Towards a Unified Nomenclature System for the Highly

Towards a Unified Nomenclature System for the Highly

Towards a Unified Nomenclature System for the Highly Pathogenic H5N1 Avian Influenza Viruses
WHO/OIE/FAO H5N1 Evolution Working Group

Contact information: Michael L. Perdue, Ph.D.
WHO Global Influenza Programme
Dept. of Epidemic and Pandemic Alert and Response
1211 Geneva 27, Switzerland
Tel: +41 22 791 4935 or 3004;
Fax: +41 22 791 4878 or 4498; E-mail: [email protected]

dkF uji an1131105
dkF uji an1203205
dkF uji an1109405
dkF uji an1093405

ck/Nongkhai/NIAH400802/07
ck/TH/NP172/06
Guangzhou/1/06
99
JapaneseWhiteEye/HK/1038/06
Anhui/1/05
dk/Laos/3295/06
ck/Malaysia/935/06
commonmagpie/HK/645/06
Zhejiang/16/06
JapaneseWhiteEye/HongKong/73720/07
WhiteBackedMunia/HongKong/82820/07
Guangxi/1/05
dk/Guiyang/3009/05
100
dk/Guiyang/3242/05
gs/Guiyang/3422/05
ck/Guiyang3/055/05
gs/Yunnan/4494/05
gs/Guangxi/3017/05
100
gs/Guangxi/345/05
gs/Guangxi/3316/05
dk/Hunan/127/05
100 dk/Hunan/149/05
dk/Hunan/152/05
dk/Hunan/139/05
Egypt/0636NAMRU320/07
Egret/Egypt/1162NAMRU3/06
dk/Egypt/22533/06
Egypt/14724NAMRU320/06
turkey/Turkey1//05
WhooperSwan/Mongolia/244/05
Nigeria/6e20/07
ck/Nigeria/641/06
Turkey/15/06
Iraq/207NAMRU3/06
Azerbaijan/001161/06
ck/Krasnodar/01/06
100
swan/Iran/754/06
ck/Liaoning/23/05
Barhdgs/Qinghai12/05
Barhdgs/Qinghai1A/05
ck/Kyoto/3/04
crow/Kyoto/53/04
99
ck/Yamaguchi/7/04
ck/Korea/ES/03
dk/Guangxi/13/04
ck/YN/115/04
ck/YN/374/04
Indonesia/CDC1046/07
Indonesia/CDC103220/07
Indonesia/CDC938/06
Indonesia/CDC887/06
Indonesia/CDC1047/07
Indonesia/283H/06
100
Indonesia/326N/06
Indonesia/CDC742/06
Indonesia/370E/06
Indonesia/5/05
Indonesia/CDC940/06
Indonesia/546bH/06
100 Indonesia/596/06
Indonesia/599/06
Indonesia/625/06
dk/Indonesia/MS/04
ck/Indonesia/4/04
ck/Indonesia/11/03
ck/Indonesia/7/03
VN/JP14/05
ck/Cambodia/013LC1b/05
VN/1194/04
VN/1203/04
VN/HN3/0408/05
TH/16/04
TH/676/05
VN/JPHN30321/05
HK/213/03

Introduction
Different names have been used in publications to describe emerging lineages of the highly pathogenic avian influenza A (H5N1) viruses.
This has made discussion and comparison of the various lineages difficult. The H5N1 viruses have now appeared in at least 53 countries
on three continents and continue to infect humans as well as to evolve and diversify at an alarming rate. Remarkably, the hemagglutinin
protein has not been replaced in the various isolates since 1996, while other genes have undergone reassortment yielding many different
genotypes. As such, following the evolution of the HA provides an initial constant by which the strains may be effectively compared. It
was proposed to develop a clade nomenclature system based upon the evolution of the HA for several reasons:

c kF uji an1031305
c kF uji an1056705
dkF uji a n96 5105
c kF uji a n98 2105
c kF uji a n10 03905
c kShant ou3 840 06
c kShant ou3 923 06
c kF uji a n11 93 305
c kF uji an1 223905
c kF uji an58406
c kShant ou1 233 06
dkShantou1 33 2305
gsG uangxi 5206
c re ste dmyna
H K 54006
CkM al aysi a93506
dkH unan32406
dkH unan34406
g sG ua ngx i5 414 05
dkF uji an1 734 05
gsG ua ngx i 5320 6
gsShantou326506
gsShanto u329 506
c kG ui yang101806
gsG ui yang130406
c ommonmagpi eH K 645 06
g sYunna n11 430 6
g sYunna n11 440 6
dkH unan8 560 6
dkH unan9 880 6
dkG ui yang29306
Anhui 10 5
dkLaos329506

