- -

Deep-Amplicon Sequencing (DAS) Analysis to Determine the Presence of Pathogenic Helicobacter species in Watewater Reused for Irrigation

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Deep-Amplicon Sequencing (DAS) Analysis to Determine the Presence of Pathogenic Helicobacter species in Watewater Reused for Irrigation

Mostrar el registro sencillo del ítem

Ficheros en el ítem

Thumbnail
Nombre: Hortelano;Moreno; ...
Tamaño: 901.0Kb
Formato: PDF
Descripción: Versión del Autor.
Abrir
[Cerrado]
Nombre: Environment_Pollu ...
Tamaño: 367.9Kb
Formato: PDF
Descripción: Versión editorial
Solicitar una copia al autor
dc.contributor.author Hortelano, Irene es_ES
dc.contributor.author Moreno Trigos, Mª Yolanda es_ES
dc.contributor.author Moreno-Mesonero, Laura es_ES
dc.contributor.author Ferrús Pérez, Mª Antonia es_ES
dc.date.accessioned 2021-02-11T04:31:58Z
dc.date.available 2021-02-11T04:31:58Z
dc.date.issued 2020-09 es_ES
dc.identifier.issn 0269-7491 es_ES
dc.identifier.uri http://hdl.handle.net/10251/161039
dc.description.abstract [EN] Wastewater has become one of the most important and least expensive water for the agriculture sector. As an alternative to the overexploitation of water resources. Inappropriate treatment before reuse can result in a negative impact in environment, such us presence of pathogens. Causing an increased risk in health and environmental safety, which can lead to an increased risk of human infection. Among all the emerging wastewater pathogens, bacteria of the genus Helicobacter are some of the most disturbing ones, since they are directly related to gastric illness and hepatobiliary and gastric cancer. Therefore, the aim of this study was to determine the presence of potentially pathogenic Helicobacter spp in treated wastewater aimed for irrigation. The next generation sequencing approach based on Illumina in combination with culture and molecular techniques (q PCR, FISH and DVC-FISH) have been used to analyzed 16 wastewater samples. All the enriched samples were negative for Helicobacter growth in any of the culture media used. Characteristic colonies, covered by a mass of non-specific bacterial growth, were analyzed by Helicobacter spp. PCR, H. pylori qPCR and sequencing. One of the direct samples was positive for H. pylori. Using FISH and DVC-FISH technique, Helicobacter spp, including H. pylori, was detected in seven out of eight samples of wastewater from the tertiary effluents, all of them viable. Although, qPCR yield only three positive results. Moreover, when wastewater microbiome was studied, Helicobacter genus was detected in 7 samples. The different molecular techniques using in the present study, provided evidence, for the first time, the presence of species belonging to the genus Helicobacter such as H. pylori, H. hepaticus, H. pullorum and H. suis in wastewater samples, even after disinfection treatment. es_ES
dc.description.sponsorship This research has been supported in part by grant ACIF/2016/150 for scientific research from the Ministry of Culture, Education and Sport of the Valencian Community, Spain and the European Social Fund 2014-2020. es_ES
dc.language Inglés es_ES
dc.publisher Elsevier es_ES
dc.relation.ispartof Environmental Pollution es_ES
dc.rights Reconocimiento - No comercial - Sin obra derivada (by-nc-nd) es_ES
dc.subject Wastewater es_ES
dc.subject Helicobacter spp es_ES
dc.subject Molecular techniques es_ES
dc.subject Metagenomics es_ES
dc.subject Pathogens es_ES
dc.subject.classification MICROBIOLOGIA es_ES
