Canine Rabies Elimination from the United States: an Epidemiological and Virological Perspective

Canine Rabies Elimination from the United States: an Epidemiological and Virological Perspective

Andrés Velasco Villa, Serena Reeder, Jesse Blanton,Lillian A Orciari and Charles E. Rupprecht

Rabies UnitPoxvirus and Rabies BranchDivision of Viral and Rickettsial DiseasesCoordinating Center of Infectious DiseasesCenters for Disease Control and Prevention

The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the funding agencies.

Use of trade names and commercial sources are for identification only and do not imply endorsement by the US Department of Health and Human services.

Rabies is an acute viral encephalomyelitis caused by the members of the Lyssavirus genus and Rhabdoviridae family

Disease definitionDisease definition

Rabies causes more than 55, 000 human deaths, every year, throughout the world.

Rabies epizootiologyRabies epizootiology

RABIES RESERVOIRSRABIES RESERVOIRS

URBAN RABIES URBAN RABIES WILD RABIESWILD RABIES

RABIES ASSOCIATED WITH TERRESTRIAL CARNIVORESRABIES ASSOCIATED WITH TERRESTRIAL CARNIVORES

SUSCEPTIBLE SPECIES (DEAD ENDS)SUSCEPTIBLE SPECIES (DEAD ENDS)

Cats

VECTORS VECTORS

Ferrets

Perros

Dogs Vampire bat Big brown

bat

Silver hair bat

Red bat Free tail bat

Mapaches

Raccoons Gray foxes

Stripped skunkSpotted skunk

Arctic foxesCoyotes

Mongooses

RABIES ASSOCIATED WITH BATSRABIES ASSOCIATED WITH BATS

Cows Goats and

Sheep

Humans and horsesPigsBeavers and

woodchucks

Raccoon dogs

ENZOOTIC RABIES ENZOOTIC RABIES

Rabies status

City Year *Controlled

Epizootic Memphis, TN 1948 1958

Enzootic Chicago, IL 1954 1958

Enzootic Pontiac, MI 1954 1958

Enzootic St Louis, MO 1954 1958

&Enzootic Los Angeles, CA 1922-1957 1975

&Enzootic Dallas, TX 1954 1976

&Enzootic Phoenix, AZ 1950 1976

&Enzootic Houston/Harris, TX 1954 1977

Last dog rabies enzootics in the United States

RABIES IN WILD & DOMESTIC ANIMALSUNITED STATES, 1950-2005

0

1000

2000

3000

4000

5000

6000

7000

8000

9000

10000

1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005

YEAR

CASE

S

TOTAL

WILD

DOMESTIC

Rabies in Wild and Domestic Animals in the United States, 1950-2005

History of rabies control and its elimination from the United States

History of rabies control and its elimination from the United States

1988

Major rabies enzootics in terrestrial carnivores and the last rabies outbreak that involved both dogs and

coyotes in the United States

Major rabies enzootics in terrestrial carnivores and the last rabies outbreak that involved both dogs and

coyotes in the United States

FOX

Major Terrestrial RABV Biotypes:Geographic distribution in the US and Mexico.

Major Terrestrial RABV Biotypes:Geographic distribution in the US and Mexico.

Northcentral Skunk

Southcentral Skunk

Dog/ Coyote

Raccoon

CA Skunk

Baja CA Skunk

Red Fox

Yucatan Skunk Yucatan Dog

Chiapas DogGuerrero-Oaxaca Dog

Puebla -Tiaxcala Dog

Estado de Mexico Dog

Michoacan Dog

US- MX Dog

AZ Gray Fox

Sinaloa-Durango Skunk

North Central Mexico Skunk

Puerto Rico Mongoose

TX Gray Fox

To characterized, at genetic level, all RABV variants and lineages historically associated with enzootic rabies in dogs in the US in order to understand and follow up its elimination, evolution and re-emergence in wildlife canines.