Anhui 20 5
dkG ui yang14 180 6
dkG ui ya ng49 706
gsShantou184420 5
muni aH K 245406
whi te bac ke dmuni aH K 24 6906
c ommonmagpi eH K 30 330 6
c ommonmagpi eH K 21 250 6
c om monmagpi eH K 225606
house c r owH K 28580
6
la r ge b
i l l e dcr owH K 251206
J apaneseW hi te EyeH K 103806
l i ttle e gret H K 71806
c kTH NP 17206
g sG uang xi4 2890 5
gsG uangxi 451305
dkG uangxi 52700 5
dkG uangxi 51650 5
c kG uangxi 49890 5
dkG uangxi 80406
dkG uangxi 483005
dkG ua ngxi 61 906
c kG ua ngxi 6830 6
gsG uang xi 58 206
dkH unan510605
dkH unan515205
G uangxi 105

4. To provide a starting point for a more extensive system to follow based upon antigenic variation and reassortment into multiple
genotypes.

r obi nH K 75 0
6
c kH K 282 06
dkG uangxi 15006
dkG ua ngxi 5075 05
dkG uangxi 545705
c kG ui yang2906
dkG ui yang126006

dkG ua ngx i2 880 6
g sG uang xi 189806
c kG uangxi 195106
dkG uangxi 125806
gsG uang xi 145806
dkG ua ngx i1 830 06

dkG uangxi 143606
g sYunnan113606
gsYunnan133 806
dkH unan1504
c kG ui yang305505
dkG ui yang300905
dkG ui yang324205

80

c kG ui yang357005
gsG ui yang342205
dkG uangxi 381905
dkG uangxi 37 410 5
c kG uangxi 379105
dkG uangxi 308505
gsYunnan449405
dkYunnan440005
dkYunnan587705
dkG uangxi 292605
gsYunnan602705

gsYunnan372005
dkG uangxi 354805
dkYunnan458905
dkYunna n58 200 5
gsYunnan412 905
c kG ui ya ng2173 05
c kG ui ya ng2147 05
dkYunnan112 606
gsYunnan636805
dkYunnan66070 5
gsG uangxi 30170 5

Large alignment consisted of 884 HA sequences each approximately 1,659 nucleotides
- identical sequences/redundant isolates were removed from the alignment to remove bias

dkG uangxi 8906
dkG uangxi 33 640 5
dkG uangxi 46 650 5
gsG ua ngx i 3714 05
dkG uangxi 418405
gsG uangx i3 4505
dkG uangx i9 5105
c kVN1005
dkVN5680 5
gsG uang xi 33 160 5
dkVN1205
qaVN15 05
c kVNTY2505
c kVNTY3105
c kVN1705
dkG uangxi 401605
c kG uangxi 24 610 4

70

c kG uangxi 24480 4
dkH una n12650 5
phShant ou2 23 906
dkH unan165205
dkH unan160805
dkG uangxi 38004
dkG uangxi 35104
qaShantou91105
c kShantou8 100 5
gr e yher onH K 8 3704
Chi ne se pondhe r onH K 1805
gr e yher onH K 72804
P hST44 04
c kG uangdo ng1 780 4

dkChi na E31 920 3

86

c kG ua ngdo ng1 910 4
DkH N580603
DkH N303 04
DkH N10104
dkH unan12705
dkH una n15 205
dkH unan1490 5
dkH unan1660 5
dkH unan1820 5
dkH unan1910 5
dkH una n13 90 5
c kH una n99 90 5
c kG uangxi 1204
dkG uangxi 1304
c kChi na120404

64

c kYunnan49 305
c kji yuan1 03
c kz heng z ho u10 2
DkYN644503
CkYN37 404
CkYN11 504
DkYN625503
r uddyshel dkQ i nghai 105
whoope r swanQ i nghai 105
c kTambov570205
whoope r swanMo ngo li a705

Large tree rooted to highly pathogenic historical Eurasian H5 isolates (turkey/England/91 and chicken/Scotland/59).

Whoopi ngswanMo ngo li a2 4405
c kVol gogr ad23606
c kSuda n211590 6
c kSuda n178410 06
c kSuda n21151206
c kSudan178 470 6

Small tree rooted at the clade 0 node (gs/Guangdong/1/96 lineage).
1000 bootstrap replicates were performed to support tree topology.

c kSudan178 406
c kNi ge ri a104 76206
c kCote dIvo ir e 1787340 6

ml dBavar i a1
06
bar hdg sM ongol i a105
Cygnusol or Cze c hRe publi c 517006
c ommonbussar dBav ar i a2 06
ml dItal y83506
tur ke yTur ke y10 5
swanSl ove ni a76006
Egypt147 25NAMRU3/ 200 6
Egypt147 24NAMRU320 06
Egypt902 782 06
c kEgypt2 06
c kEgypt1 06
c kEg ypt 960N300406
Egypt902 786 06
dkEg ypt 2253306
c kEg ypt 306
c kEg ypt 2253106
Ir aq65 906
Ir aq75606
Ir aq75406
Ir aq75 506
Ir aq106
dome sti cc atI
r aq82006
dome sti c gsIr aq8120 6
T ur key6 5124 20 6
Tur ke y1 506
Tur ke y12 06
Tur ke y6559606
G uineafo wl Shanto u134106
pi e dmag pi e L
i aoni ng 705
dkNovosi bi r sk56 05
c kCr i me a04
05
c kCr i me a08
05
dkNovosi bi r sk02 05
gsCr ime a61505
c kInne r M o ngo li a64
05

