Présentation des résultats de l'enquête effectuée sur 132 habitants du district de Karamoja en Ouganda, qui ont été examinés pour la recherche d'anticorps contre certains arbovirus dont la fièvre hémorragiqu

Gonzalez, Jean-Paul

Hannoun, C.

Helynck, B.

Larouze, B.

Mercier, E.

Rodhain, F.

Horizon / Pleins textes

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TRANSACTIONS F THE ROYAL SKIETY OF TROPICAL MEDICINE AND HYGIENE (1989) 83, 851-854, .- -- . 851 
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Arbovirus infections and viral haemorrhagic fevers in Uganda: a serological 
survey in Karamoja district, 1984 
i 
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F. Rodhain'.', J. P. Gonzalez', E. Mercie?, B. Helynck3, B. Larouze4 and C .  Hadnoun' 'Unid 
d'Ecologie des Systèmes Vectoriels, onnerly Unité d'Ecologie Virale, Institut Pasteur, 25 rue du Docteur Roux, 
(ORSTOM),  Boîte Postale 892, Bangui, Central African Republic; Rehabilitation Health Project of South 
Karamoja, Tokora, Uganda; 41NSERh4 U-13lInstitut de Médecine et d'Epìdémiologie Africaines, Hôpital 
Claude Bernard, 75944 Paris Cédex 19, France; 'Unité d'Ecologie Virale, Institut Pasteur, 25 rue du Docteur 
ROUX, 75724 Paris Cédex 15, France 
s 75724 Paris Cédex 15, France; f Institut de Recbche  Scientifique our le D h e l o p p m t  en Coopération 
Abstract 
Sera collected in May 1984 from 132 adult residents 
of Karamoja district, Uganda, were examined by 
haemagglutination inhibition tests for antibodies 
against selected arboviruses, namely Chikungunya 
and Semliki Forest alphaviruses (Togaviridae); de- 
ngue type 2, Wesselsbron, West Nile, yellow fever 
and Zika flaviviruses (Flaviviridae): Bunvamwera, 
Ilesha and Tahyna bunyaviruses (BÚnyaviridae); and 
Sicilian sanday fever phlebovirus (Bunyaviridae); and 
by immunofluorescence tests against certain haemor- 
rhagic fever viruses, Lassa fever arenavirus (Arenavir- 
idae), Ebola-Sudan, Ebola-Zaïre and Marburg filovir- 
uses (Filoviridae); Crimean-Congo haemorrhagic fev- 
er nairovirus and Rift Valley fever phlebovirus 
(Bunyaviridae). Antibodies against Chikungunya 
virus were the most prevalent (47%), followed by 
flavivirus antibodies (16%), which were probably due 
mainly to West Nile virus. No evidence of yellow 
fever or dengue virus circulation was observed. A few 
individuals had antibodies against Crimean-Congo 
haemorrhagic fever, Lassa, Ebola and Marburg 
viruses, suggesting that these viruses all circulate in 
the area. 
Introduction 
After the epidemics of yellow fever in Ethiopia in 
the 1960s and 1970s, epidemiological surveillance of 
arbovirus infections was carried out in the regions 
affected by the disease and in neighbouring regions: 
in northern Kenya, to the east of Lake Turkana (Lake 
Rudolf) (HENDERSON et al., 1968, 1970a; METSE- 
LAAR et al., 1970) and to the west of the lake, among 
the Turkana people (HENDERSON et al., 1968; 
RODHAIN et al., 1975); in south-west Ethiopia, in the 
province of Gemu Goffa (SERIE et al., 1968; RODHAIN 
et al., 1972, 1975); in northem Uganda, in the 
province of Karamoja (HENDERSON et al., 1968; 
1970b); and in southern. Sudan, in Sannar district 
(SALIM & PORTERFIELD, 1973). 
Few data have been obtained in this part of Africa 
during the last decade. We took advantage of the fact 
that 2 of us (B.H. and E.M.) were in the region to 
determine whether the socio-economic changes which 
have occurred in recent years have had.an effect on 
the epidemiology of arbovirus infections. In addition, 
the emergence of certain viral haemorrhagic fevers, 
especially in the Sudan, prompted us to include the 
main African agents of these diseases in the survey. 
Study region 
The sera were collected in the villages of Tokora 
and Namalu and in the neighbouring villages in the 
