1887

Abstract

Rotavirus evolves by using multiple genetic mechanisms which are an accumulation of spontaneous point mutations and reassortment events. Other mechanisms, such as cross-species transmission and inter-genotype recombination, may be also involved. One of the most interesting genotypes in the accumulation of these events is the G3 genotype. In this work, six new Spanish G3 sequences belonging to 0–2-year-old patients from Madrid were analysed and compared with 160 others of the same genotype obtained from humans and other host species to establish the evolutionary pathways of the G3 genotype. The following results were obtained: (i) there are four different lineages of the G3 genotype which have evolved in different species; (ii) Spanish G3 rotavirus sequences are most similar to the described sequences that belong to lineage I; (iii) several G3 genotype alleles were reassigned as other G genotypes; and (iv) inter-genotype recombination events in G3 viruses involving G1 and G2 were described. These findings strongly suggest multiple inter-species transmission events between different non-human mammalian species and humans.

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2009-04-01
2019-11-12
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References

  1. Alam, M. M., Kobayashi, N., Ishino, M., Nagashima, S., Paul, S. K., Chawla-Sarkar, M., Krishnan, T. & Naik, T. N. ( 2008; ). Identical rearrangement of NSP3 genes found in three independently isolated virus clones derived from mixed infection and multiple passages of Rotaviruses. Arch Virol 153, 555–559.[CrossRef]
    [Google Scholar]
  2. Arista, S., Giovannelli, L., Pistoia, D., Cascio, A., Parea, M. & Gerna, G. ( 1990; ). Electropherotypes, subgroups and serotypes of human rotavirus strains causing gastroenteritis in infants and young children in Palermo, Italy, from 1985 to 1989. Res Virol 141, 435–448.[CrossRef]
    [Google Scholar]
  3. Arista, S., Vizzi, E., Ferraro, D., Cascio, A. & Di Stefano, R. ( 1997; ). Distribution of VP7 serotypes and VP4 genotypes among rotavirus strains recovered from Italian children with diarrhoea. Arch Virol 142, 2065–2071.[CrossRef]
    [Google Scholar]
  4. Arista, S., Vizzi, E., Migliore, M. C., Di Rosa, E. & Cascio, A. ( 2003; ). High incidence of G9P[8] rotavirus infections in Italian children during the winter season 1999–2000. Eur J Epidemiol 18, 711–714.
    [Google Scholar]
  5. Cao, D., Barro, M. & Hoshino, Y. ( 2008; ). Porcine rotavirus bearing an aberrant gene stemming from an intergenic recombination of the NSP2 and NSP5 genes is defective and interfering. J Virol 82, 6073–6077.[CrossRef]
    [Google Scholar]
  6. Caprioli, A., Pezzella, C., Morelli, R., Giammaco, A., Arista, S., Crotti, D., Facchini, M., Guglielmetti, P., Piersimoni, C. & Luzzi, I. ( 1996; ). Enteropathogens associated with childhood diarrhea in Italy. The Italian Study Group of Gastrointestinal Infections. Pediatr Infect Dis J 15, 876–883.[CrossRef]
    [Google Scholar]
  7. Chnaiderman, J., Diaz, J., Magnusson, G., Liprandi, F. & Spencer, E. ( 1998; ). Characterization of a rotavirus rearranged gene 11 by gene reassortment. Arch Virol 143, 1711–1722.[CrossRef]
    [Google Scholar]
  8. Cook, N., Bridger, J., Kendall, K., Iturriza-Gomara, M., El-Attar, L. & Gray, J. ( 2004; ). The zoonotic potential of rotavirus. J Infect 48, 289–302.[CrossRef]
    [Google Scholar]
  9. Das, B. K., Gentsch, J. R., Hoshino, Y., Ishida, S. I., Nakagomi, O., Bhan, M. K., Kumar, R. & Glass, R. I. ( 1993; ). Characterization of the G serotype and genogroup of New Delhi newborn rotavirus strain 116E. Virology 197, 99–107.[CrossRef]
    [Google Scholar]
  10. De Grazia, S., Ramirez, S., Giammanco, G. M., Colomba, C., Martella, V., Lo Biundo, C., Mazzola, R. & Arista, S. ( 2007; ). Diversity of human rotaviruses detected in Sicily, Italy, over a 5-year period (2001–2005). Arch Virol 152, 833–837.[CrossRef]
    [Google Scholar]
  11. De Leener, K., Rahman, M., Matthijnssens, J., Van Hoovels, L., Goegebuer, T., van der Donck, I. & Van Ranst, M. ( 2004; ). Human infection with a P[14], G3 lapine rotavirus. Virology 325, 11–17.[CrossRef]
    [Google Scholar]
  12. Dennehy, P. H. ( 2008; ). Rotavirus vaccines: an overview. Clin Microbiol Rev 21, 198–208.[CrossRef]
    [Google Scholar]