93

ck/Henan/16/04

Clade designation criteria

Cygnusol or Astr akhanAst052705
dkK ur g an0 805
Cygnusol or Astr a kha nAst0 52605
Cygnusol or Astr a kha nAst0 52505
Cygnusol or Astr a kha nAst0 52405
Cygnusol or Astr a kha nAst0 52205
Cygnusol or Astr a kha nAst0 52105
Cygnusol or Astr a kha nAst0 521005
gsK r a snooz e
r ka6 270 5
c ygnusol or Cr oati a1
05
Cygnusol or Astr a kha nAst0 52305
swanG e r manyR6506
c atG er many6 0606
c kNi ge ri a104 73 406
c kNi ge r2 130
806
c kNi ge r 2130
706
dkNi ge r 914 06
c kNi ge ri a1047540 6

2.2

c kNi ge ri a10473006
c kNi ge ri a9572006
ost ri c hNi geri a10 472506
gui ne afowl Ni ger i a9571 206
c kNi ge ri a1047806
Aze r bai j an001 16 10
6
Aze r bai j an011 16 20
6
Az e r bai jan008208 0
6
Az e r bai jan006 207 0
6
Az e r bai jan002 115 0
6
c kAdyge a203 06
c ygnusc ygnusIr an7 540 6
c atDage stan8706
c kK r asnodar 19906
c ygnusol or Ital y74206
c kK r asnodar 010 6
c kAfghani stan120706
dkTuva0 106
Gr e beTyvaTyv06806
gr e beTy vaT
yv06206
gr e be TyvaT
yv06106
whooper swanMo ngoli a206
G r e be Novosi b
i r sk2905
Bar hdgsQ i nghai 120 5
Bar hdgsQ i nghai 505
Bar hdgsQ i nghai 590 5
Bar hdgsQ i nghai 600 5
Bar hdgsQ i nghai 610 5
Bar hdgsQ i nghai 620 5
Bar hdgsQ i nghai 670 5
Bar hdgsQ i nghai 680 5
Bar hdgsQ i nghai 750 5
br hdgul l Q i nghai 3 05
EnvQ i nghai 3105
G r e atb
l hdG ul l Q i ng hai 20 5
B arhdgsQ inghai 6505
mi gr atory dkJi angxi 230005
mi gr atory dkJi angxi 213605
c kM ahac hkal a0506
bar hdgsQ i nghai 051005
Bar hdgsQ i nghai 1A05
gre atcor mor antQi nghai 305
G r e atb
l hdgul l Q i nghai 105
mi gr atory dkJi angxi 229505
bar hdgsQ inghai 20 5
bar hdgsQ i nghai 405
whoope r swanM ongol i a1305
bar hdg sQ i nghai 105
bar hdgsQ ing ha i90 5
bar hdgsQ i nghai 805

98

brhdgul l Q i nghai 105

85

1) Maintain previously designated clade numbers when possible (i.e., Clade 2.2 remains 2.2 and Clade 1 remains 1)
2) New clade designations based on phylogenetic tree topology derived from the large tree
- H5N1 progenitors (closest to gs/Guangdong/1/96) designated as Clade 0
- Subsequent clades numbered starting from Clade 3 (i.e., Clades 3-9)
- Clades designated by the presence of a distinct common node shared by at least 4 isolates
- Subclades/sub-subclades designated as a single clade evolves into more than
one distinct lineage (based on sharing of a common node)

dkK or e aESD103
c kK ore aES03
c r owO saka10204
c kYamag uc hi7 04
c kO i ta80 4
c r owK yoto5
304
c kK yoto304
bl owfl yK yoto9 304
c kG ua ngdong 174 04

85

dkH ube i wp03
gsJi l i nhb03
g sShantou20 860 6
gsShantou23906
CkST42 3103
Indone si a605
Indone si a836T0 6
Indone si a83606
Indone si a73 906
Indone si a669P 06
Indone si a66906
Indone si a583H 06
Indone si a94006
Indone si a75906
Indone si a83 506
Indone si a 610 06
Indone si a542H 06
Indone si a 582 06
Indo ne si a634T06
Indo ne si a 634 P06
Indo ne si a63406
Indone si a567 H06
Indo ne si a 644 T06
Indo ne si a 644 06
Indo ne si a69 906
Indone si a604H 06
Indone si a523T06
Indone si a523E06
Indone si a52306
Indone si a88 706
Indone si a10312007|Indone si a1031T20
Indone si a938E0 6
Indone si a93806
Indone si a10322007
Indone si a104707
Indone si a104607
Indo ne si a29 8H 06
Indone si a370P 06
Indone si a370E06
Indone si a37006
Indone si a370T0 6
Indone si a39006