General and objectiveGeneral and objective

Results

East Texas-Mex BorderDog-coyote D1

Yucatan Dog D10

Puebla-TlaxcalaDog D3, D7, D8

Guerrero-OaxacaDog D9

MichoacanDog D2, D4

Estado de MexicoDog D5 and D6

ChiapasDog

West US-Mx border Dog-coyote D11

*Extinct dog rabies focus

*

****

Searching the origin of re emerging enzootic dog rabies in the US: the domestic dog/coyote case, part I

Searching the origin of re emerging enzootic dog rabies in the US: the domestic dog/coyote case, part I

1979-2003

2587txcy94 2193txhm79

835txhm76 2160txdg85 2361txdg94 834txhm79 247coahcy01

4506tampct00 4508tampct02 3288michdg00

848ormichihm89 3147qrodg95 3151mxuk 555dfdg78

3127tlxgt91 3124puedg91 3126puepg93

2184camorhm93 3138michdk91

4823slpdg96 3267mxdg01 4511mxdg02 3260dfdg00 3325hgodg03 3269zacbv00 3284mxdg99

4514mxdg03 4516mxdg02

3134dfpg91 1278dfdg91

3121dfhm91 3244mxdg98 1282dfdg91 3142dfferr90

3278grodg99 4822puedg96 3143puebv94 3299dfdg99 3281puedg00 4513puedg02 4519puedg02 3303tlxdg02 3279puedg03 3275gtoct01 3302tlxdg01 4491mxdg02

3313jaluk03 559dfdg78

4815slpdg99 3125oaxdg92

3251grodg00 3285grodg01 3287grodg03

4476yucdg95 4480yucdg01 4481yucpg02 4485yucdg03

674cagroct87 4486chisdg03

1303orchihdg91 947azsonhm81

3123michbv91 3122michct90

953cachihhm79 2830txcy95 3144chihbv94

2520cacy90 726cahm61

3128dgodg91 671sondg88 672sondg88

1274sondg88 673sondg88

87

91

85

92

92

63

65

97

66

73

75

84

87

85

60

61

63

5950

55

D1

D2

D3

D4

D5

D6

D7

D8

D9D10

D11

D

*

**

*

1989-2000

1978-1995

1999-2003 *1993-1996

1990-1998

1994-1999

1999-2006

1992-2006

1995-2006

1995-2006

1961-1995

*

? Potentially, more cases during 2006

?

Searching the origin of re emerging enzootic dog rabies in the US: the domestic dog/coyote case, part II

Searching the origin of re emerging enzootic dog rabies in the US: the domestic dog/coyote case, part II

D5 E19 D13 E20

E17 A14 A15 G5 F6 B12 C8 D6 E14 C7 G3 H2 A16 C5 C12 D8 B19 H5 B13 D15 C3 C14

A8 B14 D13 A6 A9 C13 G4 B10 B2 E12 I6 H4

C9 A1

F17 C1 B17 I4 A4 H3 B20 B16 I5 F5 B5

D2 G1 A10 C21 B4 E11 E3 A13 A3 D1 H1 C19 B7

C2 F1 E8 I3 D4 F12 A12 I2 A18 C17 A5 F11

D14 A17 B1

D3 I1 B3 D16 G6 A2 E1 D17 B15 B11 B18 C11 C6

D7 F13 E10 G2 E7 E9 E2 F10 E5 D10 F14 E4 E16 F15 F3 F2 F4 E6

E15 D2 Michoacan Dog

D3 Puebla Tlaxcala Dog D9

D6DFEdoMexDg D8PueTlxDg

D7PueTlxDg D5EdoMexDg

D4MichMorDg D10YucDg

3853 El Salvador, Central America Hm 2003 4486chisdg02

D11 West US-Mexico border dog foci 1961-1995 “Sonora Dog variant” C16 C20

W6UScaliforniaSK7494 W7Yucunidentifiedreservoir

W9MxBCSSk9002 W4732californiaSK

W5USNorthcentralSk8498 WestCAnSK

W2UsMxGrayfox7902 3886Sonsk2003

W1SinDgoSk01 E13 D12 C15 C10 W3 US Texas gray fox 83-97 D9 A11 E18 D11 B6

C18 C4

SD53304 SD55304 SD54304

11104304 F016304 SNP11104304

W11 US Southcentral Skunk 84-02 B9

W12CanadaUSRaccoon W12

W13MxNorthcentralSk LCNA

LCMx LCCi LBNA

LMx LCi

LANNA HTCi

HTAg HTMx Mevcaluc9295

MCUS MCAzCAUSA8693

PipistrellusUSA EF1aCOUSA8502 EF1

71USA72EF1b AF394869ap93ca

AF394868ap91ca MCiAg TdbrCidmtc

EF2AZ EF2US

TBCiAg Tadarida brasiliensis mexicana North America B8

Dr7 Dr6

Dr1 Dr2

Dr3 DrSA

Dr4 Dr5

Duvenhage2 EBL2

99

99

92

99

68

70

75

99

89

88

77

97

96

61

65

6089

99

87

98

66

99

96

94

886795

70

84

67

71

65

63

64

62

89

0.05

W11 US Southcentral Skunk 84-99

Tadarida brasiliensis mexicana North America

D11 West Texas US Mexico border Dog “Sonora Dog”

W3 US Texas gray fox 83-97

Coyote/Dog East US- Mexico border 1976-2002

Consensus amino acid change with respect Dog variants. Amino acid Serine change to

Threonine in position 426.

