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Serological Survey For Arboviruses In Ghana

By

Nii Saban Quao

Yale College

1971

A Thesis Presented to the Faculty of the Department of

Epidemiology and Public Health

Yale University School of Medicine

In Partial Fulfillment of the Requirements

for the Degrees of Doctor of

Medicine and Master

of Public Health

1976

To my mother because she represents the essence of the African woman - life giving and life sustaining.

TABLE OF CONTENTS

Page

I. ACKNOWLEDGEMENT. 1

II. ABSTRACT. 3

III. INTRODUCTION . 6

IV. GENERAL BACKGROUND . 6

Position and Extent . 6

Population . . 6

Relief and Structure. 6

Climate and Weather. 10

Temperature. 10

Rainfall. 10

Humidity. 12

Drainage Systems . 12

Vegetation. 12

High Forest. 15

Savannah-woodland. 15

Coastal and scrub and grassland . 17

Strand mangrove ...... 17

Some Mammalian and Insect Fauna. 17

Health Services and Conditions ...... 18

Services .. 18

Conditions .. 18

Malaria. 18

Schistosomiasis ...... 19

Trypanosomiasis. 19

Onchocerciasis .. . 19

Tuberculosis ...... 19

TABLE OF CONTENTS

Page

Yellow Fever . 19

Smallpox. 20

Yaws. 20

Other diseases. 20

V. REVIEW OF LITERATURE. 21

Arboviruses. 21

Alphaviruses . 22

Chikungunya. 22

Sindbis .... 23

Flaviviruses . 24

Dengue . 25

Uganda S . 26

Wesselsbron. 27

West Nile. 27

Yellow Fever .. 29

Zika . 34

Bunyaviruses . 35

Bunyamwera. 36

Ilesha . 37

VI. MATERIALS AND METHODS . 38

Field Methods. 38

Characteristics of Sample . 39

Geographic Distribution . 39

Age Distribution .. 39

Sex Distribution. 39

Vaccination Status 39

TABLE OF CONTENTS

Page

Laboratory Methods . 44

VII. RESULTS .. 46

Alphaviruses . 46

Flaviviruses. 48

Bunyaviruses .. 52

VIII. DISCUSSION. 52

Alphaviruses . 52

Flaviviruses . 54

Bunyaviruses . 60

Arboviruses, Administrative Regions, Population size.

Annual Rainfall and Vegetation . 61

Limitation to this investigation . 64

Perspectives for the future. 66

IX. BIBLIOGRAPHY 72

TABLE OF CONTENTS

Page

Table 1. Population Distribution . 9

Table 2. Yellow Fever Cases Notified During Period

1960-1975, West Africa . 31

Table 3. Yellow Fever Vaccination In Ghana,

1969-1970 . 33

Table 4. Geographic Distribution of Human Sera Collected

from Ghana, June-September, 1975 . 41

Table 5. Distribution of Sera according to population

size of sampling towns. 42

Table 6. Age distribution of samples of Ghanaian popu¬

lation .. 43

Table 7. Virus antigens used in HI testing:

Serological Survey, Ghana, 1975 45

Table 8. Results of Arbovirus Hemagglutination-Inhibition

Tests on 216 Ghanaian Men and Women Ages 20-69 . 47

Table 9. Arbovirus HI reactors by population of towns . . 49

Table 10. Arbovirus HI reactors by annual rainfall .... 49

Table 11. Arbovirus HI reactors by vegetation zone .... 50

Table 12. Geographical Distribution of HI arbovirus

reactors. 51

Figure 1... 7

Figure 2 ...... 8

Figure 3. 11

Figure 4. 13

Figure 5 14

TABLE OF CONTENTS

Page

Figure 6. 16

Figure 7. 10

Appendix I. Summary of Results by region, town, population,

annual rainfall, and vegetation type . 68

Appendix II. Distribution of Arbovirus Reactor and

Non-reactors of Ghanaian sera, 1975 . 70

-1-

ACKNOWLEDGEMENT

I should like to express my profound gratitude to all the fine people in Ghana and the United States, who for lack of space cannot be named, but whose encouragement, help and openness of heart helped to bring this pro¬ ject to fruition.

My special thanks to Dr. Wilbur G. Downs, my thesis advisor, who first introduced me to this field, whose enthusiasm, unstinging help and belief in my abilities were invaluable throughout this course of study; and to

Dr. Robert E. Shope whose advice and friendliness made working at the Yale

Arbovirus Research Unit (YARU) such a pleasure. My instructors in

Dr. Downs' laboratory were Miss Carole Mongillo and Mrs. Gerda Roze. All

t I know about diagnostic virology I learned from them; they were enthusiastic teachers. I also wish to thank all the members of YARU for their help during this study. Their friendliness and warmth has been sustaining.

