Multiple sublineages of influenza a virus (H5N1), Vietnam, 2005-2007.Phylogenetic phy·lo·ge·net·ic adj. 1. Of or relating to phylogeny or phylogenetics. 2. Relating to or based on evolutionary development or history. analysis of influenza subtype (programming) subtype - If S is a subtype of T then an expression of type S may be used anywhere that one of type T can and an implicit type conversion will be applied to convert it to type T. H5N1 viruses isolated from Vietnam during 2005-2007 shows that multiple sublineages are present in Vietnam. Clade 2.3.4 viruses have replaced clade 1 viruses in northern Vietnam, and clade 1 viruses have been detected in southern Vietnam. Reassortment between these 2 sublineages has also occurred. ********** Multiple sublineages of highly pathogenic avian influenza avian influenza: see influenza. (HPAI HPAI Highly Pathogenic Avian Influenza HPAI Hospital Pharmacists Association, Ireland HPAI Hewlett Packard Associates International ) virus (H5N1) have been detected from poultry in Vietnam since 2001 (1-3). However, the introduction of subtype H5N1 genotype Z virus in 2003 resulted in unprecedented widespread outbreaks in poultry and repeated interspecies transmission to humans; 93 cases were confirmed in Vietnam by the end of November 2005 (4,5). These viruses became endemic in poultry in Vietnam, causing repeated outbreaks, and have been transmitted to other Southeast Asian countries, where they have caused poultry outbreaks and human infections (3-6). This virus is designated as clade 1 in the World Health Organization (WHO) influenza (H5N1) virus nomenclature system (7). In 2005 a novel reassortant virus of subtype H5N1 (genotype G) from clade 2.3.2 (Mixed/VNM2) was also recognized in Vietnam (2). The close phylogenetic relationship of the influenza virus influenza virus n. Any of three viruses of the genus Influenzavirus designated type A, type B, and type C, that cause influenza and influenzalike infections. (H5N1) lineages in Vietnam and the southern People's Republic People's Republic n. A political organization founded and controlled by a national Communist party. of China suggests repeated introduction of subtype H5N1 virus into Vietnam (2,3,8). However, the development and evolution of influenza virus (H5N1) in Vietnam since 2005 are not clear. Since 2003, multiple sublineages of the Goose/ Guangdong/1/96 (Gs/GD-like virus became established in poultry in China (2). However, in late 2005, clade 2.3.4 (Fujian-like) influenza virus (H5N1) became dominant and replaced almost all of these previously circulating sublineages; these sublineages have also been been detected in wild birds in Hong Kong Hong Kong (hŏng kŏng), Mandarin Xianggang, special administrative region of China, formerly a British crown colony (2005 est. pop. 6,899,000), land area 422 sq mi (1,092 sq km), adjacent to Guangdong prov. Special Administrative Region A special administrative region may be:
SAR - segmentation and reassembly ), China, and from poultry in Lao People's Democratic Republic, Malaysia, and Thailand (3). Vaccination of poultry in Vietnam against H5 virus was initiated in October 2005. After that, no influenza (H5N1) outbreaks were reported in the country from December 2005 to October 2006 (9). However, renewed subtype H5N1 outbreaks in poultry have occurred in Vietnam since November 2006, with evidence of limited human infections during 2007 and 2008. Whether clade 2.3.4 viruses have been introduced into Vietnam is not known. The Study We sequenced the whole genomes of 33 avian influenza virus (H5N1) isolates collected during poultry outbreaks in Vietnam from October 2005 through May 2007. All sequences that were generated in this study have been deposited in GenBank (CY029508-CY029771). The virus was primarily detected in aquatic poultry (ducks, muskovy ducks), but it was also isolated from 2 chickens in December 2006 and January 2007. The date and location of virus isolation are summarized in the Table and Figure 1, panel A. To understand the developments of influenza virus (H5N1) in Vietnam, we characterized all 8 gene segments of these 33 viral isolates and phylogenetically phy·lo·ge·net·ic adj. 1. Of or relating to phylogeny or phylogenetics. 