dc.title Deep-Amplicon Sequencing (DAS) Analysis to Determine the Presence of Pathogenic Helicobacter species in Watewater Reused for Irrigation es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1016/j.envpol.2020.114768 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//ACIF%2F2016%2F150/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario de Ingeniería del Agua y del Medio Ambiente - Institut Universitari d'Enginyeria de l'Aigua i Medi Ambient es_ES
dc.description.bibliographicCitation Hortelano, I.; Moreno Trigos, MY.; Moreno-Mesonero, L.; Ferrús Pérez, MA. (2020). Deep-Amplicon Sequencing (DAS) Analysis to Determine the Presence of Pathogenic Helicobacter species in Watewater Reused for Irrigation. Environmental Pollution. 264:1-10. https://doi.org/10.1016/j.envpol.2020.114768 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1016/j.envpol.2020.114768 es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 10 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 264 es_ES
dc.identifier.pmid 32434114 es_ES
dc.relation.pasarela S\410539 es_ES
dc.contributor.funder European Social Fund es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.description.references Ahmed, A. M., Younis, E. E. A., Ishida, Y., & Shimamoto, T. (2009). Genetic basis of multidrug resistance in Salmonella enterica serovars Enteritidis and Typhimurium isolated from diarrheic calves in Egypt. Acta Tropica, 111(2), 144-149. doi:10.1016/j.actatropica.2009.04.004 es_ES
dc.description.references Anand, P. S. (2014). Role of dental plaque, saliva and periodontal disease inHelicobacter pyloriinfection. World Journal of Gastroenterology, 20(19), 5639. doi:10.3748/wjg.v20.i19.5639 es_ES
dc.description.references Azevedo, N. F., Almeida, C., Fernandes, I., Cerqueira, L., Dias, S., Keevil, C. W., & Vieira, M. J. (2008). Survival of Gastric and Enterohepatic Helicobacter spp. in Water: Implications for Transmission. Applied and Environmental Microbiology, 74(6), 1805-1811. doi:10.1128/aem.02241-07 es_ES
dc.description.references Bai, X., Xi, C., & Wu, J. (2016). Survival of Helicobacter pylori in the wastewater treatment process and the receiving river in Michigan, USA. Journal of Water and Health, 14(4), 692-698. doi:10.2166/wh.2016.259 es_ES
dc.description.references Bohr, U. R. M., Glasbrenner, B., Primus, A., Zagoura, A., Wex, T., & Malfertheiner, P. (2004). Identification of Enterohepatic Helicobacter Species in Patients Suffering from Inflammatory Bowel Disease. Journal of Clinical Microbiology, 42(6), 2766-2768. doi:10.1128/jcm.42.6.2766-2768.2004 es_ES
dc.description.references Bokulich, N. A., Subramanian, S., Faith, J. J., Gevers, D., Gordon, J. I., Knight, R., … Caporaso, J. G. (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods, 10(1), 57-59. doi:10.1038/nmeth.2276 es_ES
dc.description.references Botes, M., de Kwaadsteniet, M., & Cloete, T. E. (2012). Application of quantitative PCR for the detection of microorganisms in water. Analytical and Bioanalytical Chemistry, 405(1), 91-108. doi:10.1007/s00216-012-6399-3 es_ES
dc.description.references Brooks, J. P., Edwards, D. J., Harwich, M. D., Rivera, M. C., Fettweis, J. M., … Buck, G. A. (2015). The truth about metagenomics: quantifying and counteracting bias in 16S rRNA studies. BMC Microbiology, 15(1). doi:10.1186/s12866-015-0351-6 es_ES
dc.description.references Cai, L., & Zhang, T. (2013). Detecting Human Bacterial Pathogens in Wastewater Treatment Plants by a High-Throughput Shotgun Sequencing Technique. Environmental Science & Technology, 47(10), 5433-5441. doi:10.1021/es400275r es_ES
