Background. This study investigates the viable persistence of avian influenza viruses (AIVs) in various types of artificially frozen environmental water and evaluates the feasibility of similar occurrence taking place in nature, and allowing for prolonged abiotic virus survival, with subsequent biotic viral recirculation. Methods. Fresh, brackish, and salty water, taken in Japan from aquatic biotopes regularly visited by migratory waterfowl, were seeded with AIVs. We monthly monitored the viability of the seeded viruses in the frozen state at ?20°C and ?30°C, for 12 months. We also monitored virus viability following repeatedly induced freezing and thawing. Results. The viruses exhibited considerable viable persistence all along that period of time, as well as during freezing-thawing cycles. Appreciable, yet noncrucial variances were observed in relation to some of the parameters examined. Conclusions. As typical waterborne pathogens of numerous northerly aquatic birds, AIVs are innately adapted to both the body temperature of their hosts (40°C to 42°C) and, presumably, to subzero temperatures of frozen lakes (down to ?54°C in parts of Siberia) occupied and virus-seeded by subclinically infected birds, prior to freezing. Marked cryostability of AIVs appears to be evident. Preservation in environmental ice has significant ecophylogenetic and epidemiological implications, potentially, and could account for various unexplained phenomena. 1. Background A wide diversity of bacteria, protozoa, and viruses are known to exist in various water bodies worldwide, including ponds, lakes, seas, and oceans [1]. In arctic and sub-arctic regions, those water bodies are frozen, entirely or partially, for 4 months (in the southern Taiga) up to 10 months (in the northern Tundra and Arctic Ocean), annually, in the form of seasonal ice. In the Arctic, perennial ice is found too across the Arctic Ocean and freshwater bodies located in Greenland and islands of the Arctic Ocean. All those water bodies are abundantly visited by migratory aquatic birds whenever partially or completely thawed. Consequently, microorganisms that are shed through feces by the birds into water become waterborne, until contracted again by a host or entrapped within refreezing water. In the case of viruses, as obligatory parasites, they are otherwise apt to perish, sooner or later; hence, whenever entrapped in ice, their cryotolerance might constitute a critical factor, in terms of persisting viability, meaning infectivity. The higher their cryotolerance, the longer is the period of time they are
References
[1]
National Environment Research Council, Aquatic Microbes Shape Our World, http://www.nerc.ac.uk/.../other/documents/mfmb_aquaticmicrobes.pdf, 2005.
[2]
R. G. Webster, W. J. Bean, O. T. Gorman, T. M. Chambers, and Y. Kawaoka, “Evolution and ecology of influenza A viruses,” Microbiological Reviews, vol. 56, no. 1, pp. 152–179, 1992.
[3]
J. D. Brown, D. E. Stallknecht, J. R. Beck, D. L. Suarez, and D. E. Swayne, “Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses,” Emerging Infectious Diseases, vol. 12, no. 11, pp. 1663–1670, 2006.
[4]
D. E. Stallknecht and J. D. Brown, “Wild birds and the epidemiology of avian influenza,” Journal of Wildlife Diseases, vol. 43, no. 3, pp. S15–S20, 2007.
[5]
V. S. Hinshaw, R. G. Webster, and B. Turner, “Water-borne transmission of influenza A viruses?” Intervirology, vol. 11, no. 1, pp. 66–68, 1979.
[6]
R. Breban, J. M. Drake, D. E. Stallknecht, and P. Rohani, “The role of environmental transmission in recurrent Avian influenza epidemics,” PLoS Computational Biology, vol. 5, no. 4, 2009.
[7]
T. Ito, K. Okazaki, Y. Kawaoka, A. Takada, R. G. Webster, and H. Kida, “Perpetuation of influenza A viruses in Alaskan waterfowl reservoirs,” Archives of Virology, vol. 140, no. 7, pp. 1163–1172, 1995.
[8]
D. Shoham, Studies on the ecology of influenza type A viruses in Israel [Ph.D. thesis], Tel-Aviv University, Tel-Aviv, Israel, 1985.
[9]
D. Shoham, “Biotic-abiotic mechanisms for long-term preservation and reemergence of influenza type A virus genes,” Progress in Medical Virology, vol. 40, pp. 178–192, 1993.
[10]
R. G. Webster, W. J. Bean, O. T. Gorman, T. M. Chambers, and Y. Kawaoka, “Evolution and ecology of influenza A viruses,” Microbiological Reviews, vol. 56, no. 1, pp. 152–179, 1992.