province of Karamoja, northern Uganda (Figure; 
Table 1). Limited to the south by the small range of 
Kadam mountains and to the east by the FWt valley 
escarpment, the southern Karamoja region is at an 
average altitude of 1100 m and is covered with 
shrubby or grassy savannah. There are 2 rainy 
seasons: March to June and October to November. 
The inhabitants belong to the Karamajong, of 
Nilotic origin like their close relatives the Turkana of 
Kenya (GULLIVER & GULLIVER, 1968). The territorial 
group predominating in the surveyed villages was the 
Piau, with a few Bokora. They are basically livestock 
farmers breeding mainly cattle, and lead a semi- 
nomadic life-style regulated by the search for pasture. 
However, modifications in the climate, the subse- 
quent major loss of cattle, and the permanent 
insecurity of recent years practically enforced a 
sedentary life-style, and many of the cattle breeders 
became farmers. The traditional social structures have 
thus been completely altered. 
Methods 
The subjects involved were all the adults of both 
sexes, aged from 20 to 40 years and in good apparent 
health, who attended the Tokora health centre during 
the first week in May 1984; subjects with fever or 
recent history of fever were excluded. It was consi- 
dered unlikely that the selected subjects had ever been 
vaccinated against yellow fever. The following in- 
formation was obtained for each of them: surname, 
first name, sex, age, sumames of father and mother, 
village of residence (Table 1). 
Sterile blood samples were collected in 
Vacutainersm and the sera decanted within a few 
hours and frozen at -20°C until use in Paris. 
132 sera were tested for arbovirus antibodies by 
haemagglutination inhibition using a micromethod 
with 96-well plates according to the usual technique 
(BARME et al., 1969-1970). After kaolin or acetone 
treatment (sera which were positive for viruses from 
different groups after kaolin treatment were treated 
with acetone), each serum was tested against a batch 
containing the following antigens: Chikungunya 
(CHIK) and SemLiki forest (SF) alphaviruses (Toga- 
. .  
ORSTQM Fonds Documentaire 
852 
Lo G 
F p .  Map showing study WM. 
viridae); Bunyamwera (BUN), Ilesha (ILE), Tahyna 
(TAH) bunyavinrses, sandfly fever Sicily type (SFS), 
and phlebovirus (Bunyaviridae); yellow fever (YF), 
dengue type 2 (DENZ), West Nile (WN), Wessels- 
bron (WSL), and Zika (ZIKA) flaviviruses (Flavi- 
vidae). A titre of 1 : l O  was considered positive. 
Antibodies against haemorrhagic fevers were 
searched for using a classical immunoflorescent assay 
with antigen-infected Vero cells (WULFF & LANGE, 
1975). Sera were screened on polyvalent slides with 
multiple antigen-infected cells and then titrated on 
monovalent slides (JOHNSON et d., 1981). The 
Table 1. Origin of sera studied 
L .  u r k a n  4 
followins antigens were used, belonging to several 
virus strains which had been recorded previously 
from the Central African Republic (GONZALEZ et al., 
1983): Crimean-Congo haemorrhagic fever nairovirus 
(CHF-CON) and Rift Valley fever phlebovirus (RVF) 
(Bunyaviridae); Ebola Zaire (EBO-Z), Ebola-Sudan 
(EBO-S), and Marburg (MBG) íïloviruses (Filovir- 
idae); and Lassa fever arenavirus (LAS) (Arenavir- 
idael. 
Results 
Arbmimes. Seventy-two sera (543%) showed anti- 
bodies against at least one arbovirus (Table 2). All 
positive sera had low titres, at the most 1:80. No sera 
were found with antibodies to BUN or SFS. 
Haemorrhagic fevcr viruses. Twenty-five sera 
(18-9Y0) showed antibodies against at least one of the 
tested antigens (Table 3). The titres observed did not 
exceed 1:128. No senun reacted with either Marburg 
or Ebola antigens. 
No difference according to sex was observed in the 
prevalence rates of antibodies to either arbovirus or 
haemorrhagic fever viruses. 
