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Current Challenges of Streptococcus Infection and Effective Molecular, Cellular, and Environmental Control Methods in Aquaculture

  • Mishra, Anshuman (Institute of Systems Biology, Pusan National University) ;
  • Nam, Gyu-Hwi (Institute of Systems Biology, Pusan National University) ;
  • Gim, Jeong-An (Institute of Systems Biology, Pusan National University) ;
  • Lee, Hee-Eun (Institute of Systems Biology, Pusan National University) ;
  • Jo, Ara (Institute of Systems Biology, Pusan National University) ;
  • Kim, Heui-Soo (Institute of Systems Biology, Pusan National University)
  • Received : 2017.08.02
  • Accepted : 2018.04.02
  • Published : 2018.06.30

Abstract

Several bacterial etiological agents of streptococcal disease have been associated with fish mortality and serious global economic loss. Bacterial identification based on biochemical, molecular, and phenotypic methods has been routinely used, along with assessment of morphological analyses. Among these, the molecular method of 16S rRNA sequencing is reliable, but presently, advanced genomics are preferred over other traditional identification methodologies. This review highlights the geographical variation in strains, their relatedness, as well as the complexity of diagnosis, pathogenesis, and various control methods of streptococcal infections. Several limitations, from diagnosis to control, have been reported, which make prevention and containment of streptococcal disease difficult. In this review, we discuss the challenges in diagnosis, pathogenesis, and control methods and suggest appropriate molecular (comparative genomics), cellular, and environmental solutions from among the best available possibilities.

Keywords

References

  1. Abdelsalam, M., Chen, S.-C., and Yoshida, T. (2010). Dissemination of streptococcal pyrogenic exotoxin G (spegg) with an IS-like element in fish isolates of Streptococcus dysgalactiae. FEMS Microbiol. Lett. 309, 105-113.
  2. Abdelsalam, M., Asheg, A., and Eissa, A.E. (2013). Streptococcus dysgalactiae: An emerging pathogen of fishes and mammals. Int. J. Vet. Sci. Med. 1, 1-6. https://doi.org/10.1016/j.ijvsm.2013.04.002
  3. Achtman, M. (2008). Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu. Rev. Microbiol. 62, 53-70. https://doi.org/10.1146/annurev.micro.62.081307.162832
  4. Agnew, W., and Barnes, A.C. (2007). Streptococcus iniae: an aquatic pathogen of global veterinary significance and a challenging candidate for reliable vaccination. Vet. Microbiol. 122, 1-15. https://doi.org/10.1016/j.vetmic.2007.03.002
  5. Al-Harbi, A.H. (2011). Molecular characterization of Streptococcus iniae isolated from hybrid tilapia (Oreochromis $niloticus^x$ Oreochromis aureus). Aquaculture 312, 15-18. https://doi.org/10.1016/j.aquaculture.2010.12.014
  6. Aguilera, S.E., Cole, J., Finkbeiner, E.M., Cornu, E.L., Ban, N.C., Carr, M.H., Cinner, J.E., Crowder, L.B., Gelcich, S., Hicks, C.C., et al. (2015). Managing small-scale commercial fisheries for adaptive capacity: insights from dynamic social-ecological drivers of change in monterey bay. PLoS One 10, e0118992. https://doi.org/10.1371/journal.pone.0118992
  7. Austin, B., and Austin, D.A. (2007). Bacterial fish pathogens: disease of farmed and wild fish. Springer Science & Business Media.