  13. Desselberger, U. ( 1996; ). Genome rearrangements of rotaviruses. Adv Virus Res 46, 69–95.
    [Google Scholar]
  14. Desselberger, U., Iturriza-Gómara, M. & Gray, J. J. ( 2001; ). Rotavirus epidemiology and surveillance. Novartis Found Symp 238, 125–147.
    [Google Scholar]
  15. Di Stefano, D. J., Kraiouchkine, N., Mallette, L., Maliga, M., Kulnis, G., Keller, P. M., Clark, H. F. & Shaw, A. R. ( 2005; ). Novel rotavirus VP7 typing assay using a one-step reverse transcriptase PCR protocol and product sequencing and utility of the assay for epidemiological studies and strain characterization, including serotype subgroup analysis. J Clin Microbiol 43, 5876–5880.[CrossRef]
    [Google Scholar]
  16. Dunn, S. J., Greenberg, H. B., Ward, R. L., Nakagomi, O., Burns, J. W., Vo, P. T., Pax, K. A., Das, K., Gowda, K. & Rao, C. D. ( 1993; ). Serotypic and genotypic characterisation of human serotype 10 rotaviruses from asymptomatic neonates. J Clin Microbiol 31, 165–169.
    [Google Scholar]
  17. El-Attar, L., Dhaliwal, W., Howard, C. R. & Bridger, J. C. ( 2001; ). Rotavirus cross-species pathogenicity: molecular characterization of a bovine rotavirus pathogenic for pigs. Virology 291, 172–182.[CrossRef]
    [Google Scholar]
  18. Estes, M. K. ( 2001; ). Rotaviruses and their replication. In Fields Virology, 4th edn, vol. 2, pp. 1747–1785. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  19. Fujiwara, Y. & Nakagomi, O. ( 1997; ). Interspecies sharing of two distinct non-structural protein 1 alleles among human and animal rotaviruses as revealed by dot hybridisation. J Clin Microbiol 35, 2703–2705.
    [Google Scholar]
  20. Fukai, K., Takahashi, T., Tajima, K., Koike, S., Iwane, K. & Inoue, K. ( 2007; ). Molecular characterization of a novel bovine group A rotavirus. Vet Microbiol 123, 217–224.[CrossRef]
    [Google Scholar]
  21. Geier, D. A., King, P. G., Sykes, L. K. & Geier, M. R. ( 2008; ). RotaTeq vaccine adverse events and policy considerations. Med Sci Monit 14, PH9–PH16.
    [Google Scholar]
  22. Gentsch, J. R., Woods, P. A., Ramachandran, M., Das, B. K., Leite, J. P., Alfieri, A., Kumar, R., Bhan, M. K. & Glass, R. I. ( 1996; ). Review of G and P typing results from a global collection of rotavirus strains: implications for vaccine development. J Infect Dis 174, S30–S36.[CrossRef]
    [Google Scholar]
  23. Gentsch, J. R., Laird, A. R., Bielfelt, B., Griffin, D. D., Banyai, K., Ramachandran, M., Jain, V., Cunliffe, N. A., Nakagomi, O. & other authors ( 2005; ). Serotype diversity and reassortment between human and animal rotavirus strains: implications for rotavirus vaccine programs. J Infect Dis 192, S146–S159.[CrossRef]
    [Google Scholar]
  24. Gouvea, V., Glass, R. I., Woods, P., Taniguchi, K., Clark, H. F., Forrester, B. & Fang, Z. Y. ( 1990; ). Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28, 276–282.
