Abstract
Hepatopancreatic parvovirus (HPV) is one of the major shrimp parvovirus which is known to cause slow growth in penaeid shrimps. HPV has been found in wild and cultured penaeid shrimps throughout the world and there is high genetic variation among the different geographic isolates/host species. Given its high prevalence, wide distribution and ability to cause considerable economic loss in shrimp aquaculture industry, HPV deserves more attention than it has received. Till date, a total of four complete genome sequences of HPV have been reported in addition to a large number of partial sequences. HPV infection is seldom observed alone in epizootics and has occurred in multiple infections with other more pathogenic viruses and in most cases, heavy infections result in no visible inflammatory response. A great deal of information has accumulated in recent years on the clinical signs, geographical distribution, transmission and genetic diversity of HPV infection in shrimp aquaculture. However, the mechanism by which HPV enters the shrimp tissues and pathogenesis of virus is still unknown. To date, no effective prophylactic measures are available to reduce the infection in shrimps. To control and prevent HPV infection, considerable research efforts are on. This review provides information on current knowledge on HPV infection in penaeid shrimp aquaculture.
Similar content being viewed by others
References
Afanasiev BN, Galyov EE, Buchatsky LP, Kozlov YV. Nucleotide sequence and genomic organization of Aedes densonucleosis virus. Virology. 1991;185:323–36.
Anderson IG, Law AT, Shariff M. A parvo-like virus in the giant freshwater prawn, Macrobrachium rosenbergii. J Invertebr Pathol. 1990;55:447–9.
Astell CR, Chow MB, Ward DC. Sequence analysis of the termini of virion and replicative forms of minute virus of mice DNA suggests a modified rolling hairpin model for autonomous parvovirus DNA replication. J Virol. 1985;54:171–7.
Bonami JR, Trumper B, Mori J, Brehelier M, Lightner DV. Purification and characterisation of the infectious hypodermal and hematopoietic necrosis virus of penaeid shrimps. J Gen Virol. 1990;71:2657–64.
Bonami JR, Mari J, Poulos BT, Lightner DV. Characterization of hepatopancreatic parvo-like virus, a second unusual parvovirus pathogenic for penaeid shrimps. J Gen Virol. 1995;76:813–7.
Boublik Y, Jousset FX, Bergoin M. Complete nucleotide sequence and genome organization of the Aedes albopictus parvovirus (AaPV) pathogenic for Aedes aegypti larvae. Virology. 1994;200:752–63.
Brandenburger A, Legendre D, Avalosse B, Rommelaere J. NS-1 and NS-2 proteins may act synergistically in the cytopathogenicity of parvovirus MVMp. Virology. 1990;174:576–84.
Catap ES, Lavilla-Pitogo CR, Maeno Y, Travina RD. Occurrence, histopathology and experimental transmission of hepatopancreatic parvovirus infection in Penaeus monodon postlarvae. Dis Aquat Org. 2003;57:11–7.
Cater JE, Pintel DJ. The small non-structural protein NS2 of the autonomous parvovirus minute virus of mice is required for virus growth in murine cells. J Gen Virol. 1992;73:1839–43.
Chantanachookin C, Boonyaratanapalin S, Kasornchandra J, Direkbusarakom S, Ekpanithanpong U, Supamataya K, Siurairatana S, Flegel TW. Histology and ultrastructure reveal a new granulosis-like virus in Penaeus monodon affected by “yellow-head” disease. Dis Aquat Org. 1993;17:145–57.
Chen D. An overview of the disease situation, diagnostic techniques, treatments and preventives used on shrimp farms in China. In: Fulks W, Main KL, editors. Diseases of cultured penaeid shrimp in Asia and the United States. Honolulu: The Oceanic Institute; 1992. p. 47–55.
Chen SN, Chang PS, Kou GH. Observation on pathogenicity and epizootiology of Penaeus monodon Baculovirus (MBV) in cultured shrimp in Taiwan. Fish Pathol. 1989;24:189–95.
