Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America
Dengue, the most prevalent arboviral disease worldwide, is caused by any of the four dengue virus (DENV) serotypes that co-circulate constantly in hyperendemic areas such as Medellin (Colombia), and these serotypes are transmitted by mosquitoes of the genus Aedes. In this study, we evaluated the rep...
- Autores:
-
Martínez Gutiérrez, Marlén
Quintero Gil, Diana Carolina
Uribe Yepes, Alexander
Ospina, Martha
Diaz, Francisco Javier
- Tipo de recurso:
- Article of journal
- Fecha de publicación:
- 2018
- Institución:
- Universidad Cooperativa de Colombia
- Repositorio:
- Repositorio UCC
- Idioma:
- OAI Identifier:
- oai:repository.ucc.edu.co:20.500.12494/15303
- Acceso en línea:
- https://hdl.handle.net/20.500.12494/15303
- Palabra clave:
- Aedes aegypti
C6/36 cells
Colombia
Dengue
Vector competence
Viral replication
- Rights
- openAccess
- License
- Atribución
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Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America |
| title |
Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America |
| spellingShingle |
Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America Aedes aegypti C6/36 cells Colombia Dengue Vector competence Viral replication |
| title_short |
Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America |
| title_full |
Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America |
| title_fullStr |
Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America |
| title_full_unstemmed |
Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America |
| title_sort |
Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America |
| dc.creator.fl_str_mv |
Martínez Gutiérrez, Marlén Quintero Gil, Diana Carolina Uribe Yepes, Alexander Ospina, Martha Diaz, Francisco Javier |
| dc.contributor.author.none.fl_str_mv |
Martínez Gutiérrez, Marlén Quintero Gil, Diana Carolina Uribe Yepes, Alexander Ospina, Martha Diaz, Francisco Javier |
| dc.subject.spa.fl_str_mv |
Aedes aegypti C6/36 cells Colombia Dengue Vector competence Viral replication |
| topic |
Aedes aegypti C6/36 cells Colombia Dengue Vector competence Viral replication |
| description |
Dengue, the most prevalent arboviral disease worldwide, is caused by any of the four dengue virus (DENV) serotypes that co-circulate constantly in hyperendemic areas such as Medellin (Colombia), and these serotypes are transmitted by mosquitoes of the genus Aedes. In this study, we evaluated the replicative capacity of strains isolated in Medellin between 2003 and 2007 in C6/36 cells and in colonies of Aedes aegypti collected during 2010-2011 from high or low-incidence areas within the same city. The phylogenetic analysis grouped isolates according to the predominant genotypes found in the Americas, and the in vitro characterization showed differences in the morphological changes induced by the isolates of each of the isolated serotypes compared to the reference serotypes. In vitro replicative capacity studies demonstrated that genomic copy number increased at four days post-infection and that cell viability decreased significantly compared to the control for all serotypes. The largest number of genomic copies in C6/36 was produced by DENV-2, followed by DENV-1 and DENV-4; DENV-3 produced the smallest number of genomic copies and had the smallest negative effect on cell viability. Finally, differences in the in vivo replication of intercolonial serotypes between the Rockefeller colony and the field colonies and among the intracolonial serotypes were found. The replication of DENV-2 at 7 and 14 days in both high- and low-incidence colonies was higher than that of the other serotypes, and replication of DENV-3 in the mosquito colonies was the most stable on the days evaluated. Our results support the notion that replication and, possibly, DENV transmission and severity depend on many factors, including serotype and vector characteristics |