    [Google Scholar]
  25. Hoshino, Y. & Kapikian, A. Z. ( 1994; ). Rotavirus antigens. Curr Top Microbiol Immunol 185, 179–229.
    [Google Scholar]
  26. Hoshino, Y. & Kapikian, A. Z. ( 2000; ). Rotavirus serotypes: classification and importance in epidemiology, immunity, and vaccine development. J Health Popul Nutr 18, 5–14.
    [Google Scholar]
  27. Hoshino, Y., Jones, R. W. & Kapikian, A. Z. ( 2002; ). Characterization of neutralization specificities of outer capsid spike protein VP4 of selected murine, lapine, and human rotavirus strains. Virology 299, 64–71.[CrossRef]
    [Google Scholar]
  28. Hoshino, Y., Honma, S., Jones, R. W., Ross, J., Santos, N., Gentsch, J. R., Kapikian, A. Z. & Hesse, R. A. ( 2005; ). A porcine G9 rotavirus strain shares neutralization and VP7 phylogenetic sequence lineage 3 characteristics with contemporary human G9 rotavirus strains. Virology 332, 177–188.[CrossRef]
    [Google Scholar]
  29. Iizuka, M., Kaga, E., Chiba, M., Masamune, O., Gerna, G. & Nakagomi, O. ( 1994; ). Serotype G6 human rotavirus sharing a conserved genetic constellation with natural reassortants between members of the bovine and AU-1 genogroups. Arch Virol 135, 427–432.[CrossRef]
    [Google Scholar]
  30. Iturriza-Gómara, M., Desselberger, U. & Gray, J. ( 2003; ). Molecular epidemiology of rotaviruses: genetic mechanisms associated with diversity. In Viral Gastroenteritis, pp. 317–344. Edited by U. Desselberger & J. Gray. Amsterdam: Elsevier.
  31. Kapikian, A. Z., Hoshino, Y. & Chanock, R. M. ( 2001; ). Rotavirus. In Fields Virology, 4th edn, vol. 2, pp. 1787–1833. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott Williams & Wilkins.
  32. Kebaabetswe, L. P., Sebunya, T. K., Matsheka, M. I. & Ndung'u, T. ( 2005; ). Detection and molecular characterisation of group A rotavirus from children in northern Botswana. East Afr Med J 82, 203–208.
    [Google Scholar]
  33. Khamrin, P., Maneekarn, N., Peerakome, S., Yagyu, F., Okitsu, S. & Ushijima, H. ( 2006; ). Molecular characterization of a rare G3P[3] human rotavirus reassortant strain reveals evidence for multiple human-animal interspecies transmissions. J Med Virol 78, 986–994.[CrossRef]
    [Google Scholar]
  34. Kojima, K., Taniguchi, K., Kawagishi-Kobayashi, M., Matsuno, S. & Urasawa, S. ( 2000; ). Rearrangement generated in double genes, NSP1 and NSP3, of viable progenies from a human rotavirus strain. Virus Res 67, 163–171.[CrossRef]
    [Google Scholar]
  35. Kumar, S., Tamura, K. & Nei, M. ( 2004; ). mega3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5, 150–163.[CrossRef]
    [Google Scholar]
  36. Lai, H., Lin, S., Lin, H., Ku, C., Wang, L. & Yang, C. ( 2005; ). Phylogenetic analyses of human rotavirus in central Taiwan in 1996, 2001 and 2002. J Clin Virol 32, 199–217.[CrossRef]
    [Google Scholar]
  37. Lee, J. B., Young, S. J., Nakagomi, T., Park, S. Y., Kim, T. J., Song, C. S., Jang, H. K., Kim, B. S. & Nakagomi, O. ( 2003; ). Isolation, serologic and molecular characterization of the first G3 caprine rotavirus. Arch Virol 148, 643–657.[CrossRef]
    [Google Scholar]
  38. Liprandi, F., Gerder, M., Bastidas, Z., López, J. A., Pujol, F. H., Ludert, J. E., Joelsson, D. B. & Ciarlet, M. ( 2003; ). A novel type of VP4 carried by a porcine rotavirus strain. Virology 315, 373 [CrossRef]
    [Google Scholar]
  39. Maneekarn, N., Khamrin, P., Chan-it, W., Peerakome, S., Sukchai, S., Pringprao, K. & Ushijima, H. ( 2006; ). Detection of rare G3P[19] porcine rotavirus strains in Chiang Mai, Thailand, provides evidence for origin of the VP4 genes of Mc323 and Mc345 human rotaviruses. J Clin Microbiol 44, 4113–4119.[CrossRef]
