Aichivirus A Explained

Aichivirus A formerly Aichi virus (AiV)[1] belongs to the genus Kobuvirus in the family Picornaviridae.[2] Six species are part of the genus Kobuvirus, Aichivirus A-F. Within Aichivirus A, there are six different types including human Aichi virus, canine kobuvirus, murine kobuvirus, Kathmandu sewage kobuvirus, roller kobuvirus, and feline kobuvirus.[3] Three different genotypes are found in human Aichi virus, represented as genotype A, B, and C.

AiV is a non-enveloped positive sense ssRNA virus with icosahedral morphology. Aichivirus A was originally identified after a 1989 outbreak of acute gastroenteritis in the Aichi Prefecture that was linked to raw oyster consumption per genetic analysis.[4] [5] Human Aichi Virus can cause gastroenteritis with symptoms arising such as vomiting, diarrhea, abdominal pain, nausea, and feve.[6]

Aichivirus A can be found in a variety of environmental areas including sewage, groundwater, river water, and shellfish. Aichivirus A is present in many world regions, and in sometimes greater abundance than other well-known enteric viruses. Aichiviruses have been seen in Asia, Europe, South America, and Africa. It has since been isolated in populations of Finnish children,[7] Pakistani children, and Japanese travelers.[8] The widespread nature of aichivirus A can be seen in the high percentage of AiV antibodies in adult human populations found in several countries.

Transmission occurs through the fecal-oral route. After the virus is replicated in the gastrointestinal tract, the pathogen can be found in fecal samples of infected individuals. Water and shellfish contaminated with human sewage can propagate aichivirus A.

Discovery

Aichivirus A was first characterized after an outbreak of gastroenteritis in the Aichi Prefecture of Japan, this region is where the name of the virus was derived from. Fecal samples from infected individuals were taken and transported to a lab where they described the novel virus. These viral particles were 30 nm in diameter, a spherical shape, and cytopathic for BSC-1 cells (kidney cells of African green monkey). The infection was attributed to contaminated raw oyster found in vinegar.

Aichivirus A has been seen and described across many Asian countries, however the first appearance of aichivirus outside of this region was isolated in Europe and South America in 2006.[9] Through genetic analysis of isolates from Brazil and Germany, the nucleotide sequences were found to be similar to known Aichivirus nucleotide sequences. Notably, the German strain appeared to be of genotype A and the Brazil strain appeared to be of genotype B. Screening in Germany for antibodies to Aichivirus displayed a seroprevalence of 76%, which is comparable to seroprevalence in Japan. Therefore, European infection with Aichivirus is as common as it is in Asia.

Human infection

Propagation

Aichivirus A enters host cells through receptor-mediated endocytosis, a cellular uptake mechanism. After viral attachment and entry, the virion particle is uncoated releasing the genome into the cytoplasm. Similar to other viruses within the Picornaviridae family, viral replication and translation occurs in the cytoplasm.[10] The positive sense ssRNA is directly translated into protein by the host cell ribosomes, while some of the ssRNA is used as a template to replicate the viral genome. Capsid proteins, L protein, nonstructural proteins, and stable intermediates are produced after the polyprotein is processed. Protein production is directly related to synthesis of plus-strand RNA replication complex. The plus-strand RNA genome is packaged into the assembled viral particle, along with VpG (Viral genomic protein). A completed viral particle has 60 capsid proteins copies made up of 12 pentamers. The pentamer is made up by the 5S subunit composed of VP0, VP1, and VP3 protein aggregates. After the viral particle is assembled, it is released from host cells by cell lysis, making Aichivirus A a lytic virus.[11]

Characteristics

Most aichivirus A infection in humans are mild, asymptomatic infections lasting between 48–72 hours. However, it can develop into the common symptoms of gastroenteritis: fever, nausea, vomiting, abdominal pain.[12] Viral replication in the gastrointestinal tract damages the enterocyte layer in the intestinal villi interfering with water reabsorption This can lead to the symptoms appearing with infection.