D2, D3 Puebla-Tlaxcala 1978-1995Michoacan 1989-2000

Northcentral Skunk

Southcentral Skunk

Dog/Coyote

Raccoon

CA Skunk

Red Fox

Yucatan Dog

Chiapas Dog

Guerrero-Oaxaca Dog

Puebla -Tlaxcala Dog

Estado de Mexico Dog

Michoacan Dog

US- MX Dog

AZ Gray Fox

TX Gray Fox

1700Mxdfdg99 1766Mxdg02

575Mxtlxdg00 409 01550F

457Mxpuedg01 2749Mxpuepg00

177 02 2609Mxgtoct01 1769Mxpuedg02 67Mxtlxdg02

1096-00 440Mxgrodg99

657Mxdgosk01 1390Mxmxdg99

3143Mxpuebv94 3134Mxdfpg91

3121Mxdfhm91 3142Mxdffer90

3138Mxmichdk91 1407Mxmxdg00 1634-99

1587Mxdfdg00 1027 02

2509Mxmxdg02 2411-99

202Mxgrodg00 250Mxgrodg01

251Mxgrodg01 175Mxyucdg98

10Mxyucdg95 110Mxyucdg97

151Mxyuc98 428Mxyucct03 182Mxyucdg98 412Mxyucdg02

60Honddg01 3066Mxchisdg02

3122Mxmichct90 3123Mxmichbv91

3128Mxdgodg91 3144Mxchihbv94

3124Mxpuedg91 3126Mxpuepg93

3127Mxtlxgt91 3147Mxqrodg95

3151Puedg95 490Mxmichdg00

247Mxcoahcy01 3306Mxct02

B14Ustxcyken92 H2USTXWillcy98

E15USTXzavdg95 F2USTXlasallecy96

E14USTXhgocy95 G1USTXWebbcy97 B15UScyduv92

3907Mxsonbct 3140Mxsonbct94 3148Mxchihbct94

FluryLEP HEP-flury

D9USTxdglub94 YC63China

CVS11 PM1503

MRVChinahenan RAVNUCM61047 CVSFR AV01 RdfxEurope RacdgfxEastEu StepfxRdefxFareast

RedfxMiddleast Africa1b

Africa1a RCHLAB009663

NiCEAB128149 NishigaraAB044824

BrdgV2 SADB19M31046 SRV9AF499686

2840PuertoRico PrdgV1

2839PuertoRico 1629Mxbcssk01

3908Mxslpsk OrgTIndAY956319

ArctfxPakistan U11734ontario24 U03769arctica1

AY352499ArctAK ArctfxSibCan

1500AFS Viverrid Viver African AF467949

8660GUIAFR2 88636HAVAFR2

AsiandgInd-SriL AsiandgThai-Viet

2311Mxzacsk01 2818Mxslpsk02

1516-01 RaccoonCAnUs

SHBRVAY705373 LC8

3901Mxmichbv03 3902Mxmichbv03

TB1 AF394876 TB 1475 00

2153Salvhm02 3888Mxbvtamp03

460 3891verbv03 3858Mxhgoov03

3861Mxhgobv04 3878Mxslpbv04

AY573943flyfxGT7 U22845GT5

U22846GT699

100

9991

100

100

99

100

100

100100

73

83

100

100

98

85

100

100

100

100

100

57

100

100

10071

76

75

7691

100

78

100

77

98

86

68

99

89

88

84

72

65

77

100

98

100

90

100

99

99

71

9597

99

89

83100

95

75

99

7384

0.05

D1 Coyote/Dog East US Mexico border 1976 2002

D3 Dog Puebla-Tlaxcala 1978 1995 D2 Michoacan 1989 2000

W2 Arizona gray fox variant

W3 Texas gray fox variant

Vaccine strains related with CVS

Flury LEP and HEP

D11 Sonora Dog West US Mexico border 1961 1991 Michoacan 1990 1991Chiapas and Central America 2001 2003