    [Google Scholar]
  40. Martella, V., Pratelli, A., Greco, G., Gentile, M., Fiorente, P., Tempesta, M. & Buonavoglia, C. ( 2001; ). Nucleotide sequence variation of the VP7 gene of two G3-Type rotaviruses isolated from dogs. Virus Res 74, 17–25.[CrossRef]
    [Google Scholar]
  41. Martella, V., Ciarlet, M., Camarda, A., Pratelli, A., Tempesta, M., Greco, G., Cavalli, A., Elia, G., Decaro, N. & other authors ( 2003; ). Molecular characterization of the VP4, VP6, VP7, and NSP4 genes of lapine rotavirus identified in Italy: emergence of a novel VP4 genotype. Virology 314, 358–370.[CrossRef]
    [Google Scholar]
  42. Martella, V., Bányai, K., Ciarlet, M., Iturriza-Gómara, M., Lorusso, E., De Grazia, S., Arista, S., Decaro, N., Elia, G. & other authors ( 2006a; ). Relationships among porcine and human P[6] rotaviruses: evidence that the different human P[6] lineages have originated from multiple interspecies transmission events. Virology 344, 509–519.[CrossRef]
    [Google Scholar]
  43. Martella, V., Ciarlet, M., Bányai, K., Lorusso, E., Cavalli, A., Corrente, M., Elia, G., Arista, S., Camero, M., Desario, C. & other authors ( 2006b; ). Identification of a novel VP4 genotype carried by a serotype G5 porcine rotavirus strain. Virology 346, 301–311.[CrossRef]
    [Google Scholar]
  44. Martella, V., Bányai, K., Lorusso, E., Decaro, N., Bellacicco, A., Desario, C., Corrente, M., Greco, G., Moschidou, P. & other authors ( 2007; ). Genetic heterogeneity in the VP7 of group C rotaviruses. Virology 367, 358–366.[CrossRef]
    [Google Scholar]
  45. Martin, D. P., Williamson, C. & Posada, D. ( 2005; ). RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef]
    [Google Scholar]
  46. Martínez-Laso, J., Moscoso, J., Zamora, J., Lowy, E., Vargas-Alarcon, G., Serrano-Vela, J. & Arnaiz-Villena, A. ( 2004; ). Different evolutionary pathway of B*570101 and B*5801 (B17 group) alleles based in intron sequences. Immunogenetics 55, 866–872.[CrossRef]
    [Google Scholar]
  47. Martínez-Laso, J., Moscoso, J., Zamora, J., Gómez-Casado, E. & Arnaiz-Villena, A. ( 2006; ). Generation of the B*41 group of alleles as indicated by intron sequences. Tissue Antigens 67, 70–74.[CrossRef]
    [Google Scholar]
  48. Matthijnssens, J., Rahman, M., Martella, V., Xuelei, Y., De Vos, S., De Leener, K., Ciarlet, M., Buonavoglia, C. & Van Ranst, M. ( 2006; ). Full genomic analysis of human rotavirus strain B4106 and lapine rotavirus strain 30/96 provides evidence for interspecies transmission. J Virol 80, 3801–3810.[CrossRef]
    [Google Scholar]
  49. McNeal, M. M., Sestak, K., Choi, A. H., Basu, M., Cole, M. J., Aye, P. P., Bohm, R. P. & Ward, R. L. ( 2005; ). Development of a rotavirus-shedding model in rhesus macaques, using a homologous wild-type rotavirus of a new P genotype. J Virol 79, 944–954.[CrossRef]
    [Google Scholar]
  50. Nakagomi, O. & Nakagomi, T. ( 1993; ). Interspecies transmission of rotaviruses studied from the perspective of genogroup. Microbiol Immunol 37, 337–348.[CrossRef]
    [Google Scholar]
  51. Nakagomi, O. & Nakagomi, T. ( 2002; ). Genomic relationships among rotaviruses recovered from various animal species as revealed by RNA–RNA hybridization assays. Res Vet Sci 73, 207–214.[CrossRef]
    [Google Scholar]
  52. Nakagomi, O., Nakagomi, T., Hoshido, Y., Flores, J. & Kapilian, A. Z. ( 1987; ). Genetic analysis of a human rotavirus that belongs to subgroup I but has an RNA pattern typical of subgroup II human rotaviruses. J Clin Microbiol 25, 1159–1164.