Chong YC, Loh H. Hepatopancreas clamydial and parvoviral infections of farmed marine prawns in Singapore. Singap Vet J. 1985;9:51–6.
Cotmore SF, D’abramo AMJ, Carbonell LF, Bratton J, Tattersall P. The NS2 polypeptide of parvovirus MVM is required for capsid assembly in murine cells. Virology. 1997;231:267–80.
Cotmore SF, Tattersall P. The autonomously replicating parvoviruses of vertebrates. Adv Virus Res. 1987;33:91–174.
Destoumieux-Garzon D, Saulnier D, Garnier J, Jouffrey C, Bulet P, Bachere E. Crustacean immunity: antifungal peptides are generated from the C terminus of shrimp hemocyanin in response to microbial challenge. J Biol Chem. 2001;276:47070–7.
Erdman DD, Durigon EL, Wang QY, Anderson LJ. Genetic diversity of human parvovirus B19: sequence analysis of the vp1/vp2 gene from multiple isolates. J Gen Virol. 1996;77:2767–74.
FAO. The State of world fisheries and aquaculture 2010. FAO Fisheries and Aquaculture Department, Food and Agriculture Organization of the United Nations, Rome; 2010.
Fauquet CP, Perros M, Brandenburger A, Spegelaere P, Rommelaere J. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J. 1990;9:2989–95.
Flegel TW, Fegan DF, Kongsom S, Vuthikornudomkit S, Sriurairatana S, Boonyaratpalin S, Chantanachookhin C, Vickers JE, Macdonald OD. Occurrence, diagnosis and treatment of shrimp diseases in Thailand. In: Fulks W, Main KL, editors. Diseases of cultured penaeid shrimp in Asia and the United States. Honolulu: The Oceanic Institute; 1992. p. 57–112.
Flegel TW, Sriurairatana S. Black tiger prawn diseases in Thailand. In: Akiyama DM, editor. Technical bulletin of the American Soybean Association. Technical Bulletin AQ39 1993/3. Singapore: American Soybean Association; 1993. p. 30.
Flegel TW, Sriurairatana S. Shrimp health management: an environmental approach. In: Shariff M, editor. Diseases in aquaculture: the current issues. Malaysian Fisheries Society publication no. 8, Faculty of Fisheries and Marine Science, University Pertanian Malaysia, Serdang; 1994. p. 1–48.
Flegel TW, Fegan DF, Sriurairatana S. Environmental control of infectious shrimp diseases in Thailand. In: Shariff M, Arthur JR, Subasinghe RP, editors. Diseases in asian aquaculture II. Fish Health Section, Asian Fish. Society, Manila; 1995. p. 65–79.
Flegel TW, Thamavit V, Passarawipas T, Alday-Sanz V. Statistical correlation between severity of Hepatopancreatic parvovirus (HPV) infection and stunting of farmed black tiger shrimp (Penaeus monodon). Aquaculture. 1999;174:197–206.
Flegel TW. Detection of major penaeid shrimp viruses in Asia, a historical perspective with emphasis on Thailand. Aquaculture. 2006;258:1–33.
Fraser CA, Owens L. Spawner-isolated mortality virus from Australia Penaeus monodon. Dis Aquat Org. 1996;27:141–8.
Hsu YL, Wang KH, Yang YH, Tung MC, Hu CH, Lo CF, Wang CH, Hsu T. Diagnosis of Penaeus monodon-type baculovirus by PCR and by ELISA of occlusion bodies. Dis Aquat Org. 2000;40:93–9.
Jang IK, Suriakala K, Kim JS, Meng X, Choi TJ. TaqMan real-time PCR assay for quantifying type III hepatopancreatic parvovirus infections in wild broodstocks and hatchery-reared postlarvae of Fenneropenaeus chinensis in Korea. J Microbiol Biotechnol. 2011;21:1109–15.
Jeeva S, Kang SW, Lee YS, Jang IK, Seo HC, Choi TJ. Complete nucleotide sequence analysis of a Korean strain of hepatopancreatic parvovirus (HPV) from Fenneropenaeus chinensis. Virus Genes. 2012;44:89–97.
