Preventive Veterinary Medicine, 2 {1984) 541--551 541 Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands

GENETIC RESISTANCE TO ANIMAL TRYPANOSOMIASIS IN AFRICA

Max Murray* and J . C . M . Trai l**

*International Labora tory for R e s e a r c h on Animal Diseases (ILRAD),

P . O . Box 30709, Nairobi, Kenya

**Internat ional L ives tock Centre for Afr ica (ILCA), P . O . Box 46847, Nairobi, Kenya

ABSTRACT

Murray, Max and Trai l , J C M. 1984. Genetic Res i s t ance to Animal Trypanosomlas i s

i n A f r i c a . Prevent ive Veter inary Medicine , 2: 541-551.

Cer ta in indigenous taur ine b r eeds of cat t le , namely N'Dama and West Afr ican Shorthorn, in West and Centra l Afr ica a re significantly more r e s i s t a n t to t rypano- s o m i a s i s than Bos i n d i c ~ s b r e e d s . This t ra i t , t e r m e d t rypano to le rance , is an innate c h a r a c t e r i s t i c . Despite the i r smal l s ize , t rypanoto le ran t b reeds a r e at l eas t as p ro- ductive as o ther indigenous b r e e d s . Genetic d i f fe rences in r e s i s t a n c e to t rypano- somLasis have a lso been found in some B. i ~ i c u ~ types of cat t le , although to date the level demons t r a t ed is much l e s s than that of the t rypanoto le ran t b r e e d s . Trypano- to le rance can be reduced by a var ie ty of s t r e s s f ac to r s including high leve l s of t s e t s e chal lenge or it can be supplemented by previous exposure . Trypanoto le rance would appear to be re la ted to the ability to cont ro l pa ras i t aemia , a capaci ty which, at l eas t in mice infected with T~y~)ano~oma b ~ e e i , is a s soc ia ted with the ra te of pa ra s i t e d i f ferent ia t ion f r o m the rapidly dividing s l ender fo rm to the non-dividing stumpy (the f o r m which is r e spons ib l e for the induction of the immune r e sponse ) . P a r a s i t e d i f ferent ia t ion in the mouse can a lso be regula ted by immunos t imulan ts such as C o ~ e b a e t ~ i ~ ~ a ~ , c r ea t ing the poss ibi l i ty of a l t e r ing host r e s i s t a n c e by non- speci f ic means . Low maintenance r e q u i r e m e n t s , the abili ty to co n s e rv e wate r , the capaci ty to to le ra te heat and inc reased r e s i s t a n c e to o ther impor tan t infect ious d i s e a s e s a r e a lso c h a r a c t e r i s t i c s a t t r ibuted to t rypanoto le ran t b r e e d s . When all these f ac to r s a r e cons ide red , it would appear that the N'Dama and the West Afr ican Shorthorn, through a r igorous p r o c e s s of se lec t ion over s eve ra l thousand y e a r s , now provide a 'package ' for survival and product ion in the t s e t s e - i n f e s t e d savanna a r e a s of West and Centra l Afr ica .

INTR ODUC TION

The exploi tat ion of l ives tock p o s s e s s i n g genetic r e s i s t a n c e to d i sease is being

given inc reas ing cons idera t ion in l ives tock development p r o g r a m m e s , par t icu lar ly

where conventional d i s ea se con t ro l m e a s u r e s a r e not effect ive or a r e too cost ly to

0167-5877/84/$03.00 © 1984 Elsevier Science Publishers B.V.

542

implemen t or, as is a l so common, vaccines a re not avai lable . This is par t icu lar ly the

case in developing coun t r i e s . Such an approach is applicable to Afr ican animal t rypano-

somias i s , a d i s ea se that ce r t a in b r eeds of ca t t le a r e able to survive in t s e t s e fly

infested a r e a s without the aid of t r e a t m e n t but to which o ther b reeds rapidly succumb.

