First report of contamination of public water system by Giardia duodenalis and Cryptosporidium spp. in Bahia, northeastern Brazil
DOI:
https://doi.org/10.5433/1679-0359.2024v45n1p111Keywords:
Contaminated water, Water potability, Protozoa, Public Health, Watersheds.Abstract
Waterborne diseases such as cryptosporidiosis and giardiasis are among the leading public health problems worldwide because these protozoa are more resistant to water disinfection methods. This study aimed to evaluate the presence of oocysts of Cryptosporidium spp. and cysts of Giardia spp. in samples of raw and treated water. During one year, 24 raw and treated water samples were collected from the public water supply system in Canavieiras, Bahia, Brazil. Cysts and oocysts were concentrated using membrane filtration and visualized through Direct immunofluorescence assay (DFA). DNA isolated with a commercial kit was subjected to nested PCR (nPCR). The DFA obtained a better result than the nPCR in detecting both protozoa. By DFA, Cryptosporidium spp. was present in 25% (6/24) of the raw water and 4.2% (1/24) of the treated water samples. Giardia spp. was detected in 41.6% (10/24) of the raw water and 16.6% (4/24) of the treated water samples. In nPCR, Giardia spp. was detected in treated and raw water at 16.6% (4/24) and 16.6% (4/24), respectively. Cryptosporidium spp. was detected in raw water at 8.3% (2/24). The DFA and nPCR results differed despite the molecular analysis having greater sensitivity. Many inhibitors in the samples may have influenced the result. The physicochemical parameters pH and turbidity were not under the standards established by the legislation. In raw water, microbiological parameters were above the required legal standard. Precipitation and pH correlated with Cryptosporidium nPCR results in raw water. The presence of these protozoa in the water samples constitutes a potential risk for transmitting diarrheal diseases to this municipality's human and animal populations.
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Almeida, J. C., Martins, F. D. C., Ferreira, J. M., Neto, Santos, M. M. D., Garcia, J. L., Navarro, I. T., Kuroda, E. K., & Freire, R. L. (2015). Occurrence of Cryptosporidium spp. and Giardia spp. in a public water-treatment system, Paraná, Southern Brazil. Revista Brasileira de Parasitologia Veterinária, 24 (3), 303-308. doi: 10.1590/S1984-29612015051
Appelbee, A. J., Frederick, L. M., Heitman, T. L., & Olson, M. E. (2003). Prevalence and genotyping of Giardia duodenalis from beef calves in Alberta, Canada. Veterinary Parasitology, 112(4), 289-294. doi: 10.1016/S0304-4017(02)00422-3
Atherholt, T. B., LeChevallier, M. W., Norton, W. D., & Rosen, J. S. (1998). Effect of rainfall on Giardia and Crypto. Journal‐American Water Works Association, 90 (9), 66-80. doi: 10.1002/j.1551-8833.1998.tb08499.x
Ayres, M., Ayres, M., Jr., Ayres, D. L., & Santos, A. D. (2007). Bio Estat 5.0: aplicações estatística nas áreas das ciências biológicas e médicas. Monografia em Português, Sociedade Civil Mamirauá Belém, PA, Brasil.
Baldursson, S., & Karanis, P. (2011). Waterborne transmission of protozoan parasites: review of worldwide outbreaks-an update 2004-2010. Water Research, 45(20), 6603-6614. doi: 10.1016/j.watres.2011.10.013
Beatty, J. K., Akierman, S. V., Motta, J. P., Muise, S., Workentine, M. L., Harrison, J. J., Bhargava, A., Beck, P. L., Rioux, K. P., Mcknight, G. W., Wallace, J. L., & Buret, A. G. (2017). Giardia duodenalis induces pathogenic dysbiosis of human intestinal microbiota biofilms. International Journal for Parasitology, 47(6), 311-326. doi: 10.1016/j.ijpara.2016.11.010
Boni, D. M. (2016). Avaliação da viabilidade de cistos de Giardia spp. e oocistos de Cryptosporidium parvum em água filtrada obtida após tratamento convencional com flotação e ozonização. Tese de doutorado, Universidade de São Paulo, São Paulo, SP, Brasil.