Kawase S, Garzon S, Su DM, Tijssen P. Insect parvovirus diseases. In: Tijssen P, editor. Handbook of parvoviruses, vol. II. Boca Raton: CRC Press; 1990. p. 213–28.
Khawsak P, Deesukon W, Chaivisuthangkura P, Sukhumsirichart W. Multiplex RT-PCR assay for simultaneous detection of six viruses of penaeid shrimp. Mol Cell Probes. 2008;22:177–83.
Kiatpathomchai W, Jaroenram W, Arunrut N, Jitrapakdee S, Flegel TW. Shrimp Taura syndrome virus detection by reverse transcription loop-mediated isothermal amplification combined with a lateral flow dipstick. J Virol Methods. 2008;153:214–7.
Kubista M, Andrade JM, Bengtsson M, Forootan, Jona KJ, Lind K, Sindelka R, Sjoback R, Sjogreen B, Strombom L, Stahlber G, Zoric A. Review on the real-time polymerase chain reaction. Mol Aspects Med. 2006;27:95–125.
La Fauce KA, Elliman J, Owens L. Molecular characterization of hepatopancreatic parvovirus (PmergDNV) from Australian Penaeus merguiensis. Virology. 2007;362:397–403.
La Fauce KA, Layton R, Owens L. TaqMan real-time PCR for detection of hepatopancreatic parvovirus from Australia. J Virol Methods. 2007;140:10–6.
La Fauce KA, Owens L. Investigation into the pathogenicity of Penaeus merguiensis densovirus (PmergDNV) to juvenile Cherax quadricarinatus. Aquaculture. 2007;271:31–8.
La Fauce KA, Owens L. The use of insects as a bioassay for Penaeus merguiensis densovirus (PmergDNV). J Invertebr Pathol. 2008;98:1–6.
Legrand C, Rommelaere J, Fauquet CP. MVM (p) NS-2 protein expression is required with NS-1 for maximal cytotoxicity in human transformed cells. Virology. 1993;195:149–55.
Liao IC. Marine prawn culture industry of Taiwan. In: Fast AW, Lester LJ, editors. Marine shrimp culture: principles and practices. Amsterdam: Elsevier; 1992. p. 289–320.
Lightner DV, Redman RM, Bell TA. Detection of IHHN virus in Penaeus stylirostris and Penaeus vannamei imported into Hawaii. J World Maricult Soc. 1983;14:212–25.
Lightner DV, Redman RM. A parvo-like virus disease of penaeid shrimp. J Invertebr Pathol. 1985;45:47–53.
Lightner DV. Shrimp virus diseases: diagnosis, distribution and management. In: Wyban J, editor. Proceedings of the special session on shrimp farming. Baton Rouge: World Aquaculture Society; 1992. p. 238–53.
Lightner DV, Poulos BT, Bruce L, Redman RM, Mari J, Bonami JR. New developments in penaeid virology: application of biotechnology in research and disease diagnosis for shrimp viruses of concern in the Americas. In: Fulks W, Main K, editors. Diseases of cultured penaeid shrimp in Asia and the United States. Honolulu: Oceanic Institute; 1992. p. 233–53.
Lightner DV, Redman RM. Penaeid virus diseases of the prawn culture industry in the Americas. In: Fast AW, Lester LJ, editors. Marine prawn culture: principles and practices. Amsterdam: Elsevier; 1992. p. 569–88.
Lightner DV, Redman RM, Moore DW, Park MA. Development and application of a simple and rapid diagnostic method to study hepatopancreatic parvovirus of penaeid shrimp. Aquaculture. 1993;116:15–23.
Lightner DV, Redman RM, Poulos BT, Mari JL, Bonami JR, Shariff M. Distinction of HPV-Type viruses in Penaeus chinensis and Macrobrachium rosenbergii using a DNA probe. Asian Fish Sci. 1994;7:267–72.