Indone si a569H 06
Indone si a623E0 6
Indone si a62306

Indone si a74206
Indo ne si a 287 T05
Indo ne si a 287 E05
Indo ne si a 239 H 05
Indone si a35706
Indone si a304H 06
Indone si a292H 06
Indone si a326N06
Indone si a283H 06
Indone si a286H 06
Indone si a326N206
Indone si a32906
Indone si a326T06
Indone si a32606
Indo ne si a50 5
Indone si a195 H05
c kP a kunBar uBP P VII05
c kM ura oJambi BB
P VII05
Indone si a18405
Indone si a160H 05
Indone si a 705
dkIndr amay uBBP W10906
Indone si a194P 05
Indone si a175H 05
DkP ar e par eB BVM 05
CkWajoBBVM 05
c kM age tanBBVW05
c kIndone si aWate s105
c kIndone si aWate s12605
c kG unungK i dal BBVW05
c kIndone si aWate s13005
c kIndone si a2505
c kIndone si a2405
c kBa nda r LampungBBP VIII06
c kW ay K ananBBP VIII06
c kSe mbawaBP P VIII05
c kP ale mbangB P P VIII05

3) Average percentage pairwise distances between and within clades (using the Kimura 2-parameter):
- Distinct clades should have 1.5% average distances between other clades
- Distinct clades should have 1.5% average distances within the clade (may be
slightly higher in clades that have highly evolved outliers (i.e., ck/Shanxi/2/06
in Clade 7)

qaBoyol al i B
P P V404
c kK ul onP r o
goBBVe tXII204
c kK ul onP r o
goBBVe tXII104
c kK upang1NttBppv604
c kIndonesi aWate s8005
dkM adi unBBVW1 35 805
Indo ne si a59 506
Indo ne si a56 0H 06
Indo ne si a62 506
Indo ne si a62 5L0 6
Indone si a599N0 6
Indone si a59906
Indone si a59706

Indone si a546bH 06
Indone si a538H 06
Indone si a535H 06
Indone si a534H 06

CkDai r i BP P VI0 5
c kAga mBBP VI05
c kP ul auRam pa ngB BP VII06
c kSi mal anggangB P
P VI05
c kP adangBBP VII06

c kDumaBB P VII05
c kSi akBP P VII05
c kK ar oBB
P VII06
c kP i die BP P V1 05
c kM e danBBP V1 571 05
c kDe l i Ser dangBP P V105
c kM e danBPP V153405
c kTaputBBP V157605
c kTe bi ngTi nggi B
P P VI05
CkDe l i Se r dangBP P VI0 5
c kTar utungBP P VI0 5
c kDe l i Der dangBBP VI05
c kM e danBBP V1 576 05
c kM edanBPP V149805
c kSal ati gaBBVe tI05
c kIndone si aWate s770 5
c kIndone si aWate s8305
c kP angkal pi nangBP P V304
tur ke yK e dat onBPPV30 4
c kNgawi BP P V404
c kIndone si aR600 5
qaTasi kmal ayaBP P V404

2.1.1

c kIndo nesi a703
c kP e kal ong anB PP V403
c kW onosoboBP P V403

75

c kIndone si a1 103
CkIndo ne si aP A03
CkIndone si a404
c kSr age nBPP V403
DkIndone si aM S04
CkIndo ne sia 2A03
CkIndone si aBL03
CkIndone si a504
c kBangl i Bali BBP V61 04
c kBangl i Bali BP P V61 04
c kBangl i Bali Bppv620 4
c kBantul BBVe tI05
c kJe mbr anaBPP V604
c kK upang2NTTBP P V604
c kK upang3NTTBP P V604
c kM anggar a
i NttBppv 604
c kM angar ai NTTB
P P V604
c kP ur wakar taBBVe tIV04
c kM al angBBVe tIV04
dkTabananBP P V1 05
dkP al i BBVW135805
dkBufe l e ngBP P V105
CkH K YU32403
CkH K SSP 14103
bl hdgul l H K1 21 03
CkH K 317 6302
H K 21203
H K 21303

c kH K 312310
2
EgH K75730
2
e gr e t
H K 757203
G sH K73920
2
CkH K F Y15 703
CkH K 3 169 102
dkH K 82102
fe r a lp
i g eo nH K 862 7
02
g r e yher onH K 861102
ope nbi l l TH CU204
c atTHK U0204
c kChac hoe ngsao TH CU10 04
c kTH CH 204

