Susceptibility to vivax malaria in Ethiopia

342

TRANSACTIONS OFTHE ROYAL SOCIETYOFTROPICALMEDICINE ANDHYGIENE,VOL. 72, No. 4,1978

Susceptibility

to vivax malaria in Ethiopia*

J. C. ARMSTRONG Naval Medical Research Institute, Bethesda, Maryland 20014 U.S.A. Summary

vivax prevalence rates for Nilotic and Hamitic-Semitic residents of an Ethionian town were compared. Over a ten-year peiiod, 8,316 blood films from Nilotes were examined and 59 P. vivax infections (0.7%) were diagnosed. In 1.630 films from Hamito-Semites, 75 mobable -> P. vivax infections (4.6 %) were found. The problem of morphological differentiation between P. vivax and P. ovale was evaded by combining the two diagnoses. P. vivaxlovale infection rates for Hamitic-Semitic subjects were higher than for Nilotic subjects in all age groups. It was concluded that the two populations are innately different in susceptibility to patent infection with vivax malaria. Plasmodium

Introduction

The refractoriness of West Africans and New World descendants of West Africans to infection with Plasmodium vivax has been documented repeatedly from epidemiological and experimental evidence (YOUNGet al.. 1955; BRAY, 1958; GARNHAM, 1966; COATNEY et-al., 1951). hong fiamiticSemitic peoples of the Ethiopian highlands, P. vivax is the most prevalent species of malaria parasite found in many sectors (Ethiopian Malaria Control Service, unpublished reports, 1966-75). No statement has been seen regarding the innate susceptibility to vivax malaria of populations belonging to the Nilotic language family, who occupy lands along the upper Nile River and its tributaries. The purpose of this report is to compare the prevalence of patent P. vivax infections in Hamito-Semites and Nilotes residing together in a small town in the western lowlands of Ethiopia, and to draw any conclusions that seem warranted regarding the innate susceptibility of the two ethnic groups to P. vivax. Study

Subjects

and Methods

The subjects of this report were examined for malaria parasites between December 1966 and March 1977 in the town of Gambela, which is located on the Baro River 500 km west of Addis Ababa, Ethiopia. The town and environs have been described for the malariologist by KRAFSUR (1970) and ARMSTRONG(1972). Gambela has a mobile population, being the major administrative and marketing centre of a large district; perhaps a third of the people living there at any given time consider themselves permanent residents. For present purposes, the population of Gambela may be divided into two groups: Nilotes, represented mainly by members of the primitive Anuak tribe native to this malarious region, and HamitoSemites, represented by members of the Galla, Amhara and Tigre tribes from the highlands of Ethiopia where malaria is not endemic. Between

1966 and 1977, Gambela’s population increased from 1,500 to 2,000, and the proportion of HamiticSemitic residents rose from less than a fourth to nearly one half of the total. Malaria is consistentlv ranked as the leadinn cause of illness among Hamito-Semites at thz Gambela Health Centre. In Nilotic patients, according to local Health Officers. malaria is commoniy an incidental finding unr&ated to thk major complaint. A summary of records pertaining to antimalarials dispensed in Gambela during 1969-70, and kindly prepared by the Health Officer, indicated that chloroquine was prescribed three times as often, and primaquine 15 times as often, for persons with Hamitic-Semitic names as for persons with Nilotic names. Blood films were made from volunteers in malaria surveys and longitudinal studies and, at the discretion of the Health Officer, from attendance at the Gambela open clinic. The name, age, sex, tribe, duration of residence in Gambela, and a travel history were recorded for each subject at the time the blood films were prepared. Questions were also asked concerning the use of antimalarial drugs. Thick and thin blood films were prepared on separate slides for each subject and Gi&ms&stained, Thick films were examined for three to five minutes by one of three expert microscopists. Diagnoses of P. vivax and P. ovale were reviewed independently by the other two microscopists and by the author, making use of the matching thin films. When parasites were scanty and a consensus could not be reached on the diagnosis of P. vivax or P. ovale, this fact was noted and the infection was designated P. vivax for record purposes. Results

About 47% of the blood films taken over a IO-year period in Gambela were made during semesters of highest malaria prevalence, August through January, and the remainder were made during February-July, the season of lowest malaria prevalence. The median age of the 8,316 Nilotic subjects examined was 13 years; virtually all gave histories implying life-long exposure to malaria and little or no antimalarial treatment. The median age of the 1,630 Hamitic-Semitic subjects was 18 years with a median duration of residence in Gambela of eight years. Only 38 of the latter * Supported by the Naval Medical Research and Development Command, Research Work Unit No. ZF51.524.009.0072. The opinions and assertions contained herein are the private ones of the writer and are not to be construed as official or reflecting the views of the Navy Department or the Naval Service at large.