[11]
L. V. Parker and C. J. Martel, Long-Term Survival of Enteric Microorganisms in Frozen Wastewater, US Army Corps of Engineers, Engineer Research and Development Center, Washington, DC, USA, 2002.
[12]
D. Greiff and C. Greiff, “Linear nonisothermal, single-step, stability studies of dried preparations of influenza virus,” Cryobiology, vol. 9, no. 1, pp. 34–37, 1972.
[13]
M. Krasnitz, A. J. Levine, and R. Rabadan, “Anomalies in the influenza virus genome database: new biology or laboratory errors?” Journal of Virology, vol. 82, no. 17, pp. 8947–8950, 2008.
[14]
A. Jahangir, Y. Watanabe, O. Chinen et al., “Surveillance of avian influenza viruses in Northern pintails (Anas acuta) in Tohoku District, Japan,” Avian Diseases, vol. 52, no. 1, pp. 49–53, 2008.
[15]
A. Jahangir, S. Ruenphet, K. Hara et al., “Evaluation of human intestinal epithelial differentiated cells (Caco-2) for replication, plaque formation and isolation of avian influenza viruses,” Journal of Virological Methods, vol. 169, no. 1, pp. 232–238, 2010.
[16]
A. Jahangir, Y. Watanabe, O. Chinen et al., “Surveillance of avian influenza viruses in Northern pintails (Anas acuta) in Tohoku District, Japan,” Avian Diseases, vol. 52, no. 1, pp. 49–53, 2008.
[17]
A. Jahangir, S. Ruenphet, K. Hara et al., “Evaluation of human intestinal epithelial differentiated cells (Caco-2) for replication, plaque formation and isolation of avian influenza viruses,” Journal of Virological Methods, vol. 169, no. 1, pp. 232–238, 2010.
[18]
P. Villegas, “Titration of biological suspensions,” in A Laboratory Manual for the Isolation and Identification of Avian Pathogens, L. Dufour-Zavala, D. E. Swayne, J. R. Glisson et al., Eds., pp. 217–221, American Association of Avian Pathologist, Jacksonville, Fla, USA, 5th edition, 2008.
[19]
R. Chen and E. C. Holmes, “Avian influenza virus exhibits rapid evolutionary dynamics,” Molecular Biology and Evolution, vol. 23, no. 12, pp. 2336–2341, 2006.
[20]
W. M. Fitch, “The variety of human virus evolution,” Molecular Phylogenetics and Evolution, vol. 5, no. 1, pp. 247–258, 1996.
[21]
W. M. Fitch, J. M. E. Leiter, X. Li, and P. Palese, “Positive Darwinian evolution in human influenza A viruses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 10, pp. 4270–4274, 1991.
[22]
O. T. Gorman, W. J. Bean, and R. G. Webster, “Evolutionary processes in influenza viruses: divergence, rapid evolution, and stasis,” Current Topics in Microbiology and Immunology, vol. 176, pp. 75–97, 1992.
[23]
S. Lindstrom, A. Endo, S. Sugita et al., “Phylogenetic analyses of the matrix and non-structural genes of equine influenza viruses,” Archives of Virology, vol. 143, no. 8, pp. 1585–1598, 1998.
[24]
M. I. Nelson, L. Simonsen, C. Viboud et al., “Stochastic processes are key determinants of short-term evolution in influenza a virus,” PLoS pathogens, vol. 2, no. 12, p. e125, 2006.
[25]
J. D. Parvin, A. Moscona, and W. T. Pan, “Measurement of the mutation rates of animal viruses: influenza A virus and poliovirus type 1,” Journal of Virology, vol. 59, no. 2, pp. 377–383, 1986.
[26]
D. A. Buonagurio, S. Nakada, and J. D. Parvin, “Evolution of human influenza a viruses over 50 years: rapid, uniform rate of change in NS gene,” Science, vol. 232, no. 4753, pp. 980–982, 1986.
[27]
M. Verhoeyen, R. Fang, W. M. Jou et al., “Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75,” Nature, vol. 286, no. 5775, pp. 771–776, 1980.
[28]
R. S. Daniels, J. J. Shehel, and D. V. Wiley, “Amino acid sequences of the hemagglutinins of influenza viruses of the H3 subtype isolated from horses,” Journal of General Virology, vol. 66, pp. 457–464, 1985.
[29]
H. Kida, K. F. Shortridge, and R. G. Webster, “Origin of the hemagglutinin gene of H3N2 influenza viruses from pigs in China,” Virology, vol. 162, no. 1, pp. 160–166, 1988.