79

G sTH 7904
c kCambodi a704
c kChonbur i TH CU704
pi ge onTH K U0304
TH Chai yaphum6 220 4
whi te pe afowl B ang kokTH CU16 04
whi te pe afowl B ang kokTH CU29 04
c r owBangkokTH CU150 4
CkTH 7304
K al ji phBangkokTH CU1804
kal ij phTH CU404
T HL FP N200404
c kLopbur iTH CU3 80 4
c kTH CU21 04
c r owBa ngkokT HCU404
O str i c hSamutPr akanTH CU1904
ostr i c hSa mut P rakanTH CU3104
c kTH K anc hanabur i CK 1 6005
c kTH Nontabur i CK 16205
c kTH P C17 006
TH NK 16505
qaTH NakhonP at homQ A1 6105
c kRa tc habur i TH CU6804
c r e ste d
e agl eBe l gium0104
c r owBang kokTH CU3504
VN306204
CkTH 104
dkVN4804
c kNakhonSawa nTH CU3 904
TH H A2005
c r owBangkokTH CU250 4
qaM al aysi a6 309 04
VN119404
c kVN403
ml dVN30 3
VN120304
VN120404
c kVN503
M ynasRa nongTH CU20904
spar rowP hangNga TH CU20304
c kSar aburi TH CU17 04
c kSuphanbur iT HCU104
dkNakhonP at homTH CU7104
c kBangkokTH CU60 4
TH 1K AN104
TH K an353 04
c kBangko kTH CU2 004
c kNakhonSawanTH CU12 04
c kAyutthayaTH CU23 04
c kTH 204
dkT H CU204
DkTH 71104
c kLaos4404
c kSuphanbur iTH CU904
c kNakhonSawanTH CU13 04
CkTH 9104
c kBangkokTH CU30 4
c kChac hoe ngsao TH CU11 04
c kNakhonP athomTH CU14 04

Universal acceptance of this nomenclature system will:
- unify the classification of isolates so that interpretation of sequence/surveillance data from different laboratories
becomes easier
- remove stigmatizing labelling of clades by geographical reference
- provide a system for future expansion of all-inclusive phylogenetic trees that can be used to follow the global
patterns of viral evolution
- provide a starting point for a more extensive nomenclature system that can be used to follow the ever-changing
antigenic variation of H5N1 and the emergence of novel genotypes from reassortment of the viral internal genes
- may serve as a model for other influenza lineages and genes, including seasonal influenza, which currently uses
geographical names, and other avian influenza viruses that infect humans

c kLaos719104
c kVN803
dkVN4004
TH SP 83 04
dkVN1 503
H atay04
Le oSuphanbur i T HL e o1 04
bi r dTH 3104
ti ge r Suphanbur i T HT i1 04

Large and small trees containing publicly available sequences will be posted on the WHO GIP website and OFFLU
website and maintained as up-to-date (evergreen) evolutionary trees of the H5 hemagglutinin to keep an open
forum for following H5N1 evolution

c kChonbur i TH CU730 4
c kNakor nP atom TH CUK 20 4
ti ge r T
H CUT 604
ti ger T
H CUT804
ti ger T
H CUT704
ti ger T
H CUT504
ti ger T
H CUT404
ti ger T
H CUT304
dogT H Suphanbur i K U0804
c kP r a
c hi nbur i TH CU1 040 4
P r ac h
i nbur i 62310 4
c kSar abur i TH CU270 4

1

dkVN31705
dkVNntb05
dkVNNCVD050 5
dkVN50 820 5
H a noi 30 4080 5
VNH N3040 805
dkVN50 0405
dkVNNCVD0805
c kVN1105
dkVNNCVD0405
ml dVN35 205
c kVN34 805

dkVN5 001 05
dkVNNCVD060 5
dkVNNCVD0105
dkVNNCVD070 5
dkVNTG 24O 105
c kVN20 5
c kVNP 2205
c kVN805
c kVN905
c kVN605

dkVNnxx04

- WHO GIP website - http://www.who.int/csr/disease/influenza/en
- OFFLU website www.offlu.net

c kVNNCVD1005

8

dkVN27205
c kVNNCVD0905
dkVN1805
dkVN500305
c kVN3204
c kTH P C16806
c kP r a
c hi nbur i TH CU804
dkSar abur i T HCU740 4
dkChonbur i TH CU504
DkVN11 04
T H1 60 4
T H2 SP 3 304
c kVN2 703
c kVN28 03
c kVN2003
VN304 604
VN321204
c kVNG 04 04
c kVNNc vd3 104
CkVNC57 04
c kVNC5 804
c kCambodi a104
gsCambodi a2804
c kL aos719204
c kVN1903
ml dVN1 603
c kAyutthay aTH CU2 404
c kM al aysi a5
85 804
r ol le r sBa ngkokT HCU260 4
c kVN104
dkVN1703
c kVN3003
ml dVN2103
dkVN55705
VNJP1 405
dkVNS65405
c kVN3 9305
wil dbi r dVN4 34 05
dkVN5 430 5
c kCambodi a0 13L C1b05
dkVN28605
c kVN3980 5
dkVNS6 400 5
dkVN36 705
qaVN28 205
dkVN25804
VNCL115 05
VNCL200905
dkVN37605
VNJ P420705
c kVN26 004
CkVN38 04
CkVN3 904
VNCL26 04
c kVN1 340 4
VNCL01 04
c kVNDT17104
c kVN13 20 4
VNCL3604
CkVN37 04
c kVNTG 0 230 4
c kVN13504
c kVN14904
CkVN36 04
qaVN3 604
qaVN7 B04
Cambodi aJP 52 a05
VNCL020 4
qaVN17704
VNCL105 05
c kCa mbodi a022LC3b05
g sCa mbodia 022 b05
gsVN26404
dkVN14804
c kVN1 330 4
ml ddkVN13 304
c kVN1 470 4
c kVN5 204
c kVN5 304
VNCL10004
VNJP H N3032105
VNCL119 05
CkVN33 04
c kVNLD080 04
VNJP 17804
dkVN28 305
c kVN15 90 4
CkVN3504
c kVNTN02504
dkVNTG 007A04
VNCL2004
dkG uangdo ng1 73 04
CkH K 2133 103
c kVNG 62 05
dkF uji a n89 705
c kF uji a n10 420 5
gsShantou221 605
gsShantou162105