2. Relating to or based on evolutionary development or history: a phylogenetic classification of species. analyzed them with all available influenza virus (H5N1) previously isolated from Vietnam, Thailand, Malaysia, Lao People's Democratic Republic, and southern China and with reference viruses belonging to each of the designated clades of the WHO influenza (H5N1) nomenclature system. Sequence assembly, editing, multiple sequence alignment A multiple sequence alignment (MSA) is a sequence alignment of three or more biological sequences, generally protein, DNA, or RNA. In general, the input set of query sequences are assumed to have an evolutionary relationship by which they share a lineage and are descended from a , neighbor-joining, and Bayesian phylogenetic analyses were conducted as previously described (3). Maximum-likelihood trees were constructed by using Garli version 9.04 (10). The hemagglutinin hemagglutinin /he·mag·glu·ti·nin/ (-gloo´ti-nin) an antibody that causes agglutination of erythrocytes. cold hemagglutinin one which acts only at temperatures near 4° C. (HA) genes of all 33 Vietnam isolates were derived from the Gs/GD-like lineage; however, they fell into 3 distinct sublineages (Figure 1, panel B). Seventeen of 33 isolates analyzed were clade 1; however, 15 isolates between March and May 2007 belonged to clade 2.3.4. A single virus isolated in February 2006 (Muscovy duck/Vietnam/1455/2006) clustered within clade 2.3.2. Phylogenetic analyses also showed a geographic distinction among the isolates characterized in this study. Isolates from samples taken in the northern provinces of Vietnam belonged to clades 2.3.2 and 2.3.4, whereas all isolates in the southern provinces of Vietnam were clade 1 (Figure 1). The clade 1 viruses isolated in the southern provinces from October 2005 through January 2007 were most closely related to viral isolates from poultry in Cambodia in the same period. When one considers the shared land border between Cambodia and southern Vietnam, the close relatedness of these viruses is reasonable. Two of the human influenza (H5N1) cases that were detected from Cambodia were located near the Vietnam-Cambodia border region (11). The genetic similarity of strains of influenza virus (H5N1) in Cambodia and southern Vietnam have been observed since 2004 (4). The clade 2.3.2 and clade 2.3.4 viruses isolated from northern Vietnam were most closely related to virus isolated from poultry in Guangxi, China (Figure 1, panel B). Because Guangxi shares a border with Vietnam and trade is extensive between those regions, these viruses were most likely introduced into northern Vietnam through poultry trade. However, the clade 2.3.4 viruses from Vietnam do not form a monophyletic monophyletic /mono·phy·let·ic/ (mon?o-fi-let´ik) descended from a common ancestor or stem cell. mon·o·phy·let·ic adj. 1. Descended or derived from one original stock or source. group within clade 2.3.4. Therefore, unlike the single introduction of clade 1 viruses in 2003 (4), these results raise the possibility of multiple introductions of the clade 2.3.4 viruses into northern Vietnam. Phylogenetic analyses of the neuraminidase neuraminidase /neu·ra·min·i·dase/ (-ah-min´i-das) an enzyme of the surface coat of myxoviruses that destroys the neuraminic acid of the cell surface during attachment, thereby preventing hemagglutination. gene and all internal gene segments (data not shown) show that while most of the isolates were genotype Z viruses, they also formed distinct groups that were broadly similar to the evolutionary relationships seen in the HA tree. Duck/Vietnam/37/2007, which belongs to clade 2.3.4, shared the internal gene constellation of clade 1 viruses (Figure 2), providing evidence for cocirculation of these virus groups and evidence of reassortment between different sublineages within Vietnam influenza (H5N1) isolates. A single influenza (H5N1) genotype G virus (Muscovy duck/ Vietnam/1455/2006) was also identified in February 2006, which indicates that genotype G viruses may be persistent in poultry in Vietnam (Figure 2). These results confirm that the genetic diversity of strains of influenza virus (H5N1) in Vietnam is similar to that in southern China during the same period (3). [FIGURE 1 OMITTED] The motif of multiple basic amino acids at the HA cleavage site cleavage site n. See restriction site. that is characteristic of HPAI was maintained in all viruses characterized; however, clade-specific mutations were observed in different sublineages, consistent with previous reports (3,4,8,12). The receptor-binding pocket of HA1 retains Gln 222 and Gly 224 (H5 numbering), which preferentially binds avian-like [alpha]2,3-NeuAcGal linkages. However, all 12 clade 2.3.4 viruses and the single clade 2.3.2 virus have an Arg-212-Lys mutation in the HA, whereas 12 clade 1 viruses (marked on Figure 1) have a Ser-123-Pro mutation, previously reported from a Vietnam influenza (H5N1) human isolate (8), which has been associated with receptor binding. The importance of this change is not clear (13,14). Mutations in the Matrix protein 2 ion channel ion channel n. See channel. associated with amantadine amantadine /aman·ta·dine/ (ah-man´tah-den) an antiviral compound used as the hydrochloride salt to treat influenza A; also used as an antidyskinetic in the treatment of parkinsonism and drug-induced extrapyramidal reactions. resistance were detected in all clade 1 virus isolates tested. These viral strains retained the dual mutations Leu Leu leucine. Leu abbr. leucine Leu leucine. 26Ile and Ser30Asn in the M2 protein similar to previous clade 1 strains (15). No mutation associated with amantadine resistance was recognized in those clade 2.3.2 and clade 2.3.4 strains except the reassortant Dk/VNM/37/07, which had an additional Val-27-Ala mutation in the M2 protein. Thus we recorded an HPAI (H5N1) virus strain with a triple mutation associated with amantadine resistance. All viruses characterized do not have mutations in the NA gene that confer resistance to oseltamivir. Other known virulence mutations, including at polymerase basic protein 2 position 627, were not present in any of the viruses characterized. Conclusions This study confirms that clade 2.3.4 virus sublineages that are dominant in southern China have now spread to northern Vietnam (3). These viruses appear to have replaced the clade 1 viruses in northern Vietnam just as previous influenza (H5N1) sublineages were replaced in southern China (3); however, clade 1 viruses are still detected in the southern provinces of Vietnam. It is, therefore, possible that the clade 1 viruses in southern Vietnam may eventually be replaced by clade 2.3.4. The availability of extensive genetic data from southern China enables us to recognize the development of influenza virus (H5N1) in Vietnam and indicates that clade 2.3.4 viruses may have been introduced into Vietnam on multiple occasions. However, because systematic surveillance data are lacking, determining the interaction of viruses between the northern and southern provinces of Vietnam, and also between different countries in Southeast Asia Southeast Asia, region of Asia (1990 est. pop. 442,500,000), c.1,740,000 sq mi (4,506,600 sq km), bounded roughly by the Indian subcontinent on the west, China on the north, and the Pacific Ocean on the east. , is not possible. When one considers that multiple sublineages of influenza virus (H5N1) are simultaneously endemic to Southeast Asia, systematic surveillance in poultry remains essential to understand the further evolution of this subtype in this region and the potential for pandemic pandemic /pan·dem·ic/ (pan-dem´ik) 1. a widespread epidemic of a disease. 2. widely epidemic. pan·dem·ic adj. Epidemic over a wide geographic area. n. emergence, as well as to monitor the efficacy and cross-protection of poultry vaccines. [FIGURE 2 OMITTED] Acknowledgments We thank the Department of Animal Health of Vietnam for providing some of the viruses used in this study. This study was supported by the Research Grants Council (HKU HKU University of Hong Kong HKU Hogeschool voor de Kunsten Utrecht (Utrecht School of The Arts, The Netherlands) HKU Hot Key Users 1/05C) of the Hong Kong SAR government, the Li Ka-Shing