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2018 |
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2018-08 |
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2019-11-28T13:48:08Z |
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2019-11-28T13:48:08Z |
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Artículo |
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1678-4391 |
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doi: 10.1016/j.bjid.2018.07.010. |
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https://hdl.handle.net/20.500.12494/15303 |
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Quintero-Gil D. C., Uribe-Yepes A., Ospina M., Díaz FJ y Martinez-Gutierrez M. (2018). Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America. Braz J Infect Dis. 2018 Jul - Aug;22(4):257-272. Recuperado de: |
| identifier_str_mv |
1678-4391 doi: 10.1016/j.bjid.2018.07.010. Quintero-Gil D. C., Uribe-Yepes A., Ospina M., Díaz FJ y Martinez-Gutierrez M. (2018). Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America. Braz J Infect Dis. 2018 Jul - Aug;22(4):257-272. Recuperado de: |
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https://hdl.handle.net/20.500.12494/15303 |
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https://www.sciencedirect.com/science/article/pii/S1413867018300540?via%3Dihub |
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Braz J Infect Dis |
| dc.relation.references.spa.fl_str_mv |
N.E.A. Murray, M.B. Quam, A. Wilder-Smith Epidemiology of dengue: past, present and future prospects Clin Epidemiol, 5 (2013), pp. 299-309 S. Bhatt, P.W. Gething, O.J. Brady, J.P. Messina, A.W. Farlow, C.L. Moyes, et al. The global distribution and burden of dengue Nature, 496 (2013), pp. 504-507 H.A. Rothan, H. Bahrani, Z. Mohamed, N. Abd Rahman, R. Yusof Fusion of protegrin-1 and plectasin to MAP30 shows significant inhibition activity against Dengue virus replication PLoS One, 9 (2014), p. e94561 M.Q. Benedict, R.S. Levine, W.A. Hawley, L.P. Lounibos Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus Vector Borne Zoo Dis (Larchmont, NY), 7 (2007), pp. 76-85 E. Holmes, S. Twiddy The origin, emergence and evolutionary genetics of dengue virus Infect Genet Evol, 3 (2003), pp. 19-28 R. Bartenschlager, S. Miller Molecular aspects of Dengue virus replication Future Microbiol, 3 (2008), pp. 155-165 J.A. Usme-Ciro, J.A. Mendez, K.D. Laiton, A. Páez The relevance of dengue virus genotypes surveillance at country level before vaccine approval Hum Vac Immunotherapeut, 10 (2014), pp. 2674-2678 L.A. Villar, D.P. Rojas, S. Besada-Lombana, E. Sarti Epidemiological Trends of Dengue Disease in Colombia (2000-2011): A Systematic Review PLoS Negl Trop Dis, 9 (2015), pp. 1-16 H. Rodríguez, F. de la Hoz Dengue and dengue and vector behaviour in Cáqueza, Colombia Rev Sal Púb (Bogotá, Colombia), 7 (2004), pp. 1-15 J. Nicholson, S.A. Ritchie, A.F. Van Den Hurk Aedes albopictus (Diptera: Culicidae) as a potential vector of endemic and exotic arboviruses in Australia J Med Entomol, 51 (2014), pp. 661-669 J. Jaimes-Dueñez, S. Arboleda, O. Triana-Chávez, A. Gómez-Palacio Spatio-temporal distribution of Aedes aegypti (Diptera: Culicidae) mitochondrial lineages in cities with distinct dengue incidence rates suggests complex population dynamics of the dengue vector in Colombia PLoS Negl Trop Dis, 9 (2015), pp. 1-21 L.D. Kramer, G.D. Ebel Dynamics of flavivirus infection in mosquitoes Adv Virus Res, 60 (2003), pp. 187-232 C.C. Liu, S.C. Wu Mosquito and mammalian