5

mi gr a torydkJi angxi 16 530 5
mi gr a torydkJi angxi 17 010 5
mi gr a torydkJi angxi 16 570 5
dkG ua ngz hou2005
dkG ua ngxi2 77505
pe r e g
r i ne fa l
c onHK D002804
CkH K WF 1 5703
c kH ube i 140 4

83

Wi l ddkG ua ngdong3140 4
ml dG ua ngx iwt 04
c kH ena nwu04

swanG uangxi 30 704
c kH ube i 32704
dkG uangxi 5001
c kH ena n13 04
c kH ena n12 04
c kH e nan0 104

67

ck/Hunan/2292/06
ck/Shanxi/2/06
ck/Myanmar/06010011B/06
dk/Guiyang/504/06
ck/Guiyang237/06
gs/Guiyang/337/06
gs/Guiyang/1325/06
ck/Guiyang441/06
ck/Guiyang1218/06
ck/Guiyang846/06

ck/HK/8911/01

gsH ua dong22 004

c kH ena n21 00 4
c kH ube i4 89 04

swG ua ngx iwz 04
swH e nanwy04
c kH e nan1604
CkH K YU77702
DkST400303
dkShantou461003

7

dkShanghai xj02
CkH KYU220 2
c kH Ki 86302
CkH K 61902
c kJ i l i n904
c kJ i l i nhd02
c kJi l inhh02
dkYunna n523 605
gsYunna n55 390 5
dkYunna n513 305
gsYunnan331505

72

c kH e bei 32605
c kShanxi 206
tr e e sparr owH e nan104
tr e e sparr owH e nan204
tr e e sparr owH e nan304
c kJi l i nhf02
bl bi r dH unan10 4
tr e e sparr owH e nan404

53

dkH ube i wg02
swAnhui c a04
c kJi ang sucz 1 02
dkYokohama aq1 003
swF uji a n1 03
swF uji anF 101

76

dkZhe ji ang5200
c kJi l i nho03
dkVNNc vd102
te al Chi na2978102
c kVNNc vd8 03
dkG uangxi 13 780 4
gsG uangxi 91404
c kG uangxi 243904
gsG uangxi 211204
dkG uangxi 66 804
dkG uangxi 15 860 4
dkG uangxi 168104
dkG uangxi 179304
gsG uangxi 109704
gsG uangxi 183204
dkG ua ngxi 23 96 04
gsG uang xi 23 830 4
dkG uangxi 22 910 4
dkG uangxi 131104

4

gsG uangxi 119804
dkZhe ji ang bj 02
c kG ui ya ng12 180 6
gsG ui ya ng1 175 06
c kG ui ya ng84 60 6
c kG ui yang44 106
gsG ui yang3 3706
dkG ui yang223105

98
dkG ua ngdo ng 2202
gsF uji anbb03
CkH K 31402
CkH K 409 102
CkH K 961 02

66

dkH K 380501
gsVN11301
gsVN32401
dkG uangx i22 01
c kH e bei 718 01
dkG uangxi 3501
dkG uangxix a01
gsH K ww10001
gsH K 3014500
gsH K 3014800
c kH K
F Y1 5001
phH K F Y15501
c kH KF Y7701
c kH K 71 550 1
c kH K NT873301
dkG uangdong 010 1
gsH K 76 101
dkF uji a n1 701
dkShanghai 1301
dkH K 298 610 0
c kH K YU562 01
c kH K YU56301
P i ge on
H K SF 215 01

3

qaH KSF 20301
c kH K YU822201
c kH K SF 219
01
c kH K 879101
c kH K 891101
Sil ky c kH K S
F 18901

9
8
7
5
4
3

gsH K ww2600
gsH K ww28 00
c kJi l inhk04
g sChinaF 304
c kJi l i nha 03
g sH uado ng1 00
gsH K 38 530 0
g sH K 3 85500
c kJ i l inxv02
CkH K 31202
P hH K 67514
02
G fH K3802
CkH K 37402
SCkH K YU1 0002
dkShandong09304
c kJi ande1 218 01