Lightner DV. A handbook of shrimp pathology and diagnostic procedures for diseases of penaeid shrimp. Baton Rouge: World Aquaculture Society; 1996. p. 304.
Limsuwan CH. Shrimp culture in Thailand toward year 2000. In: Tonguthai K, Chinabut S, Somsiri T, Chanratchakul P, Kanchanakan S, editors. The AAHRI newsletter. Bangkok: Department of Fisheries, Kasertsart University; 1999. p. 5–6.
Lungu O, Sun XW, Wright TC, Ferenczy A Jr, Richard RM, Silverstein S. A polymerase chain reaction-enzyme-linked immunosorbent assay method for detecting human papillomavirus in cervical carcinomas and high-grade cervical cancer precursors. Obstet Gynecol. 1995;85:337–42.
Manivannan S, Otta SK, Karunasagar I, Karunasagar I. Multiple viral infections in Penaeus monodon prawn post larvae in an Indian hatchery. Dis Aquat Org. 2002;48:233–6.
Manjanaik B, Umesha KR, Karunasagar I, Karunasagar I. Detection of hepatopancreatic parvovirus (HPV) in wild prawn from India by nested polymerase chain reaction (PCR). Dis Aquat Org. 2005;63:255–9.
Mari J, Bonami JR, Lightner DV. Partial cloning of the genome of infectious hypodermal and hematopoietic necrosis virus, an unusual parvovirus pathogenic for penaeid shrimps; diagnosis of the disease using a specific probe. J Gen Virol. 1993;74:2637–43.
Mari J, Lightner DV, Poulos BT, Bonami JR. Partial cloning of the genome of an unusual shrimp parvovirus (HPV): use of gene probes in disease diagnosis. Dis Aquat Org. 1995;22:129–34.
Naeger LK, Cater J, Pintel DJ. The small nonstructural protein (NS2) of the parvovirus minute virus of mice is required for efficient DNA replication and infectious virus production in a cell-type-specific manner. J Virol. 1990;64:6166–75.
Naeger LK, Salome N, Pintel DJ. NS2 is required for efficient translation of viral mRNA in minute virus of mice-infected murine cells. J Virol. 1993;67:1034–43.
Nimitphaka T, Kiatpathomchaia W, Flegel TW. Shrimp hepatopancreatic parvovirus detection by combining loop-mediated isothermal amplification with a lateral flow dipstick. J Virol Methods. 2008;154:56–60.
Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res. 2000;28:e63.
Otta SK, Shubha G, Joseph B, Chakraborty A, Karunasagar I, Karunasagar I. Polymerase chain reaction (PCR) detection of white spot syndrome virus (WSSV) in cultured and wild crustaceans in India. Dis Aquat Org. 1999;38:67–70.
Owens L. Special topic review: the history of the emergence of viruses in Australian prawn aquaculture. World J Microbiol Biotechnol. 1997;13:427–31.
Owens L, Haqshenas G, McElnea C, Coelen R. Putative spawner-isolated mortality virus associated with mid-crop mortality syndrome in farmed Penaeus monodon from northern Australia. Dis Aquat Org. 1998;34:177–85.
Owens L, McElnea C. Natural infection of the redclaw crayfish Cherax quadricarinatus with presumptive spawner-isolated mortality virus. Dis Aquat Org. 2000;40:219–23.
Owens L, Liessmann L, La Fauce K, Nyguyen T, Zeng C. Intranuclear bacilliform virus and hepatopancreatic parvovirus (PmergDNV) in the mud crab Scylla serrata (Forskal) of Australia. Aquaculture. 2010;310:47–51.
Panichareon B, Khawsak P, Deesukon W, Sukhumsirichart W. Multiplex real-time PCR and high-resolution melting analysis for detection of white spot syndrome virus, yellow-head virus, and Penaeus monodon densovirus in penaeid shrimp. J Virol Methods. 2011;178:16–21.
Pantoja CR, Lightner DV. A non-destructive method based on the polymerase chain reaction for detection of hepatopancreatic parvovirus (HPV) of penaeid shrimp. Dis Aquat Org. 2000;39:177–82.