This t r a i t has been t e r m e d t rypanoto le ranee and is general ly a t t r ibuted to the taur ine

b r eeds of cat t le in West and Central Afr ica , namely the N'Dama and the West Afr ican

Shorthorn.

While t rypanoto le ran t b reeds a r e a well r eeogn i sed component of l ives tock produc-

t ion in c e r t a i n a r e a s of Afr ica , they r e p r e s e n t only about 5% (8 of 147 million) of the

total ca t t le population in the 38 count r ies where t s e t s e occur (ILCA, 1979; FAO, 1982).

Fa i lu re to exploit these b reeds can possibly be at t r ibuted to the bel ief that because of

the i r sma l l s ize they were not productive and that t he i r t rypanoto le rance was a r e su l t of

acqui red r e s i s t a n c e to local t rypanosome populations. However, it has now been con-

f i rmed that t rypanoto le rance is an innate c h a r a c t e r i s t i c and may, t he r e fo re , be genet-

ically exploited (reviewed by Murray , ¢ ~ ; . , 1982). F u r t h e r m o r e , in a r ecen t survey

of the s ta tus of t rypanoto le ran t l ives tock in 18 coun t r i es in West and Centra l Afr ica

(ILCA, 1979), indices of productivi ty were examined using all the basic production data

that could be found for each region, each management s y s t em and for d i f fe rent levels of

t s e t s e chal lenge . The r e su l t s indicated that in a r e a s of no or low t s e t s e chal lenge the

product ivi ty of t rypanoto le ran t ca t t le re la t ive to other indigenous b reeds was much

higher than previously a s sumed . Comparat ive data between b reeds were not

avai lable in many a r e a s because the level of t r ypano s o mi as i s r i sk was such that b reeds

o ther than t rypanoto le ran t ones could not su rv ive . As a r e su l t of these f indings, there

is cu r ren t ly cons ide rab le i n t e r e s t in the use of t rypanoto le ran t b reeds in t s e t s e - i n f e s t e d

a r e a s of Af r i ca .

In this paper the c u r r e n t informat ion on the genetic bas is of t rypano to le rance ,

env i ronmenta l f ac to r s which can influence i ts s tabil i ty and, the poss ib le mechan i sms

re spons ib le a r e examined.

EVIDENCE IN CATTLE OF GENETIC RESISTANCE TO TRYPANOSOMIASIS

In one of the f i r s t accounts of West Afr ican l ivestock, P i e r r e (1906) r eco rded the

abili ty of c e r t a i n cat t le to survive in t s e t s e - i n f e s t e d a r e a s . Subsequently, in both field

inves t igat ions and in expe r imen ta l s tud ies the r e s i s t a n c e of the taur ine an imals was

increas ing ly recogn i sed (Stewart, 1951; Chandler, 1952, 1958; Desowitz , 1959). The

validity of these observa t ions carmot be quest ioned, but it was not poss ib le to evaluate

the re la t ive contr ibut ion of innate and acqui red r e s i s t a n c e because the h is tory of the

543

a n i m a l s under study was not known.

More r ecen t ly , however , t h e r e have been a s e r i e s of r e p o r t s which have con f i rmed

tha t the d i f f e rences in r e s i s t a n c e to t r y p a n o s o m i a s i s found between b r e e d s ex i s t a s an

innate c h a r a c t e r i s t i c . Us ing a n i m a l s which had never been previous ly exposed to

t r y p a n o s o m i a s i s and, in some c a s e s , us ing a n i m a l s bo rn of dams neve r p rev ious ly

exposed, i t was found that N~Dama were s igni f icant ly more r e s i s t a n t than Zebu to

e x p e r i m e n t a l cha l lenge with wild caught t s e t s e (Stephen, 1966; Robe r t s and Gray, 1973),

natura~ field exposure (Toure e t a l . , 1978; Murray e t a l . , 1981) and to t rypano-

s o m e s inoculated by sy r inge {Murray e t a l . , 1979; Sa ro r e t a l . , 1981).