Dr T.D. Nguyen has been the head of the Department of Virology virology, study of viruses and their role in disease. Many viruses, such as animal RNA viruses and viruses that infect bacteria, or bacteriophages, have become useful laboratory tools in genetic studies and in work on the cellular metabolic control of gene expression in the National Institute of Veterinary Research since 1988. His research interests include viral diseases viral diseases Diseases caused by viruses. Long-term immunity usually follows viral childhood diseases (see chickenpox). The common cold recurs into adulthood because many different viruses cause its symptoms, and immunity against one does not protect against others. of poultry and swine. References (1.) Nguyen DC, Uyeki TM, Jadhao S, Maines T, Shaw M, Matsuoka Y, et al. Isolation and characterization of avian influenza viruses, including highly pathogenic H5N1, from poultry in live bird markets in Hanoi, Vietnam, in 2001. J Virol. 2005;79:4201-12. (2.) Chen H, Smith GJD GJD Great Japanese Dog , Li KS, Wang J, Fan XF, Rayner JM, et al. Establishment of multiple sub-lineages of H5N1 influenza virus in Asia--implications for pandemic control. Proc Natl Acad Sci U S A. 2006; 103:2845-50. (3.) Smith GJ, Fan XH, Wang J, Li KS, Qin K, Zhang JX, et al. Emergence and predominance of an H5N1 influenza variant in China. Proc Natl Acad Sci U S A. 2006;103:16936-41. (4.) Smith GJD, Naipospos TSP, Nguyen TD, de Jong De Jong is the most common Dutch surname. Many people bear this name, including many important historical figures. Some of these people are mentioned below. De Jong may mean:
(5.) World Health Organization. Epidemiological record of WHO-confirmed human cases of avian influenza A (H5N1) infection. Wkly Epidemiol Rec. 2006;81:249-60. (6.) Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM, Nguyen VC, et al. Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med. 2004;350:1179-88. (7.) World Health Organization. Towards a unified nomenclature system for the highly pathogenic H5N1 avian influenza viruses. 2007 [cited 2007 Oct 10]. Available from http://www.who.int/csr/disease/ avian_influenza/guidelines/nomenclature/en (8.) World Health Organization Global Influenza Program Surveillance Network. Evolution of H5N1 avian influenza viruses in Asia. Emerg Infect Dis. 2005; 11:1515-21. (9.) Food and Agricultural Organization of the United Nations. Avian Influenza Disease Emergency Bulletin. 2006; issue 43 [cited 2007 Oct 10]. Available from http://www.fao.org/avianflu/en/AIDEnews.html (10.) Zwickl DJ. Genetic algorithm genetic algorithm - (GA) An evolutionary algorithm which generates each individual from some encoded form known as a "chromosome" or "genome". Chromosomes are combined or mutated to breed new individuals. approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion [dissertation]. Austin (TX): The University of Texas at Austin “University of Texas” redirects here. For other system schools, see University of Texas System. The University of Texas at Austin (often referred to as The University of Texas, UT Austin, UT, or Texas ; 2006. Available from www.bio.utexas.edu/faculty/ antisense/garli/Garli.html (11.) Buchy P, Mardy S, Vong S, Toyoda T, Aubin JT, Miller M, et al. Influenza A/H A/H Ampere/Hour A/H Air Handling 5N1 virus infection in humans in Cambodia. J Clin Virol. 2007;39:164-8. (12.) Zhu QY, Qin ED, Wang W, Yu J, Liu Bid, Hu Y, et al. Fatal infection with influenza A influenza A n. Influenza caused by infection with a strain of influenza virus type A. influenza A Infectious disease An avian virus, especially of ducks–which in China live near the pig reservoir and 'vector'; (H5N1) virus in China. N Engl J Med. 2006;354:2731-2. (13.) Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA. Structure and receptor specificity of the hemagglutinin from and H5N1 influenza virus. Science. 