dc.description.references Cao, Y., Fanning, S., Proos, S., Jordan, K., & Srikumar, S. (2017). A Review on the Applications of Next Generation Sequencing Technologies as Applied to Food-Related Microbiome Studies. Frontiers in Microbiology, 8. doi:10.3389/fmicb.2017.01829 es_ES
dc.description.references Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., … Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335-336. doi:10.1038/nmeth.f.303 es_ES
dc.description.references Casswall, T. H., Németh, A., Nilsson, I., Wadström, T., & Nilsson, H.-O. (2010). Helicobacterspecies DNA in liver and gastric tissues in children and adolescents with chronic liver disease. Scandinavian Journal of Gastroenterology, 45(2), 160-167. doi:10.3109/00365520903426915 es_ES
dc.description.references Cellini, L., Grande, R., Di Campli, E., Di Bartolomeo, S., Di Giulio, M., Traini, T., & Trubiani, O. (2008). Characterization of anHelicobacter pylorienvironmental strain. Journal of Applied Microbiology, 105(3), 761-769. doi:10.1111/j.1365-2672.2008.03808.x es_ES
dc.description.references Chan, V., Crocetti, G., Grehan, M., Zhang, L., Danon, S., Lee, A., & Mitchell, H. (2005). Visualization of Helicobacter Species Within the Murine Cecal Mucosa Using Specific Fluorescence In Situ Hybridization. Helicobacter, 10(2), 114-124. doi:10.1111/j.1523-5378.2005.00298.x es_ES
dc.description.references Chen, D.-F. (2007). H pyloriare associated with chronic cholecystitis. World Journal of Gastroenterology, 13(7), 1119. doi:10.3748/wjg.v13.i7.1119 es_ES
dc.description.references Corry, J. E. L., Atabay, H. I., Forsythe, S. J., & Mansfield, L. P. (2003). Chapter 18 Culture media for the isolation of campylobacters, helicobacters and arcobacters. Progress in Industrial Microbiology, 271-316. doi:10.1016/s0079-6352(03)80021-8 es_ES
dc.description.references Cunachi, A. M., Fernández-Delgado, M., Suárez, P., Contreras, M., Michelangeli, F., & García-Amado, M. A. (2015). Detection of Helicobacter DNA in different water sources and penguin feces from Greenwich, Dee and Barrientos Islands, Antarctica. Polar Biology, 39(9), 1539-1546. doi:10.1007/s00300-015-1879-5 es_ES
dc.description.references Fernández-Delgado, M., Giarrizzo, J. G., García-Amado, M. A., Contreras, M., Salazar, V., Barton, H., & Suárez, P. (2016). Evidence of Helicobacter spp. in freshwaters from Roraima Tepui, Guayana Shield, South America. Antonie van Leeuwenhoek, 109(4), 529-542. doi:10.1007/s10482-016-0658-9 es_ES
dc.description.references Fukuda, K. (2002). Comparative analysis of Helicobacter DNAs and biliary pathology in patients with and without hepatobiliary cancer. Carcinogenesis, 23(11), 1927-1932. doi:10.1093/carcin/23.11.1927 es_ES
dc.description.references García, A. (2014). Biofilm andHelicobacter pylori: From environment to human host. World Journal of Gastroenterology, 20(19), 5632. doi:10.3748/wjg.v20.i19.5632 es_ES
dc.description.references Goldman, C. G., Loureiro, J. D., Matteo, M. J., Catalano, M., Gonzalez, A. B., Heredia, S. R., … Cremaschi, G. A. (2009). Helicobacter spp. from gastric biopsies of stranded South American fur seals (Arctocephalus australis). Research in Veterinary Science, 86(1), 18-21. doi:10.1016/j.rvsc.2008.04.001 es_ES
dc.description.references De Groote, D., Van Doorn, L.-J., Van den Bulck, K., Vandamme, P., Vieth, M., Stolte, M., … Ducatelle, R. (2005). Detection of Non-pylori Helicobacter Species in «Helicobacter heilmannii»-Infected Humans. Helicobacter, 10(5), 398-406. doi:10.1111/j.1523-5378.2005.00347.x es_ES