cells grown on microcarriers for four‐serotype dengue virus production: variations in virus titer, plaque morphology, and replication rate Biotechnol Bioeng, 85 (2004), pp. 482-488 M.L. Muñoz, A. Cisneros, J. Cruz, P. Das, R. Tovar, A. Ortega Putative dengue virus receptors from mosquito cells FEMS Microbiol Lett, 168 (1998), pp. 251-258 J. Salas-Benito, J. Reyes-Del Valle, M. Salas-Benito, I. Ceballos-Olvera, C. Mosso, R.M. del Angel Evidence that the 45-kD glycoprotein, part of a putative dengue virus receptor complex in the mosquito cell line C6/36, is a Heat-Shock-related protein Am J Trop Med Hyg, 77 (2007), pp. 283-290 P. Sakoonwatanyoo, V. Boonsanay, D.R. Smith Growth and production of the dengue virus in C6/36 cells and identification of a laminin-binding protein as a candidate serotype 3 and 4 receptor protein Intervirology, 49 (2006), pp. 161-172 G. Kuno Early history of laboratory breeding of Aedes aegypti (Diptera: Culicidae) focusing on the origins and use of selected strains J Med Entomol, 47 (2014), pp. 957-971 J.L. Hardy, E.J. Houk, L.D. Kramer, W.C. Reeves Intrinsic factors affecting vector competence of mosquitoes for arboviruses Ann Rev Entomol, 28 (1983), pp. 229-262 J.R. Anderson, R. Rico-Hesse Aedes aegypti vectorial capacity is determined by the infecting genotype of dengue virus Am J Trop Med Hyg, 75 (2006), pp. 886-892 D.J. Gubler, S. Nalim, R. Tan, H. Saipan, J. Sulianti Saroso Variation in susceptibility to oral infection with dengue viruses among geographic strains of Aedes aegypti Am J Trop Med Hyg, 28 (1979), pp. 1045-1052 C. Gomez-Machorro, K.E. Bennett, M. del Lourdes Munoz, W.C. Black 4th Quantitative trait loci affecting dengue midgut infection barriers in an advanced intercross line of Aedes aegypti Insect Mol Biol, 13 (2004), pp. 637-648 L.B. Dickson, I. Sanchez-Vargas, M. Sylla, K. Fleming, W.C. Black 4th Vector competence in West African Aedes aegypti Is Flavivirus species and genotype dependent PLoS Negl Trop Dis, 8 (2014), p. e3153 J.M. Cadavid, G. Rúa, O. Campo, G. Bedoya, W. Rojas Microgeographic and temporal genetic changes of Aedes aegypti from Medellín, Colombia Biomédica, 35 (2014), pp. 53-61 M.C. Ospina, F.J. Diaz, J.E. Osorio Prolonged co-circulation of two distinct Dengue virus Type 3 lineages in the hyperendemic area of Medellin, Colombia Am J Trop Med Hyg, 83 (2010), pp. 72-78 O.P. Forattini Culicidologia Médica: Identificação, Biologia, Epidemiologia, vol. 2 (1996), p. 549 L.J. Chien, T.L. Liao, P.Y. Shu, J.H. Huang, D.J. Gubler, G.J. Chang Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses J Clin Microbiol, 44 (2006), pp. 1295-1304 S. Kumar, G. Stecher, K. Tamura MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets Mol Biol Evol (2016) msw054 L. Gutiérrez-Ruiz, D.C. Quintero-Gil, M. Martínez-Gutiérrez Actualización en diagnóstico del dengue: evolución de las técnicas y su aplicación real en la clínica Medicina y laboratorio, 18 (2012), pp. 411-441 M. Hussain, S. Asgari MicroRNA-like viral small RNA from Dengue virus 2 autoregulates its replication in mosquito cells Proc Natl Acad Sci U S A, 111 (2014), pp. 2746-2751 M.I. Salazar, J.H. Richardson, I. Sánchez-Vargas, K.E. Olson, B.J. Beaty Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes BMC Microbiol, 7 (2007), p. 9 I. Sánchez-Vargas, J.C. Scott, B.K. Poole-Smith, A.W. Franz, V. Barbosa-Solomieu, J. Wilusz, et al. Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito’s RNA interference pathway PLoS Pathog, 5 (2009), p. e1000299 X.X. Guo, X.J. Zhu, C.X. Li, Y.D. Dong, Y.M. Zhang, D. Xing, et al. Vector competence of Aedes albopictus and Aedes aegypti (Diptera: Culicidae) for DEN2-43 and New Guinea C virus strains of dengue 2 virus Acta Trop, 128 (2013), pp. 566-570 J. Junjhon, J.G. Pennington, T.J. Edwards, R. Perera, J. Lanman, R.J. Kuhn Ultrastructural characterization and three-dimensional architecture of replication sites in dengue virus-infected mosquito cells J Virol, 88 (2014), pp. 4687-4697 |
