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D0cbac65e89cd810e3983705d8 International Journal of Environmental Research and Public Health Article Prevalence of Rotavirus Genogroup A and Norovirus Genogroup II in Bassaseachic Falls National Park Surface Waters in Chihuahua, Mexico Ma. Carmen E. Delgado-Gardea 1,2, Patricia Tamez-Guerra 2, Ricardo Gomez-Flores 2, Aurora Mendieta-Mendoza 1, Francisco Javier Zavala-Díaz de la Serna 1, Juan Francisco Contreras-Cordero 2, Gilberto Erosa-de la Vega 1, María Concepción Pérez-Recoder 3, Blanca Sánchez-Ramírez 1, Carmen González-Horta 1 and Rocío Infante-Ramírez 1,* 1 Laboratorio de Biotecnología, Facultad de Ciencias Químicas, Universidad Autónoma de Chihuahua, Circuito Nuevo Campus Universitario No.1, Chihuahua 31125, Mexico; [email protected] (M.C.E.D.-G.); [email protected] (A.M.-M.); [email protected] (F.J.Z.-D.d.l.S.); [email protected] (G.E.-d.l.V.); [email protected] (B.S.-R.); carmengonzalez@uach (C.G.-H.) 2 Departamento de Microbiología e Inmunología, Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León, Ave. Universidad s/n, San Nicolás de los Garza 66455, Mexico; [email protected] (P.T.-G.); [email protected] (R.G.-F.); [email protected] (J.F.C.-C.) 3 Comisión Nacional de Áreas Naturales Protegidas, Dirección Regional Norte y Sierra Madre Occidental, Parque Nacional Cascada de Bassaseachic, Ocampo, Chihuahua 31203, Mexico; [email protected] * Correspondence: [email protected]; Tel.: +52-(614)-236-6000 (ext. 4265) Academic Editor: Paul B. Tchounwou Received: 13 February 2017; Accepted: 26 April 2017; Published: 5 May 2017 Abstract: In areas lacking potable water treatment, drinking contaminated water may represent a public health threat. In addition to enteropathogenic bacteria and parasites, fecal contamination in water environments is associated with the transmission of enteric viruses and other causal agents of infectious disease. Rotavirus and norovirus are the main enteric viral agents responsible for diarrheic outbreaks. The aim of the present study was to detect seasonal variation of rotavirus and norovirus in the surface water at Bassaseachic Falls National Park during 2013. Rivers and streams within and nearby this park were sampled once in each season during 2013. Viral concentration was carried out by a handmade filtration equipment, using a commercial electropositive membrane coupled with the virus absortion elution technique (VIRADEL©). Detection of rotavirus and norovirus was performed by SYBR Green reverse transcription-real time polymerase chain reaction (SYBR GREEN© RT-qPCR) analyses. Norovirus genogroup II was detected in samples collected in June and October 2013. In the case of rotavirus, genogroup A was detected in March and June. The presence of rotavirus and norovirus was related to viral acute diarrhea in children less than five years of age, who were inhabiting the sampled areas. This may indicates that the contaminated water was potentially a risk factor for regional diarrheic outbreaks. Keywords: norovirus; rotavirus; surface water; VIRADEL; virus detection; environment 1. Introduction Viral gastroenteritis outbreaks are associated with water contamination due to wastewater containing the viral particles, which is discharged in surface waters and rivers. Infectious agents can be spread in this way, particularly during periods of low flow [1,2]. Although the number of viral particles in the surface water is very low, ten viral particles are sufficient for a healthy individual to be infected [3,4]. Int. J. Environ. Res. Public Health 2017, 14, 482; doi:10.3390/ijerph14050482 www.mdpi.com/journal/ijerph Int. J. Environ. Res. Public Health 2017, 14, 482 2 of 11 Bassaseachic Falls National Park is located in the western side of the state of Chihuahua, Mexico, in the Sierra Madre Occidental. Basaseachi Waterfall is the main flowing part of the Basaseachi and DuraznoInt. J. Environ. micro-basins. Res. Public Health 2017 This, 14, 482 park is a natural, protected area that is considered2 aof 12 unique ecosystem, with endemic flora and wildlife species. Environmental conditions favor the development Bassaseachic Falls National Park is located in the western side of the state of Chihuahua, Mexico, of a forestin the ecosystem Sierra Madre in theOccidental. highest Basaseachi areas, whereas Waterfal inl loweris the main areas, flowing such aspart “Barranca of the Basaseachi de Candameña”, and the ecosystemDurazno micro-basins. is that of jungle This park vegetation. is a natural, Bassaseachic protected area Falls that Nationalis considered park a unique has peculiar ecosystem, climatic ◦ characteristicswith endemic as aflora result and ofwildlife the latitudespecies. Environmen and altitude,tal conditions with temperatures favor the development ranging of from a forest 26 C to 16 ◦C.ecosystem