dc.description.references Haesebrouck, F., Pasmans, F., Flahou, B., Chiers, K., Baele, M., Meyns, T., … Ducatelle, R. (2009). Gastric Helicobacters in Domestic Animals and Nonhuman Primates and Their Significance for Human Health. Clinical Microbiology Reviews, 22(2), 202-223. doi:10.1128/cmr.00041-08 es_ES
dc.description.references Hamada, T., Yokota, K., Ayada, K., Hirai, K., Kamada, T., Haruma, K., … Oguma, K. (2009). Detection ofHelicobacter hepaticusin Human Bile Samples of Patients with Biliary Disease. Helicobacter, 14(6), 545-551. doi:10.1111/j.1523-5378.2009.00729.x es_ES
dc.description.references Johnson, C. H., Rice, E. W., & Reasoner, D. J. (1997). Inactivation of Helicobacter pylori by chlorination. Applied and Environmental Microbiology, 63(12), 4969-4970. doi:10.1128/aem.63.12.4969-4970.1997 es_ES
dc.description.references Karagin, P. H. (2010). Helicobacterspecies and common gut bacterial DNA in gallbladder with cholecystitis. World Journal of Gastroenterology, 16(38), 4817. doi:10.3748/wjg.v16.i38.4817 es_ES
dc.description.references Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., & Glöckner, F. O. (2012). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research, 41(1), e1-e1. doi:10.1093/nar/gks808 es_ES
dc.description.references Kopylova, E., Noé, L., & Touzet, H. (2012). SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics, 28(24), 3211-3217. doi:10.1093/bioinformatics/bts611 es_ES
dc.description.references Kumaraswamy, R., Amha, Y. M., Anwar, M. Z., Henschel, A., Rodríguez, J., & Ahmad, F. (2014). Molecular Analysis for Screening Human Bacterial Pathogens in Municipal Wastewater Treatment and Reuse. Environmental Science & Technology, 48(19), 11610-11619. doi:10.1021/es502546t es_ES
dc.description.references Li, D., Tong, T., Zeng, S., Lin, Y., Wu, S., & He, M. (2014). Quantification of viable bacteria in wastewater treatment plants by using propidium monoazide combined with quantitative PCR (PMA-qPCR). Journal of Environmental Sciences, 26(2), 299-306. doi:10.1016/s1001-0742(13)60425-8 es_ES
dc.description.references Logares, R., Sunagawa, S., Salazar, G., Cornejo-Castillo, F. M., Ferrera, I., Sarmento, H., … Acinas, S. G. (2013). Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environmental Microbiology, 16(9), 2659-2671. doi:10.1111/1462-2920.12250 es_ES
dc.description.references Lyu, S., Chen, W., Zhang, W., Fan, Y., & Jiao, W. (2016). Wastewater reclamation and reuse in China: Opportunities and challenges. Journal of Environmental Sciences, 39, 86-96. doi:10.1016/j.jes.2015.11.012 es_ES
dc.description.references Ma, Q., Qu, Y., Shen, W., Zhang, Z., Wang, J., Liu, Z., … Zhou, J. (2015). Bacterial community compositions of coking wastewater treatment plants in steel industry revealed by Illumina high-throughput sequencing. Bioresource Technology, 179, 436-443. doi:10.1016/j.biortech.2014.12.041 es_ES
dc.description.references Mateos Muñoz, B., Pérez de la Serna, J., Ruiz de León, A., Serrano Falcón, B., Casabona Francés, S., Velasco Cerrudo, A., & Rey Díaz-Rubio, E. (2013). Enterohepatic Helicobacter other than Helicobacter pylori. Revista Española de Enfermedades Digestivas, 105(8), 477-485. doi:10.4321/s1130-01082013000800006 es_ES
dc.description.references Moreno, Y., & Ferrús, M. A. (2012). Specific Detection of CultivableHelicobacter pyloriCells from Wastewater Treatment Plants. Helicobacter, 17(5), 327-332. doi:10.1111/j.1523-5378.2012.00961.x es_ES