  8. Baeck, G.W., Kim, J.H., Gomez, D.K., and Park, S.C. (2006). Isolation and characterization of Streptococcus sp. from diseased flounder (Paralichthys olivaceus) in Jeju Island. J. Vet. Sci. 7, 53-58. https://doi.org/10.4142/jvs.2006.7.1.53
  9. Barnes, A.C., and Ellis, A.E. (2004). Role of capsule in serotypic differences and complement fixation by Lactococcus garvieae. Fish Shellfish Immunol. 16, 207-214. https://doi.org/10.1016/S1050-4648(03)00079-2
  10. Barnes, A.C., Guyot, C., Hansen, B.G., Mackenzie, K., Horne, M.T., and Ellis, A.E. (2002). Resistance to serum killing may contribute to differences in the abilities of capsulate and non-capsulated isolates ofLactococcus garvieae to cause disease in rainbow trout (Oncorhynchus mykiss L.). Fish Shellfish Immunol. 12, 155-168. https://doi.org/10.1006/fsim.2001.0361
  11. Barnett, T.C., Cole, JN., Rivera-Hernandez, T., Henningham, A., Paton, J.C., Nizet, V., and Walker, M.J. (2015). Streptococcal toxins: role in pathogenesis and disease. Cell Microbiol. 17, 1721-1741. https://doi.org/10.1111/cmi.12531
  12. Bennedsen, M., Stuer-Lauridsen, B., Danielsen, M., and Johansen, E. (2011). Screening for antimicrobial resistance genes and virulence factors via genome sequencing. Appl. Environ. Microbiol. 77, 2785-2787. https://doi.org/10.1128/AEM.02493-10
  13. Bondad-Reantaso, M.G., Subasinghe, R.P., Arthur, J.R., Ogawa, K., Chinabut, S., Adlard, R., Tan, Z., and Shariff, M. (2005). Disease and health management in Asian aquaculture. Vet. Parasitol. 132, 249-272. https://doi.org/10.1016/j.vetpar.2005.07.005
  14. Bosshard, P.P., Zbinden, R., Abels, S., Boddinghaus, B., Altwegg, M., and Bottger, E.C. (2006). 16S rRNA gene sequencing versus the API 20 NE system and the VITEK 2 ID-GNB card for identification of nonfermenting Gram-negative bacteria in the clinical laboratory. J. Clin. Microbiol. 44, 1359-1366. https://doi.org/10.1128/JCM.44.4.1359-1366.2006
  15. Brimil, N., Barthell, E., Heindrichs, U., Kuhn, M., Lutticken, R., and Spellerberg, B. (2006). Epidemiology of Streptococcus agalactiae colonization in Germany. Int. J. Med. Microbiol. 296, 39-44.
  16. Bromage, E.S., Thomas, A., and Owens, L. (1999). Streptococcus iniae, a bacterial infection in barramundi Lates calcarifer. Dis. Aquat. Organ. 36, 177-181. https://doi.org/10.3354/dao036177
  17. Buchanan, J.T., Colvin, K.M., Vicknair, M.R., Patel, S.K., Timmer, A.M., and Nizet, V. (2008). Strain-associated virulence factors of Streptococcus iniae in hybrid-striped bass. Vet. Microbiol. 131, 145-153. https://doi.org/10.1016/j.vetmic.2008.02.027
  18. Carson, J., Gudkovs, N., and Austin, B. (1993). Characteristics of an Enterococcus-like bacterium from Australia and South Africa, pathogenic for rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 16, 381-388. https://doi.org/10.1111/j.1365-2761.1993.tb00871.x
  19. Carey-Ann, D., Burnhama, and Gregory, J.T. (2003). Virulence factors of group B streptococci. Rev. Med. Microbiol. 14, 109-118. https://doi.org/10.1097/00013542-200310000-00002
  20. Chain, P.S., Grafham, D.V., Fulton, R.S., Fitzgerald, M.G., Hostetler, J., Muzny, D., Ali, J., Birren, B., Bruce, D.C., Buhay, C., et al. (2009). Genomics. Genome project standards in a new era of sequencing. Science 326, 236-237. https://doi.org/10.1126/science.1180614
  21. Chang, P., and Plumb, J. (1996). Effects of salinity on Streptococcus infection of Nile tilapia, Oreochromis niloticus. J. Appl. Aquaculture. 6, 39-45.