A d r a m a t i c example of the d i f f e r ences in suscep t ib i l i ty and product iv i ty was

r epo r t ed by Mur ray e t a l . , {1981) who exposed 10 Zebu cows and 10 N 'Dama cows to

a na tu r a l field cha l lenge f r o m Glossina morsitans submorsitans. The a n i m a l s were

2½ to 3 y e a r s old and had not been previous ly exposed to t r y p a n o s o m i a s i s . All Zebu

died of t r y p a n o s o m i a s i s within 8 months of f i r s t exposu re . In con t r a s t , while a l l

N~Dama b e c a m e infected, only 3 NVDama died of t r y p a n o s o m i a s i s ; t he se a n i m a l s had

a l l been suckt ing ca lves before they succumbed 11 to 14 months a f t e r in i t ia l exposu re .

These d i f f e r ences in suscep t ib i l i ty w e r e a s soc ia t ed with the fact tha t the p reva lence ,

leve l and dura t ion of p a r a s i t a e m i a were s ignif icant ly l e s s in the NVDama. C o r r e s -

pondingly, the N~Dama developed l e s s s e v e r e anaemia than the Zebu. The packed r ed

ce i l volume (PCV) of the N~Dama was not s igni f icant ly d i f fe rent be tween 8 months a f t e r

exposure , when a l l Zebu were dead, and 21 months , when the e x p e r i m e n t was t e r m i -

nated, and was within n o r m a l r ange . In addi t ion to reduced mor ta l i ty , the I~Dama

expe r i enced no abor t ions and produced 5 ca l ve s . In the Zebu, in m a r k e d con t r a s t ,

abo r t ions o c c u r r e d both in ea r ly and ~ t e p regnancy and no l ive ca lves were produced .

Although v a r i a t i o n in suscep t ib i l i ty o c c u r r e d within each breed, the v a r i a n c e found

between b r e e d s showed tha t they ex i s ted as two s igni f icant ly d i f fe ren t popula t ions .

While c r i t i c a l e x p e r i m e n t a l in fo rmat ion is lacking, t h e r e is ev idence to sugges t

tha t t r ypano to l e r an t b r e e d s may a l so be r e s i s t a n t to s e v e r a l o ther impor t an t infec t ious

d i s e a s e s . Thus, 17Damn have been r e p o r t e d to be more r e s i s t a n t to t i c k - b o r n e

d i s e a s e s , inc luding b e a r t w a t e r (Cvwdria r ~ a ~ i r ~ n t i ~ ) , a n a p l a s m o s i s and b a b e s i o s i s

(Epstein , 1971). These o b s e r v a t i o n s might r e f l ec t a g r e a t e r r e s i s t a n c e to the t i ck p e r

se . In addi t ion, N ~Dama and West Af r i can Shor thorn have been shown to be r e s i s t a n t

to s t r e p t o t h r i c o s i s (Stewart , 1937; Coleman, 1967) and a r e a l so said to be more r e s i -

s tan t to h e l m i n t h i a s i s {A.A. I lemobade, pe r sona l communica t ion , 1982).

The poss ib i l i ty tha t genetic d i f f e r ences to t r y p a n o s o m i a s i s might have developed

in o the r b r e e d s of ca t t l e and in o the r reg ions of Af r i ca has genera l ly not been given

544

se r ious cons ide ra t i on because most o b s e r v e r s bel ieve that if it did exis t to any s ignif i -

cant extent it would have been we l l -documented by this t ime . t towever, the re is ev i -

dence that d i f f e r ences in r e s i s t a n c e do occur in c e r t a i n -~oz; ~]-[cu~; types in some

a r e a s . Cunningham (1966) pointed out that many thousands of Zebu surv ive around the

s h o r e s of Lake Vic tor ia without the aid of t rypanocidaI drugs despi te continuous t s e t s e

fly chal lenge . Di f fe rences in r e s i s t a n c e have a lso been demons t r a t ed in Zebu cat t le

f r o m endemic t s e t s e fly a r e a s in Kenya (J. M. Monirei , pe r sona l communica t ion , 1982)

and Upper Volta (CRTA Annual Repor t , 1981), following needle inoculat ion with blood-

s t r e a m f o r m s of t r y p a n o s o m e s . Similar ly , Zebu belonging to the Orma people in South