Borja-Serrano, P., Ochoa-Herrera, V., Maurice, L., Morales, G., Quilumbaqui, C., Tejera, E., & Machado, A. (2020). Determination of the microbial and chemical loads in rivers from the Quito capital province of Ecuador (Pichincha)—A preliminary analysis of microbial and chemical quality of the main rivers. International Journal of Environmental Research and Public Health, 17(14), 5048. doi: 10.3390 ijerph17145048
Branco, N., Leal, D. A. G., & Franco, R. M. B. (2012). A parasitological survey of natural water springs and inhabitants of a tourist city in southeastern Brazil. Vector-Borne and Zoonotic Diseases, 12(5), 410-417. doi: 10.1089/vbz.2011.0679
Brandão, M. L. L., Oliveira Rosas, C. de, Mello Medeiros, V. de, Warnken, M. B., Bricio, S. M. L., Silva, A. M. L. da, & Azeredo, D. R. P. (2012). Comparação das técnicas do número mais provável (NMP) e de filtração em membrana na avaliação da qualidade microbiológica de água mineral natural. Revista do Instituto Adolfo Lutz, 71(1), 32-39. doi: 10.53393/rial.2012.v71.32387
Buret, A. G., Cacciò, S. M., Favennec, L., & Svärd, S. (2020). Update on Giardia: highlights from the seventh International Giardia and Cryptosporidium Conference. Parasite, 27(49), 1-7. doi: 10.1051/parasite/2020047
Cantusio, R., Neto, & Bueno Franco, R. M. B. (2004). Ocorrência de oocistos de Cryptosporidium spp. e cistos de Giardia spp. em diferentes pontos do processo de tratamento de água em Campinas, São Paulo, Brasil. Tese de Doutorado. Universidade Estadual de Campinas.
Cantusio, R., Neto, Santos, L., Sato, M., & Franco, R. (2010). Cryptosporidium spp. and Giardia spp. in samples of natural water from the Atibaia River, city of Campinas, São Paulo, Brazil. Water Science Technology, 62(1), 217-222. doi: 10.2166/wst.2010.312
Carmena, D., Aguinagalde, X., Zigorraga, C., Fernández‐Crespo, J. C., & Ocio, J. A. (2007). Presence of Giardia cysts and Cryptosporidium oocysts in drinking water supplies in northern Spain. Journal of Applied Microbiology, 102(3), 619-629. doi: 10.1111/j.1365-2672.2006.03193.x
Centers for Disease Control and Prevention (2023). DPDx. Laboratory diagnosis of Giardiasis. https://www.cdc.gov/dpdx/resources/pdf/benchAids/Giardia_benchaid.pdf.
Coelho, C. H., Durigan, M., Leal, D. A. G., Schneider, A. D. B., Franco, R. M. B., & Singer, S. M. (2017). Giardiasis as a neglected disease in Brazil: Systematic review of 20 years of publications. PLoS Neglected Tropical Diseases, 11(10), e0006005. doi: 10.1371/journal.pntd.0006005
Costa, C. F. S. D., & Mendoza-Sassi, R. A. (2007). Identificação de patógenos humanos nas águas que margeiam a cidade do Rio Grande/RS. http://repositorio.furg.br/handle/1/1533.
