Restrepo A, 2011. Histoplasmosis: results of the Colombian national survey, 1992–2008. Biomedica 31: 344–356.
-
23.
Ordóñez N, Tobón A, Arango M, Tabares A, De Bedout C, Gómez B, Castañeda E, Restrepo A, 1997. Brotes de histoplasmosis registrados en el área andina colombiana. Biomedica 17: 105.
-
24.
Jiménez RA, Urán ME, de Bedout C, Arango M, Tobón AM, Cano LE, Restrepo A, 2002. Outbreak of acute histoplasmosis in a family group: identification of the infection source. Biomedica 22: 155–159.
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