POXVIRUS IN WEST AFRICAN NO" PRIMATES:

SEROLOGIC SURVEY RESULTS'

J . G . BREPIAN2

J. BERNADOU3

J.H. NAIUO~

1. Presented in part at the Ninth Annual Meeting of the Society for Epidemiologic Research, Toronto, June 16-19, 1976.

2 . Medical Epidemiologist, Bureau of Smallpox Eradication (BSE), Center for Disease Control (CDC), Atlanta, Georgia 30333, USA, attached to the Organization for the Coordination and Cooperatlbn of Endemic Disease Control (Organisation de Coordination et de Coopération pour la lutte contre les Grandes Endgmies (OCCCE)), Bobo-Dioulasso, Upper Volta.

3. Technical Officer, Office f o r Overseas Scientific and Technical Research (Office de la Recherche Scientifique et Technique d'outre-Mer (ORSTOH)), Entomclogy Laboratory, Centre Muraz, OCCGE, Bobo-Dioulasso, Upper Volta.

4. Chief, Viral Exanthems Branch, Virology Division, Bureau of Laboratories, CDC, Atlanta, Georgia 30333, USA.

U.S. DEPARTMENT OF HEALTH, EDUCATION, AND WELFARE PUBLIC HEALTH SERVlCE C E N T E R F O R DISEASE CONTROL

ATLANTA, GEORGIA 30333

*, AJ

i .

ACKNOWLEDGMENTS

Our g r a t i t u d e i s expressed t o t h e M i n i s t r i e s of A g r i c u l t u r e and t o

t h e Na t iona l Park S e r v i c e s of the Ivo ry Coast, Mali, and Upper Volta

f o r t h e i r e x c e l l e n t coope ra t ion . ' .

Appreciat ion i s extended t o D r . J. Mouchet, D r . G. Chauvet,

D r . A. C h a l l i e r , and D r . R. C o r d e l l i e r of the O f f i c e d e l a Recherche

S c i e n t i f i q u e e t Technique d'outre-Mer (O.R.S.T.O.M.), Centre Muraz,

Organisat ion d e Coordinat ion e t d e Coopération pour l a l u t t e c o n t r e

l es Grande's Endémies (O.C.C.G.E.), Bobo-Dioulasso, Upper Volta ,

1 t o M r . V. Ouedraogo of t h e O.C.C.G.E., and t o D r . Y. Robin,

D r . R. T a u f f l i e b , and D r . J. Coz of t h e I n s t i t u t P a s t e u r and O.R.S.T.O.M.,

Dakar, Senegal, f o r a s s i s t a n c e i n o b t a i n i n g serum samples f o r t h i s

s tudy. - D r . I. Arita of t h e World Hea l th Organizat ion k i n d l y reviewed t h e

manuscript . We thank D r . A.C. Hekker of t h e R i j k s I n s t i t u u t voor de

Volksgezondheid, U t rech t , The Nether lands, and M s . P.G. Bingham of

t h e Center f o r Disease Control , A t l a n t a , f o r s p e c i a l l a b o r a t o r y

a s s i s t a n c e .

Thanks are a l s o extended t o M r . P. S a l e s , M s . M.A. Ouandaogo,

M s . R. Cohen, and M s . M. C r a i g f o r h e l p i n manuscript p r e p a r a t i o n .

C

ii

ABSTRACT

Poxvirus in 'Wes t Af r i can Nonhuman Primates: S e r o l o g i c Survey R e s u l t s .

J . G . Breman, J. Bernadou, J . H . Nakano (Center f o r Disease Control ,

A t l a n t a , Ga. 30333, Organ i sa t ion d e Coordinat ion et d e Coopération

pour l a l u t t e c o n t r e l e s Grandes Endgmies (OCCGE), BP 153, Bobo-Didulasso,

Upper Volta , O f f i c e d e l a Recherche S c i e n t i f i q u e et TechnTque d'outre-Mer

(ORSTOM), BP 153, Bobo-Dioulasso, Upper V o l t a ) .

Ten s p e c i e s of nonhuman p r ima tes i n West Af r i can h a b i t a t were analyzed

f o r var iola-vacc. inia subgroup hemagg lu t ina t ion - inh ib i t i on (HI) and

n e u t r a l i z a t i o n ( n e u t ) a n t i b o d i e s . The animals were taken i n 27 d i f f e r e n t

sampling zones i n p a r t s of t h e Ivo ry Coast, Mali, and Upper Volta . Eight %

(15 of 195 t e s t e d ) had e l e v a t e d H I a n t i b o d i e s a f t e r n o n s p e c i f i c react ions-

were reduced w i t h KIO4 p re t r ea tmen t .

i n 21% ( 4 4 of 206) . Antibodies were d e t e c t e d i n serum from monkeys l i v i n g

nea r 2 areas where monkeypox cases i n humans have occurred. Four samples

P o s i t i v e neu t a n t i b o d i e s were found

were t e s t e d f o r monkeypox s p e c i f i c a n t i b o d i e s u s i n g an i n d i r e c t immuno-

f l u o r e s c e n t (IFA) t e s t ; 3 were p o s i t i v e . Desp i t e t h e . s i g n i f i c a n t p reva lence

of poxvirus a n t i b o d i e s i n monkeys (and o t h e r animals) i n West Af r i ca ,

smallpox e r a d i c a t i o n has been maintained i n t h e area s i n c e 1970; t h u s ,

animal r e s e r v o i r s of poxvirus appea r t o pose no t h r e a t t o t h e worldwide

smallpox e r a d i c a t i o n program.

1

INTRODUCTION

Monkeypox v i r u s w a s f i r s t i s o l a t e d i n 1958, from c a p t i v e Cynomolgus

monkeys w i t h exanthematous d i s e a s e i n Denmark (1).

ou tb reaks have occur red i n nonhuman p r ima te popu la t ions i n t h e USA,

The Nether lands and France ( 2 , 3 ) .

humans i n t h e t r o p i c a l r a i n ' f o r e s t of t h e Republic of Zaire i n 1970 ( 4 )

Nine subsequent .

Since monkeypox w a s i ' den t i f i ed i n

and i n 4 o t h e r c o u n t r i e s of West A f r i c a i n 1 9 7 1 ( 5 , 6 ) , v a r i o u s a t t e m p t s

have been made t o l i n k a nonhuman pr imate r e s e r v o i r t o human cases.

Serum samples from 2242 monkeys of several s p e c i e s from v a r i o u s

p a r t s of Af r i ca and A s i a were tested by d i f f e r e n t l a b o r a t o r i e s f o r

I n e u t r a l i z i n g (neu t ) a n t i b o d i e s t o v a r i o l a - v a c c i n i a a n t i g e n ( 7 ) . No sermil

w a s f e l t t o c o c t a i n s i g n i f i c a n t neu t ant ibody.

r h e s u s monkeys f a i l e d t o d e t e c t e i t h e r hemagglutination-inhibition"(H1) ...

A survey of 100 Ind ian ~

o r neu t poxvirus a n t i b o d i z s ( 8 ) . Other s t u d i e s have shown s i g n i f i c a n t

v a r i o l a - v a c c i n i a group neu t a n t i b o d i e s i n serum of monkeys a s s o c i a t e d

w i t h humans wi th smallpox (9) and i n t h e v i c i n i t y of humans w i t h .

monkeypox (6,1.0,11).

To d e f i n e p o s s i b l e nonhuman p r ima te r e s e r v o i r s of poxviruses i n

West A f r i c a , ve car - i - ied out su rveys i n a r e a s where t h e s e pr imates w e r e

known t o l i v e n a t u r a l l y .

g e n e r a l geographic zone where human monkeypox c a s e s have occurred (5 ,6 ) .

These areas of West Af r i ca are wi th in t h e

2

METH O DS

The s tudy used serum samples c o l l e c t e d i n a s t u d y t o d e f i n e t h e

p re sence of yel low f e v e r v i r u s c i r c u l a t i n g i n monkey popu la t ions i n

member c o u n t r i e s of t h e Organizat ion f o r t h e Coordinat ion and Cooperation

of .Endemic Disease Control (Organisat ion d e Coordinat ion e t de Coop6ration

pour l a l u t t e c o n t r e l e s Grandes Endémies) (OCCGE)* between January, 1973,

’ ,and May , 1’974.

A map of West Af r i ca w a s d iv ided i n t o deg rees by p a r a l l e l s

( l a t i t u d e s ) and mer id i ans ( long i tudes ) ( f i g . 1). A hun te r (J.B.) w a s

employed t o shoot wild pr imates i n 1 o r 2 squa re deg rees p e r month.

Each squa re deg ree c o n t a i n s approximately 12,100 km . s h o t i n 27 s q u a r e deg rees comprising about 327,000 km , con ta in ing -

2 Primates were

2

Y,

p a r t s of t h e Ivo ry Coast, Mali, and Upper Volta . Some zones bordered

Ghana, Guinea, and L i b e r i a .

zones, t h e f o r e s t and h e a v i l y wooded p r e f o r e s t (5’fN - 8’N) and t h e

savanna (8ON - 15ON).

Pr ima tes were found i n 2 major b io -c l imá t i c I

Immediately a f t e r shoo t ing a monkey t h e hun te r i d e n t i f i e d and

inspec‘ted t h e animal f o r age (young, young a d u l t , a d u l t , o l d ) , s ex ,

and g r o s s s u p e r f i c i a l l e s i o n s . H e drew blood by a s e p t i c h e a r t puncture .

. T h i s w a s allowed t o c l o t under r e f r i g e r a t i o n f o r less than 24 hours .

Serum w a s c e n t r i f u g e d and then poured i n t o a s t e r i l i z e d g l a s s v i a l

* Benin ( fo rmer ly Dahomey), Ivo ry Coast, Mali, Mauri tania , Niger,

Senegal, Togc, Upper Vol ta .

mycin, colymycin, and kanamycin.

packed i n dry i c e , and s e n t by a i r t o t h e Center f o r Disease Control

Serum samples w e r e f r o z e n a t -209C,

f o r test ing.

H I a n t i b o d i e s to v a c c i n i a a n t i g e n were measured a t t h e V i r a l

Exanthems Branch, Virology Div i s ion , CDC, by t h e m i c r o t i t e r technique

of Hierholzer and Suggs (12,13) and neut a n t i b o d i e s by a plaque

r educ t ion method ( 1 4 ) . An H I an t ibody t i ter of $ 1 0 ( r e c i p r o c a l of

t h e d i l u t i o n ) and a neu t ant ibody t i t e r of $ 4 w e r e considered p o s i t i v e .

I f t h e H I tes t w a s p o s i t i v e o r enough serum w a s a v a i l a b l e , t h e tes t was

repeated a f t e r t h e serum w a s t r e a t e d ' w i t h potassium p e r i o d a t e ( K I O 4 )

t o r u l e ou t a n o n s p e c i f i c r e a c t i o n (15) .

A subsample of serum t h a t w a s H I - and/or neu t -pos i t i ve was t e s t e d

f o r monkeypox an t ibody w i t h an i n d i r e c t immunofluorescence (IFA) test

ir

. .

4

RESULTS

t , Two hundred f o r t y - s i x p r ima tes from 10 savanna- and fo res t -dwe l l ing

s p e c i e s w e r e s h o t ( t a b l e 1); 56% of t h e s e w e r e savanna-dwelling Af r i can

green monkeys (Cercopi thecus a e t l i i o p s ) . No animal w a s noted t o have

e x t e r n a l l e s i o n s c o n s i s t e n t w i th a poxvirus d i s e a s e . .

Serum from 206 animals wa,s t e s t e d f o r H I and n e u t r a l i z i n g a n t i -

.bodies ( t a b l e 2 ) ; 43% (89/206) had H I a n t i b o d i e s , b u t on ly 8% (15/195)

w e r e p o s i t i v e a f t e r RIO4 pre t r ea tmen t . Fourteen of 15 HI-posi t ive serum

samples w e r e f r o m Cercopi thecus monkeys. Eleven of t h e HI-posi t ive

serum s a m p l e s w e r e from fo res t -dwe l l ing monkeys. Monkeys were about

e q u a l l y d iv ided by sex . Female monkeys w i t h s i g n i f i c a n t HI-antibody

l e v e l s predominated over males, 11 t o 4 ( t a b l e 3 ) ; 21% (44/206) o f . *

t h e p r ima tes had d e t e c t a b l e neu t a n t i b o d i e s . Animals w i t h neu t a n t i -

bodies w e r e e q u a l l y d iv ided between sexes. Among young monkeys on ly 11%

had neu t a n t i b o d i e s , whereas 27% of a d u l t s had n e u t a n t i b o d i e s . N o sex-

r e l a t e d d i f f e r e n c e s i n neu t an t ibody p reva lence w a s observed.

F igu re 2 i n d i c a t e s t h e d i s t r i b u t i o n of t h e t i ters of animals w i t h

p o s i t i v e neu t J n t i b o à i e s . Colobus monkeys had h i g h e r neut t i t e rs than

Cercopi thecus monkeys. Younger monkeys, i f p o s i t i v e , tended t o have

higher n e u t t i terP.

Four specimens were t e s t e d f o r s p e c i f i c monkeypgx a n t i b o d i e s .

Three were p o s i t i v e ( t a b l e 4 ) .

w i t h i n 200 km. of a r e a s where human monkeypox c a s e s have occurred.

These 3 animals were found i n zones

5

The geographic d i s t r i b u t i o n of monkeys wi th p o s i t i v e a n t i b o d i e s i s

shown i n f i g . 1.

h e a v i l y wooded savanna and t h e f o r e s t .

The h i g h e s t c o n c e n t r a t i o n of p o s i t i v e animals w a s i n

DISCUSSION

These s e r o l o g i c su rveys i n d i c a t e t h a t bo th savanna- and f o r e s t -

dwe l l ing Cercopi thecus and fo res t -dwe l l ing Colobus monkeys i n West

A f r i c a have been i n f e c t e d w i t h a poxvirus , probably an Orthopoxvirus,

t h e subgroup c o n t a i n i n g v a r i o l a , vaccinia , ' monkeypox and whitepox.

Monkeypox i n f e c t i o n s have occurred i n s p e c i e s of bo th Cercopithecus

and Colobus.

The 15 p o s i t i v e H I t i ters a f t e r K I 0 4 p re t r ea tmen t are somewhat

d i f f i c u l t t o i n t e r p r e t .

of r e c e n t poxvirus i n f e c t i o n (17), t h e r e is some evidence from t h i s

If one c o n s i d e r s H I a n t i b o d y ' t b b e a r e f l e c f i o n u.

s tudy t h a t a c t i v e i n f e c t i o n s w e r e occu r r ing w i t h i n t h e yea r preceding

t h e su rveys . Only 1 animal w i t h H I a n t i b o d i e s w a s considered young,

s o w e cannot conclude t h a t . t h e s e i n f e c t i o n s are u s u a l l y acquired a t

a n e a r l y age. However, t h e h i g h titers of neu t a n t i b o d i e s i n several

young monkeys may r e p r e s e n t r e l a t i v e l y r e c e n t ' i n f e c t i o n s . The' r e l a t i o n -

s h i p of an t ibody t i t e r level and maintenance of a poxvirus i n f e c t i o n

i s s t i l l u n c l e a r . A v a r i o l a - l i k e v i r u s i s o l a t e d from t h e kidney of a

h e a l t h y champanzee found i n t h e Republic of Z a i r e (10) was a s s o c i a t e d

w i t h a H I t i t e r of 1:1280 and a neu t t i ter of 1:>40 (18) i n d i c a t i n g t

t h a t premunit ion does occur .

\

6

It i s d i f f i c u l t t o e s t i m a t e t h e type and i n t e n s i t y of con tac t

t h e s e monkeys have with humans.

p r ima tes are captured and kep t as p e t s . They are a l s o sho t f o r food

I n many of t h e s e areas nonhuman

and are o f t e n cons idered a c u l i n a r y de l i cacy .

monkeys a r e used t o make c l o a k s and o t h e r r e g a l i a f o r t r i b a l ceremonies.

Skins of ‘Colobus

While nonhuman ?rimates u s u a l l y s t a y away from major popula t ion c e n t e r s ,

t hey f r e q u e n t l y t ake f o o l fì-um f i e l d s under c u l t i v a t i o n .

A human monkeypox c a s e i n e a s t e r n L i b e r i a (zone 6 6 ) (5) occurred

less than 50 km. from Guiglo Department (Toulepleu r eg ion - zone 66)

i n t h e Ivory Coast where 3 of 6 Colobus badius monkeys had neut

a n t i b o d i e s an¿ less than 200 km. from a zone where monkeypox-specific

an t ibody w a s found i n t h e s a m e spec ie s .

w i t h neut a n t i b o d i e s w a s cap tu red i n Abengourou Department (Agnib i lekmu

r e g i o n - zone 118), near t h e area (zone 119) where a case of human

A Cercopi thecus mona monkey

monkeypox w a s a s s o c i a t e d w i t h p o s i t i v e neut t i ters i n serum from

Cercopi thecus nona. C. d i a n a , and C . p e t a u r i s t a monkeys a s w e l l ’ a s

from roden t s , l a r g e r mammals, and b i r d s (6 ) . The 2.C:petaurista

monkeys w i t h monkeypox-specific a n t i b o d i e s were. found wi th in 200 kn.

of where t h i s 1;uman mozkeypox c a s e occurred. These fores t -dwel l ing

monkey popular lons m s v s h a r e t h e same a r b o r e a l h a b i t a t s (19); they

have been observed mixing t o g e t h e r .

p a s s under p r ima tes and, i f s u s c e p t i b l e , could conceivably become

i n f e c t e d by this a s s o c i a t i o n .

S m a l l mammals such as roden t s

The p o t e n t i a l wide hos t range of

i 7

monkeypox virus was demonstrated in Holland, where a strain, isolated

from anteaters and monkeys, was transmitted to rabbits and suckling

mice (20).

It seems obvious that a reliable serologic test that could dis-

tinguish the various poxviruses would be an important epidemiologic

tool for poxvirus research.

is the most promising recent development in this field. .

The IFA test using cross-absorbed antigen

Isolating monkeypox virus and other poxviruses from wild animals

‘would be helpful in defining the epidemiology of these viruses. .However,

experience has been that a great number of animals would have to be

captured in order to isolate even a few viruses. More information is

needed.on the possible contacts that wild animals with evidence of

prior monkeypox infection have with human populations as well as on %

associations !>.?tueen animals of the same and other species.

Despite the eiridence of recent rind past poxvirus infections among

different anhial populations in this zone, there i.s little reason to.\

think that Lhe worldwide smallpox eradication program is endangered.

There have becn cnly 20 known cases of monkeypox in humans in West and

Central Africa; a l l have occurred since 1970 (21) . All but I of the out- -

breaks have been observed in forest villages of less than 300 persons.

Human-to-human transmission occurs with difficulty.

cases of human monkeypox among intimately exposed family contacts have

Only 2 secondary

8

been r epor t ed . The 6% secondary a t t a c k ra te f o r s u s c e p t i b l e persons i n

c o n t a c t w i th human monkeypox i s much less t h a n t h a t of c lass ic smallpox,

which ranges between 35% and 45%. Even a f t e r t h e mass v a c c i n a t i o n

campaigns, t h e West and C e n t r a l A f r i c a n popu la t ion h a s never been much

more than 80% i m u n e t o smallpox, an immunity which appears t o p r o t e c t

a l s o a g a i n s t monkeypox. A s t h e r u r a l f o r e s t and savanna popu la t ion h a s

r e g u l a r c o n t a c t w i t h nonhuman p r ima tes as w e l l as w i t h o t h e r animals

w i t h poxvirus a n t i b o d i e s , more human c a s e s due t o monkeypox o r o t h e r I Orthopoxviruses would b e expected i f t h e s e v i r u s e s had an a f f i n i t y f o r

man. Large numbers of human cases have n o t been found d e s p i t e i n t e n s i f i e d

s u r v e i l l a n c e f o r human.poxvirus d i s e a s e s i n c e 1970.

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9

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Species

TABLE 2

VARIOLA-VACCINIA ANTIBODIES FOUND I N WILD PRIMATES

Cercopi thecus a e t h i o p s

C. mona

1. p e t a u r i s t a

C. d i ana

C. n i c t i t a n s

Genus T o t a l

Colobus bad ius

C. polykomos

C. v e r u s

Genus.Tota1

Erythrocebus p a t a s

Papio anubis

HI*

N o . Tes t ed No. Pos, Z Pos.

99

29

31

6

5

170

-

15

O

1

1 6

-

5

4

195

-

4

3

5

1

1

1 4

. .

-

1

- O

1

-

O

O

15

-

4

10

* 16

17

20 - 8

7

- O

6

-

O

O

8

-

Neut

No. Tested No. Pos. % Pos.

101

33

' 31

10

5 ' - 180

15

1

1

17

-

5

4

206

- n

25

6

6

O

1

38

-

5

1

O

6

-

O

25

25

19

O

20

2 1

-

33

100

O

\* 35

-

O

* 206 were H I p o s i t i v e ; these 195 were t e s t e d a g a i n a f t e r be ing t r e a t e d w i t h K I 0 4 .

Spec ie s

Cercopi thecus a e t h i o p s

11 I I

I I I I

Cercopi thecus d i ana

Colobus b a d i u s

Cercopi thecus n i c t i t a n s

Cercopi thecus p e t a u r i s t a

11 1 1

Cercopi thecus a e t h i o p s

Cercopi thecus p e t a u r i s t a

I I I I

11 11

Cercopi thecus mona

II ? I

?I I ?

Tab le 3

Monkeys w i t h P o s i t i v e H I Ti ters

Number

334

344

34 6

503

511

5 30

538

541

38 7

557

.5 7 5

577

582

581

559

Zone

74

. 75

75

77

77

87

98

98

107

108

117

117

117

1 1 7

-

i18

A

A

A

A

A

A

YA

A

A

YA

A

Y

YA

A

A

Sex H I

F 40

M 10

M * 20

F 1 0

F 1 0

F 10

M 40

F 20

M . 20

F 40

F 1 0

F 40

F 20

F 40

F 80

- -

100

-

A - Adult

Y - Youth

Table 4

9 Titers on Serum Tes ted For

Variola-Vacciniai Group and Monkeypox Ant ibodies

Number Zone HI* Neut*

Colobus bad ius 492 89 c 5 2500

Cercopi thecus p e t a u r i s t a 576 117 5 450

Cercopi thecus pe t a u r i s t a 577 117 40 450

* Center f o r Disease Con t ro l

** R i j k s I n s t i t u u t voor de Volksgezondheid

I

. .

I F T i t e r * * A f t e r a b s o r p t i o n A f t e r a b s o r p t i o n

w i t h v a c c i n i a a g a i n s t Vac cinia Monkeypox Vaccinia Monkeypox

w i t h monkeypox a g a i n s t

< 8 8 < 8 < 8

c 8

c 8

. ( 8

c 8

< 8 64

c 8 64

t

U

N 16"- 15"- 14"- 13"- 12"-

1 1"- 10"-

9"-

8"

7"-

6 O-

Figure 1 cf

Geographic Distribution of Orthopoxvirus Antibodies in Non-Human Primates

ATLP

Neut 0%

Neut Neut Neut H I 1-24% 25 -49 "/o >5O% (after KI041

+-Human Monkeypox . O-Monkeypox Antibody

I' . I

' Neutralizing Anti body, Titers in Nonhuman Primates Figure 2

> 2049

1025 -2048

cn [r w

I- !I

513 -1024

257-512

129-256

65-128

33-64

17-32

9-16

5-8

4

. 0 .

2500

. e.

o

. . .

e

.

e

I I 1 I I c - 1 I I I a

Cercopithecus C.mona C. petaurista G. nictitans Colobus Colobus aet hiops badius polykomos