The success of the serum collection,in large measure,was the work of

Dr. K Saakwa-Mante, Director of the Center for Health Statistics, Ministry of

Health, Ghana, who is my joint thesis advisor. He obtained the permission

from the Director of Medical Services which allowed me to carry out this

survey; wrote letters to the various Regional Medical Officers of Health to

introduce me; suggested people to see whose advice were instrumental in

planning of the survey; and also placed the facilities of the Centre for

Health Statistics at my disposal. His warm-heartedness and guidance were

valueless and will long be cherished.

A great many individuals of the Ministry of Health and the Mission

Health Services also own a part of the credit for this study. In particular,

I wish to express my gratitude to Messrs. Attuquayefio and Nelson of the

Centre for Health Statistics, Dr. Benard Doku and all the Medical Officers

in the hospitals I visited. Their dedication and enthusiasm helped to

-2- harden my resolve that my place is alongside them in Ghana. To Mama, my friend and companion in my travels, I say thank you, without you I could not have accomplished a fraction of what I was able to do.

Finally I would like to thank my parents for their invaluable support for the many years of preparation for the medical career. My gratitude to the McCarthy's, the McCravens, the Russos, the Truslows, and Mrs. Lillian

Dalton who have made my stay here in the United States such a rich and abiding experience.

t

-3-

ABSTRACT

1. A serological survey for hemagglutination-inhibition antibodies to 11

arboviruses was conducted for 216 Ghanaians between the ages of 20

to 29.

2. The objective of this investigation was to determine some of the

arboviruses that infect the Ghanaian population.

3. Pertinent findings were: a) One hundred and fifty-four (71%) of the

sera tested were positive for the alphaviruses. There were 113

specific reactors of which 112 were to chikungunya and one to Sindbis.

b) One hundred and twenty-four (57%) of the 216 sera were positive to

the flaviviruses. Eight of those positive gave specific reaction

% with Zika, three with yellow fever and two each with West Nile and

Wesselsbron and one with dengue-1.

c) Forty-seven (22%) of the 216 sera were positive to the Bunya-viruses

and of these eight were specific reactions to Ilesha and two to Bunyam-

wera. d) The activity of these viruses appears to be more concentrated

in the drier savannah areas of the Northern and Upper Regions.

4. There were several limitations to this investigation notably those in¬

herent in the HI test method employed and the age group studied.

5. This study suggests need for further serological surveys of Ghana to

determine antibody characteristics of the human and animal populations,

to isolate and identify viruses, and to elucidate vertebrate hosts and

vector characteristics.

-4-

INTRODUCTION

Nearly all tropical diseases are of an infectious nature and prevent¬ able. A physician in the tropics must have a thorough knowledge of the etiologies of infections he may encounter if he is to appreciate the sig¬ nificance of his diagnosis and to take rational steps to prevent the dis¬ ease from spreading. The mode of transmission of tropical diseases is seldom simple and straight forward, for there is often not only the para¬ site itself but an insect vector and intermediate host, and/or an animal reservoir of infection. Indeed with few exceptions, notably diseases due

to nutritional diseases and intestinal fluxes, the vast majority of tropi¬ cal diseases are transmitted to man through agency of an animal and an in¬ sect, either alone or jointly.

It is only in the last quarter century that transmissable diseases

in the tropics have been studied in a systematic manner to characterize

them and help in their diagnosis. Among the transmissable diseases major attraction has been paid the viral diseases and in particular arthropod- borne viral diseases. Within the past 20 years several virus research

centres have been organized in the tropics in Ibadan, Nigeria; Dakar,

Senegal; Bangui, Central African Republic; Kampala, Uganda; India and

South America.

The recorded history of virus research in West Africa dates back to

1913 when the International Health Commission was set up by the Rockefeller

Foundation Yellow Fever Commission. This commission was organized for fear

of spread of yellow fever to the Orient via the Panama Canal which had just

opened. The commission succeeded in eliminating yellow fever from several

South American countries and in 1925 established the West African Yellow

Fever Commission at Yaba, Lagos. In 1954 the Virus Research Laboratory

-5- became a unit of the West African Council for Medical Research. At this point the scope of the work of the laboratory was broadened to include the study of the virology of West Africa, with special emphasis on the arthropod-borne viruses. Since then many serological surveys have been conducted in some West African countries to determine the prevalence of antibodies to arboviruses in the various populations.