Aichivirus A can become an opportunistic pathogen in those with HIV and is seen in high levels in the feces of those with HIV.[13] [14] Aichivirus A is also suspected as an opportunistic pathogan in those with X-linked agammaglobulinemia. Aichivirus is an emerging pathogen in those with B-cell deficiencies, however there is no explanation why In patients with primary immune deficiencies, chronic aichivirus infection can cause immunodysregulation.[15] Human aichivirus was deemed to effect multiple organs leading to the clinical symptom presentation. The aichivirus genome was detected in symptomatic patients and in infected organs, while it was not seen in asymptomatic individuals. Notably, in Japan there is a correlation with aichivirus A infection and lower respiratory tract disease.

Genome

The RNA genome of AiV A is composed of 8280 nucleotides. Along the 5' end of the RNA, there is an untranslated region consisting of 744 nucleotides, a VpG protein, and an internal ribosomal entry site (IRES). Following the 5' untranslated region, the open reading frame is approximately 7.3kB consisting of 2432 amino acids. The L protein, leader peptide, is the first protein translated within the polypeptide, followed by the structural proteins, and then nonstructural proteins. Cleavage into the different proteins occurs by viral proteases.[16] The capsid proteins are made up of three segments in the RNA: VP0, VP3, and VP1. These capsid proteins together are known as the P1 region on the genome. The encoded capsid proteins form a protomer that form into 12 pentamers during self-assembly.[17] X-ray crystallography of human aichi virus virion structure determined that the VP3 knob structure and VP0 surface loop are smaller compared to other viruses in picornaviruses. P2 and P3 are the regions of the RNA genome that are the non-structural proteins involved in replication control.[18] For example, the protein 3D within the P3 region encodes for the viral RNA-dependent RNA polymerase used in replication.[19] The 3B protein also in the P3 region encodes for the VpG protein, which is important promoting replication. Following the P2 and P3 region, there is a 3' untranslated region of about 237 nucleotides and a poly-A tail.

Genotypic differences

Differences at the 3CD nonstructural protein junction in the viral genome results in distinct genotypic differences.[20] When comparing the junction between the C-terminus of the 3C region and the N-terminus of the 3D region, three distinct genotypic types are seen. In studies, there appeared to be a geographical distribution to the genotypes. In some countries genotype B is prevalent, while in others genotype A dominates. In Finland and Spain genotype A was more prevalent.[21] However, in China, Bangladesh, and Pakistan genotype B is more widely seen in gastroenteritis outbreaks.[22] [23] However, genotype C is not widely seen to cause human infection and has only been described in one study a fecal sample from a child case of gastroenteritis after a trip to Mali. The VP1 region is used to classify the picornaviruses and can also be used to differentiate between aichivirus A genotypes. Some studies have seen more variation in the VP1 region and suggest that this region may be a better region to differentiate between genotypes.

Environmental occurrence

Aichivirus A can be found in a variety of environmental sources potentially leading to infection through food and water consumption. Aichivirus A causes infection through the fecal-oral route, where contaminated food and water sources are ingested. Some studies suggest using Aichivirus A as a method to detect viral contamination in environmental samples.

Shellfish

Enteric viruses can propagate through bivalve mollusks which filter surrounding water for food and retain enteric viruses. Many safety protocols only take into account bacteria and not viruses, which makes shellfish a vector for viral transmission.[24] Aichivirus A was first detected in an outbreak due to contaminated oysters, and contaminated seafood has been associated with aichivrius A outbreaks worldwide. In a year-long study in Japan on viral detection in clams, 33% of the grocery store samples contained aichivirus A.[25]

Sewage

Aichivirus A has been reported at high rates in wastewater but was first seen in 2010.[26] Wastewater treatment cannot get rid of all the viral particles before being discharged into the environment. Due to the stability of aichivirus in sewage before and after treatment, aichivirus A is likely a human fecal pollutant indicator. Aichivirus A has been detected in wastewater in America, Europe, Africa, and Asia. In one study, samples of treated sewage contained a 91.7% prevalence of aichivirus A.[27]

River and ground water

River water and ground water can be a reservoir for aichivirus A, due to viruses not being removed during the natural filtration cycle. Aichivirus A was first studied in river water in Venezuela in 2010 with detection in 45% of samples. Aichivirus A has since been detected in water sources worldwide, including in tap water and ground water in America.