0

gsG uangdong xb0 1
dkAnyangAVL1 01
dkShang hai 35 02
dkShanghai 3801
c kl uohuo303
c kz houkou202
dkG uangxi 5302
dkShanghai 3702
dkF uji an1302
c kH e bei 10802
dkF uji an0102
dkG uangdong4000
EnvH K 437499
EnvH K 437 899
EnvH K 4371099
c kH K 317501
EnvH K 437 699
dkG ua ngdong 0700
dkH K ww38100
dkH K ww38200
gsH K ww49 100
dkH K ww46100
dkH K ww48 700
c kJi li nx w03
c kH ube i wj97
c kH ube iwl 97
c kH ube iwh97
dkShanghai 080 1
dkF uji an1 900
dkG uangdong1200
c kChina102

0.005

Establishes a system and guidelines to name/number existing clades of highly pathogenic H5N1 avian influenza, including
criteria for assigning a new clade name/number to a newly emerging group of variants.

dkVN2 1904
dkVN22004

4) Bootstrap support for clade defining node (based on 1000 replicates)
- >60 at clade defining node

99

c kRokanH i l li BP P VII05
c kSal amBBP VII05

99

ck/Henan/01/04

100

gs/VNGZ3/05
HK/156/97
gs/Guangdong/1/96

2.1.2

Indone si a59606
Indone si a59406
Indone si a546H 06

Tur ke yLangka tBB P VI0 5
c kLangka tBBP V157 605

6

ck/HK/SF219/01
ck/HK/8791/01

Conclusions
The results support the hypothesis that the HPAI H5N1 viruses can be grouped into several clades designated by a
numbering system that can continue to be expanded as the virus continues to evolve.

qaYogjakar taB BVe tIX0 4
c kYogjakar taB BVe tIX0 4

87

dkVN1 905
dkVN2 005

99

96

Clade descriptions
0 = early progenitors; predominately 1996-2002 from Hong Kong (HK) and China (mostly avian, few human)
3 = 2000-2001 from HK, China, Vietnam (all avian)
4 = 2002/2003 lineage from HK and China; 2005/2006 from Guiyang Prov. (all avian)
5 = 2000-2003 from China and Vietnam; 2004 lineage from Guangxi Province (all avian)
6 = 2002/2004 from China (all avian)
7 = 2002/2004 from China; 2005/2006 from Yunnan, Hebei, Shanxi Provinces (all avian)
8 = 2001-2004 from HK and China (all avian)
9 = 2003-2005 from China (all avian)
1 = 2002/2003 progenitors from HK; 2003-2006 from Vietnam, Cambodia, Thai, Laos, Malaysia (mixed A/H)
2.1 = 2003-2007 from Indonesia (mixed avian/human)
2.2 = 2005 progenitors from Qinghai Lake outbreak and Mongolia; 2005-2007 isolates from
Eastern and Western Europe, the Middle East, and Africa (mixed avian/human)
2.3 = 2003-2006 from China, HK, Vietnam, Thailand, Laos, and Malaysia (mixed avian/human)
2.4 = 2002-2005 from China (predominately Yunnan and Guangxi Provinces) (all avian)
2.5 = 2003/2004 from Korea, Japan, China; 2006 lineage from Shantou Prov. (all avian)

CkP ur wor e joBBVW05

9

99

2.1.3

Indone si a341H 06
Indone si a624E06
Indone si a62406

Indone si a292T0 5
Indone si a292N0 5
Indone si a245H 05

c kVNTY9 05

ck/HK/YU22/02
migdk/Jiangxi1653/05
dk/Guangxi/2775/05
ck/Hunan/41/04
blbird/Hunan1/04
treesparrow/Henan/4/04
dk/Hubei/wg/02
sw/Anhui/ca/04
dk/Guangxi/1378/04
91
dk/Guangxi/1681/04
dk/Guangxi/1311/04
dk/Guangxi/2396/04

93

2.5

bar hdgsQ i nghai 305
bar hdgsQ ingha i1 005
G r e at b
l hdgul lQ i nghai 305

ml dVN34 705
musdkVNNCVD0 205

ck/Henan/13/04
ck/Henan/12/04
dk/Guangxi/50/01
ck/HK/YU777/02

2.2

wi l ddkO msk1030105
Cy gnuso lor Astr a khanAst052905
Cy gnuso lor Astr a khanAst052805

1

Maximum likelihood and maximum parsimony trees also generated to confirm clade topology.

Isolates in the small tree match the clade designations of the large tree
- overall tree topology from big tree to small tree varies because fewer isolates
were used in the small tree, which distorts the hierarchical structure of the tree
- despite this, all clade designations remain the same

c kK ur gan305
dkCotedIv oi r e 17871806
c kNi ge ri a 64106
c kK ur g an0 505

2.1.1

100

2.4

whooper swanMo ngoli a405
whoope r swanM ongol i a30 5
whoope r swanMo ngo li a605

2.1.2

Phylogenetic trees
Neighbor-joining trees were generated using MEGA (Version 3.1) and PAUP (Version 4.0) using the Kimura 2-parameter.