343

J. C. ARMSTRONG

Table II shows estimates of the actual prevalence rates of the four Plasmodium species in children and adults representing the two ethnic groups. Nearly 55% of the Nilotic sample, and only 42% of the Hamitic-Semitic sample, were children below the age of 15 years. P. ovale diagnoses were based upon adequate numbers of characteristic forms found in well-stained thin blood films. The diagnosis of P. vivax was applied to all other findings of tertian parasites; 24 of 59 P. vivax diagnoses recorded for Nilotes, and 19 of 75 P. vivax diagnoses recorded for Hamito-Semites, could not be distinguished from P. ovale with any degree of confidence. In sharp contrast with the infection rates for falciparum and quartan malaria, P. vivax infections were far more prevalent in Hamitic-Semitic children and adults than in their Nilotic counterparts. In Table III, the infection rates for P. vivax/ovaZe

subjects admitted travel to malarious areas before arrival in Gambela, and none with less than five weeks’ residence in the area was found to be infected; almost all reported seeking treatment for fevers at the Health Centre. Table I shows the relative prevalence of infections caused by the four species of Plasmodium in residents of Gambela by ethnic group. P. vivax and P. ovale infections were combined in this Table because of the frequent difficulty in distinguishing between the two species. Mixed infections, identified by the presence of two or three species in single blood films, were counted here as two or three separate infections. P. falciparum was the dominant parasite in both ethnic groups, followed by P. malariae in Nilotes. The relative prevalence of P. vivax/ovaZe was seven-fold greater in HamitoSemites than in Nilotes. Table I-Relative Ethiopia

prevalence

Ethnic group

of Plasmodium

species

No. examined

No. infected

8316 1630

3903 388

Nilotic Hamitic-Semitic

in Nilotic

actual Ethiopia

prevalence

Hamitic-Semitic

Relative

prevalence,

P. falciparum

of Plasmodium

Age in years

wup Nilotic

No. examined

<15 15+
HamiticSemitic

4546 3770 686 944

species

48.57 27.40 23.18 12.71

* Includes tentative diagnoses not differentiable

y0 P. vivax/ovale* 2:

similarity in Nilotic

and

infected

with :

P. malariae

P. falciparum

subjects,

14 7

Percent Ethnic

P. malariae

83 72

* P. vivax and P. ovale combined because of their morphological Table II-Estimated children and adults,

and

Hamitic-Semitic

P. vivax*

P. ovale

9.90 2.81 2.62 1.06

0.97 0.40 6.27 3.39

0.88 o-19 0.15 o-53

Nilotic

(N) and Hamitic-Semitic

from P. ovale

Table III-Statistical significance of the difference infection rates for P. vivaxlovale, by age group

between

(H-S)

P. vivaxlovale Age in years

Ethnic group

No. examined

No. pos.

N

2396

45

2351

1.9

H-S

288

12

216

5.3

2150

39

2111

1.8

458

32

426

7.0

3770

22

3748

0.6

944

37

907

3.9

No. neg.

% pas.