Other 
Sex 
Male 14 - 8 30 13 65 492 
Fende 13 13 11 28 2 67 508 
Total 27 13 19 58 15 132 IC4 
'Kokuwm! 2 (lF, 1M); Lokatapaa: 3 (lF, 2M); Lorcgai: 1 (IM); 
Nakapiripirit: 4 (4M); Kaiku: 1 (IM); Napenanys: 2 (2M); 
Nabftuk: 1 (1M); Amaler: 1 (IM) [M=male, F=female]. 
Table 2. bvdence rates of arbviral antibodies' 
Tokora Nadip Alanacar Namalu villags'TotalPercenenrage 
- .. -~ Total 
Village CHIK SF YF DEN2 WN WSL ZIKA flavivirusesb ILE TA€ 
uverau 
I positives' No. sera tested . 
1 2 - - -  1 - 1  2 2 1 14(51*8%) 27 
13 
19 
Tokora - - 8(61*5%) Nadip 8 - 1 - 1 2 2  4 -1.- ~-,. 7 - - - 2 1 -  2 2 - X~4~1U/o) 
8 3 4 34(58*6%) 
OthCI 4 - 1 2 4 2 3  6 - 2 8(53*3%) 
AIamäEar 
31 1 1  1 5 6 2 Namalu 58 
i r  L> 
62 1 3 3 13 11 8 22 7 7 72(54.5%) 132 
16.6 5.3 5.3 
TÖd 
Percentage 46.9 075  2.2 2.2 9.8 8.3 . 6 
'See text for key to abbreviations. 
%e number of sera positive for at least one virus in this group. 
The number of sera positive for at least one arbovirus. 
853 
Table 3. Prevalence rates of antibodies against haemorrhagic fever viruses' 
Village CHF-CON RFV EBO-Z EBO-S MBG LAS positivesb 
Tokora 2 
Nadip 
Alamacar 
Namalu 1 1 - 1' Other 
Total 3 4 4 4 
Percentage 2.2 3.0 3.0 3.0 4 5  6.0 
'See text for key to abbreviations. 
%e number of sera positive for at least one virus. 
'Nakapiripirit village. 
dNapenanya village. 
Overall No. sera 
tested 
- 1 5( 18.5%) 27 
- - 2( 15.3%) 13 1 3 1 - 1 1 
- - - . -  2 2(10*5%) 19 
58 5 14(24* 1%) - 2(13*3%) 15 
132 8 
- 
- - 2 5 - - Id 
6 25( 18.9%) - - 
Discussion 
The arbovirus prevalence rates showed only moder- 
ate differences between villages (4241%). Because of 
the relatively similar results obtamed from ecological- 
ly comparable regions, the discussion will deal with 
the overall findings. 
The overail positive rate for arboviruses (54-5%) is 
comparable to that observed in 1971 in the Kibish 
river region (Ethiopian-Sudanese border), about 
300 km to the north (RODHAIN et al . ,  1972). 
Antibodies against the Chikungunya virus were by 
far the most frequent in all villages, with an overall 
prevalence rate of 46.9% and titres ranging from 1 : l O  
to 1:M. In 1967-1969 HENDERSON et a l .  (1970b) 
observed a prevalence rate of only 9 9 %  among 182 
subjects aged over 15 years. It is possible that some of 
the antibodies detected were the result of infection 
with O'Nyong Nyong virus (ONN), which is closely 
related to CHIK. CHIK virus is present in man and 
monkeys throughout Uganda and epidemics of CHIK 
and 0" occur periodically in Uganda. Epidemics of 
CHIK occurred in the Zika forest in 1968 (MCCRAE et 
al . ,  1971) and in Mukono (Kampala region) in 1982 
(KALUNDA et al . ,  1985). Such an epidemic probably 
occurred in south Karamoja in recent years, but as no 
children's sera were included in our survey it was not 
possible to date th is event. 
The prevalence rate of 16% for flaviviruses which 
we detected is much higher than the 1.6% reported by 
HENDERSON et al. (1970b), with high titres mainly for 
WN virus and no YF antibodies (though prevalence 
rates up to 69% were observed in other parts of 
Uganda). Qualitatively, however, our results are 
comparable: no trace of YF or DEN2 circulation was 
observed, since positive sera had only low titres and 
were also slightly posithe for antibodies to other 
Viruses belonging to the same group; isolated W" 
antibodies were detected in 7 subjects (with titres up 
to 1:80), in all the villages, and WSL and ZIKA 
antibodies in 3 and 4 subjects respectively. These 
results indicatè that WN virus is present throughout 
the region, and that WSL and ZIKA are probably not 
so common. These results are comparable to those we 
found in 1972 in Turkana district (RODHAIN et al . ,  
1975). 
This region therefore seems to be free of yellow 
fever, and has been for 20 years, although the virus 