Research

Under an electron microscope, Aichivirus A appears as a small, round virus making it hard to distinguish it from other viruses with a similar morphology.[28] Under electron microscopy, a canyon-like valley is seen on the surface of the capsid, likely where receptor binding occurs for entry. The viral particle is stable in acidic conditions until a pH of 2 and remains stable under known experimental methods to disrupt the viral particle.[29] These methods include heat, hydrostatic pressure, and detergent conditions. In human cell lines like HeLa, a cytopathic effect is not seen, however a cytopathic effect is seen in BSC-1 cell lines and Vero Cells.

An enzyme-linked immunoabsorbant assay (ELISA) has been developed to detect aichivirus A antigens. Reverse transcription-RNA polymerase chain reaction is also widely used in aichivirus research for identification and genotype differentiation.[30] A loop-mediated isothermal amplification (LAMP) assay has been created for aichivirus A to be used in water samples.[31] The LAMP assay allows for a rapid and specific detection of aichivirus A. Reverse transcription-quantitative PCR (RT-qPCR) is also widely used for detection and to determine viral numbers.

Notes and References

  1. Carmona-Vicente N, Buesa J, Brown PA, Merga JY, Darby AC, Stavisky J, Sadler L, Gaskell RM, Dawson S, Radford AD . 6 . Phylogeny and prevalence of kobuviruses in dogs and cats in the UK . Veterinary Microbiology . 164 . 3–4 . 246–252 . June 2013 . 23490561 . 7127238 . 10.1016/j.vetmic.2013.02.014 .
  2. Kitajima M, Gerba CP . Aichi virus 1: environmental occurrence and behavior . Pathogens . 4 . 2 . 256–268 . May 2015 . 25996404 . 4493473 . 10.3390/pathogens4020256 . free .
  3. Rivadulla E, Romalde JL . A Comprehensive Review on Human Aichi Virus . Virologica Sinica . 35 . 5 . 501–516 . October 2020 . 32342286 . 7223127 . 10.1007/s12250-020-00222-5 .
  4. Book: A Dictionary of Virology . Mahy BW . 2001 . Academic Press . 978-0-12-465327-6 . 3rd . San Diego, California . 9 . Aichi virus (AiV) . https://books.google.com/books?id=vYotjPWL_2IC&pg=PA9.
  5. Book: Viral Gastroenteritis . Desselberger U . Gulf Professional Publishing . 2003 . 978-0-444-51444-8 . 645–.
  6. Yamashita T, Ito M, Tsuzuki H, Sakae K . Identification of Aichi virus infection by measurement of immunoglobulin responses in an enzyme-linked immunosorbent assay . Journal of Clinical Microbiology . 39 . 11 . 4178–4180 . November 2001 . 11682554 . 88511 . 10.1128/JCM.39.11.4178-4180.2001 .
  7. Kaikkonen S, Räsänen S, Rämet M, Vesikari T . Aichi virus infection in children with acute gastroenteritis in Finland . Epidemiology and Infection . 138 . 8 . 1166–1171 . August 2010 . 19961643 . 10.1017/S0950268809991300 . 39830543 .
  8. Yamashita T, Sakae K, Kobayashi S, Ishihara Y, Miyake T, Mubina A, Isomura S . Isolation of cytopathic small round virus (Aichi virus) from Pakistani children and Japanese travelers from Southeast Asia . Microbiology and Immunology . 39 . 6 . 433–435 . 1995 . 8551977 . 10.1111/j.1348-0421.1995.tb02225.x . 11933842 .