2.3.1

qaG uangxi 57505
dkG uangxi 79305
c kG uangxi 60405

2.1.3

Small alignment consisted of 109 HA sequences each approximately 1,659 nucleotides
- isolates chosen include vaccine strains, reference strains, many human isolates,
pathogenesis study strains, geographically diverse isolates

2.3.2

dkG uangxi 419605

0

Sequence alignments
Nucleotide sequences of the highly pathogenic H5N1 hemagglutinin (HA) (only nearly complete sequences) were collected from publicly
available databases: GenBank (NCBI) and Influenza Sequence Database of Los Alamos National Laboratories (LANL)

Some clade topology lost if partial HA sequences are used (i.e., < 800 ntds.) - partial HA sequences appropriate for checking clade designation - ideal alignments should have nearly compete HA sequence c kG ua ngxi 31 54 05 gsYunnan480 405 dkYunna n52 510 5 2.4 82 2.3.3 dkG uangxi 39206 gsG uangxi 22406 c kG uangxi 121206 2.5 Methodology Clade topology nearly identical regardless of phylogenetic analysis/algorithm used (i.e., NJ, ML, MP algorithms produce nearly identical trees) dkG uangxi 214306 c kG uangxi 46306 g sG uang xi 163306 2.3.1 An international core group of 8 scientists and their collaborators were convened to initiate this process with the encouragement and approval of three international agencies: World Health Organization (WHO), World Animal Health Organization (OIE) and the Food and Agriculture Organization (FAO). Phylogenetic analysis was performed by a variety of approaches on all of the publicly available H5 HA sequences that have evolved in the A/Goose/Guangdong/96-like H5N1 lineage. The initial results support the idea that the currently circulating HPAI H5N1 viruses could be effectively grouped into numerous clades easily designated by a hierarchical numbering system. For example, the 'Fujian-like lineage' within the antigenically diverse Clade 2 of H5N1 would be designated Clade 2.3.4, with other distinct branches called 2.3.1 and 2.3.2 etc.., while the 'Qinghai lineage' would be designated Clade 2.2. If such a system could become universally accepted, it might serve as a model for other influenza lineages and genes, including seasonal influenza, which currently uses geographical names, and other avian influenza viruses that infect humans. The progress of the international working group and collaborators will be provided in this late breaker presentation. 5) Antigenic properties as measured by the hemagglutination inhibition assay should be used as a correlate of clade designation when the data is available dkG uangxi 74406 gsYunnan139606 c kH K 947 06 95 2.3.2 3. To provide for easy future expansion of the phylogenetic tree. 2.3.4 dkF uji an66806 dkF uji an67106 dkG ui ya ng3 996 05 dkG ui yang383405 2.3.3 2. To remove stigmatizing labelling of clades by geographical reference. Clade 2 is highly divergent with 5 subclades within the clade (2.1-2.5). - subclades 2.1 and 2.3 further delineated into sub-subclades due to distinct evolution of more than one lineage c kG ui yang372105 c kG ui ya ng4 059 05 2.3.4 1. To unify the system so that interpretation of sequence/surveillance data from different labs becomes easier. Results 9 unique clades defined from analysis of publicly available H5N1 sequences. dkF uji a n97 1305 c kShandong K 010 4 swShandong203 dkG uangxi 0799 gsG uangdong397 H K 1569 7 gsG ua ngdong 196 tur ke yEngl and509291 c kSc otl and59 0. 02 6 WHO/OIE/FAO H5N1 Evolution Working Group participants Mike Purdue, WHO, GIP, Geneva, Switzerland* Ian Brown, VLA-Weybridge, UK Hualan Chen, Harbin Veterinary Research Institute, CAAS, China Ruben Donis, Influenza Division, CDC, Atlanta, GA USA Ron A.M. Fouchier, Erasmus University, Netherlands Yoshi Kawaoka, U of Wisconsin, USA & Inst of Medical Sciences Tokyo, Japan John Mackenzie, John Curtin School of Medicine, Australia Gavin Smith, The University of Hong Kong, HK SAR, China Yuelong Shu, China CDC, China Collaborators Ilaria Capua, IZSVE, Padova, Italy Nancy Cox, Influenza Division, CDC, , Atlanta, GA USA Todd Davis, Influenza Division, CDC, Atlanta, GA USA Rebecca Garten, Influenza Division, CDC, Atlanta, GA USA Yi Guan, The University of Hong Kong, HK SAR, China Elizabeth Mumford, WHO, GIP, Geneva, Switzerland Collin A. Russell, Department of Zoology, University of Cambridge, UK Catherine Smith, Influenza Division, CDC, Atlanta, USA Derek Smith, Department of Zoology, University of Cambridge, UK Dhanasekaran Vijaykrishna, The University of Hong Kong, HK SAR, China

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