Curriero, F. C., Patz, J. A., Rose, J. B., & Lele, S. (2001). The association between extreme precipitation and waterborne disease outbreaks in the United States, 1948-1994. American Journal of Public Health, 91(8), 1194-1199. doi: 10.2105/AJPH.91.8.1194
Davies, C. M., Ferguson, C. M., Kaucner, C., Krogh, M., Altavilla, N., Deere, D. A., & Ashbolt, N. J. (2004). Dispersion and transport of Cryptosporidium oocysts from fecal pats under simulated rainfall events. Applied and Environmental Microbiology, 70(2), 1151-1159. doi: 10.1128/AEM.70.2.1151-1159.2004
Dias, G. M. F., Bevilacqua, P. D., Bastos, R. K. X., Oliveira, A. A., & Campos, G. M. M. (2008). Giardia spp. and Cryptosporidium spp. in a fresh water supply source contaminated with human and animal excreta and waste water. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 60(6), 1291-1300. doi: 10.1590/S0102-09352008000600001
Dorny, P., Praet, N., Deckers, N., & Gabriël, S. (2009). Emerging food-borne parasites. Veterinary Parasitology, 163(3), 196-206. doi: 10.1016/j.vetpar.2009.05.026
Empresa Baiana de Águas e Saneamento (2015). Sistema de abastecimento de água do município de Canavieiras- Análise da água. EMBASA. http://www.embasa.ba.gov.br/content/Analise-da-água
Fayer, R., Dubey, J. P., & Lindsay, D. S. (2004). Zoonotic protozoa: from land to sea. Trends in Parasitology, 20(11), 531-536. doi: 10.1016/j.pt.2004.08.008
Fayer, R., Morgan, U., & Upton, S. J. (2000). Epidemiology of Cryptosporidium: transmission, detection and identification. International Journal for Parasitology, 30(12-13), 1305-1322. doi: 10.1016/S0020-7519(00)00135-1
Feng, Y., & Xiao, L. (2011). Zoonotic potential and molecular epidemiology of Giardia species and Giardiasis. Clinical Microbiology Reviews, 24(1), 110-140. doi: 10.1128/CMR.00033-10
Franco, R. M. B., Branco, N., & Leal, D. A. G. (2012b). Parasitologia ambiental: métodos de concentração e detecção de Cryptosporidium spp. e Giardia spp. em amostras de água. Revista de Patologia Tropical/Journal of Tropical Pathology, 41(2), 119-135. doi 10.5216/rpt.v41i2.19320
Franco, R. M. B., Hachich, E. M., Sato, M. I. Z. S., Naveira, R. M. L., Silva, E. D. C., Campos, M. M. D. C., Cantusio, R. Neto, Cerqueira D. A., Nilson B., & Leal, D. A. G. (2012a). Avaliação da performance de metodologias de detecção de Cryptosporidium spp. e Giardia spp. em água destinada ao consumo humano, para o atendimento às demandas da Vigilância em Saúde Ambiental no Brasil. Epidemiologia e Serviços de Saúde, 21(2), 233-242. doi:. 10.5123/S1679-49742012000200006
Franco, R. M. B., Rocha-Eberhardt, R., & Cantusio, R., Neto. (2001). Occurrence of Cryptosporidium oocysts and Giardia cysts in raw water from the Atibaia River, Campinas, Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 43(2), 109-111. doi: 10.1590/S0036-46652001000200011
Freitas, D. A. D., Paiva, A. L. R. D., Carvalho, J. A. A. D., Fº., Cabral, J. J. D. S. P., & Rocha, F. J. S. (2015). Occurrence of Cryptosporidium spp., Giardia spp., and other pathogenic intestinal parasites in the Beberibe River in the State of Pernambuco, Brazil. Revista da Sociedade Brasileira de Medicina Tropical, 48(1), 220-223. doi: 10.1590/0037-8682-0174-2014
Fundo das Nações Unidas para a Infância (2017). 7,000 newborns die every day, despite a steady decrease in under-five mortality, a new report says. UNICEF. https://www.unicef.org/media/media_101066.html
Grecca, M., Thomaz-Soccol, V., Ribeiro, M. C. C., Truppel, J. H., Pereira, J. T., & Osaki, S. C. (2013). Occurrence of Cryptosporidium sp. in dogs and cats from Curitiba and its metropolitan area. Archives of Veterinary Science, 18 (3), 1-6. doi: 10.5380/avs.v18i3.29522