    [Google Scholar]
  53. Nakagomi, O., Ohshima, A., Aboudy, Y., Shif, I., Mochizuki, M., Nakagomi, T. & Gotlieb-Stematsky, T. ( 1990; ). Molecular identification by RNA-RNA hybridization of a human rotavirus that is closely related to rotaviruses of feline and canine origin. J Clin Microbiol 28, 1198–1203.
    [Google Scholar]
  54. Nguyen, T. A., Khamrin, P., Trinh, Q. D., Phan, T. G., Pham, D., Hoang, P., Hoang, K. T., Yagyu, F., Okitsu, S. & Ushijima, H. ( 2007; ). Sequence analysis of Vietnamese P[6] rotavirus strains suggests evidence of interspecies transmission. J Med Virol 79, 1959–1965.[CrossRef]
    [Google Scholar]
  55. Nishikawa, K., Hoshino, Y., Taniguchi, K., Green, K. Y., Greenberg, H. B., Kapilian, A. Z., Chanock, R. M. & Gorziglia, M. ( 1989; ). Rotavirus VP7 neutralization epitopes of serotype 3 strains. Virology 171, 503–515.[CrossRef]
    [Google Scholar]
  56. Palombo, E. A. ( 2002; ). Genetic analysis of Group A rotaviruses: evidence for interspecies transmission of rotavirus genes. Virus Genes 24, 11–20.[CrossRef]
    [Google Scholar]
  57. Palombo, E. A., Clark, R. & Bishop, R. F. ( 2000; ). Characterisation of a ‘European-like’ serotype G8 human rotavirus isolated in Australia. J Med Virol 60, 56–62.[CrossRef]
    [Google Scholar]
  58. Parra, G. I., Bok, K., Martínez, M. & Gomez, J. A. ( 2004; ). Evidence of rotavirus intragenic recombination between two sublineages of the same genotype. J Gen Virol 85, 1713–1716.[CrossRef]
    [Google Scholar]
  59. Parra, G. I., Vidales, G., Gomez, J. A., Fernandez, F. M., Parreño, V. & Bok, K. ( 2008; ). Phylogenetic analysis of porcine rotavirus in Argentina: increasing diversity of G4 strains and evidence of interspecies transmission. Vet Microbiol 126, 243–250.[CrossRef]
    [Google Scholar]
  60. Patton, J. T., Taraporewala, Z., Chen, D., Chizhikov, V., Jones, M., Elhelu, A., Collins, M., Kearney, K., Wagner, M. & other authors ( 2001; ). Effect of intragenic rearrangement and changes in the 3′ consensus sequence on NSP1 expression and rotavirus replication. J Virol 75, 2076–2086.[CrossRef]
    [Google Scholar]
  61. Phan, T. G., Okitsu, S., Maneekarn, N. & Ushijima, H. ( 2007a; ). Evidence of intragenic recombination in G1 rotavirus VP7 genes. J Virol 81, 10188–10194.[CrossRef]
    [Google Scholar]
  62. Phan, T. G., Okitsu, S., Maneekarn, N. & Ushijima, H. ( 2007b; ). Genetic heterogeneity, evolution and recombination in emerging G9 rotaviruses. Infect Genet Evol 7, 656–663.[CrossRef]
    [Google Scholar]
  63. Ramig, R. F. ( 1997; ). Genetics of rotaviruses. Annu Rev Microbiol 51, 225–255.[CrossRef]
    [Google Scholar]
  64. Reidy, N., O'Halloran, F., Fanning, S., Cryan, B. & O'Shea, H. ( 2005; ). Emergence of G3 and G9 rotavirus and increased incidence of mixed infections in the southern region of Ireland 2001–2004. J Med Virol 77, 571–578.[CrossRef]
    [Google Scholar]