  22. Cheng, S., Hu, Y.H., Jiao, X.D., and Sun, L. (2010). Identification and immunoprotective analysis of a Streptococcus iniae subunit vaccine candidate. Vaccine 28, 2636-2641. https://doi.org/10.1016/j.vaccine.2010.01.016
  23. Chettri, J.K., Raida, M.K., Holten-Andersen L., Kania, P.W., and Buchmnann, K. (2011). PAMP induced expression of immune relevant genes in head kidney leukocytes of rainbow trout (Oncorhynchus mykiss) Dev. Comp. Immunol. 35, 476-482. https://doi.org/10.1016/j.dci.2010.12.001
  24. Clarridge, J.E., Attorri, S.M., Zhang, Q., and Bartell, J. (2001). 16S ribosomal DNA sequence analysis distinguishes biotypes of Streptococcus bovis: Streptococcus bovis Biotype II/2 is a separate genospecies and the predominant clinical isolate in adult males. J. Clin. Microbiol. 39, 1549-1552. https://doi.org/10.1128/JCM.39.4.1549-1552.2001
  25. Darwish, A.M., and Hobbs, M.S. (2005). Laboratory efficacy of amoxicillin for the control of Streptococcus iniae infection in blue tilapia. J. Aquat. Anim. Health. 17, 197-202. https://doi.org/10.1577/H04-033.1
  26. Delannoy, C., Zadoks, R., Crumlish, M., Rodgers, D., Lainson, F., Ferguson, H., Turnbull, J., and Fontaine, M. (2016). Genomic comparison of virulent and non-virulent Streptococcus agalactiae in fish. J. Fish Dis. 39, 13-29. https://doi.org/10.1111/jfd.12319
  27. Diler, O., Altun, S., Adiloglu, A., Kubilay, A., and Istklt, B. (2002). First occurrence of Streptococcosis affecting farmed rainbow trout (Oncorhynchus mykiss) in Turkey. Bull. Eur. Ass. Fish Pathol. 22, 21-26.
  28. Dobrindt, U., and Hacker, J. (2001). Whole genome plasticity in pathogenic bacteria. Curr. Opin. Microbiol. 4, 550-557. https://doi.org/10.1016/S1369-5274(00)00250-2
  29. Dodson, S., Maurer, J., and Shotts, E. (1999). Biochemical and molecular typing of Streptococcus iniae isolated from fish and human cases. J. Fish Dis. 22, 331-336. https://doi.org/10.1046/j.1365-2761.1999.00170.x
  30. Eldar, A., Bejerano, Y., Livoff, A., Horovitcz, A., and Bercovier, H. (1995). Experimental streptococcal meningo-encephalitis in cultured fish. Vet. Microbiol. 43, 33-40. https://doi.org/10.1016/0378-1135(94)00052-X
  31. Eyngor, M., Zlotkin, A., Ghittino, C., Prearo, M., Douet, D.-G., Chilmonczyk, S., and Eldar, A. (2004). Clonality and diversity of the fish pathogen Lactococcus garvieae in Mediterranean countries. Appl. Environ. Microbiol. 70, 5132-5137. https://doi.org/10.1128/AEM.70.9.5132-5137.2004
  32. Facklam, R., Elliott, J., Shewmaker, L., and Reingold, A. (2005). Identification and characterization of sporadic isolates of Streptococcus iniae isolated from humans. J. Clin. Microbiol. 43, 933-937. https://doi.org/10.1128/JCM.43.2.933-937.2005
  33. Fuller, J.D., Bast, D.J., Nizet, V., Low, D.E., and de Azavedo, J.C. (2001). Streptococcus iniae virulence is associated with a distinct genetic profile. Infect. Immun. 69, 1994-2000. https://doi.org/10.1128/IAI.69.4.1994-2000.2001
  34. Gao, X.Y., Zhi, X.Y., Li, H.W., Klenk, H.P., and Li, WJ.. (2014). Comparative genomics of the bacterial genus Streptococcus illuminates evolutionary implications of species groups. PLoS One. 9, e101229 https://doi.org/10.1371/journal.pone.0101229
  35. Ghittino, C., Accornero, P., Prearo, M., Rogato, F., Zlotkin, A., and Eldar, A. (1999). Coldwater streptococcoses in salmonids, with particular reference to Vagococcus salmoninarum infection, Proceedings of Workshop in Fish Streptococcoses, IZS-State Veterinary Institute, Turin, Italy.
  36. Hastein, T., Gudding, R., and Evensen, O. (2005). Bacterial vaccines for fish--an update of the current situation worldwide. Dev. Biol. (Basel). 121, 55-74.