E a s t e r n Kenya show g r e a t e r r e s i s t a n c e than o ther B. i ~ c ~ types to natural t s e t s e

fly chal lenge (A.R. Njogn, pe rsona l communica t ion , 1982). However, as an imals in

t hese s tudies had all been previous ly exposed to chal lenge with t r y p a n o s o m e s of unde-

fined ant igenic c h a r a c t e r i s t i c s , it was not poss ib le to a s s e s s the re la t ive contr ibut ion

of innate and acqui red r e s i s t a n c e .

Some p re l im ina ry evidence for genetic d i f f e r ences in r e s i s t a n c e in B. i ~ g i v ~

does ex is t . Boran ca t t le which w e r e r e a r e d in a t s e t s e f r ee a r ea were found to be less

suscep t ib le to t r ypanoso rn i a s i s than A y r s h i r e s following syr inge chal lenge with blood-

s t r e a m f o r m s of 2. eon~:jo~enze ( J .M. Monirei , pe r sona l communica t ion , 1982).

Susceptibi l i ty was a s s e s s e d by the seve r i ty of anaemia , the level of pa r a s i t a emia and

surv iva l r a t e s . F u r t h e r indicat ions of a more c i r cums tan t i a l nature were obtained

f rom a da i ry r anch in Kenya where approximate ly 800 breeding females exposed to what

was cons ide red a very low t s e t s e chal lenge were followed over a period of 6 y e a r s .

Using t rypanocida l drug t r e a t m e n t as an indicat ion of infection, it was concluded that

§ Sahiwal - ½ A y r s h i r e cat t le were s ignif icant ly l e s s suscept ib le than ½ Sahiwal - §

A y r s h i r e s because they requ i red l e s s than half the number of t r e a t m e n t s in the 13

months following pa r tu r i t ion (Trai l eV ~ . , in p r e s s ) . While c r i t i ca l compara t ive

s tudies on t rypano to l e r ance and productivi ty a r e requi red , it was c l e a r that the deg ree

of r e s i s t a n c e exhibi ted by the Boran and the ~ Sahiwal was much l e s s than that of the

r ecogn i sed t rypano to l e ran t b r e e d s . Never the less , the genetic d i f fe rence in r e s i s t a n c e

found be tween the two types of ca t t le on the dairy ranch was an economic a s s e t to the

r a n c h e r 0hrissocq e~ ~ . , in p r e s s ) and it would appear that the development of B.

indivn~ b r e e d s with a s ignif icant deg ree of r e s i s t a n c e is a long t e r m poss ib i l i ty .

Cur ren t in format ion indica tes that a s p e c t r u m of r e s i s t a n c e to t r y p an o s o mi as i s

ex i s t s be tween d i f fe ren t b r e e d s of cat t le , with N'Dama and West Afr ican Shorthorn at

one e x t r e m e , impor ted exotic ca t t le at the o ther ex t r eme and ~. i ~ i ~ u ~ types being

s o m e w h e r e in between.