Grott, S. C., Hartmann, B., Silva, H. H. da, Fº., Franco, R. M. B., & Goulart, J. A. G. (2016). Detection of Giardia spp. cysts and Cryptosporidium spp. oocysts in untreated water collected from treatment plants in Blumenau, Santa Catarina State, Brazil. Ambiente e Agua-An Interdisciplinary Journal of Applied Science, 11(3), 689-701. doi: 10.4136/1980-993X
Hachich, E. M., Sato, M. I. Z., Galvani, A. T., Menegon, J. R. N., & Mucci, J. L. N. (2004). Giardia and Cryptosporidium in source waters of Sao Paulo state, Brazil. Water Science and Technology, 50(1), 239-245. doi: 10.2166/wst.2004.0061
Harvey, T. V., Tang, A. M., Paixao Sevá, A. da, Albano dos Santos, C., Santos Carvalho, S. M., Magalhaes da Rocha, C. M. B., Oliveira, B. C M., & Albuquerque, G. R. (2020). Enteric parasitic infections in children and dogs in resource-poor communities in northeastern Brazil: identifying priority prevention and control areas. PLoS Neglected Tropical Diseases, 14(6), e0008378. doi: 10.1371/journal.pntd.0008378
Hopkins, R. M., Meloni, B. P., Groth, D. M., Wetherall, J. D., Reynoldson, J. A., & Thompson, R. A. (1997). Ribosomal RNA sequencing reveals differences between the genotypes of Giardia isolates recovered from humans and dogs living in the same locality. The Journal of Parasitology, 83(1), 44-51. doi: 10.2307/3284315
Ignacio, C. F., Silva, M. E. C. D., Handam, N. B., Alencar, M. D. F. L., Sotero-Martins, A., Barata, M. M. D. L., & Moraes, A. H. A. D. (2017). Socioenvironmental conditions and intestinal parasitic infections in Brazilian urban slums: a cross-sectional study. Revista do Instituto de Medicina Tropical de São Paulo, 59 e56, 1-10. doi: 10.1590/S1678-9946201759056
Instituto Brasileiro de Geografia e Estatística (2010). Censo demográfico. http://www.ibge.gov.br/cidades/topwindow.htm?1
Instituto Brasileiro de Geografia e Estatística (2017). Divisão regional do Brasil em regiões geográficas imediatas e regiões geográficas intermediárias 2017. Coordenação de Geografia. https://www.ibge.gov. br/apps/regioes_geograficas/
Ithoi, I. (2009). Occurrence of Giardia and Cryptosporidium (oo) cysts in the river water of two recreational areas in Selangor, Malaysia. Tropical Biomedicine, 26(3), 289-302. doi: 20237443
Karanis, P., Kourenti, C., & Smith, H. (2007). Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learned. Journal of Water and Health, 5(1), 1-38. doi: 10.2166/wh.2006.002
Kumar, T., Majid, M. A. A., Onichandran, S., Jaturas, N., Andiappan, H., Salibay, C. C., Tabo, H. A. L., Tabo, N., Dungca, J. Z., Tangpong, J., Phiriyasamith, S., Yuttayong, B., Polseela, R., Do, B. N., Sawangjaroen, N., Tan, T.-C., Lim, Y. A. L., & Nissapatorn, V. (2016). Presence of Cryptosporidium parvum and Giardia lamblia in water samples from Southeast Asia: towards an integrated water detection system. Infectious Diseases of Poverty, 5(3), 1-12. doi 10.1186/s40249-016-0095-z
Ligda, P., Claerebout, E., Kostopoulou, D., Zdragas, A., Casaert, S., Robertson, L. J., & Sotiraki, S. (2020). Cryptosporidium and Giardia in surface water and drinking water: animal sources and towards the use of a machine-learning approach as a tool for predicting contamination. Environmental Pollution, 264, 114766. doi: 10.1016/j.envpol.2020.114766
Mackinnon, A. A. (2000). Spreadsheet for the calculation of comprehensive statistics for the assessment of diagnostic tests and inter-rater agreement. Computers in Biology and Medicine, 30(3), 127-34. doi: 10.1016/S0010-4825(00)00006-8
Mariano, A. P. M., Santos, E. N., Santos, T. D., Mota, T. N., Silva, J. A., Carvalho, S. M. S., & Silva, M. F. (2015). Parasites in South Bahia: focus on Giardiasis and ascariasis among preschoolers of Itabuna. International Journal of Health Sciences, 3(1), 61-75. doi: 10.15640/ijhs.v3n1a4
Ministério da Saúde (2011). Portaria nº 2914/2011: Dispõe sobre os procedimentos de controle e de vigilância da qualidade da água para consumo humano e seu padrão de potabilidade. MS.