There has been two such surveys recorded for Ghana, one in 1934 by

Beeuwkes and Mahaffy and the other in 1961 by the Rockefeller Virus Foun¬ dation Virus Laboratory - New York (RFVL-NY). The purpose of this survey is to contribute to the information on arboviruses in Ghana which would, hopefully, give some indication to physicians in Ghana as to the prevalence of diseases caused by these viral agents in the population. To this end serum samples were collected from individuals above the age of 10 in 37 localities, representing vegetational, climatic, and population size variations, in Ghana. Two hundred and sixteen of these samples from the age range 20 to 29 were then studied by hemagglutination-inhibition methods to elucidate the prevalence of arboviral antibodies in the Ghanaian popula¬ tion.

In the succeeding presentation of this study a general background in¬

formation on Ghana is presented; the literature on arboviruses is reviewed

for Africa and West Africa in particular; the materials, methods and the

results are described; and a discussion of the findings is presented.

-6 -

GENERAL BACKGROUND

Position and Extent

The Republic of Ghana is almost centrally located among the countries of the West African coast. Togoland lies to the east. Ivory Coast to the

West and Upper Volta lies along her northern boundaries (Fig. 1).

Her southern coast extends between latitude 4° 30'N in the west to

6° 30'N in the east; the country stretches 420 miles inland from the coast to her northern borders. From the east to the west the country lies be¬ tween 1° 30*E and 3° 30*W and measures 334 miles. The total land area is approximately 92,000 square miles and is divided into nine administrative regions. (Fig. 2).

Population

In 1970 the population of Ghana was 8,599,313 and was distributed in the various regions as shown in Table 1. Although an increasing number of the population is moving to the urban centers, the majority of the popula¬

tion live in what might be described as "rural" to "semi-rural" setting.

Fifty seven percent of the working populations were employed in agriculture

in 1970. Of the population engaged in agriculture the highest proportion

come from the Brong- (77%) followed by the (72%)

and Upper Region (69%). (Ghana Population Census, 1970). The majority of

the agricultural population is involved in subsistence farming.

Relief and Structure

For the most part the land is between zero to 500 feet above sea level.

The few exceptions are the Plateau in the extreme north-east, and

the Kwahu Plateau which runs approximately from Kintampo to Koforidua in a

-7-

Figure 1

Figure 2

-9-

Table 1

Population Distribution

Region Population3

Western 770,087

Central 890,135

Greater 851,614

Eastern 1,261,661

Volta 947,268

Ashanti 1,481,698

Brong-Ahafo 766,509

Northern 727,618

| Upper 862,723

. .- .. -

All Regions 8,559,313

a1970 Population Census.

-10- north-west to south-east direction. These plateaus average 1750 feet and at their highest points reach 2,500 feet above sea level. (Fig. 3).

Structurally the land mass is composed of Voltaic rocks which consists mainly of sandstone and covers nearly 45% of the country; the rest of the

country is made up of a variety of rock forms among which granite, quart¬

zite and phyllites predominate.

Climate and Weather

Ghana's climate is characterized by a high and uniform temperature,

great variations in amount, duration and seasonal distribution of rainfall

from the south to the north, and dry seasons which grow longer and more harsh with distance from the sea.

Temperature

With the exception of a few places where temperatures are reduced by

high altitudes, the annual mean temperature for the entire country ranges

from 79°F to 84°F with the lowest temperatures near the coast and the

highest in the northern savannah. The remarkable characteristic about the

temperature is the mean daily range which can be 12 or 13°F along the coast

and as much as 18 to 30°F in the northern savannah.

Rainfall

There are two distinct seasons, dry and rainy. The distribution of

the latter varies considerably during the year, but grossly two types are

distinguishable: 1) a single rainy season between March and September,

and 2) two rainy seasons with peaks in May-June and October. The former

occurs in an area approximately north of a line through Kintampo and

and the latter is south of this line.

-11-

Figure 3

o yC, Gambc^a.Y

yUm v. M

& \ - '&*%?.''< \T—^ k. \v<

5^-frWerichi1- ■-' • - » -'• -•

ijytamgdng

Moraeso • Bo»u»l*l CJ

ACCRA

,5/Sekondi RELIEF Axinv Takoradt

500 /000 ^000

-12-

The highest annual rainfall occurs in the with over 86 inches in some localities, and diminishes gradually northwards to between

40 and 50 inches annually in the Northern Region. The only major departure from this pattern is an area between Cape Coast and where the rainfall decreases to under 30 inches annually, in what is known as the coastal grass¬ land region. (Fig. 4).