[30]
H. Kida, Y. Kawaoka, C. W. Naeve, and R. G. Webster, “Antigenic and genetic conservation of H3 influenza virus in wild ducks,” Virology, vol. 159, no. 1, pp. 109–119, 1987.
[31]
K. Nakajima, E. Nobusawa, T. Ogawa, and S. Nakajima, “Genetic divergence of the NS genes of avian influenza viruses,” Virology, vol. 158, no. 2, pp. 465–468, 1987.
[32]
Y. Kawaoka and R. G. Webster, “Evolution of the A/chicken/Pennsylvania/83 (H5N2) influenza virus,” Virology, vol. 146, no. 1, pp. 130–137, 1985.
[33]
A. Jahangir, S. Ruenphet, D. Shoham, M. Okamura, M. Nakamaura, and K. Takehara, “Phenotypic, genetic, and phylogeographical characterization of avian influenza virus subtype H5N2 isolated from northern pintail (Anas acuta) in Japan,” Virus Research, vol. 145, no. 2, pp. 329–333, 2009.
[34]
H. Hayashida, H. Toh, R. Kikuno, and T. Miyata, “Evolution of influenza virus genes,” Molecular Biology and Evolution, vol. 2, no. 4, pp. 289–303, 1985.
[35]
J. V. Kozlov, V. G. Gorbulev, and A. G. Kurmanova, “On the origin of the H1N1 (A/USSR/90/77) influenza virus,” Journal of General Virology, vol. 56, no. 2, pp. 437–440, 1981.
[36]
D. Anchlan, S. Ludwig, P. Nymadawa, J. Mendsaikhan, and C. Scholtissek, “Previous H1N1 influenza A viruses circulating in the Mongolian population,” Archives of Virology, vol. 141, no. 8, pp. 1553–1569, 1996.
[37]
I. V. Demiyanenko, A. A. Shilov, Z. K. Chuvakova et al., “Comparative characteristics of hemagglutinins of influenza A viruses (Hsw1N1) isolated from man and animals,” Voprosy Virusologii, vol. 33, no. 2, pp. 157–162, 1988.
[38]
G. Zhang, D. Shoham, D. Gilichinsky, S. Davydov, J. D. Castello, and S. O. Rogers, “Evidence of influenza a virus RNA in Siberian lake ice,” Journal of Virology, vol. 80, no. 24, pp. 12229–12235, 2006.
[39]
T. G. Fanning, R. D. Slemons, A. H. Reid, T. A. Janczewski, J. Dean, and J. K. Taubenberger, “1917 Avian influenza virus sequences suggest that the 1918 pandemic virus did not acquire its hemagglutinin directly from birds,” Journal of Virology, vol. 76, no. 15, pp. 7860–7862, 2002.
[40]
Y. Li, Z. Lin, J. Shi et al., “Detection of Hong Kong 97-like H5N1 influenza viruses from eggs of Vietnamese waterfowl,” Archives of Virology, vol. 151, no. 8, pp. 1615–1624, 2006.
[41]
S. Nakajima, Y. Takeuchi, and K. Nakajima, “Location on the evolutionary tree of influenza H3 haemagglutinin genes of Japanese strains isolated during 1985-6 season,” Epidemiology and Infection, vol. 100, no. 2, pp. 301–310, 1988.
[42]
M. H. Bikour, E. H. Frost, S. Deslandes, B. Talbot, J. M. Weber, and Y. Elazhary, “Recent H3N2 swine influenza virus with haemagglutinin and nucleoprotein genes similar to 1975 human strains,” Journal of General Virology, vol. 76, no. 3, pp. 697–703, 1995.
[43]
M. H. Bikour, E. H. Frost, S. Deslandes, B. Talbot, and Y. Elazhary, “Persistence of a 1930 swine influenza A (H1N1) virus in Quebec,” Journal of General Virology, vol. 76, no. 10, pp. 2539–2547, 1995.
[44]
D. K. Lvov, V. M. Zhdanov, F. Sadykhova, S. S. Yamnikova, V. A. Isachenko, and E. A. Vladimirtseva, “Isolation of a natural recombinant of influenza A virus (H1N3) from a sick child,” The Lancet, vol. 2, no. 8361, pp. 1246–1247, 1983.
[45]
H. S. Ip, P. L. Flint, J. C. Franson et al., “Prevalence of Influenza A viruses in wild migratory birds in Alaska: patterns of variation in detection at a crossroads of intercontinental flyways,” Virology Journal, vol. 5, p. 71, 2008.
[46]
A. Wallensten, V. J. Munster, A. D. M. E. Osterhaus et al., “Mounting evidence for the presence of influenza A virus in the avifauna of the Antarctic region,” Antarctic Science, vol. 18, no. 3, pp. 353–356, 2006.