9.7

t5 N 5-14

H-S N

I5f * Chi-square

X2 value*

H-S

test with Yates’ correction

P < a003

36

< *OOl

65

< *OOl

344

SUSCEPTIBILITY

TO VIVAX

in the two ethnic groups are compared and shown to differ significantly in the chi-square test for three age groups. Higher rates of tertian malaria were found in Hamito-Semites at every age interval where adequate numbers of subjects made the comparison possible. When the disparity in prevalence of P. vivax between Nilotes and Hamito-Semites became apparent, attempts were made to ascertain the genealogy of Nilotic subjects with a recorded diagnosis of P. vivax. Only nine of these subjects could be found; all were children living with their Nilotic mothers. The fathers of four children were said to be Sudanese of mixed Nilotic-Semitic origin, and physical features of these children lent weight to the assertions. Mixed parentage, at least in recent generations, was denied for the other five children. Discussion As a temperate zone parasite, P. vivax thrives in those parts of the Ethiopian mid-highlands, 1,000 to 2,000 metres elevation, that have not been reached by the national Malaria Control Service. At elevations above 2,000 meters, where it is estimated that 60% of Ethiopia’s population lives, temperatures are normally too low even for P. vivar The possibility that important transmission. numbers of vivax infections were brought to Gambela (elev. 500 m) from the highlands of Ethionia bv the Hamitic-Semitic subiects of this ‘No malaria repori can almost be dismissed. infections were detected in persons who had lived in Gambela for less than five weeks, and barely 2% of the former highlanders gave histories of travelling in areas of endemic malaria before taking up residence in Gambela. Assuming equal susceptibility, Nilotes showed far fewer infections with P. vivaw than would be expected from a comparison with their HamiticSemitic co-residents in Gambela. The difference was greater than could be accounted for by random diagnostic error in the blood film examinations. Heal& Center records and subjects’ statements at anti-malarials, especially agreed in indicatin primaquine, were Ytake much more frequently by Hamito-Semites than by Nilotes. Given equal anti-malarial drug use, the difference in P. vivax rates for the two ethdc groups would have been even larger. The designation as L-. vivax of all questionable tertian malaria diagnoses stems from the fact that P. ovale was not recognized in Ethionia before 1966 The P. o&ale diagnoses (ARMSTRONG, 1969).presented here were probably made with excessive caution. It is uossible that no more than 35 of the 106 tertian malaria infections found in Nilotic subjects were actually due to P. vivux. And it was apparent from questions into the genealogy of some of these subjects that at least a few ‘Nilotes’ with P. vivax were fathered by Semitic Sudanese, who appear to have no genetic refractoriness to infection with this parasite. The prevalence of P. vivux remains unknown or confused with that of P. ova/e over wide areas of Africa. In East Africa, for example, ONORI (1967) has provided evidence that ovale malaria is more prevalent than vivax malaria in Uganda, contrary

MALARIA

IN ETHIOPIA

to earlier reports on the relative prevalence of the two species. In West Africa, GARNHAM (1966) has observed the tendency to identify all tertian malaria parasites as P. o&e, even among populations where miscegenation has introduced susceptibility to P. vivax.

MILLER et al. (1975) have offered an hypothesis to explain the enigmatic distribution of P. vivax in Af;ica. They have proposed that the recentor sites on human erythrocytes for penetration by P. vivax merozoites mav coincide with the Duffv blood group determinants. Blood typing surveys cited by MILLER et al. (1975) show that Duffypositive genotypes predominate among ethnic groups susceptible to P. vivax, whereas O-10% of West Africans, who are generally insusceptible, are Duffy-positive. An effort is underway to examine the Duffy factor-P. vivax relationship in the eastern African populations represented in the present report. Whatever its explanation may be, the conclusion seems warranted that Ethiopian Nilotes are less susceptible than Ethiopians of Hamitic-Semitic stock to patent infection with P. vivax. Refractoriness to this parasite appears to be more widespread than previously reported and not limited to West Africans. References Armstrong, J. C. (1969). Plasmodium ovale endemic in Ethiopia. Transactions of the Royal Society of Tropical

Medicine

and Hygiene,

63, 287-288.

Armstrong, J. C:( 1972). Evaluation of the results of an indirect hemagglutination test for malaria in an Ethiopian population. Proceedings of the Helminthological Society of Washington, 39, 545553 (Special Issue). Bray, R. S. (1958). The susceptibilitv of Liberians to the Madagascar strain o-f Plasmodium vivax. ‘fburnal

of Parasitologv.

44.371-373.

Coatney, 6. R., Coll&, W.‘E., Warren, McW. & Contacos, P. G. (1971). The Primate Malarias. Washington, D.C. : United States Government Printing Office. Garnham, P. C. C. (1966). Malaria Parasites and Other Haemosporidia. Oxford : Blackwell Scientific Publications, p. 118. Krafsur, E. S. (1970). Estimation of the theoretical daily survival rate in some malaria vectors in a lowland region of Ethiopia. Parassitologia, 12, 47-61. Miller, L. H., Mason, S. J., Dvorak, J. A. McGinnis, M. H., & Rothman, I. K. (1975). Erythrocyte receptors for (Plasmodium knowlesi) malaria : Duffy blood group determinants. Science, ‘8!j, 561-563. Onori, E. (1967). Distribution of Plasmodium ovale in the Eastern, Western and Northern Regions of Uganda. Bulletin of the World Health Organization, 37, 665-668.

Young, M. D., Eyles, D. E., Burgess, R. W. & Jeffery, G. M. (1955). Experimental testing of the immunity of Negroes to Plasmodium vivax. Journal of Parasitology, 41, 315-318.

Accepted

for publication

7th January,

1978.