  37. Holmer, M. (2010). Environmental issues of fish farming in offshore waters: perspectives, concerns and research needs. Aquac. Environ. Interact. 1, 57-70. https://doi.org/10.3354/aei00007
  38. Johri, A.K., Paoletti, L.C., Glaser, P., Dua, M., Sharma, P.K., Grandi, G., and Rappuoli, R. (2006). Group B Streptococcus: global incidence and vaccine development. Nat. Rev. Microbiol. 4, 932-942. https://doi.org/10.1038/nrmicro1552
  39. Jolley, K.A., Bliss, C.M., Bennett, J.S., Bratcher, H.B., Brehony, C., Colles, F.M., Wimalarathna, H., Harrison, O.B., Sheppard, S.K., Cody, A.J., et al. (2012). Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158, 1005-1015. https://doi.org/10.1099/mic.0.055459-0
  40. Klesius, P., Evans, J., Shoemaker, C., Yeh, H., Goodwin, A., Adams, A., and Thompson, K. (2006). Rapid detection and identification of Streptococcus iniae using a monoclonal antibody-based indirect fluorescent antibody technique. Aquaculture 258, 180-186. https://doi.org/10.1016/j.aquaculture.2005.06.040
  41. Klijn, N., Weerkamp, A.H., and de Vos, W.M. (1991). Identification of mesophilic lactic acid bacteria by using polymerase chain reaction-amplified variable regions of 16S rRNA and specific DNA probes. Appl. Environ. Microbiol. 57, 3390-3393.
  42. Lau, S.K., Woo, P.C., Luk, W.K., Fung, A.M., Hui, W.T., Fong, A.H., Chow, C.W., Wong, S.S., and Yuen, K.Y. (2006). Clinical isolates of Streptococcus iniae from Asia are more mucoid and beta-hemolytic than those from North America. Diagn. Microbiol. Infect. Dis. 54, 177-181. https://doi.org/10.1016/j.diagmicrobio.2005.09.012
  43. Li, L., Wang, R., Liang, W., Huang, T., Huang, Y., Luo, F., Lei, A., Chen, M., and Gan, X. (2015). Development of live attenuated Streptococcus agalactiae vaccine for tilapia via continuous passage in vitro. Fish Shellfish Immunol. 45, 955-963. https://doi.org/10.1016/j.fsi.2015.06.014
  44. Lowe B.A., Miller J.D., and Neely M.N. (2007). Analysis of the polysaccharide capsule of the systemic pathogen Streptococcus iniae and its implications in virulence. Infect. Immun. 75, 1255-1264. https://doi.org/10.1128/IAI.01484-06
  45. Magnadottir, B. (2006). Innate immunity of fish (overview). Fish Shellfish Immunol. 20, 137-151. https://doi.org/10.1016/j.fsi.2004.09.006
  46. Maiden, M.C. (2006). Multilocus sequence typing of bacteria. Annu. Rev. Microbiol. 60, 561-588. https://doi.org/10.1146/annurev.micro.59.030804.121325
  47. Medini, D., Serruto, D., Parkhill, J., Relman, D.A., Donati, C., Moxon, R., Falkow, S., Rappuoli, R. (2008). Microbiology in the post-genomic era. Nat. Rev. Microbiol. 6, 419-430. https://doi.org/10.1038/nrmicro1901
  48. Mishra, A., Nam, G.H., Gim, J.A., Seong, M., Choe, Y., Lee, H.E., Jo, A., Kim, S., Kim, D.H., Cha, H.J., et al. (2017). Comparative evaluation of 16S rRNA gene in world-wide strains of Streptococcus iniae and Streptococcus parauberis for early diagnostic marker. Genes Genom. 39 , 779-791. https://doi.org/10.1007/s13258-017-0542-7
  49. Mora, D., Ricci, G., Guglielmetti, S., Daffonchio, D., and Fortina, M.G. (2003). 16S-23S rRNA intergenic spacer region sequence variation in Streptococcus thermophilus and related dairy streptococci and development of a multiplex ITS-SSCP analysis for their identification. Microbiology 149, 807-813. https://doi.org/10.1099/mic.0.25925-0
  50. Muzquiz, J., Royo, F., Ortega, C., De Blas, I., Ruiz, I., and Alonso, J. (1999). Pathogenicity of streptococcosis in rainbow trout (Oncorhynchus mykiss): dependence on age of diseased fish. Bull. Eur. Ass. Fish Pathol. 19, 114-119.