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Martínez Gutiérrez, MarlénQuintero Gil, Diana CarolinaUribe Yepes, AlexanderOspina, MarthaDiaz, Francisco Javier 22(4)2019-11-28T13:48:08Z2019-11-28T13:48:08Z2018-081678-4391doi: 10.1016/j.bjid.2018.07.010.https://hdl.handle.net/20.500.12494/15303Quintero-Gil D. C., Uribe-Yepes A., Ospina M., Díaz FJ y Martinez-Gutierrez M. (2018). Differences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South America. Braz J Infect Dis. 2018 Jul - Aug;22(4):257-272. Recuperado de:Dengue, the most prevalent arboviral disease worldwide, is caused by any of the four dengue virus (DENV) serotypes that co-circulate constantly in hyperendemic areas such as Medellin (Colombia), and these serotypes are transmitted by mosquitoes of the genus Aedes. In this study, we evaluated the replicative capacity of strains isolated in Medellin between 2003 and 2007 in C6/36 cells and in colonies of Aedes aegypti collected during 2010-2011 from high or low-incidence areas within the same city. The phylogenetic analysis grouped isolates according to the predominant genotypes found in the Americas, and the in vitro characterization showed differences in the morphological changes induced by the isolates of each of the isolated serotypes compared to the reference serotypes. In vitro replicative capacity studies demonstrated that genomic copy number increased at four days post-infection and that cell viability decreased significantly compared to the control for all serotypes. The largest number of genomic copies in C6/36 was produced by DENV-2, followed by DENV-1 and DENV-4; DENV-3 produced the smallest number of genomic copies and had the smallest negative effect on cell viability. Finally, differences in the in vivo replication of intercolonial serotypes between the Rockefeller colony and the field colonies and among the intracolonial serotypes were found. The replication of DENV-2 at 7 and 14 days in both high- and low-incidence colonies was higher than that of the other serotypes, and replication of DENV-3 in the mosquito colonies was the most stable on the days evaluated. Our results support the notion that replication and, possibly, DENV transmission and severity depend on many factors, including serotype and vector characteristicshttps://scienti.colciencias.gov.co/cvlac/visualizador/generarCurriculoCv.do?cod_rh=0000213748https://orcid.org/0000-0002-9429-0058Marlen.martinezg@campucucc.edu.cohttps://scholar.google.es/citations?user=flSrsSIAAAAJ&hl=es257-272Universidad Cooperativa de Colombia, Facultad de Ciencias de la Salud, Medicina Veterinaría y Zootecnia, BucaramangaMedicina veterinaria y zootecniaBucaramangahttps://www.sciencedirect.com/science/article/pii/S1413867018300540?via%3DihubBraz J Infect DisN.E.A. Murray, M.B. Quam, A. Wilder-Smith Epidemiology of dengue: past, present and future prospects Clin Epidemiol, 5 (2013), pp. 299-309S. Bhatt, P.W. Gething, O.J. Brady, J.P. Messina, A.W. Farlow, C.L. Moyes, et al. The global distribution and burden of dengue Nature, 496 (2013), pp. 504-507H.A. Rothan, H. Bahrani, Z. Mohamed, N. Abd Rahman, R. Yusof Fusion of protegrin-1 and plectasin to MAP30 shows significant inhibition activity against Dengue virus replication PLoS One, 9 (2014), p. e94561M.Q. Benedict, R.S. Levine, W.A. Hawley, L.P. Lounibos Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus Vector Borne Zoo Dis (Larchmont, NY), 7 (2007), pp. 76-85E. Holmes, S. Twiddy The origin, emergence and evolutionary genetics of dengue virus Infect