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ENVIRONMENTAL INFLUENCES ON TRYPANOTOLERANCE

Trypano to l e r ance can be reduced o r supp lemented by a n u m b e r of f a c t o r s a f fec t ing

the host and i ts e n v i r o n m e n t . These f ac to r s include s t r e s s (work, pregnancy, pa r tu -

r i t ion , lac ta t ion, suckl ing) , i n t e r c u r r e n t d i sease and poor nu t r i t ion (reviewed by

M u r r a y e~ a ~ . , 1982). One of the most impor t an t f ac to r s which would a p p e a r to a f fec t

the s tab i l i ty of t r ypano t o l e r ance is the s eve r i t y of the t r y p a n o s o m i a s i s r i s k to which

a n i m a l s a r e exposed . While c r i t i c a l data e s t i m a t i n g the level of t r y p a n o s o m i a s i s r i s k

a r e lacking, p r e l i m i n a r y f indings indicate , tha t as the level of r i s k i n c r e a s e s p roduc-

t ivi ty fa l ls and tha t N 'Dama can suf fe r s eve re ly f r o m the d i s ea se a s judged by

s tunt ing, was t ing , abor t ion and even death (ILCA, 1979).

Ano the r s igni f icant fac to r which inf luences suscep t ib i l i ty to t r y p a n o s o m i a s i s i s

age. Severa l groups of w o r k e r s have noted tha t ca lves a r e s igni f icant ly more r e s i s t a n t

to t r y p a n o s o m i a s i s ( reviewed by F iennes , 1970). While th i s might be a t t r ibu ted to

ma te rna l ly de r ived an t ibodies in younger ca lves , i t is r ecogn i sed tha t i n c r e a s e d r e s i s t -

ance can l a s t for as long as 8 months and that i t s loss is a s s o c i a t e d with weaning (W.W.

Lutz, pe r sona l communica t ion , 1982). It has been proposed that the t r a n s f e r of

c o l o s t r u m f r o m an immune dam supp lemented by ea r ly exposure to local s t r a i n s of

t r y p a n o s o m e will c r e a t e a r e s i s t a n t an imal , p rovid ing it is not moved to ano the r

loca t ion (Desowitz, 1970).

In th i s r e s p e c t , t h e r e a r e now s e v e r a l r e p o r t s which indica te tha t ca t t le , both of

t r ypano to [e ran t (Chandler , 1958; Desowitz, 1959; Toure v t a l . , 1978; Sa ro r e~ a l . ,

1981; CRTA, 1981) and t r ypanos us cep t i b l e b r e e d s (Bevan, 1936; Whi tes ide , 1962;

F i ennes , 1970; Wilson e$ ate., 1976; Bourn and Scott, 1978; CRTA, 1981; T r a i l

e~ a l . , in p r e s s ) which su rv ive t r y p a n o s o m i a s i s , with o r without the aid of c h e m o -

the rapy , gradual ly become more r e s i s t a n t to cha l l enge . This s i tua t ion probably c a u s e s

much of the c o n t r o v e r s y over the be l ie f held by many tha t the r e s i s t a n c e of t rypano-

t o l e r a n t b r e e d s is l a rge ly the r e s u l t of acqu i r ed immuni ty to local t r y p a n o s o m e s t r a i n s

and that t o l e r a n c e d i s a p p e a r s if ca t t l e a r e moved to d i s t an t loca t ions . While exposu re

to new t r y p a n o s o m e s t r a i n s will undoubtedly lead to infect ion, the s u p e r i o r genet ic

r e s i s t a n c e of the t r y pano t o l e r an t b r e e d s will mean tha t t h e i r chances of su rv iva l and

a c q u i r i n g r e s i s t a n c e in new loca t ions will be s igni f icant ly g r e a t e r than for trypano--

suscep t ib l e b r e e d s . This has been conf i rmed by the s u c c e s s f u l movemen t f r o m West

Af r ica of Lagune in 1904 and N 'Dama in 1920 to Za i r e and m o r e r ecen t ly the i n t rodnc -

t ion of 1~ Dama into the Cen t ra l A f r i c an Republ ic , Gabon and Congo (ILCA, 1979).

However , i t mus t be r ecogn i sed tha t the movemen t of ca t t l e of any breed , e spec ia l ly

546

heifers, over large distances with resultant exposure to different diseases, different

environments and different management systems will mean that a period of adaptation

will be required.