  51. Kwong, J.C., McCallum, N., Sintchenko, V., and Howden, B.P. (2015). Whole genome sequencing in clinical and public health microbiology. Pathology 47, 199-210. https://doi.org/10.1097/PAT.0000000000000235
  52. Nho, S.W., Shin, G.W., Park, S.B., Jang, H.B., Cha, I.S., Ha, M.A., Kim, Y.R., Park, Y.K., Dalvi, R.S., Kang, B.J., et al. (2009). Phenotypic characteristics of Streptococcus iniae and Streptococcus parauberis isolated from olive flounder (Paralichthys olivaceus). FEMS Microbiol. Lett. 293, 20-27. https://doi.org/10.1111/j.1574-6968.2009.01491.x
  53. Nho, S.W., Hikima, J., Park, S.B., Jang, H.B., Cha, I.S., Yasuike, M., Nakamura, Y., Fujiwara, A., Sano, M., Kanai, K., et al. (2013). Comparative genomic characterization of three Streptococcus parauberis strains in fish pathogen, as assessed by wide-genome analyses. PLoS One 8, e80395. https://doi.org/10.1371/journal.pone.0080395
  54. Nielsen, X.C., Justesen, U.S., Dargis, R., Kemp, M., and Christensen, J.J. (2009). Identification of clinically relevant nonhemolytic Streptococci on the basis of sequence analysis of 16S-23S intergenic spacer region and partial gdh gene. J. Clin. Microbiol. 47, 932-939. https://doi.org/10.1128/JCM.01449-08
  55. Nishiki, I., Noda, M., Itami, T., and Yoshida, T. (2010). Homogeneity of Streptococcus dysgalactiae from farmed amberjack Seriola dumerili in Japan. Fish. Sci. 76, 661-668. https://doi.org/10.1007/s12562-010-0243-5
  56. Park, Y.K., Nho, S.W., Shin, G.W., Park, S.B., Jang, H.B., Cha, I.S., Ha, M.A., Kim, Y.R., Dalvi, R.S., Kang, B.J., et al. (2009). Antibiotic susceptibility and resistance of Streptococcus iniae and Streptococcus parauberis isolated from olive flounder (Paralichthys olivaceus). Vet. Microbiol. 136, 76-81. https://doi.org/10.1016/j.vetmic.2008.10.002
  57. Pereira, U., Mian, G., Oliveira, I., Benchetrit, L., Costa, G., and Figueiredo, H. (2010). Genotyping of Streptococcus agalactiae strains isolated from fish, human and cattle and their virulence potential in Nile tilapia. Vet. Microbiol. 140, 186-192. https://doi.org/10.1016/j.vetmic.2009.07.025
  58. Rajagopal L. (2009). Understanding the regulation of Group B Streptococcal virulence factors. Future Microbiol. 4, 201-221. https://doi.org/10.2217/17460913.4.2.201
  59. Ravelo, C., Magarinos, B., Romalde, J.L., and Toranzo, A.E. (2001). Conventional versus miniaturized systems for the phenotypic characterization of Lactococcus garvieae strains. Bull. Eur. Ass. Fish Pathol. 21, 136-144.
  60. Ruiz-Zarzuela, I., de Bias, I., Girones, O., Ghittino, C., and Muazquiz, J. (2005). Isolation of Vagococcus salmoninarum in rainbow trout, Oncorhynchus mykiss (Walbaum), broodstocks: characterization of the pathogen. Vet. Res. Commun. 29, 553-562. https://doi.org/10.1007/s11259-005-2493-8
  61. Sakai, M. (1999). Current research status of fish immunostimulants. Aquaculture. 172, 63-92. https://doi.org/10.1016/S0044-8486(98)00436-0
  62. Sakala, R., Hayashidani, H., Kato, Y., Kaneuchi, C., and Ogawa, M. (2002). Isolation and characterization of Lactococcus piscium strains from vacuum-packaged refrigerated beef. J. Appl. Microbiol. 92, 173-179. https://doi.org/10.1046/j.1365-2672.2002.01513.x
  63. Shoemaker, C.A., Evans, J.J., and Klesius, P.H. (2000). Density and dose: factors affecting mortality of Streptococcusiniae infected tilapia (Oreochromisniloticus). Aquaculture 188, 229-235. https://doi.org/10.1016/S0044-8486(00)00346-X
  64. Shoemaker, C.A., Klesius, P.H., and Evans, J.J. (2001). Prevalence of Streptococcus iniae in tilapia, hybrid striped bass, and channel catfish on commercial fish farms in the United States. Am. J. Vet. Res. 62, 174-177. https://doi.org/10.2460/ajvr.2001.62.174
  65. Sommerset, I., Krossoy, B., Biering, E., and Frost, P. (2005). Vaccines for fish in aquaculture. Exp. Rev. Vaccines. 4, 89-101. https://doi.org/10.1586/14760584.4.1.89
  66. Springman, A.C., Lacher, D.W., Wu, G., Milton, N., Whittam, T.S., Davies, H.D., and Manning S.D. (2009). Selection, Recombination, and Virulence gene diversity among Group b Streptococcal Genotypes. J. Bacteriol. 17, 5419-5427.