[47]
Influenza Research Database—Details for A/arctic tern/Alaska/300/1975 virus, http://www.fludb.org/brc/fluSegmentDetails.do?ncbiGenomicAccession=CY015153&decorator=influenza, 2011.
[48]
S. M. Short and C. M. Short, “Quantitative PCR reveals transient and persistent algal viruses in Lake Ontario, Canada,” Environmental Microbiology, vol. 11, no. 10, pp. 2639–2648, 2009.
[49]
L. E. Wells and J. W. Deming, “Modelled and measured dynamics of viruses in Arctic winter sea-ice brines,” Environmental Microbiology, vol. 8, no. 6, pp. 1115–1121, 2006.
[50]
R. Maranger, D. F. Bird, and S. K. Juniper, “Viral and bacterial dynamics in Arctic sea ice during the spring algal bloom near Resolute, NWT, Canada,” Marine Ecology Progress Series, vol. 111, no. 1-2, pp. 121–128, 1994.
[51]
A. López-Bueno, J. Tamames, D. Velázquez, A. Moya, A. Quesada, and A. Alcamí, “High diversity of the viral community from an Antarctic lake,” Science, vol. 326, no. 5954, pp. 858–861, 2009.
[52]
M. M. Gowing, “Large viruses and infected microeukaryotes in Ross Sea summer pack ice habitats,” Marine Biology, vol. 142, no. 5, pp. 1029–1040, 2003.
[53]
J. D. Castello, S. O. Rogers, J. E. Smith, W. T. Starmer, and Y. Zhao, “Plant and bacterial viruses in the Greenland ice sheet,” in Life in Ancient Ice, J. D. Castello and S. O. Rogers, Eds., pp. 196–207, Princeton University Press, Princeton, NJ, USA, 2005.
[54]
L. V. Parker and C. J. Martel, Long-Term Survival of Enteric Microorganisms in Frozen Wastewater, US Army Corps of Engineers, Engineer Research and Development Center, Vicksburg, Miss, USA, 2002.
[55]
D. Greiff and C. Greiff, “Linear nonisothermal, single-step, stability studies of dried preparations of influenza virus,” Cryobiology, vol. 9, no. 1, pp. 34–37, 1972.
[56]
T. F. Smith and L. Reichrath, “Comparative recovery of 1972-1973 influenza virus isolates in embryonated eggs and primary rhesus monkey kidney cell cultures after one freeze thaw cycle,” American Journal of Clinical Pathology, vol. 61, no. 5, pp. 579–584, 1974.
[57]
R. G. Webster, V. S. Hinshaw, and W. J. Bean, “Antigenic shift in myxoviruses,” Medical Microbiology and Immunology, vol. 164, no. 1–3, pp. 57–68, 1977.
[58]
D. K. Lvov and S. S. Yanmilova, “Natural focality of onfluenza viruses,” Meditsinskaia Parazitologiia i Parazitarnye Bolezni, vol. 1, pp. 27–30, 1986.
[59]
J. D. Brown, D. E. Swayne, R. J. Cooper, R. E. Burns, and D. E. Stallknecht, “Persistence of H5 and H7 avian influenza viruses in water,” Avian Diseases, vol. 51, no. 1, pp. 285–289, 2007.
[60]
D. E. Stallknecht, M. T. Kearney, S. M. Shane, and P. J. Zwank, “Effects of pH, temperature, and salinity on persistence of avian influenza viruses in water,” Avian Diseases, vol. 34, no. 2, pp. 412–418, 1990.
[61]
D. E. Stallknecht, S. M. Shane, M. T. Kearney, and P. J. Zwank, “Persistence of avian influenza viruses in water,” Avian Diseases, vol. 34, no. 2, pp. 406–411, 1990.
[62]
J. Nazir, R. Haumacher, A. Ike, P. Stumpf, R. Bhm, and R. E. Marschang, “Long-term study on tenacity of avian influenza viruses in water (distilled water, normal saline, and surface water) at different temperatures,” Avian Diseases, vol. 54, no. 1, pp. 720–724, 2010.
[63]
G. Zhang, D. Shoham, D. Gilichinsky, S. Davydov, J. D. Castello, and S. O. Rogers, “Evidence of influenza a virus RNA in Siberian lake ice,” Journal of Virology, vol. 80, no. 24, pp. 12229–12235, 2006.
[64]
A. S. Lang, A. Kelly, and J. A. Runstadler, “Prevalence and diversity of avian influenza viruses in environmental reservoirs,” Journal of General Virology, vol. 89, no. 2, pp. 509–519, 2008.