Pantoja CR, Lightner DV. Detection of hepatopancreatic parvovirus (HPV) of penaeid shrimp by in situ hybridization at the electron microscope level. Dis Aquat Org. 2001;44:87–96.
Paynter JL, Lightner DV, Lester RGJ. Prawn virus from juvenile Penaeus esculentus. In: Rothlisberg RC, Hill BY, Staples DY, editors. Proceedings of the second Australian national prawn seminar. Cleveland; 1985. p. 61–4.
Phromjai J, Sukhumsirichart W, Pantoja C, Lightner DV, Flegel TW. Different reactions obtained using the same DNA detection reagents for Thai and Korean hepatopancreatic parvovirus of penaeid shrimp. Dis Aquat Org. 2001;46:153–8.
Phromjai J, Boosaeng V, Withyachumnarmkul B, Flegel TW. Detection of hepatopancreatic parvovirus (HPV) in Thai shrimp Penaeus monodon by in situ hybridization, dot blot hybridization and PCR amplification. Dis Aquat Org. 2002;51:227–32.
Poulos BT, Lightner DV, Trumper B. Monoclonal antibodies to a penaeid shrimp parvovirus, infectious hypodermal and hematopoietic necrosis virus (IHHNV). J Aquat Anim Health. 1994;6:149–54.
Prakasha BK, Ramakrishna RP, Karunasagar I, Karunasagar I. Detection of Laem-Singh virus (LSNV) in cultured Penaeus monodon from India. Dis Aquat Org. 2007;77:83–6.
Rai P, Pradeep B, Karunasagar I, Karunasagar I. Detection of viruses in Penaeus monodon from India showing signs of slow growth syndrome. Aquaculture. 2009;289:231–5.
Rai P, Pradeep B, Safeena MP, Karunasagar I, Karunasagar I. Simultaneous presence of infectious hypodermal and hematopoietic necrosis virus (IHHNV) and type A virus-related sequence in Penaeus monodon from India. Aquaculture. 2009;295:168–74.
Roekring S, Nielsen L, Owens L, Pattanakitsakul S, Malasit P, Flegel TW. Comparison of penaeid shrimp and insect parvoviruses suggests that viral transfers may occur between two distantly related arthropod groups. Virus Res. 2002;87:79–87.
Roubal FR, Paynter JL, Lester RJG. Electron microscope observation of hepatopancreatic parvo-like virus (HPV) in the penaeid prawn, Penaeus merguiensis de Man, from Australia. J Fish Dis. 1989;12:199–201.
Rukpratanporn S, Sukhumsirichart W, Chaivisuthangkura P, Longyant S, Sithigorngul W, Menasveta P, Sithigorngul P. Generation of monoclonal antibodies specific to hepatopancreatic parvovirus (HPV) from Penaeus monodon. Dis Aquat Org. 2005;65:85–9.
Safeena MP, Tyagi A, Rai P, Karunasagar I, Karunasagar I. Complete nucleic acid sequence of Penaeus monodon densovirus (PmDNV) from India. Virus Res. 2010;150:1–11.
Shike H, Dhar AK, Burns JC, Shimizu C, Jousset FX. Infectious hypodermal and hematopoietic necrosis virus of shrimp is related to mosquito brevidensoviruses. Virology. 2000;277:167–77.
Sithigorngul P, Rukpratanporn S, Longyant S, Chaivisuthangkura P, Sithigorngul W, Menasveta P. Monoclonal antibodies specific to yellow-head virus (YHV) of Penaeus monodon. Dis Aquat Org. 2002;49:71–6.
Sivakumar VK, Sarathi M, Venkatesan C, Sivaraj A, Sahul Hameed AS. Experimental exposure of artemia to hepatopancreatic parvo-like virus and subsequent transmission to post-larvae of Penaeus monodon. J Invert Pathol. 2009;102:191–5.