  67. Teng, L.J., Hsueh, P.R., Tsai, J.C., Chen, P.W., Hsu, J.C., Lai, H.C., Lee, C.N., and Ho, S.W. (2002). groESL sequence determination, phylogenetic analysis, and species differentiation for viridans group streptococci. J. Clin. Microbiol. 40, 3172-3178. https://doi.org/10.1128/JCM.40.9.3172-3178.2002
  68. Toranzo, A.E., Magarinos, B., and Romalde, J.L. (2005). A review of the main bacterial fish diseases in mariculture systems. Aquaculture 246, 37-61. https://doi.org/10.1016/j.aquaculture.2005.01.002
  69. Tung, S.K., Teng, L.J., Vaneechoutte, M., Chen, H.M., and Chang, T.C. (2007) Identification of species of Abiotrophia, Enterococcus, Granulicatella and Streptococcus by sequence analysis of the ribosomal 16S-23S intergenic spacer region J. Med. Microbiol. 56, 504-513 https://doi.org/10.1099/jmm.0.47027-0
  70. Vendrell, D., Balcazar, J.L., Ruiz-Zarzuela, I., De Blas, I., Girones, O., Muzquiz, J.L. (2006). Lactococcus garvieae in fish: a review. Comp. Immunol. Microbiol. Infect. Dis. 29, 177-198. https://doi.org/10.1016/j.cimid.2006.06.003
  71. Villegas, J.G., Fukada, H., Masumoto, T., and Hosokawa, H. (2006). Effect of Dietary Immunostimulants on Some Innate Immune Responses and Disease Resistance against Edwardsiella tarda Infection in Japanese Flounder (Paralichthys olivaceus). Aquaculture Science 2, 153-162.
  72. Weinstein, M.R., Litt, M., Kertesz, D.A., Wyper, P., Rose, D., Coulter, M., McGeer, A., Facklam, R., Ostach, C., Willey, B.M., et al. (1997). Invasive infections due to a fish pathogen, Streptococcus iniae. S. iniae Study Group. N. Engl. J. Med. 337, 589-594. https://doi.org/10.1056/NEJM199708283370902
  73. Woo, S.H., and Park, S.I. (2014). Effects of phosphoglucomutase gene (PGM) in Streptococcus parauberis on innate immune response and pathogenicity of olive flounder (Paralichthys olivaceus). Fish Shellfish Immunol. 41, 317-325. https://doi.org/10.1016/j.fsi.2014.09.012
  74. Wren, B.W. (2000). Microbial genome analysis: insights into virulence, host adaptation and evolution. Nat. Rev. Genet. 1, 30-39. https://doi.org/10.1038/35049551
  75. Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., and Chun, J. (2017). Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole genome assemblies. Int. J. Syst. Evol. Microbiol. 67, 1613-1617 https://doi.org/10.1099/ijsem.0.001755
  76. Zlotkin, A., Chilmonczyk, S., Eyngor, M., Hurvitz, A., Ghittino, C., and Eldar, A. (2003). Trojan horse effect: phagocyte-mediated Streptococcus iniae infection of fish. Infect. Immun. 71, 2318-2325. https://doi.org/10.1128/IAI.71.5.2318-2325.2003

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