There is frostyin the weatherhighest areas, from Octoberwhereas in to lower May, whileareas, theresuch as is snowy“Barranca weather de Candameña”, from November the to Marchecosystem [5]. is that of jungle vegetation. Bassaseachic Falls National park has peculiar climatic Itcharacteristics is usually difficult as a result to detectof the latitude viruses and in altitude, water samples with temperatures becauseof ranging their veryfrom 26 low °C concentrationto 16 °C. There is frosty weather from October to May, while there is snowy weather from November to March and the presence of inhibitors, such as humic and fulvic acid, polysaccharides, bacterial debris, [5]. nucleases and metal ions that make it difficult to extract RNA. For this reason, the detection of It is usually difficult to detect viruses in water samples because of their very low concentration virusesand in waterthe presence requires of specificinhibitors, methods such as involving humic and viral fulvic particle acid, polysaccharides, concentration, suchbacterial as ultrafiltration. debris, Largenucleases water volumes and metal (100–1000 ions that make L) usually it difficult need to extract to be RNA. processed. For this reason, Ultrafiltration the detection techniques of viruses with electropositivein water requires commercial specificmembranes, methods involving coupled viral withparticle a SYBRconcentration, Green reversesuch as ultrafiltration. transcription-real Large time polymerasewater chainvolumes reaction (100–1000 (RT-qPCR) L) usually assay need are inexpensiveto be processed. and useful Ultrafiltrat to amplifyion techniques genes for with detecting low viruselectropositive concentrations commercial [6–8 ].membranes, Using this coupled method, with in a recentSYBR Green years, reverse more transcription-real than 100 types oftime viruses that canpolymerase be transmitted chain reaction to humans (RT-qPCR) have assay been are reported inexpensive in contaminatedand useful to amplify waters, genes such for asdetecting adenovirus low virus concentrations [6–8]. Using this method, in recent years, more than 100 types of viruses (AdV), rotavirus (RV), norovirus (NV) and hepatitis virus (HepV) [9]. RV and NV are the major that can be transmitted to humans have been reported in contaminated waters, such as adenovirus etiological(AdV), agents rotavirus responsible (RV), norovirus for the (NV) known and cases hepatitis of viral virus gastroenteritis (HepV) [9]. RV worldwide and NV are [ 10the]. major The aim of the presentetiological study agents was responsible to detect for RV the and known NV ascases well of viral as their gastroenteritis concentration worldwide variations [10]. The in aim the of surface waterthe ofBassaseachic present study Fallswas to National detect RV Park and duringNV as well the as seasons their concentration in 2013. variations in the surface water of Bassaseachic Falls National Park during the seasons in 2013. 2. Experimental Section 2. Experimental Section 2.1. Collection of Samples 2.1. Collection of Samples The sites sampled, as previously determined by the Mexican governmental agency “Statistics and GeographyThe National sites sampled, Institute” as previously (Instituto determined Nacional deby Estadthe Mexicanística ygovernmental Geografía—INEGI), agency “Statistics are shown in and Geography National Institute” (Instituto Nacional de Estadística y Geografía—INEGI), are Figure1. shown in Figure 1. Figure 1. Bassaseachic Falls National Park geographical area. The numbered circles indicate the Figuresampling 1. Bassaseachic sites. Source: Falls INEGI National digital Park map, geographical Cartographic Package area. The 2010; numbered Scale 1:41062. circles Samples indicate 5 the sampling(28°10 sites.′47.45 Source:″N, 108°12 INEGI′45.49″W) digital and 6 map, (28°12 Cartographic′40.80″N, 108°13 Package′20.49″W) 2010; during Scale June 1:41062. were missing, Samples 5 ◦ 0 00 ◦ 0 00 ◦ 0 00 ◦ 0 00 (28 10while47.45 sampleN, 108 1312 45.49during W)March and 6was (28 12also40.80 missingN, 108(28_10127.36”N,13 20.49 W) 108_12144.97”W). during June were See missing, while sampleSupplementary 13 during Material March Table was S1 also for missingsampling (28_10127.36 site names. 00 N, 108_12144.9700 W). See Supplementary Materials Table S1 for sampling site names. Int. J. Environ. Res. Public Health 2017, 14, 482 3 of 11 In Bassaseachic Falls National Park, we selected 13 sampling points located near rural settlements which may drain their sewage into the surface waters. In order to detect enteric viruses in the water, 1 L samples were collected in UV-light sterile polypropylene bottles [11] during March (spring conditions), June (drought conditions), October (raining conditions) and December (winter conditions) in 2013.
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