dc.description.references Moreno, Y., Ferrús, M. A., Alonso, J. L., Jiménez, A., & Hernández, J. (2003). Use of fluorescent in situ hybridization to evidence the presence of Helicobacter pylori in water. Water Research, 37(9), 2251-2256. doi:10.1016/s0043-1354(02)00624-3 es_ES
dc.description.references Moreno, Y., Piqueres, P., Alonso, J. L., Jiménez, A., González, A., & Ferrús, M. A. (2007). Survival and viability of Helicobacter pylori after inoculation into chlorinated drinking water. Water Research, 41(15), 3490-3496. doi:10.1016/j.watres.2007.05.020 es_ES
dc.description.references Moreno-Mesonero, L., Moreno, Y., Alonso, J. L., & Ferrús, M. A. (2016). DVC-FISH and PMA-qPCR techniques to assess the survival of Helicobacter pylori inside Acanthamoeba castellanii. Research in Microbiology, 167(1), 29-34. doi:10.1016/j.resmic.2015.08.002 es_ES
dc.description.references Moreno-Mesonero, L., Hortelano, I., Moreno, Y., & Ferrús, M. A. (2020). Evidence of viable Helicobacter pylori and other bacteria of public health interest associated with free-living amoebae in lettuce samples by next generation sequencing and other molecular techniques. International Journal of Food Microbiology, 318, 108477. doi:10.1016/j.ijfoodmicro.2019.108477 es_ES
dc.description.references Ndour, N. Y. B., Baudoin, E., Guissé, A., Seck, M., Khouma, M., & Brauman, A. (2008). Impact of irrigation water quality on soil nitrifying and total bacterial communities. Biology and Fertility of Soils, 44(5), 797-803. doi:10.1007/s00374-008-0285-3 es_ES
dc.description.references Øverby, A., Yamagata Murayama, S., Matsui, H., & Nakamura, M. (2016). In the Aftermath of Helicobacter pylori: Other Helicobacters Rising Up to Become the Next Gastric Epidemic? Digestion, 93(4), 260-265. doi:10.1159/000445399 es_ES
dc.description.references Parsons, L. R., Sheikh, B., Holden, R., & York, D. W. (2010). Reclaimed Water as an Alternative Water Source for Crop Irrigation. HortScience, 45(11), 1626-1629. doi:10.21273/hortsci.45.11.1626 es_ES
dc.description.references Pathak, E., El-Borai, F. E., Campos-Herrera, R., Johnson, E. G., Stuart, R. J., Graham, J. H., & Duncan, L. W. (2012). Use of real-time PCR to discriminate parasitic and saprophagous behaviour by nematophagous fungi. Fungal Biology, 116(5), 563-573. doi:10.1016/j.funbio.2012.02.005 es_ES
dc.description.references Pedrero, F., Kalavrouziotis, I., Alarcón, J. J., Koukoulakis, P., & Asano, T. (2010). Use of treated municipal wastewater in irrigated agriculture—Review of some practices in Spain and Greece. Agricultural Water Management, 97(9), 1233-1241. doi:10.1016/j.agwat.2010.03.003 es_ES
dc.description.references Pedrero, F., Mounzer, O., Alarcón, J. J., Bayona, J. M., & Nicolás, E. (2012). The viability of irrigating mandarin trees with saline reclaimed water in a semi-arid Mediterranean region: a preliminary assessment. Irrigation Science, 31(4), 759-768. doi:10.1007/s00271-012-0359-8 es_ES
dc.description.references Pereira, R. P. A., Peplies, J., Brettar, I., & Höfle, M. G. (2017). Development of a genus-specific next generation sequencing approach for sensitive and quantitative determination of the Legionella microbiome in freshwater systems. BMC Microbiology, 17(1). doi:10.1186/s12866-017-0987-5 es_ES
dc.description.references Petersen, R. F., Harrington, C. S., Kortegaard, H. E., & On, S. L. W. (2007). A PCR-DGGE method for detection and identification of Campylobacter, Helicobacter, Arcobacter and related Epsilobacteria and its application to saliva samples from humans and domestic pets. Journal of Applied Microbiology, 103(6), 2601-2615. doi:10.1111/j.1365-2672.2007.03515.x es_ES