Genet Evol, 3 (2003), pp. 19-28R. Bartenschlager, S. Miller Molecular aspects of Dengue virus replication Future Microbiol, 3 (2008), pp. 155-165J.A. Usme-Ciro, J.A. Mendez, K.D. Laiton, A. Páez The relevance of dengue virus genotypes surveillance at country level before vaccine approval Hum Vac Immunotherapeut, 10 (2014), pp. 2674-2678L.A. Villar, D.P. Rojas, S. Besada-Lombana, E. Sarti Epidemiological Trends of Dengue Disease in Colombia (2000-2011): A Systematic Review PLoS Negl Trop Dis, 9 (2015), pp. 1-16H. Rodríguez, F. de la Hoz Dengue and dengue and vector behaviour in Cáqueza, Colombia Rev Sal Púb (Bogotá, Colombia), 7 (2004), pp. 1-15J. Nicholson, S.A. Ritchie, A.F. Van Den Hurk Aedes albopictus (Diptera: Culicidae) as a potential vector of endemic and exotic arboviruses in Australia J Med Entomol, 51 (2014), pp. 661-669J. Jaimes-Dueñez, S. Arboleda, O. Triana-Chávez, A. Gómez-Palacio Spatio-temporal distribution of Aedes aegypti (Diptera: Culicidae) mitochondrial lineages in cities with distinct dengue incidence rates suggests complex population dynamics of the dengue vector in Colombia PLoS Negl Trop Dis, 9 (2015), pp. 1-21L.D. Kramer, G.D. Ebel Dynamics of flavivirus infection in mosquitoes Adv Virus Res, 60 (2003), pp. 187-232C.C. Liu, S.C. Wu Mosquito and mammalian cells grown on microcarriers for four‐serotype dengue virus production: variations in virus titer, plaque morphology, and replication rate Biotechnol Bioeng, 85 (2004), pp. 482-488M.L. Muñoz, A. Cisneros, J. Cruz, P. Das, R. Tovar, A. Ortega Putative dengue virus receptors from mosquito cells FEMS Microbiol Lett, 168 (1998), pp. 251-258J. Salas-Benito, J. Reyes-Del Valle, M. Salas-Benito, I. Ceballos-Olvera, C. Mosso, R.M. del Angel Evidence that the 45-kD glycoprotein, part of a putative dengue virus receptor complex in the mosquito cell line C6/36, is a Heat-Shock-related protein Am J Trop Med Hyg, 77 (2007), pp. 283-290P. Sakoonwatanyoo, V. Boonsanay, D.R. Smith Growth and production of the dengue virus in C6/36 cells and identification of a laminin-binding protein as a candidate serotype 3 and 4 receptor protein Intervirology, 49 (2006), pp. 161-172G. Kuno Early history of laboratory breeding of Aedes aegypti (Diptera: Culicidae) focusing on the origins and use of selected strains J Med Entomol, 47 (2014), pp. 957-971J.L. Hardy, E.J. Houk, L.D. Kramer, W.C. Reeves Intrinsic factors affecting vector competence of mosquitoes for arboviruses Ann Rev Entomol, 28 (1983), pp. 229-262J.R. Anderson, R. Rico-Hesse Aedes aegypti vectorial capacity is determined by the infecting genotype of dengue virus Am J Trop Med Hyg, 75 (2006), pp. 886-892D.J. Gubler, S. Nalim, R. Tan, H. Saipan, J. Sulianti Saroso Variation in susceptibility to oral infection with dengue viruses among geographic strains of Aedes aegypti Am J Trop Med Hyg, 28 (1979), pp. 1045-1052C. Gomez-Machorro, K.E. Bennett, M. del Lourdes Munoz, W.C. Black 4th Quantitative trait loci affecting dengue midgut infection barriers in an advanced intercross line of Aedes aegypti Insect Mol Biol, 13 (2004), pp. 637-648L.B. Dickson, I. Sanchez-Vargas, M. Sylla, K. Fleming, W.C. Black 4th Vector competence in West African Aedes aegypti Is Flavivirus species and genotype dependent PLoS Negl Trop Dis, 8 (2014), p. e3153J.M. Cadavid, G. Rúa, O. Campo, G. Bedoya, W. Rojas Microgeographic and temporal genetic changes of Aedes aegypti from Medellín, Colombia Biomédica, 35 (2014), pp. 53-61M.C. Ospina, F.J. Diaz, J.E. Osorio Prolonged co-circulation of two distinct Dengue virus Type 3 lineages in the hyperendemic area of Medellin, Colombia Am J Trop Med Hyg, 83 (2010), pp. 72-78O.P. Forattini Culicidologia Médica: Identificação, Biologia, Epidemiologia, vol. 2 (1996), p. 