W O R L D H E A L T H ORGANIZATION ORGANISATION M O N D I A L E D E L A SANTÉ EXPERT COMMITTEE ON YELLOW FEVER
VIR/YF/71.3 ORIGINAL: FRENCH
INDEXED
E n t e b b e , 9 - 1 5 March 1 9 7 1
NATURAL HISTORY OF YELLOW FEVER IN AFRICA by
J . Hamon and M. C o r n e t M e d i c a l e n t o m o l o g i s t s , O.R.S.T.O.M,
1.
Introduction
In urban e p i d e m i c s , t r a n s m i s s i o n i s s o l e l y i n t e r - h u m a n and f o r m e r l y t h e v e c t o r was c o n s i d e r e d t o be always Aedes (Stegomyia) a e g y p t i . T h i s i s p r o b a b l y t r u e i n towns, b u t i s n o t a l w a y s t h e case i n r u r a l a r e a s . For t h e l a s t 3 0 y e a r s i t has a l s o been known t h a t t h e r e a r e f o r e s t c y c l e s o f t r a n s m i s s i o n i n t r o p i c a l A f r i c a i n v o l v i n g v e r t e b r a t e s and w i l d v e c t o r s and l e a d i n g t o t h e f o r t u i t o u s i n f e c t i o n o f man. T h i s type o f c y c l e i s o f very g r e a t p r a c t i c a l i m p o r t a n c e s i n c e i n t h i s way t h e v i r u s can remain i n c i r c u l a t i o n i n t h e absence o f e p i d e m i c s , which i t may i n i t i a t e . 2, Cycles
The most thorough s t u d i e s o f y e l l o w f e v e r f o r e s t t r a n s m i s s i o n c y c l e s i n A f r i c a a r e those w h i c h have been made i n Bwamba c o u n t y , Uganda. They have r e v e a l e d t h e v i t a l p a r t p l a y e d by two v e c t o r s , Aedes (Stegomyia) a f r i c a n u s and Aedes ( S t e g o m y i a ) s i m p s o n i ( S m i t h b u r n & Haddow 1946- Haddow e t a l . , 1 9 4 8 k 1 9 5 1 ; M a h a f f y , 1 9 4 9 ; Smithburn e t a l . , 1 9 4 9 ; Ross k G i l l e t t , 1 9 5 0 > Haddow, 1 9 6 5 ) . Ae. a f r i c a n u s , which shows c r e p u s c u l a r a c t i v i t y i n t r e e t o p s and whose l a r v a e l i v e i n t r e e - h o l e s , t r a n s m i t s y e l l o w f e v e r from monkey t o monkey when these take t o t h e f o r e s t canopy t o s l e e p . D u r i n g t h e day t h e monkeys sometimes wander i n t o p l a n t a t i o n s o u t s i d e v i l l a g e s i n s e a r c h o f f o o d , and h e r e they come i n t o c o n t a c t w i t h Ae. s i m p s o n i , whose l a r v a e l i v e i n t h e a x i l s o f p l a n t s w i t h s h e a t h - l i k e l e a v e s (banana, t a r o s , p i n e a p p l e , S a n s e v e r i a , e t c The a d u l t s o f t h i s s p e c i e s show d i u r n a l a c t i v i t y . Ae. s i m p s o n i b i t e s both monkeys and man, thus c a u s i n g s p o r a d i c c a s e s o f y e l l o w f e v e r i n man. Ae. s i m p s o n i may a l s o a t times p e n e t r a t e i n t o t h e f o r e s t and become i n f e c t e d a f t e r b i t i n g monkeys i n t h e t r e e canopy (Haddow, 1 9 5 0 ) . These t r a n s m i s s i o n c y c l e s , o b s e r v e d i n a g r e a t r a i n - f o r e s t and i n the v i l l a g e s n e a r b y , c a l l f o r a permanent p o p u l a t i o n o f non-immune monkeys and o f Ae. a f r i c a n u s , and t h e p r e s e n c e at l e a s t from time t o time o f a n t h r o p o p h i l i c Ae. s i m p s o n i . These c o n d i t i o n s a r e o n l y s a t i s f i e d i n l i m i t e d areas of t r o p i c a l A f r i c a . Monkeys a r e f r e q u e n t l y r a r e o r l i t t l e a f f e c t e d (Haddow, 1 9 5 2 ; Lumsden e t a l . , 1 9 5 5 k 1 9 5 6 ; T a y l o r , 1 9 5 5 ) . Ae. s i m p s o n i i s n o t always a n t h r o p o p h i l i c ( G i l l e t t , 1 9 5 1 k 1 9 5 5 ; M a t t i n g l y , 1 9 5 2 ) . L a s t l y , Ae. a f r i c a n u s i s g e n e r a l l y absent o r r a r e o u t s i d e d e n s e l y wooded and humid a r e a s . I n a d d i t i o n , v e c t o r s seem to be absent f o r a l a r g e p a r t o f t h e y e a r i n a l l a r e a s w i t h a l o n g d r y s e a s o n , w h i c h w o u l d a p p a r e n t l y p r e c l u d e maintenance o f j u n g l e y e l l o w f e v e r f o c i ( M a t t i n g l y , i n M a h a f f y , 1 9 4 9 ; Ross k G i l l e t t , 1 9 5 0 ) , a l t h o u g h t h e e x i s t e n c e o f s u c h f o c i seems t o have been p r o v e d s e r o l o g i c a l l y ( S m i t h b u r n e t a l . , 1 9 4 9 ; Lumsden k Buxton, 1 9 5 1 ; Haddow, 1 9 5 2 ; D i c k , 1 9 5 3 ; Taylor, 1955).