Spann KM, Adlard RD, Hudson DA, Dyecroft SB, Jones TC, Voigt MOC. Hepatopancreatic parvo-like virus (HPV) of Penaeus japonicus cultured in Australia. Dis Aquat Org. 1997;31:239–41.
Srisuk C, Chaivisuthangkura P, Sukhumsirichart W, Sridulyakul P, Longyant S, Rukpratanporn S, Sithigorngul P. Improved immunodetection of Penaeus monodon densovirus with monoclonal antibodies raised against recombinant capsid protein. Aquaculture. 2011;311:19–24.
Sukhumsirichart W, Wongteerasupaya C, Boonsaeng V, Panyim S, Sriurairatana S, Withyachumnarnkul B, Flegel TW. Characterization and PCR detection of hepatopancreatic parvovirus (HPV) from Penaeus monodon in Thailand. Dis Aquat Org. 1999;38:1–10.
Sukhumsirichart W, Kisytsyhomchai W, Wongteerasupaya C, Withyachumnarmkul B, Flegel TW, Boonsaeng V, Panyim S. Detection of hepatopancreatic parvovirus (HPV) Penaeus monodon using PCR–ELISA. Mol Cell Probes. 2002;16:409–13.
Sukhumsirichart W, Pongsopee A, Boonsaeng V, Panyim S. Complete nucleotide sequence and genomic organization of hepatopancreatic parvovirus (HPV) of Penaeus monodon. Virology. 2006;46:266–77.
Tang KFJ, Pantoja CR, Lightner DV. Nucleotide sequence of Madagascar hepatopancreatic parvovirus (HPV) and comparison of genetic variation among geographic isolates. Dis Aquat Org. 2008;80:105–12.
Tang KFJ, Lightner DV. Duplex real-time PCR for detection and quantification of monodon baculovirus (MBV) and hepatopancreatic parvovirus (HPV) in Penaeus monodon. Dis Aquat Org. 2011;93:191–8.
Uma A, Koteeswaran A, Karunasagar I, Karunasagar I. Prevalence of hepatopancreatic parvovirus (HPV) in Penaeus monodon postlarvae from commercial shrimp hatcheries in Tamilnadu, southeast coast of India. Asian Fish Sci. 2006;9:113–6.
Uma A, Ramanathan N, Saravanabava K. Study by PCR on the prevalence of white spot syndrome virus, monodon baculovirus and hepatopancreatic parvovirus infection in Penaeus monodon post larvae in Tamil Nadu, Southeast coast of India. Asian Fish Sci. 2007;20:227–39.
Umesha KR, Uma A, Otta SK, Karunasagar I, Karunasagar I. Detection by polymerase chain reaction (PCR) of hepatopancreatic parvovirus (HPV) and other viruses in hatchery-reared postlarvae of Penaeus monodon. Dis Aquat Org. 2003;57:141–6.
Umesha KR, Dass MKB, Manjanaik B, Venugopal MN, Karunasagar I, Karunasagar I. High prevalence of dual and triple viral infections in blacktiger shrimp ponds in India. Aquaculture. 2006;258:91–6.
Vega-Villasante F, Puente ME. A review of viral diseases of cultured shrimp. Prev Vet Med. 1993;17:271–82.
Yan DC, Tang KF, Lightner DV. A real-time PCR for the detection of hepatopancreatic parvovirus (HPV) of penaeid shrimp. J Fish Dis. 2010;33:507–11.
Zerbini M, Gallinella G, Manaresi E, Musiani M, Gentilomi G, Venturoli S. Standardization of a PCR-ELISA in serum samples: diagnosis of active parvovirus B19 infection. J Med Virol. 1999;59:239–44.
Acknowledgments
The authors gratefully acknowledge the financial support received from the Department of Biotechnology, Govt. of India and the facilities of the Bioinformatics centre of DBT.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Safeena, M.P., Rai, P. & Karunasagar, I. Molecular Biology and Epidemiology of Hepatopancreatic parvovirus of Penaeid Shrimp. Indian J. Virol. 23, 191–202 (2012). https://doi.org/10.1007/s13337-012-0080-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13337-012-0080-5