549L.J. Chien, T.L. Liao, P.Y. Shu, J.H. Huang, D.J. Gubler, G.J. Chang Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses J Clin Microbiol, 44 (2006), pp. 1295-1304S. Kumar, G. Stecher, K. Tamura MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets Mol Biol Evol (2016) msw054L. Gutiérrez-Ruiz, D.C. Quintero-Gil, M. Martínez-Gutiérrez Actualización en diagnóstico del dengue: evolución de las técnicas y su aplicación real en la clínica Medicina y laboratorio, 18 (2012), pp. 411-441M. Hussain, S. Asgari MicroRNA-like viral small RNA from Dengue virus 2 autoregulates its replication in mosquito cells Proc Natl Acad Sci U S A, 111 (2014), pp. 2746-2751M.I. Salazar, J.H. Richardson, I. Sánchez-Vargas, K.E. Olson, B.J. Beaty Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes BMC Microbiol, 7 (2007), p. 9I. Sánchez-Vargas, J.C. Scott, B.K. Poole-Smith, A.W. Franz, V. Barbosa-Solomieu, J. Wilusz, et al. Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito’s RNA interference pathway PLoS Pathog, 5 (2009), p. e1000299X.X. Guo, X.J. Zhu, C.X. Li, Y.D. Dong, Y.M. Zhang, D. Xing, et al. Vector competence of Aedes albopictus and Aedes aegypti (Diptera: Culicidae) for DEN2-43 and New Guinea C virus strains of dengue 2 virus Acta Trop, 128 (2013), pp. 566-570J. Junjhon, J.G. Pennington, T.J. Edwards, R. Perera, J. Lanman, R.J. Kuhn Ultrastructural characterization and three-dimensional architecture of replication sites in dengue virus-infected mosquito cells J Virol, 88 (2014), pp. 4687-4697Aedes aegyptiC6/36 cellsColombiaDengueVector competenceViral replicationDifferences in the replicative capacities of clinical isolates of dengue virus in C6/36 cells and in urban populations of Aedes aegypti from Colombia, South AmericaArtículohttp://purl.org/coar/resource_type/c_6501http://purl.org/coar/resource_type/c_2df8fbb1http://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionAtribucióninfo:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2PublicationORIGINAL1-s2.0-S1413867018300540-main.pdf1-s2.0-S1413867018300540-main.pdfArtículoapplication/pdf2554219https://repository.ucc.edu.co/bitstreams/49eb194c-9885-4242-a7fa-51598d429c98/downloade44837f0ab87974419e0ac15972795ecMD51Licencia_de_uso_Differences_2018.pdfLicencia_de_uso_Differences_2018.pdfLicencia de usoapplication/pdf212812https://repository.ucc.edu.co/bitstreams/3ffadfd4-1e18-4676-accb-d329406a9773/download7d341ca864c11c9842245a927887251dMD53LICENSElicense.txtlicense.txttext/plain; charset=utf-84334https://repository.ucc.edu.co/bitstreams/4367c6bc-b1db-41fd-b7f1-e9917c83b3f6/download3bce4f7ab09dfc588f126e1e36e98a45MD54THUMBNAIL1-s2.0-S1413867018300540-main.pdf.jpg1-s2.0-S1413867018300540-main.pdf.jpgGenerated Thumbnailimage/jpeg5483https://repository.ucc.edu.co/bitstreams/481fd1c9-1867-48aa-8870-3cb5f59b381f/downloadc4c4bcb7fd8e61ced2c6936e364224e7MD55Licencia_de_uso_Differences_2018.pdf.jpgLicencia_de_uso_Differences_2018.pdf.jpgGenerated Thumbnailimage/jpeg5230https://repository.ucc.edu.co/bitstreams/f2a46d5c-986f-4a52-91b2-100920cc6e9f/download405b0d341abdad8451479bfab93abd07MD56TEXT1-s2.0-S1413867018300540-main.pdf.txt1-s2.0-S1413867018300540-main.pdf.txtExtracted texttext/plain67118https://repository.ucc.edu.co/bitstreams/39c461d5-daf6-451e-9553-790d289491d7/download6e321682a452d195853ade3489868951MD57Licencia_de_uso_Differences_2018.pdf.txtLicencia_de_uso_Differences_2018.pdf.txtExtracted texttext/plain5508https://repository.ucc.edu.co/bitstreams/f9b1d6d4-7989-4a19-b6f8-5d043c1cb616/download4fe3692c2145cb1e8a34d378eb226b17MD5820.500.12494/15303oai:repository.ucc.edu.co:20.500.12494/153032024-08-10 22:41:26.529restrictedhttps://repository.ucc.edu.coRepositorio Institucional Universidad Cooperativa de Colombiabdigital@metabiblioteca.com |