The issue of this document does not constitute formal publication. It should not be reviewed, Authors alone abstracted or quoted without the agreement of the World Health Organization. articles. are responsible for views expressed in signed
Ce
document ne constitue pas une publication.
Il ne doit faire l'objet d'aucun compte rendu ou résumé ni d'aucune citation sans l'autorisation de l'Organisation Mondiale de la Santé. Les opinions exprimées dans les articles signés n'engagent que leurs auteurs.
\IR/YK/71.3
page 2 3. 3.1 A n a l y s i s o f some r e c e n t e p i d e m i c s and c a s e s of human i n f e c t i o n In t r o p i c a l Sudan Africa
In 1940 a major urban y e l l o w f e v e r e p i d e m i c o c c u r r e d i n the Nuba mountains a r e a . Aedes ( S t e g o m y i a ) v i t t a t u s and Aedes ( D i c e r o m y i a ) of the t a y l o r i - f u r c i f e r group were c o n s i d e r e d m a i n l y r e s p o n s i b l e f o x t r a n s m i s s i o n w i t h Ae. a e g y p t i and Aedes (Stegomyia) m e t a l l i c u s ( K i r k , 1941; Lewis, 1943; Lewis e t a l . , 1 9 4 2 ) a l s o perhaps i n v o l v e d , t o a minor e x t e n t . In the 1959 e p i d e m i c i n the Upper N i l e and South Fung a r e a s , the i n i t i a l c a s e s o f human i n f e c t i o n were put down to Aedes v i t t a t u s , w i t h subsequent t r a n s m i s s i o n from man t o man Liirough x h i s mosquito o r Ae. a e g y p t i ( S a t t i & Ilaseeb, 1 9 6 6 ) . 3.2 Ethiopia
In 1960-62 a major y e l l o w f e v e r e p i d e m i c was o b s e r v e d i n E t h i o p i a . In f o r e s t g a l l e r i e s the e p i d e m i c was s p r e a d from monkey t o monkey by Ae. a f r i c a n u s . In the Omo v a l l e y , monkeys from f o r e s t g a l l e r i e s i n f e c t e d Ae. s i m p s o n i near v i l l a g e s and t h i s mosquito was t h e s o l e v e c t o r r e s p o n s i b l e f o r an i n t e n s i v e inter-human t r a n s m i s s i o n . In t h e D i d e s s a v a l l e y , w h e r e Ae. s i m p s o n i i s r a r e or a b s e n t , the m a j o r i t y of human c a s e s were s p o r a d i c and t r a n s m i t t e d d i r e c t l y from monkey t o man through Ae. a f r i c a n u s i n the f o r e s t or a t t h e f o r e s t edge (Série e t a l . , 1968 ( a ) and ( b ) ) . I t i s i n t e r e s t i n g t o note t h a t d u r i n g t h i s e p i d e m i c a y e l l o w f e v e r v i r u s s t r a i n was i s o l a t e d from a f r u i t b a t of the genus Epomophorus (Série e t a l , , 1968 ( b ) ) . 3.3 Kenya - Uganda
S u r v e y s made i n the F o r t p o r t a l area i n Kenya i n 1953 and i n C e n t r a l Uganda i n 1964, when s c a t t e r e d human c a s e s o c c u r r e d , showed t h a t i n t h i s area Ae. a f r i c a n u s a l o n e i s r e s p o n s i b l e f o r t r a n s m i s s i o n from monkey to monkey and from monkey t o man (Haddow, 1 9 5 3 ; Simpson e t a l . , 1965).