  65. Sánchez-Fauquier, A., Montero, V., Moreno, S., Solé, M., Colomina, J., Iturriza-Gómara, M., Revilla, A., Wilhelmi, I., & Gray, J., Gegavi/VIGESS-Net Group ( 2006; ). Human rotavirus G9 and G3 as major cause of diarrhea in hospitalized children, Spain. Emerg Infect Dis 12, 1536–1541.[CrossRef]
    [Google Scholar]
  66. Santos, N. & Hoshino, Y. ( 2005; ). Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 15, 29–56.[CrossRef]
    [Google Scholar]
  67. Santos, N., Volotao, E. M., Soares, C. C., Albuquerque, M. C., da Silva, F. M., de Carvalho, T. R., Pereira, C. F., Chizhikov, V. & Hoshino, Y. ( 2001; ). Rotavirus strains bearing genotype G9 or P[9] recovered from Brazilian children with diarrhea from 1997 to 1999. J Clin Microbiol 39, 1157–1160.[CrossRef]
    [Google Scholar]
  68. Schnepf, N., Deback, C., Dehee, A., Gault, E., Parez, N. & Garbarg-Chenon, A. ( 2008; ). Rearrangements of rotavirus genomic segment 11 are generated during acute infection of immunocompetent children and do not occur at random. J Virol 82, 3689–3696.[CrossRef]
    [Google Scholar]
  69. Steyer, A., Poljsak-Prijatelj, M., Barlic-Maganja, D. & Marin, J. ( 2008; ). Human, porcine and bovine rotaviruses in Slovenia: evidence of interspecies transmission and genome reassortment. J Gen Virol 89, 1690–1698.[CrossRef]
    [Google Scholar]
  70. Theamboonlers, A., Bhattarakosol, P., Chongsrisawat, V., Sungkapalee, T., Wutthirattanakowit, N. & Poovorawan, Y. ( 2008; ). Molecular characterization of group A human rotaviruses in Bangkok and Buriram, Thailand during 2004–2006 reveals the predominance of G1P[8], G9P[8] and a rare G3P[19] strain. Virus Genes 36, 289–298.[CrossRef]
    [Google Scholar]
  71. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  72. Tsugawa, T. & Hoshino, Y. ( 2008; ). Whole genome sequence and phylogenetic analyses reveal human rotavirus G3P[3] strains Ro1845 and HCR3A are examples of direct virion transmission of canine/feline rotaviruses to humans. Virology 380, 344–353.[CrossRef]
    [Google Scholar]
  73. Urasawa, S., Hasegawa, A., Urasawa, T., Taniguchi, K., Wakasugi, F., Suzuki, H., Inouye, S., Pongprot, B., Supawadee, J. & Suprasert, S. ( 1992; ). Antigenic and genetic analyses of human rotaviruses in Chiang Mai, Thailand: evidence for a close relationship between human and animal rotaviruses. J Infect Dis 166, 227–234.[CrossRef]
    [Google Scholar]
  74. Varghese, V., Das, S., Singh, N. B., Kojima, K., Bhattacharya, S. K., Krishnan, T., Kobayashi, N. & Naik, T. N. ( 2004; ). Molecular characterization of a human rotavirus reveals porcine characteristics in most of the genes including VP6 and NSP4. Arch Virol 149, 155–172.
    [Google Scholar]
  75. Zomer, T. P., van Duynhoven, Y. T., Mangen, M. J., van der Maas, N. A., Vennema, H., Boot, H. & de Melker, H. E. ( 2008; ). Assessing the introduction of universal rotavirus vaccination in the Netherlands. Vaccine 26, 3757–3764.[CrossRef]
    [Google Scholar]
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