ME CHA NISMS

Increased resistance to trypanosomiasis would appear to depend upon an inherent

capacity to control parasitaemia. The fact that inoculation of trypanosomes by syringe

leads to no significant differences in infection rates or prepatent periods in breeds of

cattle and strains of mice of different susceptibilities, suggests that the capacity of

resistant animals to control parasitaemia may be related to a superior innate immune

response.

i . Immune response

Differences in immunological responses to trypanosomes have been demonstrated

between trypanotolerant and trypanosusceptible breeds of cattle. Thus, Desowitz (1959)

found that N'Dama with previous experience of trypanosomiasis were able to eliminate

trypanosomes more rapidly than Zebu following renewed challenge. He concluded that

the trypanotolerant nature of the N'Dama lay in their capacity to mount a superior sec-

ondary immune response to trypanosomes. Further evidence that the N~Dama might

possess a better innate immune response was reported by Shapiro and Murray (1982)

who demonstrated an association between the greater capacity of N' Dama (compared to

Zebu) to control 2". ~)~c~{ infections and their ability to recognise at least one of 3

common trypanosome antigens of molecular weight 110, 000, 150, 000 and 300,000 daltons

Similarly, work in mice has shown that resistant strains produce a more consistent

antibody response to 2". congo~n~ than susceptible strains (W.I. Morrison, personal

communication, 1982), while with 2". b~cv{ infections the antibody response reaches

much higher levels in resistant strains (Black e~ ~ . , in press). However, no differ-

ences were found in the immune response between strains of mice of different suscepti-

bility when they were inoculated with non-dividing irradiated T. b~c~ i or 2". con(jo-

~en~e (Black eL ~Z., in press; W.I. Morrison, personal communication, 1982).

These findings suggested that some other factor(s), possibly involved in the induction of

the immune response, was responsible for the differences in the immune response to a

live trypanosome infection observed in both cattle and mice of different susceptibilities.

Studies in mice have shown that the rate of differentiation of 2". ])~ucvi from

rapidly dividing slender forms to non-dividing senescent stumpy forms, together with

the rate of production of protective antibodies, regulates the capacity of the host to

547

con t ro l and reduce p a r a s i t a e m i a s (Sendashonga and Black, 1982). F u r t h e r m o r e , the

r a t e of p a r a s i t e d i f f e ren t i a t ion inf luences the k ine t ics of ant ibody produc t ion because

ant ibody r e s p o n s e a r e s t imu la t ed by stumpy but not by dividing s l e n d e r f o r m s (Black e t

a ~ . , 1982; Sendashonga and Black, 1982). These f indings sugges ted tha t the f a c to r s

which regu la te the r a t e of p a r a s i t e d i f fe ren t i a t ion might play a ro le in the induct ion of

the immune r e s p o n s e and, as a r e su l t , might inf luence the s eve r i t y of infect ion, i . e . ,

the host d e t e r m i n e s the level of suscep t ib i l i ty by con t ro l l i ng the r a t e at which p a r a s i t e s

d i f f e ren t i a t e . This hypothes i s was tes ted in r e s i s t a n t C57B1/6 mice which a r e capab le

of con t ro l l i ng p a r a s i t a e m i a to a s igni f icant ly g r e a t e r ex tent than C3H/He mice which

a r e highly suscep t ib le to infect ion. It was found tha t p a r a s i t e d i f f e ren t i a t ion o c c u r r e d

e a r l i e r and ant ibody leve ls were h igher in the more r e s i s t a n t C57B1/6 mice . While

t h e r e is no morpholog ica l equ iva len t of the s tumpy t r y p a n o s o m e in T. eongo~er~se and