  9. Oh DY, Silva PA, Hauroeder B, Diedrich S, Cardoso DD, Schreier E . Molecular characterization of the first Aichi viruses isolated in Europe and in South America . Archives of Virology . 151 . 6 . 1199–1206 . June 2006 . 16421634 . 10.1007/s00705-005-0706-7 . 9503348 .
  10. Book: Bergelson JM, Coyne CB . Picornavirus Entry . 2013 . Viral Entry into Host Cells . 24–41 . Pöhlmann S, Simmons G . Advances in Experimental Medicine and Biology . 790 . New York, NY . Springer . en . 10.1007/978-1-4614-7651-1_2 . 23884584 . 978-1-4614-7651-1 .
  11. Zell R . Picornaviridae-the ever-growing virus family . Archives of Virology . 163 . 2 . 299–317 . February 2018 . 29058149 . 10.1007/s00705-017-3614-8 . 254051304 .
  12. Carter MJ . Enterically infecting viruses: pathogenicity, transmission and significance for food and waterborne infection . Journal of Applied Microbiology . 98 . 6 . 1354–1380 . June 2005 . 15916649 . 10.1111/j.1365-2672.2005.02635.x . 37373796 .
  13. Oude Munnink BB, Canuti M, Deijs M, de Vries M, Jebbink MF, Rebers S, Molenkamp R, van Hemert FJ, Chung K, Cotten M, Snijders F, Sol CJ, van der Hoek L . 6 . Unexplained diarrhoea in HIV-1 infected individuals . BMC Infectious Diseases . 14 . 22 . January 2014 . 24410947 . 3925291 . 10.1186/1471-2334-14-22 . free .
  14. Meyts I, Bucciol G, Jansen K, Wollants E, Breuer J . Aichivirus: an Emerging Pathogen in Patients with Primary and Secondary B-Cell Deficiency . Journal of Clinical Immunology . 43 . 3 . 532–535 . April 2023 . 36449139 . 10.1007/s10875-022-01410-6 . 254094615 .
  15. Fourgeaud J, Lecuit MM, Pérot P, Bruneau J, Regnault B, Da Rocha N, Bessaud M, Picard C, Jeziorski É, Fournier B, Levy R, Marçais A, Blanche S, Frange P, Fischer A, Cavazzana M, Ferroni A, Jamet A, Leruez-Ville M, Eloit M, Neven B . 6 . Chronic Aichi Virus Infection As a Cause of Long-Lasting Multiorgan Involvement in Patients With Primary Immune Deficiencies . Clinical Infectious Diseases . 77 . 4 . 620–628 . August 2023 . 37078608 . 10.1093/cid/ciad237 .
  16. Sabin C, Füzik T, Škubník K, Pálková L, Lindberg AM, Plevka P . Structure of Aichi Virus 1 and Its Empty Particle: Clues to Kobuvirus Genome Release Mechanism . Journal of Virology . 90 . 23 . 10800–10810 . December 2016 . 27681122 . 5110158 . 10.1128/JVI.01601-16 . López S .
  17. Palmenberg AC . In vitro synthesis and assembly of picornaviral capsid intermediate structures . Journal of Virology . 44 . 3 . 900–906 . December 1982 . 6294338 . 256349 . 10.1128/jvi.44.3.900-906.1982 .
  18. Zhu L, Wang X, Ren J, Kotecha A, Walter TS, Yuan S, Yamashita T, Tuthill TJ, Fry EE, Rao Z, Stuart DI . 6 . Structure of human Aichi virus and implications for receptor binding . Nature Microbiology . 1 . 11 . 16150 . September 2016 . 27595320 . 10.1038/nmicrobiol.2016.150 . 13732698 .
  19. Yamashita T, Sakae K . VI, 3. Molecular biology and epidemiology of Aichi virus and other diarrhoeogenic enteroviruses . Perspectives in Medical Virology . 9 . 645–657 . 2003 . 32336843 . 7172506 . 10.1016/S0168-7069(03)09040-2 . 9780444514448 .
  20. Ambert-Balay K, Lorrot M, Bon F, Giraudon H, Kaplon J, Wolfer M, Lebon P, Gendrel D, Pothier P . 6 . Prevalence and genetic diversity of Aichi virus strains in stool samples from community and hospitalized patients . Journal of Clinical Microbiology . 46 . 4 . 1252–1258 . April 2008 . 18256215 . 2292896 . 10.1128/JCM.02140-07 .