D10 Yucatan 1995 2002

D9 Guerrero Oaxaca 1992 2003

D5 Estado de Mexico 1991 2002 D4 Michoacan 1991 1993

D6 Estado de Mexico 1991 1998

D7 Dog Puebla Tlaxcala 1994 2001

D8 Dog Puebla Tlaxcala 1999 2002

Mexican

do

g lin

eages

European and Middle east red foxAfrican 1 dog

SADB19 and Puerto RicoSouth American Dog variant

Baja California Sur, skunk

Arctic fox and arctic like variant

African mongooseWest African dog, Africa 2Asian dog

Vaccine strains red fox related

North American Skunk and raccoon variants

North American RV bat variants

Outgroup, other Lyssavirus species

Co

smo

po

litan d

og

varian

t

Ra

bie

s a

ss

oc

iate

d w

ith

te

rre

str

ial

ca

rniv

ore

s

Rabies associated with bats

1700Mxdfdg99 1766Mxdg02

575Mxtlxdg00 409 01550F

457Mxpuedg01 2749Mxpuepg00

177 02 2609Mxgtoct01 1769Mxpuedg02 67Mxtlxdg02

1096-00 440Mxgrodg99

657Mxdgosk01 1390Mxmxdg99

3143Mxpuebv94 3134Mxdfpg91

3121Mxdfhm91 3142Mxdffer90

3138Mxmichdk91 1407Mxmxdg00 1634-99

1587Mxdfdg00 1027 02

2509Mxmxdg02 2411-99

202Mxgrodg00 250Mxgrodg01

251Mxgrodg01 175Mxyucdg98

10Mxyucdg95 110Mxyucdg97

151Mxyuc98 428Mxyucct03 182Mxyucdg98 412Mxyucdg02

60Honddg01 3066Mxchisdg02

3122Mxmichct90 3123Mxmichbv91

3128Mxdgodg91 3144Mxchihbv94

3124Mxpuedg91 3126Mxpuepg93

3127Mxtlxgt91 3147Mxqrodg95

3151Puedg95 490Mxmichdg00

247Mxcoahcy01 3306Mxct02

B14Ustxcyken92 H2USTXWillcy98

E15USTXzavdg95 F2USTXlasallecy96

E14USTXhgocy95 G1USTXWebbcy97 B15UScyduv92

3907Mxsonbct 3140Mxsonbct94 3148Mxchihbct94

FluryLEP HEP-flury

D9USTxdglub94 YC63China

CVS11 PM1503

MRVChinahenan RAVNUCM61047 CVSFR

AV01 RdfxEurope RacdgfxEastEu StepfxRdefxFareast

RedfxMiddleast Africa1b

Africa1a RCHLAB009663

NiCEAB128149 NishigaraAB044824

BrdgV2 SADB19M31046 SRV9AF499686

2840PuertoRico PrdgV1

2839PuertoRico 1629Mxbcssk01

3908Mxslpsk OrgTIndAY956319

ArctfxPakistan U11734ontario24 U03769arctica1

AY352499ArctAK ArctfxSibCan

1500AFS Viverrid Viver African AF467949

8660GUIAFR2 88636HAVAFR2

AsiandgInd-SriL AsiandgThai-Viet

2311Mxzacsk01 2818Mxslpsk02

1516-01 RaccoonCAnUs

SHBRVAY705373 LC8

3901Mxmichbv03 3902Mxmichbv03

TB1 AF394876 TB 1475 00

2153Salvhm02 3888Mxbvtamp03

460 3891verbv03 3858Mxhgoov03

3861Mxhgobv04 3878Mxslpbv04

AY573943flyfxGT7 U22845GT5

U22846GT699

100

9991

100

100

99

100

100

100

100

73

83

100

100

98

85

100

100

100

100

100

57

100

100

100

71

76

75

76

91

100

78

100

77

98

86

68

99

89

88

84

72

65

77

100

98

100

90

100

99

99

71

9597

99

89

83100

95

75

99

73

84

0.05

Rabies associated with bats

1700Mxdfdg99 1766Mxdg02

575Mxtlxdg00 409 01550F

457Mxpuedg01 2749Mxpuepg00

177 02 2609Mxgtoct01 1769Mxpuedg02 67Mxtlxdg02

1096-00 440Mxgrodg99

657Mxdgosk01 1390Mxmxdg99

3143Mxpuebv94 3134Mxdfpg91

3121Mxdfhm91 3142Mxdffer90

3138Mxmichdk91 1407Mxmxdg00 1634-99

1587Mxdfdg00 1027 02

2509Mxmxdg02 2411-99

202Mxgrodg00 250Mxgrodg01

251Mxgrodg01 175Mxyucdg98

10Mxyucdg95 110Mxyucdg97

151Mxyuc98 428Mxyucct03 182Mxyucdg98 412Mxyucdg02

60Honddg01 3066Mxchisdg02

3122Mxmichct90 3123Mxmichbv91

3128Mxdgodg91 3144Mxchihbv94

3124Mxpuedg91 3126Mxpuepg93

3127Mxtlxgt91 3147Mxqrodg95

3151Puedg95 490Mxmichdg00

247Mxcoahcy01 3306Mxct02

B14Ustxcyken92 H2USTXWillcy98

E15USTXzavdg95 F2USTXlasallecy96

E14USTXhgocy95 G1USTXWebbcy97 B15UScyduv92

3907Mxsonbct 3140Mxsonbct94 3148Mxchihbct94

FluryLEP HEP-flury

D9USTxdglub94 YC63China

CVS11 PM1503

MRVChinahenan RAVNUCM61047 CVSFR AV01 RdfxEurope RacdgfxEastEu StepfxRdefxFareast

RedfxMiddleast Africa1b

Africa1a RCHLAB009663

NiCEAB128149 NishigaraAB044824

BrdgV2 SADB19M31046 SRV9AF499686

2840PuertoRico PrdgV1

2839PuertoRico 1629Mxbcssk01

3908Mxslpsk

100

100

100

100

75

76

91

100

78

100

98

86

99

89

88

84

72

65

77

100

98

100

90

100

99

99

71

9597

99

89

83100

95

75

99

73

84

D1 Coyote/Dog East US Mexico border 1976 2002

D3 Dog Puebla-Tlaxcala 1978 1995 D2 Michoacan 1989 2000

W2 Arizona gray fox variant

W3 Texas gray fox variant

Vaccine strains related with CVS

Flury LEP and HEP

D11 Sonora Dog West US Mexico border 1961 1991 Michoacan 1990 1991Chiapas and Central America 2001 2003

D10 Yucatan 1995 2002

D9 Guerrero Oaxaca 1992 2003

D5 Estado de Mexico 1991 2002

D4 Michoacan 1991 1993

D6 Estado de Mexico 1991 1998

D7 Dog Puebla Tlaxcala 1994 2001

D8 Dog Puebla Tlaxcala 1999 2002

Mexican

do

g lin

eages

European and Middle east red fox

African 1 dog

SADB19 and Puerto Rico

South American Dog variant

Baja California Sur, skunk

Vaccine strains red fox related

Co

smo

po

litan d

og

varian

t

Dog Rabies and Human MigrationsDog Rabies and Human Migrations

Northcentral Skunk

Southcentral Skunk

Dog/ Coyote

Raccoon

CA Skunk

Baja CA Skunk

Red Fox

Yucatan Dog

Chiapas DogGuerrero-Oaxaca Dog

Puebla -Tiaxcala Dog

Estado de Mexico Dog

Michoacan Dog

US- MX Dog

AZ Gray Fox

Puerto Rico Mongoose

TX Gray Fox

SAD B19 Puerto Rico Monngoose conection

We were able to detect historic movement patterns of major dog rabies enzootics which in turn are consistent with the demographics and immigration patterns of the Mexican and Central American populations described by the Sociologist Jorge Durand 2005.

We also showed potential historic disseminations of enzootic dog rabies into wild life populations such as those illustrated by the phylogenetic analysis in gray foxes and coyotes in Texas.

This findings stress out the importance of the historic follow up of rabies epizootics in order to assess future burdens for animal and public health.

Final RemarksFinal Remarks

Our study showed that rabies virus associated with enzootics in dog populations has evolved over time, in discrete geographic lineages which may be translocated by human related activities.

To: Texas Department of Health, Austin, TXL. ZuckeroP. HuntS. OertliL. RobinsonNational Zoonoses Program from the Ministry of Health, Mexico.Dr Fernando Vargas Pino and Rabies Laboratory at InDRE, from the Ministry of Health, Mexico.

AcknowledgementsAcknowledgements