3.4
Congo -
Kinshasa
A p a r t from a few s p o r a d i c c a s e s of j u n g l e y e l l o w f e v e r , two minor e p i d e m i c s were o b s e r v e d i n 1958 i n E a s t e r n P r o v i n c e and i n E q u a t e u r P r o v i n c e . In E a s t e r n P r o v i n c e t h e t r a n s m i s s i o n c y c l e was c o n s i d e r e d t o be the same as t h a t d e s c r i b e d f o r Bwamba c o u n t y (Courtois et a l . , 1960). In the E q u a t e u r P r o v i n c e Ae. s i m p s o n i and Ae. a e g y p t i were r e g a r d e d as r e s p o n s i b l e f o r i n t e r - h u m a n t r a n s m i s s i o n ( P a n t h i e r e t a l . , 1962; Lebrun, 1 9 6 3 ) . 3.5 Nigeria
A p a r t from s p o r a d i c c a s e s , f a i r l y l a r g e e p i d e m i c s were r e c o r d e d between 1946 and 1953 i n the s o u t h - w e s t and t h e e a s t of the c o u n t r y but no d e t a i l e d e p i d e m i o l o g i c a l s t u d y a p p e a r s to have been p u b l i s h e d (MacNamara, 1 9 5 4 ) . In 1969 an e p i d e m i c o u t b r e a k was r e p o r t e d i n the Jos d i s t r i c t . A d u l t males were i n f e c t e d t o a much g r e a t e r degree than women o r c h i l d r e n , seeming t o i n d i c a t e t h a t t r a n s m i s s i o n took p l a c e away from v i l l a g e s ( B r e s , 1970; Quenum, 1 9 7 0 ) , The e p i d e m i o l o g i c a l s t u d y , made somewhat b e l a t e d l y , showed t h a t Ae. a f r i c a n u s and Ae. l u t e o c e p h a l u s were a b u n d a n t and a g g r e s s i v e ; Ae. s i m p s o n i abundant and n o n - a g g r e s s i v e , w h i l e Ae. a e g y p t i was r a r e . An e a r l i e r s t u d y i n the same a r e a had s t r e s s e d the p r o b a b l e i m p o r t a n c e o f Ae. v i t t a t u s and Ae. l u t e o c e p h a l u s (Boorman, 1 9 6 1 ) . T r a n s m i s s i o n was thus a p p a r e n t l y due m a i n l y t o f o r e s t vectors.
VIR/YF/71.3
page 3 3.6 Upper V o l t a
A f a i r l y l a r g e o u t b r e a k of y e l l o w f e v e r o c c u r r e d i n 1 9 5 9 i n the s o u t h - c e n t r a l p a r t of t h e c o u n t r y i n an a r e a where Ae. a e g y p t i was o n l y m o d e r a t e l y a b u n d a n t i n v i l l a g e s w h i l e A e . l u t e o c e p h a l u s , A e ^ _ ^ f r i c a n u s and Aedes o f the t a y l o r i - f u r c j f g r o u p were v e r y abundant and aggressive i n forest g a l l e r i e s . Human c a s e s were s c a t t e r e d o v e r an e x t e n s i v e a r e a , w h x l e t h e r e appeared t o be massive i n f e c t i o n i n monkeys. T r a n s m i s s i o n was p r o b a b l y ensured b o t h by w i l d v e c t o r s and by Ae. a e g y p t i ( P i c h o n e t a l . , 1 9 6 9 ; B a l a y & Hamon, 1 9 6 8 ; G a y r a l & Kambou, 1 9 6 9 ; Compaore U S e n t i l h e s , 1 9 7 0 ; Cornet & Robin, 1 9 7 0 ) . 3.7 Ghana