2006;312:404-10. (14.) Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, Sakai-Tagawa Y, et al. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature. 2006;444:378-82. (15.) Cheung CL, Rayner JM, Smith GJD, Wang P, Naipospos TSP, Zhang J, et al. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J Infect Dis. 2006;193:1626-9. Address for correspondence: Tien Dung Nguyen, National Institute of Veterinary Research, 86 Truong Chinh Truong Chinh orig. Dang Xuan Khu (born Feb. 9, 1907, Ha Nam Ninh province, Viet.—died Sept. 30, 1988, Hanoi) Vietnamese statesman, writer, and communist intellectual. He was an anticolonialist activist as a youth, joining Ho Chi Minh in 1928. Rd, Dong Da, Hanoi, Vietnam; email: dzungntd@gmail.com The opinions expressed by authors contributing to this journal do not necessarily reflect the opinions of the Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. or the institutions with which the authors are affiliated. Tien Dung Nguyen, * The Vinh Nguyen, * Dhanasekaran Vijaykrishna, ([dagger]) Robert G. Webster, ([double dagger double dagger n. A reference mark (  ) used in printing and writing. Also called diesis.Noun 1. ]) Yi Guan guan: see curassow. , ([dagger]) J.S. Malik Peiris, ([dagger]) [section] and Gavin J.D. Smith ([dagger]) * National Institute of Veterinary Research, Hanoi, Vietnam; ([dagger]) University of Hong Kong The University of Hong Kong (commonly abbreviated as HKU, pronounced as "Hong Kong U") is the oldest tertiary institution in Hong Kong. Its motto is "Sapientia et Virtus" in Latin, and " , Hong Kong Special Administrative Region, People's Republic of China; ([double dagger]) St. Jude Children's Research Hospital St. Jude Children's Research Hospital, founded in 1962, is a leading pediatric treatment and research facility focused on children's catastrophic diseases. It is located in Memphis, Tennessee. In 1996, Peter Doherty, Ph.D., of St. , Memphis, Tennessee, USA; and ([section]) The HKU-Pasteur Research Centre, Pokfulam, Hong Kong Special Administrative Region, China
Table. Influenza virus isolates from poultry in Vietnam, 2005--2007
Sublineage
Province ([double
Isolate * Genotype Date ([dagger]) dagger])
DkNNM/1228/05 Z 2005 Oct Dong Thap (S) Clade 1
Dk/VNM/1231/05 Z 2005 Nov Soc Trang (S) Clade 1
Dk/VNM/1233/05 Z 2005 Nov An Giang (S) Clade 1
MusDk/VNM/1455/06 G 2006 Feb Ha Tay (N) Clade 2.3.2
Dk/VNM/1469/05 Z 2005 Nov Vinh Long (S) Clade 1
Dk/VNM/1771/05 Z 2005 Oct Can Tho (S) Clade 1
Dk/VNM/1/07 Z 2007 Jan Ca Mau (S) Clade 1
Dk/VNM/2/07 Z 2007 Jan Ca Mau (S) Clade 1
MusDk/VNM/4/07 Z 2007 Jan Ca Mau (S) Clade 1
Dk/VNM/5/07 Z 2007 Jan Ca Mau (S) Clade 1
Dk/VNM/6/07 Z 2007 Jan Ca Mau (S) Clade 1
Dk/VNM/7/07 Z 2007 Jan Ca Mau (S) Clade 1
Dk/VNM/8/07 Z 2007 Jan Bac Lieu (S) Clade 1
Ck/VNM/15/07 Z 2007 Jan Soc Trang (S) Clade 1
Dk/VNM/18/07 Z 2007 Jan Kien Giang (S) Clade 1
CkNNM/29/07 Z 2006 Dec Hau Giang (S) Clade 1
MusDk/VNM/33/07 Z 2007 Jan Ca Mau (S) Clade 1
Dk/VNM/34/07 Z 2007 Jan Can Tho (S) Clade 1
Dk/VNM/37/07 Z 2007 Mar Lai Chau (N) Clade 2.3.4
Dk/VNM/38/07 Z 2007 Mar Hai Duong (N) Clade 2.3.4
MusDk/VNM/39/07 Z 2007 Mar Hanoi (N) Clade 2.3.4
MusDk/VNM/41/07 Z 2007 Mar Hanoi (N) Clade 2.3.4
Dk/VNM/43/07 Z 2007 Apr Ha Tay (N) Clade 2.3.4
MusDk/VNM/48/07 Z 2007 May Hanoi (N) Clade 2.3.4
MusDk/VNM/49/07 Z 2007 Apr Hanoi (N) Clade 2.3.4
Dk/VNM/50/07 Z 2007 May Hanoi (N) Clade 2.3.4
MusDk/VNM/51/07 Z 2007 Apr Ha Nam (N) Clade 2.3.4
Dk/VNM/52/07 Z 2007 May Phu Tho (N) Clade 2.3.4
Dk/VNM/53/07 Z 2007 May Nghe An (N) Clade 2.3.4
MusDk/VNM/54/07 Z 2007 May Hanoi (N) Clade 2.3.4
Dk/VNM/55/07 Z 2007 May Hanoi (N) Clade 2.3.4
MusDk/VNM/56/07 Z 2007 May Hanoi (N) Clade 2.3.4
MusDk/VNM/57/07 Z 2007 Apr Hanoi (N) Clade 2.3.4
* Ck, chicken; Dk, duck; MusDk, muscovy duck; VNM, Vietnam.
([dagger]) The letters S and N denote southern Vietnam and northern
Vietnam, respectively.
([double dagger]) Based on the World Health Organization influenza
(H5N1) nomenclature system (7).
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