circulates actively in west and central Uganda in forest 
monkeys (MCCRAE & -YA, 1982). However, hu- 
man cases are extremely rare in these enzootic areas 
(low anthropophilia of potential vectors?). Furth- 
ermore? the Zika virus is no longer considered to 
interfere with the circulation of yellow fever virus 
(HENDERSON et a l . ,  1970a; CORNET et al.,  1979). 
Although there was na trace of BUN in our study, 
5.3% of the subjects were carriers of ILE antibodies. 
In the sweys  carried out in 1967-1969, considerable 
differences (0.4°/6-81-5%) in the prevalence rates of 
BUN antibodies (the only one tested for) were 
observed according to the region of Uganda, with 
3.3% ín Karamoja (HENDERSON et al . ,  1970b). Our 
studies in 1971 and 1972 found a marked circulation 
of ILE (0.9 to 6.1%) and practically no BUN in 
Turkana or in the lower Omo valley (Ethiopia). 
Finally, we found a relatively high frequency (5.3%) 
of TAH antibodies, which could indicate activity of 
Lumbo virus. We found no trace of it in Turkana in 
1972. 
There are many other arboviruses in this region, 
amongst which the Kadam (prototype isolated in 
Namalu) and Dugbe viruses were isolated from 
Karamoja (TUKEI er al . ,  1970), and antibodies against 
the Dugbe and Bhanja viruses are regularly found in 
cattle (UGANDA, 1975). 
Antibodies against all 6 viral haemorrhagic fever 
antigens used were found, and sera from all the 
villages were positive for at least one of these viruses. 
The prevalence rates were moderate, however, com- 
parable to those observed in other African countries. 
CHF-CON has been known to be present for a long 
time in Uganda, both in man and animals (especially 
cattle). One of its usual vectors, Amb!ymm varkga- 
rum, is common on cattle in K.aramoja (TUKEI et al. ,  
1970), and it is not surprismg that we detected 
antibodies in 2 of the surveyed villages. The same 
applies to RVF, which has also been h o w n  for a long 
time in Uganda (FINDLAY et al., 1936) and caused 
enzootics in Sudan in 1976. In the Turkana, at 
Lodwar, antibodies have been found in 90% of 
examined subjects (JOHNSON er al . ,  1983). 
To our knowledge, LAS virus has not previously 
been found in Uganda, but our results need to be 
backed up by a larger survey. However, antibodies 
have apparently been found in west Sudan. The 
positive results which we detected may imply that 
another, related, virus is present in the region, with 
little or no pathogeniciry for man. 
We have observed a simiiar frequency (3%) of 
854 
antibodies against both types of Ebola viruses. This 
agrees with the results of JOHNSON et al. (1983), who 
found 7.8% of EBO-2 antibody carriers at Lodwar, 
and those reported by the World Health Organkation 
(WHO, 1984): 4% for the 20-40 year age range in 
Turkana. The same applies to the Marburg virus: 6% 
of positive subjects in our study, 3.8% at Lodwar 
(JOHNSON et al . ,  1983), and 2.3% in Turkana (WHO, 
1984). Although the number of subjects was low, we 
noted, as did the authors working prevlously III 
Kenya and Zaire, the marked preponderance of EBO 
antibodies in femdes (6 of 8). By contrast, for MBG 5 
of the 6 positive subjects were male. These results, 
together with those of JOHNSON et al. (1982, 1983) III 
man and monkeys, suggest that EBO, MBG and RFV 
are present, at least temporarily, in dry areas inha- 
bited by Nilo-Hamite cattle breeders in north Uganda 
and Kenya. 
Acknowledgements 
We thank Mrs M. T. Drouet and M. Rousseau for their 
excellent technical assistance and J. Alix and C. Ten Have 
for translating and typing the manuscript. 
, 
8 
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Arbovirus infections and viral haemorrhagic fevers in Uganda : a serological survey in Karamoja district, 1984

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