S p o r a d i c c a s e s and minor e p i d e m i c s were r e c o r d e d a t i n t e r v a l s i n the s o u t h o f the country. In the case of a s m a l l outbreak i n the A s h a n t i r e g i o n i n 1 9 5 7 , t r a n s m i s s i o n , which was o f the f o r e s t type, was a t t r i b u t e d to Ae. a f r i c a n u s . but Ae, l u t e o c e p h a l u s was a l s o p r e s e n t (Boorman k P o r t e r f i e l d , 1 9 5 7 ) . ' A r e l a t i v e l y l a r g e y e l l o w f e v e r e p i d e m i c o c c u r r e d i n t h e n o r t h of the c o u n t r y i n 1 9 6 9 and e a r l y 1970, Cases were s c a t t e r e d o v e r an e x t e n s i v e a r e a ( B r e s , 1 9 7 0 ; Quenum, 1 9 7 0 ) . I n t h e r e g i o n a f f e c t e d Ae. a e g y p t i was f r e q u e n t l y very abundant i n v i l l a g e s and c o u l d have b e e n r e s p o n s i b l e f o r inter-human t r a n s m i s s i o n (Mouchet, 1 9 7 0 ) . 3.8 Senegal
A s e r i o u s y e l l o w f e v e r epidemic was o b s e r v e d i n the west o f the c o u n t r y i n 1 9 6 5 . It was o f the c o n v e n t i o n a l type w i t h t r a n s m i s s i o n by Ae. a e g y p t i and was l i m i t e d t o a r e a s w i t h a h i g h d e n s i t y of t h i s v e c t o r . T h i s e p i d e m i c was h a l t e d b o t h by i n s e c t i c i d e t r e a t m e n t and by t h e f a l l i n temperature i n the w i n t e r (Wone e t a l . , 1 9 6 6 ; B r e s e t a l . , 1 9 6 6 & 1 9 6 7 ; Cornet et a l . , 1 9 6 8 ) . There was no l o c a l f o r e s t f o c u s and the o r i g i n of the y e l l o w f e v e r v i r u s c o u l d not be d e t e r m i n e d w i t h any c e r t a i n t y s i n c e permanent f o c i seem to e x i s t both i n e a s t e r n Senegal and i n Guinea - B i s s a o . 3.9 Other States
One c a s e of human y e l l o w f e v e r was c o n f i r m e d i n 1 9 7 0 i n t h e Ayos d i s t r i c t o f Cameroon w h i l e p o s i t i v e s e r o l o g i c a l t e s t s were r e c o r d e d i n young n o n - v a c c i n a t e d c h i l d r e n i n the s o u t h of the Central A f r i c a n Republic. In both these a r e a s Ae. a f r i c a n u s and Ae. s i m p s o n i a r e abundant and a n t h r o p o p h i l i c and monkeys are a l s o p r e s e n t . The t r a n s m i s s i o n c y c l e was p e r h a p s the same as t h a t d e s c r i b e d f o r Bwamba county (A. R i c k e n b a c h , F . X. P a j o t k R. C o r d e l l i e r 1970). I s o l a t e d c a s e s and some grouped c a s e s of y e l l o w f e v e r were c o n f i r m e d i n 1 9 6 7 i n L i b e r i a , i n 1969 i n M a l i and i n 1 9 6 9 and 1 9 7 0 i n Togo. They seem p r o b a b l y t o have been o f j u n g l e o r i g i n ( R o b i n k P i c h o n , 1 9 6 8 ; Agbodjan, 1 9 7 0 ; Sow, 1 9 7 0 ; P. P a n g a l e t , 1 9 7 0 , p e r s . comm.). 4. Discussion
A l a r g e p r o p o r t i o n of y e l l o w f e v e r c a s e s o c c u r r i n g i n A f r i c a a r e p r o b a b l y n e v e r d i a g n o s e d (Hamon & B r e s , 1966), w h i l e most o f the c a s e s o b s e r v e d a r e not o f f i c i a l l y n o t i f i e d t o WHO (Quenum, 1970). Under these c o n d i t i o n s i t i s d i f f i c u l t t o g i v e an o v e r a l l p i c t u r e o f the situation in tropical Africa. Ae. a e g y p t i i s u n d e n i a b l y one of the major v e c t o r s i n t r o p i c a l A f r i c a but i t s h o u l d be n o t e d t h a t i t has p l a y e d o n l y a minor p a r t , i f any, i n two of the major y e l l o w f e v e r e p i d e m i c s of the l a s t 30 y e a r s and t h a t i t has not always been the dominant component i n l e s s e r o u t b r e a k s , w h i l e a l l i s o l a t e d c a s e s appear t o be j u n g l e y e l l o w f e v e r .