~. vivax, the fact tha t r e s i s t a n c e in mice to T. congo~en~e and T. u i v a x (S. Mahan,

pe r sona l communica t ion , 1983) is a l so a s soc i a t ed with the capaci ty to con t ro l p a r a s i -

t a e m i a as well as with d i f f e r ences in the immune r e s p o n s e sugges t s tha t a s i m i l a r

m e c h a n i s m may be ope ra t ive . Not only a r e the f ac to r s r e s p o n s i b l e for p a r a s i t e growth

under genetic con t ro l but i t is a l so poss ib le to manipula te t hem us ing i m m u n o s t i m u l a n t s

such as Co~yr~e~)aete~iur~ pa~)~. Thus, when mice were t r e a t e d with C. pa~vum,

d i f f e ren t i a t ion of ~. ~ e e i o c c u r r e d e a r l i e r and the subsequen t peaks of p a r a s i t a e m i a

were lower and s h o r t e r dura t ion .

Ano the r poss ib le explanat ion for t r y p a n o t o l e r a n c e is tha t r e s i s t a n t a n i m a l s a r e l e s s

suscep t ib le to i m m u n o d e p r e s s i o n , a c o m m o n fea tu re of t r y p a n o s o m e infec t ions which is

e spec ia l ly s e v e r e in l abo ra to ry a n i m a l s (Goodwin e t a ~ . , 1972). Evidence for a

r e l a t i onsh ip be tween i m m u n o s u p p r e s s i o n and suscep t ib i l i ty of mice to T. ~)r~eei has

been r epo r t ed by Selk i rk and Sacks (1980). It was found tha t s t r a i n s of mice of d i f fe ren t

suscep t ib i l i t i e s showed c o r r e s p o n d i n g d i f f e rences in d e p r e s s i o n to he te ro logous an t igens ,

with IgM r e s p o n s e s becoming rapid ly d e p r e s s e d in the mos t suscep t ib le s t r a i n s . It was

concluded tha t the ex tent and rapid i ty of onse t of s u p p r e s s i o n of IgM r e s p o n s e s d e t e r -

mined the c o u r s e of infect ion.

The ro le of p a r a s i t e d i f f e ren t i a t ion and p a r a s i t e induced i m m u n o d e p r e s s i o n in

inf luencing host suscep t ib i l i ty to A f r i c a n t r y p a n o s o m e s need not be mutual ly exc lus ive .

It may be tha t the f a c t o r s which regu la te p a r a s i t e growth and d i f fe ren t ia t ion , and as a

r e s u l t con t ro l the induct ion of the immune r e sponse , may a l so be i m m u n o s u p p r e s s i v e .

It is known tha t fol lowing infect ion by t s e t s e p a r a s i t e s f i r s t become e s t ab l i shed in

the skin w h e r e they mult iply for s e v e r a l days p r i o r to d i s s e m i n a t i o n to the b l o o d s t r e a m .

Thus, i t is poss ib le tha t the f a c t o r s which regu la te p a r a s i t e growth and d i f fe ren t i a t ion

548

could be operat ive in the skin and might be impor tant in de te rmin ing suscept ibi l i ty of the

host . The possibi l i ty that this might be the ea se was suggested f rom work on t rypano-

to le ran t wild an imals , including buffalo, oryx, eland and waterbuck, in which pa ra s i -

t aemias following infect ion a re low, and there is l i t t le c l inical evidence of d i s ea s e . The

skin r eac t ions (chancres) which develop a f t e r bi tes with t rypanosome- in fec t ed t s e t s e in

these wild an imals spec i e s a r e much s m a l l e r and the t ime to pa ras i t aemia is much

longer than in suscept ib le cat t le and goats (J .G. Grootenhuis , persona l communicat ion,

1982), sugges t ing that paras i te growth is being control led at the level of the skin. The

role of the skin in de te rmin ing r e s i s t a n c e to t rypanosomias i s of d i f ferent b reeds of

cat t le is cu r r en t ly being invest igated.