Ministério da Saúde (2014). Manual de controle da qualidade da água para técnicos que trabalham em ETAS. MS. www.funasa.gov.br/site/wp...mf/manualcont_quali_agua_tecnicos_trab_emetas.pdf
Muniz Neta, E de S., Sampaio, D. C., Galvão, G. da S., & Munhoz, A. D. (2010). Cryptosporidium oocysts (Apicomplexa: Criptosporidiidae) in dairy cattle of an endemic area at microregion of Ilheus-Itabuna in the State of Bahia, Brazil. Revista Brasileira de Medicina Veterinária, 32(2), 75-78. https://bjvm.org.br/BJVM/article/view/842
Niehaus, M. D., Moore, S. R., Patrick, P. D., Derr, L. L., Lorntz, B., Lima, A. A., & Guerrant, R. L. (2002). Early childhood diarrhea is associated with diminished cognitive function 4 to 7 years later in children in a northeast Brazilian shantytown. The American Journal of Tropical Medicine and Hygiene, 66(5), 590-593. Doi: 10.4269/ajtmh.2002.66.590
Olson, M. E., Goh, J., Philips, M., Guselle, N., & McAllister, T. A. (1999). Giardia cyst and cryptosporidium oocyst survival in water, soil, and cattle feces. Journal of Environmental Quality 28(6), 1991-1996. doi: 10.2134/jeq1999.00472425002800060040x
Onichandran, S., Kumar, T., Salibay, C. C., Dungca, J. Z., Tabo, H. A., Tabo, N., Tian-Chye Tan, Lim, Y. A. L., Sawangjaroen, N., Phiriyasamith, S., Andiappan, H., Ithoi, I., Lau, Y.-L., & Nissapatorn, V. (2014). Waterborne parasites: a current status from the Philippines. Parasites & Vectors, 7(244), 1-8. doi: 10.1186/1756-3305-7-244
Pacheco, F. T. F., Silva, R. K. N. R., Mendes, A. V. A., Mendonça, N., Ribeiro, T. C. M., Soares, N. M., & Teixeira, M. C. A. (2014). Infecção por Giardia duodenalis e outros enteroparasitos em crianças com câncer e crianças de creche em Salvador, Bahia. Revista de Ciências Médicas e Biológicas 13(3), 280-286. https://repositoriodev.ufba.br/handle/ri/23176
Pessoa, J. O., Orrico, S. R. M., & Lordêlo, M. S. (2018). Qualidade da água de rios em cidades do Estado da Bahia. Engenharia Sanitária e Ambiental, 23(4), 687-696. doi: 10.1590/S1413-41522018166513
Prado, M. D. S., Cairncross, S., Strina, A., Barreto, M. L., Oliveira-Assis, A. M., & Rego, S. (2005). Asymptomatic Giardiasis and growth in young children; a longitudinal study in Salvador, Brazil. Parasitology, 131(1), 51-56. doi: 10.1017/S0031182005007353
Redlinger, T., Corella-Barud, V., Graham, J., Galindo, A., Avitia, R., & Cardenas, V. (2002). Hyperendemic Cryptosporidium and Giardia in households lacking municipal sewer and water on the United States-Mexico border. American Journal of Tropical Medicine and Hygiene, 66(6), 794-798. doi: 10.4269/ajtmh.2002.66.794
Ribeiro, L. A., Santos, L. K., Brito, P. A., Jr., Maciel, B. M., Silva, A. V. da, & Albuquerque, G. R. (2015). Detection of Toxoplasma gondii DNA in Brazilian oysters (Crassostrea rhizophorae). Genetics and Molecular Research, 14(2), 4658-4665. doi: 10.4238/2015.May.4.25
Rose, J. B., Darbin, H., & Gerba, C. P. (1988). Correlations of the protozoa, Cryptosporidium, and Giardia, with water quality variables in a watershed. Water Science and Technology, 20(11-12), 271-276. doi: 10.2166/wst.1988.0295
Ryan, U., & Cacciò, S. M. (2013). Zoonotic potential of Giardia. International Journal for Parasitology, 43(12-13), 943-956. doi: 10.1016/j.ijpara.2013.06.001
Santin, M. (2020). Cryptosporidium and Giardia in ruminants. Veterinary Clinics of North America: Food Animal Practice, 36(1), 223-238. doi: 10.1016/j.cvfa.2019.11.005