VIR/YF/71.3
page 4 Other p o t e n t i a l v e c t o r s i m p l i c a t e d i n r e c e n t human cases a l l belong t o t h e s u b - g e n e r a Stegomyia and Diceromya of t h e genus Aedes but i t s h o u l d n o t be f o r g o t t e n t h a t y e l l o w f e v e r v i r u s has a l s o been i s o l a t e d from Aedes (Aedimorphus) d e n t a t u s (Série e t a l . , 1968 ( a ) ) a n d from Phlebotomus (Smithburn eL a l . , 1949) w h i l e i t has been t r a n s m i t t e d under l a b o r a t o r y c o n d i t i o n s by E r e t m a p o d i t e s group c h r y s o g a s t e r (Bauer, 1928), by Mansonia a f r i c a n a ( P h i l i p , 1930) by C u l e x t h a l a s s i u s ( K e r r , 1932), and even by Culex p i p i e n s f a t i g a n s ( D a v i s , 1 9 3 3 ) , I t s h o u l d a l s o be n o t e d t h a t t h e v e c t o r p o t e n t i a l i t i e s o f many groups of A f r i c a n haematophageous a r t h r o p o d s have been s t u d i e d o n l y very s u p e r f i c i a l l y . W i t h a s i n g l e e x c e p t i o n , a l l A f r i c a n p r i m a t e s appear r e c e p t i v e t o t h e y e l l o w f e v e r v i r u s ( S m i t h b u r n , 1949; Smithburn & Haddow, 1949). Only a few of t h e o t h e r A f r i c a n v e r t e b r a t e s s t u d i e d c i r c u l a t e t h e v i r u s , i n p a r t i c u l a r one s p e c i e s o f hedgehog, a genet ( D i c k , 1 9 5 2 ) , and b a t s b e l o n g i n g t o the genera E i d o l o n , Epomophorus, R o u s e t t u s and T a d a r i d a (Série e t a l . 1968 ( b ) ; Simpson & O ' S u l l i v a n , 1968). Our knowledge of t h e r e a l s i g n i f i c a n c e o f t h e v a r i o u s s p e c i e s i n t h e f o r e s t t r a n s m i s s i o n c y c l e i s f a r from s a t i s f a c t o r y . No s t u d y has y e t been made t o d e t e r m i n e whether permanent n a t u r a l y e l l o w f e v e r f o c i e x i s t i n A f r i c a o r whether t h e v i r u s c i r c u l a t e s i n e p i z o o t i c waves, as appears t o be t h e c a s e i ri C e n t r a l A m e r i c a , o r whether t h e two systems o f m a i n t a i n i n g and s p r e a d i n g t h e v i r u s e x i s t s i d e by s i d e . The two known t r a n s m i s s i o n c y c l e s may be no more than s e c o n d a r y c y c l e s s p r e a d i n g from an unknown p r i m a r y c y c l e i n v o l v i n g none o f t h e c o n v e n t i o n a l v e r t e b r a t e s and vectors. 5. Conclusions
Y e l l o w f e v e r remains one o f t h e major endemic d i s e a s e s o f t r o p i c a l A f r i c a , i n b o t h i t s e p i d e m i c and i t s j u n g l e forms. A l t h o u g h Ae. A e g y p t i may be r e s p o n s i b l e f o r t r a n s m i s s i o n t o man, t h e p r i n c i p a l v e c t o r s i n many a r e a s a r e f o r e s t s p e c i e s o f Aedes. Wild primates a r e f r e q u e n t l y i n f e c t e d i n endemic a r e a s . The t r a n s m i s s i o n c y c l e s d e s c r i b e d f o r E a s t A f r i c a are p r o b a b l y v a l i d f o r most f o r e s t a r e a s i n C e n t r a l A f r i c a , as f a r as Cameroon and t h e Central A f r i c a n Republic. T r a n s m i s s i o n c y c l e s i n f o r e s t a r e a s i n West A f r i c a and i n wooded a r e a s and savannah w i t h a l o n g d r y season have s t i l l t o be d e t e r m i n e d . The mechanism whereby the v i r u s p e r s i s t s d u r i n g i n t e r - e p i d e m i c p e r i o d s i s n o t known w i t h any c e r t a i n t y . 7. References
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