  21. Rivadulla E, Varela MF, Romalde JL . Epidemiology of Aichi virus in fecal samples from outpatients with acute gastroenteritis in Northwestern Spain . Journal of Clinical Virology . 118 . 14–19 . September 2019 . 31382225 . 10.1016/j.jcv.2019.07.011 . 199452036 .
  22. Pham NT, Khamrin P, Nguyen TA, Kanti DS, Phan TG, Okitsu S, Ushijima H . Isolation and molecular characterization of Aichi viruses from fecal specimens collected in Japan, Bangladesh, Thailand, and Vietnam . Journal of Clinical Microbiology . 45 . 7 . 2287–2288 . July 2007 . 17522267 . 1932998 . 10.1128/JCM.00525-07 .
  23. Yang S, Zhang W, Shen Q, Yang Z, Zhu J, Cui L, Hua X . Aichi virus strains in children with gastroenteritis, China . Emerging Infectious Diseases . 15 . 10 . 1703–1705 . October 2009 . 19861087 . 2866408 . 10.3201/eid1510.090522 .
  24. Polo D, Varela MF, Romalde JL . Detection and quantification of hepatitis A virus and norovirus in Spanish authorized shellfish harvesting areas . International Journal of Food Microbiology . 193 . 43–50 . January 2015 . 25462922 . 10.1016/j.ijfoodmicro.2014.10.007 .
  25. Hansman GS, Oka T, Li TC, Nishio O, Noda M, Takeda N . Detection of human enteric viruses in Japanese clams . Journal of Food Protection . 71 . 8 . 1689–1695 . August 2008 . 18724766 . 10.4315/0362-028X-71.8.1689 . free .
  26. Alcalá A, Vizzi E, Rodríguez-Díaz J, Zambrano JL, Betancourt W, Liprandi F . Molecular detection and characterization of Aichi viruses in sewage-polluted waters of Venezuela . Applied and Environmental Microbiology . 76 . 12 . 4113–4115 . June 2010 . 20418428 . 10.1128/AEM.00501-10 . 2893485 . 2010ApEnM..76.4113A .
  27. Kitajima M, Haramoto E, Phanuwan C, Katayama H . Prevalence and genetic diversity of Aichi viruses in wastewater and river water in Japan . Applied and Environmental Microbiology . 77 . 6 . 2184–2187 . March 2011 . 21257803 . 3067340 . 10.1128/AEM.02328-10 . 2011ApEnM..77.2184K .
  28. Yamashita T, Sakae K, Ishihara Y, Isomura S, Utagawa E . Prevalence of newly isolated, cytopathic small round virus (Aichi strain) in Japan . Journal of Clinical Microbiology . 31 . 11 . 2938–2943 . November 1993 . 8263178 . 10.1128/jcm.31.11.2938-2943.1993 . 266163 .
  29. Yamashita T, Sakae K, Tsuzuki H, Suzuki Y, Ishikawa N, Takeda N, Miyamura T, Yamazaki S . 6 . Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans . Journal of Virology . 72 . 10 . 8408–8412 . October 1998 . 9733894 . 110230 . 10.1128/JVI.72.10.8408-8412.1998 .
  30. Yamashita T, Sugiyama M, Tsuzuki H, Sakae K, Suzuki Y, Miyazaki Y . Application of a reverse transcription-PCR for identification and differentiation of Aichi virus, a new member of the Picornavirus family associated with gastroenteritis in humans . Journal of Clinical Microbiology . 38 . 8 . 2955–2961 . August 2000 . 10921958 . 10.1128/JCM.38.8.2955-2961.2000 . 87158 .
  31. Lee JY, Kim JH, Rho JY . Development of Rapid and Specific Detection for the Human Aichivirus A Using the Loop-Mediated Isothermal Amplification from Water Samples . Indian Journal of Microbiology . 59 . 3 . 375–378 . September 2019 . 31388217 . 6646635 . 10.1007/s12088-019-00803-3 .