Santos, S. F., Silva, H. D., Souza, E. S., Jr., Anunciação, C. E., Silveira-Lacerda, E. P., Vilanova-Costa, C. A., & Garcíazapata, M. T. (2010). Environmental monitoring of opportunistic protozoa in rivers and lakes in the neotropics based on yearly monitoring. Water Quality, Exposure and Health, 2(2), 97-104. doi 10.1007/s12403-010-0027-2
Sato, M. I. Z., Galvani, A. T., Padula, J. A., Nardocci, A. C., Souza Lauretto, M. de, Razzolini, M. T. P., & Hachich, E. M. (2013). Assessing the infection risk of Giardia and Cryptosporidium in public drinking water delivered by surface water systems in Sao Paulo State, Brazil. Science of the Total Environment, 442, 389-396. doi: 10.1016/j.scitotenv.2012.09.077
Secretaria da Saúde (2019). Departamento de vigilância epidemiológica. Boletim epidemiológico perfil das doenças diarreicas agudas Bahia. Nº 01. SESAB. http://www.saude.ba.gov.br/wp-content/uploads/2017/11/ boletimDDA_n%C2%BA-01_2019.pdf
Thompson, R. C. A., & Ash, A. (2016). Molecular epidemiology of Giardia and Cryptosporidium infections. Infection, Genetics, and Evolution, 40, 315-323. doi: 10.1016/j.meegid.2015.09.028
Thompson, R. C. A., & Smith, A. (2011). Zoonotic enteric protozoa. Veterinary Parasitology, 182(1), 70-78. doi: 10.1016/j.vetpar.2011.07.016
Thompson, R. C. A., Palmer, C. S., & O’Handley, R. (2008). The public health and clinical significance of Giardia and Cryptosporidium in domestic animals. The Veterinary Journal, 177(1), 18-25. doi: 10.1016/j.tvjl.2007.09.022
Toledo, R. D. S., Martins, F. D. C., Ferreira, F. P., Almeida, J. C. de, Ogawa, L., Santos, H. L. E. P. L. dos, Santos, M. M., Pinheiro, F. A., Navarro, I. T., & Freire, R. L. (2017). Cryptosporidium spp. and Giardia spp. in feces and water and the associated exposure factors on dairy farms. PLoS One, 12(4), e0175311. doi: 10.1371/journal.pone.0175311
United States Environmental Protection Agency (2005). Method 1623: Cryptosporidium and Giardia in Water by Filtration/IMS/FA. USEPA. www.epa.gov/ microbes/documents/1623de05.pd
Vermeulen, L. C., van Hengel, M., Kroeze, C., Medema, G., Spanier, J. E., van Vliet, M. T., & Hofstra, N. (2019). Cryptosporidium concentrations in rivers worldwide. Water Research, 149, 202-214. doi: 10 1016/j.watres.2018.10.069.
Widmer, G., Carmena, D., Kváč, M., Chalmers, R. M., Kissinger, J. C., Xiao, L., Sateriale, A., Striepen, B., Laurent, F., Lacroix-Lamandé, S., Gargala, G., & Favennec, L. (2020). Update on Cryptosporidium spp.: highlights from the Seventh International Giardia and Cryptosporidium Conference. Parasite, 27(14), 1-10. doi: 10.1051/parasite/2020011
World Health Organization (2009). Water, sanitation, and health team. Risk assessment of Cryptosporidium in drinking water. WHO. https://apps.who.int/iris/handle/10665/70117
World Health Organization (2013). Ending preventable child deaths from Pneumonia and Diarrhea by 2025: Global Action Plan for Prevention and Control of Pneumonia and Diarrhoea. WHO. https://www.who.int/maternal_child_adolescent/documents/global_action_plan_pneumonia_diarrhoea/en/
Xavier, R. P., Siqueira, L. P., Vital, F. A. C., Rocha, F. J. S., Irmão, J. I., & Calazans, G. M. T. (2011). Microbiological quality of drinking rainwater in the inland region of Pajeú, Pernambuco, Northeast Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 53(3), 121-124. doi: 10.1590/S0036-46652011000300001
Xiao, L., Morgan, U. M., Limor, J., Escalante, A., Arrowood, M., Shulaw, W., Thompson, R. C. A., Ronald Fayer, & Lal, A. A. (1999). Genetic diversity within Cryptosporidium parvum and related Cryptosporidium species. Applied and Environmental Microbiology, 65(8), 3386-3391. doi: 10.1128/AEM.65.8.3386-3391.1999
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