[65]
N. J. Negovetich and R. G. Webster, “Thermostability of subpopulations of H2N3 influenza virus isolates from mallard ducks,” Journal of Virology, vol. 84, no. 18, pp. 9369–9376, 2010.
[66]
E. A. Gould, Virus Cryopreservation and Storage, http://www.springerlink.com/index/k782431871q16001.pdf.
[67]
U.S. Department of Agriculture, Animal and Plant Health Inspection Service and Veterinary Services [USDA APHIS, VS], “Highly pathogenic avian influenza. A threat to U.S. poultry,” 2002, USDA APHIS, VS, http://www.aphis.usda.gov/oa/pubs/avianflu.html, 2004.
[68]
P. De Benedictis, M. S. Beato, and I. Capua, “Inactivation of avian influenza viruses by chemical agents and physical conditions: a review,” Zoonoses and Public Health, vol. 54, no. 2, pp. 51–68, 2007.
[69]
I. V. Polozov, L. Bezrukov, K. Gawrisch, and J. Zimmerberg, “Progressive ordering with decreasing temperature of the phospholipids of influenza virus,” Nature Chemical Biology, vol. 4, no. 4, pp. 248–255, 2008.
[70]
Y. Fujiyoshi, N. P. Kume, K. Sakata, and S. B. Sato, “Fine structure of influenza A virus observed by electron cryo-microscopy,” EMBO Journal, vol. 13, no. 2, pp. 318–326, 1994.
[71]
E. M. Smith, C. P. Gerba, and J. L. Melnick, “Role of sediment in the persistence of enteroviruses in the estuarine environment,” Applied and Environmental Microbiology, vol. 35, no. 4, pp. 685–689, 1978.
[72]
J. D. Brown, D. E. Swayne, R. J. Cooper, R. E. Burns, and D. E. Stallknecht, “Persistence of H5 and H7 avian influenza viruses in water,” Avian Diseases, vol. 51, no. 1, pp. 285–289, 2007.
[73]
D. Shoham, “The modes of evolutionary emergence of primal and late pandemic influenza virus strains from viral reservoir in animals: an interdisciplinary analysis,” Influenza Research and Treatment, vol. 2011, Article ID 861792, 27 pages, 2011.
[74]
V. Trifonov, H. Khiabanian, and R. Rabadan, “Geographic dependence, surveillance, and origins of the 2009 influenza A (H1N1) virus,” New England Journal of Medicine, vol. 361, no. 2, pp. 115–119, 2009.
[75]
A. Jahangir, S. Ruenphet, S. Ueda et al., “Avian influenza and Newcastle disease viruses from northern pintail in Japan: isolation, characterization and inter-annual comparisons during 2006–2008,” Virus Research, vol. 143, no. 1, pp. 44–52, 2009.
[76]
A. Jahangir, S. Ruenphet, D. Shoham, M. Okamura, M. Nakamaura, and K. Takehara, “Phenotypic, genetic, and phylogeographical characterization of avian influenza virus subtype H5N2 isolated from northern pintail (Anas acuta) in Japan,” Virus Research, vol. 145, no. 2, pp. 329–333, 2009.
[77]
M. Worobey, “Phylogenetic evidence against evolutionary stasis and natural abiotic reservoirs of influenza A virus,” Journal of Virology, vol. 82, no. 7, pp. 3769–3774, 2008.
[78]
R. G. Webster, “Influenza: an emerging disease,” Emerging Infectious Diseases, vol. 4, no. 3, pp. 436–441, 1998.
[79]
R. Chen and E. C. Holmes, “Avian influenza virus exhibits rapid evolutionary dynamics,” Molecular Biology and Evolution, vol. 23, no. 12, pp. 2336–2341, 2006.
[80]
C. W. Olsen, A. Karasin, and G. Erickson, “Characterization of a swine-like reassortant H1N2 influenza virus isolated from a wild duck in the United States,” Virus Research, vol. 93, no. 1, pp. 115–121, 2003.
[81]
M. A. Ramakrishnan, P. Wang, M. Abin et al., “Triple reassortant swine influenza a (H3N2) virus in waterfowl,” Emerging Infectious Diseases, vol. 16, no. 4, pp. 728–730, 2010.
[82]
H. M. Yassine, M. Q. Al-Natour, C. W. Lee, and Y. M. Saif, “Interspecies and intraspecies transmission of triple reassortant H3N2 influenza A viruses,” Virology Journal, vol. 4, pp. 129–134, 2007.