2. Other m e c h a n i s m s

Trypanoto le rance may be re la ted not only to the capaci ty to contro l pa ras i t e growth

but it may a lso be a s soc ia t ed with reduced suscept ib i l i ty to the effects of the d i sease ,

because a number of physiological f ac to r s which aid survival a re p o s s e s s e d by t rypano-

to le ran t b r eeds . These f ac to r s probably include low maintenance r eq u i r emen t s , heat

t o l e rance and the capaci ty to conse rve water , although, as yet , c r i t i ca l data concern ing

these p a r a m e t e r s a r e not avai lable .

Another explanation for surviva l of ce r t a in b reeds or spec i e s in a r e a s infested with

t s e t s e is that these an imals a r e r a r e ly subjected to t s e t s e at tack. It is well recognised

f r o m s tudies on blood meal analys is that t s e t s e exhibit definite host feeding p r e f e r e n c e s

which vary with spec ies of t s e t s e and a re affected by a la rge number of env i ronmenta l

f ac to r s (Weitz, 1963). Fac to r s such as colour and s ize of the host may be impor tan t

while Vale (1980) has recent ly demons t r a t ed that powerful a t t r ac tan t s for t s e t s e a re the

CO 2 and acetone in bovine brea th . The potential s ignif icance of t s e t s e p r e f e r e n c e s was

shown by Rober t s ~ a ~ . , (1980) when they compared the a t t r a c t i v en es s of cat t le and

oryx to t s e t s e fly under c r i t i ca l expe r imen ta l condi t ions . They found that five t imes as

many t s e t s e were a t t r ac ted to cat t le and w e r e able to count full engorgement on cat t le

of 279 t s e t s e dur ing the period of obse rva t ion . Only four t s e t s e were seen to obtain

par t ia l blood meals f r o m oryx dur ing the same t ime; this was part ly the resu l t of oryx

kil l ing t s e t s e with the i r horns . Whether a t t r ac t i venes s to t s e t s e d i f fe rs between b reeds

of cat t le is not known but r e s u l t s f r o m The Gambia, where groups of N'Dama and Zebu

were exposed to G.r~. s~br~orgi~anz chal lenge (cf above), would indicate that the re

was no major d i f f e r ences in a t t r a c t i v e n e s s , as all cat t le became infected and t h e r e was

no s ignif icant d i f fe rence in the t ime to f i r s t p a r a s i t a e m i a between b reeds (Murray ~

a~ . , 1981).

549

CONCLUSIONS

The exploi ta t ion of t r ypano to [e ran t b r e e d s of ca t t le of fers one of the most i m p o r t a n t

a p p r o a c h e s to the con t ro l of the p rob lem of Af r i can a n i m a l t r y p a n o s o m i a s i s . This con-

c lus ion is based on the knowledge, f i r s t l y , tha t t r ypano to l e r ance is an innate genetic

c h a r a c t e r i s t i c and, secondly, tha t b r e e d s such as the N'Dama and West Af r i can

Shor thorn a r e much more product ive than previous ly supposed. However, t r ypano-

t o l e r a n c e can be reduced under c e r t a i n a d v e r s e condi t ions such as high levels of t s e t s e

cha l lenge or it can be supplemented by prev ious exposure . The re fo re , to r e a l i s e the

full potent ia l of t r ypano to l e r an t b reeds , i t is impor t an t tha t the main e n v i r o n m e n t a l

f a c to r s which affect t r ypano t o l e r ance be identif ied and the extent of t h e i r inf luence

quant i f ied . Ful l c o m p r e h e n s i o n of the f ac to r s in t r ypano to l e r an t an ima l s which con t ro l

pa r a s i t e growth and al low the deve lopment of an effect ive immune r e s p o n s e might pro-

vide m a r k e r ( s ) for s e l ec t ive b r e e d i n g of t r y p a n o r e s i s t a n t l ivestock, or it might al low

methods to be devised for enhanc ing r e s i s t a n c e to t r y p a n o s o m i a s i s in more suscep t ib le

b r e e d s .

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