dc.description.references Piqueres, P., Moreno, Y., Alonso, J. L., & Ferrús, M. A. (2006). A combination of direct viable count and fluorescent in situ hybridization for estimating Helicobacter pylori cell viability. Research in Microbiology, 157(4), 345-349. doi:10.1016/j.resmic.2005.09.003 es_ES
dc.description.references Razzolini, M. T. P., Breternitz, B. S., Kuchkarian, B., & Bastos, V. K. (2020). Cryptosporidium and Giardia in urban wastewater: A challenge to overcome. Environmental Pollution, 257, 113545. doi:10.1016/j.envpol.2019.113545 es_ES
dc.description.references Rognes, T., Flouri, T., Nichols, B., Quince, C., & Mahé, F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4, e2584. doi:10.7717/peerj.2584 es_ES
dc.description.references Vicente-Sánchez, J., Nicolás, E., Pedrero, F., Alarcón, J. J., Maestre-Valero, J. F., & Fernández, F. (2013). Arbuscular mycorrhizal symbiosis alleviates detrimental effects of saline reclaimed water in lettuce plants. Mycorrhiza, 24(5), 339-348. doi:10.1007/s00572-013-0542-7 es_ES
dc.description.references Schloss, P. D., Gevers, D., & Westcott, S. L. (2011). Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies. PLoS ONE, 6(12), e27310. doi:10.1371/journal.pone.0027310 es_ES
dc.description.references Steele, T. W., & McDermott, S. N. (1984). The use of membrane filters applied directly to the surface of agar plates for the isolation of campylobacter jejuni from feces. Pathology, 16(3), 263-265. doi:10.3109/00313028409068535 es_ES
dc.description.references Twing, K. I., Kirchman, D. L., & Campbell, B. J. (2011). Temporal study of Helicobacter pylori presence in coastal freshwater, estuary and marine waters. Water Research, 45(4), 1897-1905. doi:10.1016/j.watres.2010.12.013 es_ES
dc.description.references Vierheilig, J., Savio, D., Ley, R. E., Mach, R. L., Farnleitner, A. H., & Reischer, G. H. (2015). Potential applications of next generation DNA sequencing of 16S rRNA gene amplicons in microbial water quality monitoring. Water Science and Technology, 72(11), 1962-1972. doi:10.2166/wst.2015.407 es_ES
dc.description.references Wagner, M., & Loy, A. (2002). Bacterial community composition and function in sewage treatment systems. Current Opinion in Biotechnology, 13(3), 218-227. doi:10.1016/s0958-1669(02)00315-4 es_ES
dc.description.references Wang, X., Hu, M., Xia, Y., Wen, X., & Ding, K. (2012). Pyrosequencing Analysis of Bacterial Diversity in 14 Wastewater Treatment Systems in China. Applied and Environmental Microbiology, 78(19), 7042-7047. doi:10.1128/aem.01617-12 es_ES
dc.description.references Ye, L., & Zhang, T. (2011). Pathogenic Bacteria in Sewage Treatment Plants as Revealed by 454 Pyrosequencing. Environmental Science & Technology, 45(17), 7173-7179. doi:10.1021/es201045e es_ES
dc.description.references Ye, L., & Zhang, T. (2012). Bacterial communities in different sections of a municipal wastewater treatment plant revealed by 16S rDNA 454 pyrosequencing. Applied Microbiology and Biotechnology, 97(6), 2681-2690. doi:10.1007/s00253-012-4082-4 es_ES
dc.description.references Yu, X., Jiang, W., Shi, Y., Ye, H., & Lin, J. (2019). Applications of sequencing technology in clinical microbial infection. Journal of Cellular and Molecular Medicine, 23(11), 7143-7150. doi:10.1111/jcmm.14624 es_ES
dc.description.references Zhang, J., Kobert, K., Flouri, T., & Stamatakis, A. (2013). PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics, 30(5), 614-620. doi:10.1093/bioinformatics/btt593 es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem