serological survey results - Horizon documentation-IRD

POXVIRUS IN WEST AFRICAN "ON
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 C O N T R O L
A T L A N T A , G E O R G I A 30333
*,
AJ
i
.
ACKNOWLEDGMENTS
Our g r a t i t u d e i s e x p r e s s e d 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 N a t i o n a l P a r k S e r v i c e s of the I v o r y Coast, Mali, and Upper Volta
f o r t h e i r excellent cooperation.
'
.
A p p r e c i a t i o n 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.),
C e n t r e Muraz,
O r g a n i s a t i o n d e C o o r d i n a t i o n e t d e Coopération pour l a l u t t e c o n t r e
l e s Grande's Endémies (O.C.C.G.E.),
1
Bobo-Dioulasso,
t o M r . V. Ouedraogo of t h e O.C.C.G.E.,
Upper V o l t a ,
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
study.
D r . I. Arita of t h e World H e a l t h O r g a n i z a t i o n k i n d l y reviewed t h e
manuscript.
We t h a n k D r . A.C.
Hekker of t h e R i j k s I n s t i t u u t voor d e
Volksgezondheid, U t r e c h t , The N e t h e r l a n d s , and M s . P.G. Bingham of
t h e Center f o r Disease C o n t r o l , 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
assistance.
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 i n ' W e s t A f r i c a n Nonhuman P r i m a t e s :
J.G.
Breman, J. Bernadou, J . H .
A t l a n t a , Ga.
S e r o l o g i c Survey R e s u l t s .
Nakano ( C e n t e r f o r Disease C o n t r o l ,
30333, O r g a n i s a t i o n d e C o o r d i n a t i o n e t 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 V o l t a , 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 i m a t e s i n West A f r i c a n h a b i t a t were analyzed
f o r v a r i o l a - v a c c . i n i a subgroup h e m a g g l u t i n a t i o n - i n h i b i t i o n (HI) and
neutralization (neut) antibodies.
The a n i m a l s were t a k e n 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 I v o r y Coast, Mali, and Upper V o l t a .
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 r e a c t i o n s were reduced w i t h KIO4 p r e t r e a t m e n t .
i n 21% ( 4 4 of 2 0 6 ) .
P o s i t i v e n e u t a n t i b o d i e s were found
A n t i b o d i e s were d e t e c t e d i n serum from monkeys l i v i n g
n e a r 2 areas where monkeypox cases i n humans have o c c u r r e d .
Four samples
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 immunof 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 .
Despite t h e . s i g n i f i c a n t prevalence
of p o x v i r u s a n t i b o d i e s i n monkeys (and o t h e r animals) i n West A f r i c a ,
smallpox e r a d i c a t i o n h a s been maintained i n t h e area s i n c e 1970;
thus,
animal r e s e r v o i r s of p o x v i r u s a p p e a 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). Nine subsequent .
o u t b r e a k s have o c c u r r e d i n nonhuman p r i m a t e p o p u l a t i o n s i n t h e USA,
The N e t h e r l a n d s and F r a n c e ( 2 , 3 ) .
S i n c e monkeypox w a s i ' d e n t i f i e d i n
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 )
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 p r i m a t e r e s e r v o i r t o human cases.
Serum samples from 2 2 4 2 monkeys of several s p e c i e s from v a r i o u s
p a r t s of A f r i c a 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
neutralizing (neut) antibodies t o variola-vaccinia antigen (7).
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 neut antibody.
No sermil
A survey of 100 I n d i a n
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) ...
o r neut 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 n e u 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 w i t h 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 i m a t e r e s e r v o i r s of p o x v i r u s e s i n
West A f r i c a , ve c a r - i - i e d o u t s u r v e y s i n a r e a s where t h e s e p r i m a t e s w e r e
known t o l i v e n a t u r a l l y .
These areas of West A f r i c a a r e w i t h i n t h e
g e n e r a l geographic zone where human monkeypox c a s e s have o c c u r r e d ( 5 , 6 ) .
~
2
METHO DS
The s t u d y 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 r e s e n c e of y e l l o w f e v e r v i r u s c i r c u l a t i n g i n monkey p o p u l a t i o n s i n
member c o u n t r i e s of t h e O r g a n i z a t i o n f o r t h e C o o r d i n a t i o n and Cooperation
of .Endemic Disease C o n t r o l ( O r g a n i s a t i o n d e C o o r d i n a t i o n 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 J a n u a r y , 1973,
’
,and May , 1’974.
A map o f West A f r i c a w a s d i v i d e d i n t o d e g r e e s by p a r a l l e l s
( l a t i t u d e s ) and m e r i d i a n s ( l o n g i t u d e s ) ( f i g . 1). A h u n t e r (J.B.)
was
employed t o s h o o t w i l d p r i m a t e s i n 1 o r 2 s q u a r e d e g r e e s p e r month.
Each s q u a r e d e g r e e c o n t a i n s approximately 12,100 km
.
2
s h o t i n 27 s q u a r e d e g r e e s comprising about 327,000 km
2
P r i m a t e s were
, containing Y,
p a r t s of t h e I v o r y Coast, Mali, and Upper V o l t a .
I
Ghana, Guinea, and L i b e r i a .
Some zones bordered
P r i m a t e s were found i n 2 major b i o - c l i m á t i c
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
savanna (8ON
-
-
8’N)
and t h e
15ON).
Immediately a f t e r s h o o t i n g a monkey t h e h u n t e 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 e x ,
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 p u n c t u r e .
. 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 t h a n 24 h o u r s .
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 ( f o r m e r l y Dahomey), I v o r y Coast, Mali, M a u r i t a n i a , Niger,
Senegal, Togc, Upper Vol t a .
mycin, colymycin, and kanamycin.
Serum samples w e r e f r o z e n a t -209C,
packed i n d r y i c e , and s e n t by a i r t o t h e Center f o r Disease C o n t r o l
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 D i v i s i o n , CDC, by t h e m i c r o t i t e r t e c h n i q u e
of H i e r h o l z e r and Suggs (12,13) and n e u t a n t i b o d i e s by a p l a q u e
r e d u c t i o n method ( 1 4 ) .
An H I a n t i b o d y t i t e r 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 n e u t a n t i b o d y t i t e r of $ 4 w e r e c o n s i d e r e d p o s i t i v e .
I f t h e H I t e s 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 t e s t was
r e p e a t e d 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 out 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 - a n d / o r n e u t - p o s i t i v e was t e s t e d
f o r monkeypox a n t i b o d y w i t h an i n d i r e c t immunofluorescence (IFA) t e s t
ir
.
.
4
RESULTS
t,
Two hundred f o r t y - s i x p r i m a t e s from 10 savanna- and f o r e s t - d w e l l i n g
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 A f r i c a n
green monkeys ( C e r c o p i t h e c u s a e t l i i o p s ) .
No animal w a s n o t e d 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 with a poxvirus d i s e a s e . .
Serum from 206 a n i m a l s 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 o n l y 8% (15/195)
w e r e p o s i t i v e a f t e r RIO4 p r e t r e a t m e n t .
F o u r t e e n of 15 H I - p o s i t i v e
samples w e r e f r o m C e r c o p i t h e c u s monkeys.
Eleven of t h e H I - p o s i t i v e
serum s a m p l e s w e r e from f o r e s t - d w e l l i n g monkeys.
e q u a l l y d i v i d e d by s e x .
serum
Monkeys were about
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 o v e r males, 11 t o 4 ( t a b l e 3 ) ; 21% (44/206) o f .
t h e p r i m a t e s had d e t e c t a b l e n e u t a n t i b o d i e s .
b o d i e s w e r e e q u a l l y d i v i d e d between sexes.
Animals w i t h n e u t a n t i Among young monkeys o n l y 11%
had n e u 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 n e u t a n t i b o d y p r e v a l e n c e w a s observed.
F i g u r e 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 t e r s of a n i m a l s w i t h
positive neut Jntiboàies.
C e r c o p i t h e c u s monkeys.
Colobus monkeys had h i g h e r n e u t t i t e r s t h a n
Younger monkeys, i f p o s i t i v e , tended t o have
higher n e u t titerP.
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 ) .
*
These 3 a n i m a l s were found i n zones
w i t h i n 200 km. of a r e a s where human monkeypox c a s e s have o c c u r r e d .
5
The g e o g r a p h i c d i s t r i b u t i o n of monkeys w i t h 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. 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 a n i m a l s w a s i n
h e a v i l y wooded savanna and t h e f o r e s t .
DISCUSSION
These s e r o l o g i c s u r v e y s i n d i c a t e t h a t b o t h savanna- and f o r e s t d w e l l i n g C e r c o p i t h e c u s and f o r e s t - d w e l l i n g 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 p o x v i r u s , p r o b a b l y a n Orthopoxvirus,
t h e subgroup c o n t a i n i n g v a r i o l a , v a c c i n i a , ' monkeypox and whitepox.
Monkeypox i n f e c t i o n s have o c c u r r e d i n s p e c i e s of b o t h Cercopithecus
and Colobus.
The 15 p o s i t i v e H I t i t e r s a f t e r K I 0 4 p r e t r e a t m e n t are somewhat
difficult t o interpret.
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
of r e c e n t p o x v i r u s i n f e c t i o n (17), t h e r e i s some e v i d e n c e from t h i s
study t h a t a c t i v e i n f e c t i o n s w e r e occurring w i t h i n t h e year preceding
the surveys.
Only 1 animal w i t h H I a n t i b o d i e s w a s c o n s i d e r e d young,
s o w e c a n n o t c o n c l u d e 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 a c q u i r e d a t
a n e a r l y age.
However, t h e h i g h titers of n e u 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 a n t i b o d y t i t e r l e v e l and maintenance of a p o x v i r u s i n f e c t i o n
i s still unclear.
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
t
w i t h a H I t i t e r of 1:1280 and a n e u t t i t e r of 1:>40 (18) i n d i c a t i n g
t h a t premunition does occur.
u.
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 t y p e and i n t e n s i t y of c o n t a c t
t h e s e monkeys have w i t h humans.
I n many of t h e s e areas nonhuman
p r i m a t e s a r e c a p t u r e d and k e p t as p e t s .
They a r e a l s o s h o t f o r food
and a r e o f t e n c o n s i d e r e d a c u l i n a r y d e l i c a c y .
S k i n s of ‘Colobus
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.
While nonhuman ?rimates u s u a l l y s t a y away from major p o p u l a t i o n c e n t e r s ,
t h e y f r e q u e n t l y t a k e 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) o c c u r r e d
l e s s t h a n 50 km. from Guiglo Department (Toulepleu r e g i o n
-
zone 66)
i n t h e I v o r y Coast where 3 o f 6 Colobus b a d i u s monkeys had neut
\
a n t i b o d i e s an¿ l e s s t h a n 200 km. from a zone where monkeypox-specific
a n t i b o d y w a s found i n t h e s a m e s p e c i e s .
A C e r c o p i t h e c u s mona monkey
w i t h neut a n t i b o d i e s w a s c a p t u r e d i n Abengourou Department ( A g n i b i l e k m u
region
-
zone 118), n e a r t h e area (zone 119) where a case of human
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 n e u t t i t e r s i n serum from
C e r c o p i t h e c u s 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 r o d e n 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 w i t h i n 200 kn.
of where t h i s 1;uman mozkeypox c a s e occurred.
These f o r e s t - d w e l l i n g
monkey p o p u l a r l o n s 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); t h e y
have been observed mixing t o g e t h e r .
S m a l l mammals s u c h as r o d e n t s
p a s s under p r i m a t e s and, i f s u s c e p t i b l e , could c o n c e i v a b l y become
i n f e c t e d by this a s s o c i a t i o n .
The p o t e n t i a l wide h o s t r a n g e 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 distinguish the various poxviruses would be an important epidemiologic
tool for poxvirus research. The IFA test using cross-absorbed antigen
is the most promising recent development in this field.
.
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 !>.?tueenanimals 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 t o . \
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 ( 2 1 ) .
All but I of the o u t - -
breaks have been observed in forest villages of less than 300 persons.
Human-to-human transmission occurs with difficulty.
Only 2 secondary
cases of human monkeypox among intimately exposed family contacts have
8
been r e p o r t e d .
The 6% secondary a t t a c k r a t e f o r s u s c e p t i b l e p e r s o n s i n
c o n t a c t w i t h human monkeypox i s much l e s s t h a n t h a t of c l a s s i c 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 p o p u l a t i o n h a s n e v e r been much
more t h a n 80% i m u n e t o smallpox, an immunity which a p p e a r s 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 p o p u l a t i o n h a s
r e g u l a r c o n t a c t w i t h nonhuman p r i m a t e s as w e l l as w i t h o t h e r a n i m a l s
I
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
Orthopoxviruses would b e expected i f t h e s e v i r u s e s had a n a f f i n i t y f o r
man.
Large numbers of human cases have n o t b e e n 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.
t
t
9
REFERENCES
1.
von Magnus, P.; Andersen, E.K.; P e t e r s e n , K.B.;
46:156.
.1959, Acta. P a t h . Microbiol. Scand. -
1968, Bull.’Wld. H l t h . Org., 39:277.
2 . . A r i t a , I.; Henderson, D.A.:
.
3.
Milhaud, C.;
2:121.
-
4.
Ladnyj, I . D . ;
46: 593.
K l e i n , M.;
Birch-Andersen,A.:
Virat, J.:’
Zieyler, P.;
1969, E x p g r i m e n t a t i o n a n i m a l e ,
K i m , E.:
1972, B u l l . Wld. H l t h . Org.
5.
F o s t e r , S.O.; B r i n k , E.W.; H u t c h i n s , D.L.; P i f e r , J . M . ; L o u r i e , B . ;
Moser, C . R . ; Cummings, E.C.; K u t e y i , O.E.K.;
Eke, R.E.A.;
Titus,
J . B . ; Smith, E.A.; H i c k s , J . W . ;
Foege, W.H.:
1972, B u l l . Wld.
H l t h . Org., 46:569.
6.
B r e r k n , J . G . ; Nakano, J . H . ; C o f f i , E . ;
1977, Am. J . Trop. Med. Hyg., 26:273.
7.
Arita,
Godfrey, H.;
-
S.S.;
Gautun, J . C . :
I . ; Gispen, R . ; K a l t e r , . S.S.;
Lim Teong Wah; Marennikova,
N e t t e r , R . ; Tagaya, I . : 1972, B u l l . Wld. H l t h . O r g . , 5 : 6 2 5 .
8.
S e h g a l , C.L.;
9.
Mack, T.M.;
Ray, S.N.:
1974, J . Com. Dis. ( I n d i a ) , $:233.
Noble, J . , J r . :
1970, Lancet i:752.
10.
F o s t e r , S.O.:
1973, I X I n t e r n a t i o n a l Conference on T r o p i c a l
Medicine and Malaria, A b s t r a c t s o f I n v i t e d P a p e r s , L:113.
11.
Marennikova, S.S.;
Gurvic’, E.B.;
V i r u s f o r s h . , -33:201.
12.
H i e r h o l z e r , 2.C.:
Suggs, N.T.:
1969, Appl. Microb., 18:816.
13.
Hierholzer, J . C . ;
Suggs, M.T.:
1969, Appl. Microb., =:824.
14.
Wulff, H. ; C h i n , T . D . Y . ;
15.
WHO, 1959,
16.
Gispen, R.; Brand-Saathof, B.; Hekker, A.C.:
1976, WHO Informal
Group C o n s u l t a t i o n on Monkeypox and R e l a t e d V i r u s e s . Geneva,
53:355.
1976, B u l l . Wld. H l t h . Org., -
W
S e l u h i n a , E.M.:
Wenner, H.A.
:.
1971, Arch. G e s .
1969, Am. J . E p i . , 99:312.
T e c h n i c a l Report S e r i e s , No. 170, 41.
Y
10
I
17. Kitamura, T.; Shinjo, N.:
d
1972, Bull. Wld. Hlth. Org., 46:15..
-
O
18. Marrenikova, S . S . ; Seluhina, E.M.; Mal'ceva, N.N.; Ladnyj, I . D . :
1972, Bull. Wld. Hlth. Org., 46:613.
.
19. Dorst, J.; Dandelot, P.:
1969, A Field Guide to the Larger Mammals
of Africa. Houghton Mifflin,Company,Boston, pp. 51-83.
20.
Gispen, R.:
1975, Trans. Roy. Soc. Trop. Med. Hyg., 69:299.
21. Arita, I.; Henderson, D.A.:
v
1976, Bull. Wld. Hlth. Org., 53:347.
P,
B
O
: c r
. P ,
cr
m
r-
d
3
C
Y
ri
cc
s
S
a
Y
ID
Y
O
C
m
o
O
ID
d
e
GY
G
Y
ID
n
F
cc
g
G
m
El.
O
P
O
d
o
ID
mP,
ma
C a
P b
c art
r t m
3n
3
Y
O S I D
M
rc
.
-
-
o
6
C
m
c,
O
o
a
ID
Y
2
ID
..
P
cn
ID
m
O
o
Y.
rt
7
Et
E'
Y.
GY
P.
ID
ID
Y
P
P
P,
309
1-4
O0
rt
n
3
P,
rr
PI
Y
v1
Y.
P,
Y
ID
'd
'd
C
Y.
rt
ID
m
O
Y
ID
m
v)
1
d3
P,
m
ID
a
a
2O
).
rt
m
ID
Y
2 5.
ID
P
rt
P,
.ID
Y.
cn
h,
R
O
'd
C
Y
O
Y
O
U
ID
g
w
F
v
w
Et
O
'3
R
ID
P
P
ID
P,
os
rt
ID
m
M
Y
O
U
O
3'
c
GY
rt
n,
O
Y
ID
Y.
g
P,
Y
-I
m
(D
P
b.
a
W.
El
sa
Y
s
c,
o
Y.
4 mi2.D
3
m
ID
09
r
Y
n,
Y
GY
R
Y
ID
A
g
0
a
ID
m
O
::
m
rt
3
1-4
Y
P,P,
3
O
Y.
Y.
Ort
w
N m
o\Y
I I D
ah
mw
Y
o m
mm
b,
6 3
IDO
IDO
E<
rtP,
o 3
a
wP,
Y
0 3
PP,
P C
mv3
cc
F
8
El
3
ID
Y
Y
O0
O
rt
rd
c
Y
P-
E
m
ID
G,
0)
P
w
4
P,
w
P
U
1-4
P
O
El
a
ID
I
3
O
m
ID
i.r.
Y
ID
ocn
I:
TABLE 2
VARIOLA-VACCINIA ANTIBODIES FOUND I N WILD PRIMATES
HI*
Species
Neut
N o . T e s t e d No. Pos,
Cercopithecus a e t h i o p s
4
99
.
Z Pos.
No. T e s t e d
No. Pos.
4
101
25
25
10
33
6
25
31
6
19
O
O
.
C. mona
29
3
1. p e t a u r i s t a
31
5
6
1
17
10
20
-
5
-
C. d i a n a
% Pos.
*
16
'
C. n i c t i t a n s
5
-
1
-
Genus T o t a l
170
14
8
180
38
21
15
1
7
15
5
33
O
-
-
1
Colobus b a d i u s
C. polykomos
C. v e r u s
Genus.Tota1
Erythrocebus p a t a s
Papio anubis
*
'
1
-
1
100
1
-
O
-
O
-
1
-
O
-
16
1
6
17
6
5
O
O
5
O
4
-
O
-
195
15
O
-
O
8
20
-
4
-
\*
35
O
n
206
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 b e i n g t r e a t e d w i t h K I 0 4 .
Table 3
Monkeys w i t h P o s i t i v e H I T i t e r s
Species
Number
Cercopithecus aethiops
Zone
-
Sex
-
HI
-
334
74
A
F
40
344
. 75
A
M
10
34 6
75
A
M
Cercopithecus diana
503
77
A
F
10
Colobus b a d i u s
511
77
A
F
10
Cercopithecus n i c t i t a n s
5 30
87
A
F
10
Cercopithecus p e t a u r i s t a
538
98
YA
M
40
541
98
A
F
20
Cercopithecus aethiops
38 7
107
A
M
Cercopithecus p e t a u r i s t a
557
108
YA
F
40
.5 7 5
117
A
F
10
577
117
Y
F
40
582
117
YA
F
20
581
117
A
F
40
559
i18
A
F
80
11
II
II
II
11
11
II
II
11
11
C e r c o p i t h e c u s mona
II
?I
?I
I?
A
-
Adult
Y
-
Youth
20
*
.
20
100
Table 4
9
T i t e r s on Serum T e s t e d For
Variola-Vacciniai Group and Monkeypox A n t i b o d i e s
..
Number
Zone
Colobus b a d i u s
492
89
Cercopithecus p e t a u r i s t a
576
C e r c o p i t h e c u s pe t a u r i st a
577
*
**
HI*
Neut*
I F Titer**
After absorption
After absorption
w i t h monkeypox a g a i n s t
with vaccinia against
Vac cinia
Monkeypox
Vaccinia
Monkeypox
5
2500
< 8
8
< 8
117
5
450
< 8
64
c 8
117
40
450
c 8
64
c 8
c
< 8
.
( 8
c 8
C e n t e r f o r Disease C o n t r o l
R i j k s I n s t i t u u t v o o r d e Volksgezondheid
I
t
U
Figure 1
cf
Geographic Distribution of Orthopoxvirus Antibodies
in Non-Human Primates
N 16"15"14"-
13"12"-
11"10"9"-
8"
7"6O-
ATLP
Neut
25 -49 "/o
Neut
1-24%
Neut
0%
+-Human
Monkeypox
.
Neut
>5O%
O-Monkeypox
HI
(after KI041
Antibody
I'
Figure 2
.
I
'
Neutralizing Anti body,Titers in Nonhuman Primates
>2049
2500
1025-2048
513-1024
.
257-512
e.
129-256
cn
[r
w
65-128
!
I
I-
33-64
e
o
.
0 .
.
.
.
e
17-32
.
9-16
5-8
4
I
I
Cercopithecus C.mona
aet hiops
1
I
1
I
I
I
C. petaurista
G.nictitans
I
a
Colobus
badius
c
Colobus
polykomos