Humidity

Ghana is generally humid. Relative humidities of 90 to 100 percent prevail with minor variations over most of the country during the night and early morning. In the day, humidity falls to a minimum with average relative humidities varying between 45 to 75 percent; however, during the

Harmattan, a period of cool dry north-easterly winds occurring in December

to February, the relative humidity can drop to as low as 12 percent.

Drainage Systems

Ghana is drained by large number of streams and rivers forming a net¬ work over most of the country (Fig. 5). Although all the main rivers carry

a good volume of water all year round, there are variations in flow due to

the rainfall pattern with rapid run-off from watersheds especially in the

north. Most streams overflow their banks after the heavy downpour which

occurs during the rainy season. The flooding of the bank creates stagnant

pools of water which become breeding grounds for vectors of such diseases

as malaria, trypanosomiasis, and schistosomiasis. With the construction of

industrial and various irrigational dams, the vectors of bilharzia continue

to spread, and the vectors of onchocerciasis may thrive.

Vegetation

The distribution of vegetation is determined primarily by the amount

of rainfall and its duration. Four broad vegetation types are distinguished

-13'

Figure 4

SOm/l@s

-14-

Figure 5

-15- in Ghana. These are the high forest, savannah-woodland, coastal scrub and grassland and strand mangrove (Fig, 6).

High Forest.

With the exception of a narrow belt extending 10 to 20 miles from the coast between Sekondi-Takoradi and Ada, the high forest occupies the entire south-west part of Ghana, and covers an area of approximately 25,000 square miles. The annual rainfall in this area varies from 85 inches along the coast to 50 inches along the inland boundaries of the high forest.

The vegetation zone is made up of a variety of plants arranged in a series of distinctive layers. Near the ground are found small herbs, shrubs and grasses. At about 60 feet occurs the next layer of trees with low branches and heavy crowns. Above this comes the upper layer formed by trees with tall straight stems usually with small crowns forming canopy at about

130 feet high. This is the predominant cocoa growing area.

The occurrence of high temperatures, high humidity and high rainfall creates an environment which breeds insects which serve as vectors for many communicable diseases. The existence of mosquitoes in the high forest and

sylvan populations provide ample conditions for the maintenance of foci of jungle yellow fever which occasionally is transmitted to man in this setting.

Savannah-woodland.

The savannah-woodland or the guinea savannah is the most extensive

vegetation type. Totalling approximately 65,000 square miles it covers the

region north of the high forest. In its typical form it is composed of

short trees, often widely spaced, with more or less continuous carpet of

grass. Although most of this area has annual rainfall of 40 to 50 inches,

the dry season is long and severe. This grass land is above the tsetse-fly

belt and grazing is important and widespread here.

-16-

Figure 6

VEGETATION ^ForestReserves j'i jfjjjRain Forest

(/ A Moist. semi- Guineo Savannah- f / Jdeciduous Forest Ytoodland [I'i'I'ICoasta! Scrub [:• -Strand and I * ■1»'land Grassland L_vj Mangrove Zone

y SO m i/p*

-17-

Coastal scrub and grassland.

This vegetation zone is a narrow strip of land which extends along the coast from Takoradi to Keta and measures nowhere wider than 20 miles.

Rainfall is very low averaging 33 inches annually. The vegetation con¬ sists of grassland studded with clumps of bush and patches of scrub. Un¬ like the northern grasslands, the grass of the coastal grassland is un¬ suitable for cattle so grazing is scarce here.

Strand mangrove.

Strand mangrove is confined to the immediate coastal area, both along the sea front and beds of lagoons. Rather succulent erect or creeping herbs, tufted plants and grasses are the characteristic vege¬ tation of this zone. The lagoons are breeding grounds for mosquitoes and this represent a public health problem.

Some Mammalian and Insect Fauna

Owing to the spread of food and cocoa farming in the rain forest, the larger wild animals are becoming rare, though there are many kinds of small animals and myriads of insects including various species of

Aedes, Anopheles, Culex and Mansonia. Certain kinds of duiker may still be seen, and in the western forest buffalo, bongo and bush back. An occasional leopard is sometimes sighted and monkeys of various species are found in some parts. Cattle grazing is minimal in the rain forest due to the presence of the tsetse-fly, the vector of sleeping sickness, which is widespread in this area.

The northern grasslands have escaped some of the necessary but often destructive agricultural practices of the south and larger wild animals can be found here. Some of these animals are duikers, antelopes, lions and hyenas. Families of baboons and other monkey species are frequently

-18-

seen and often can be nuissance to farmers. Luckily for herders, the large proportion of the northern savannah is above the tsetse-fly belt and animal husbandry can be practiced on a large basis here. Like the rain forest insects abound in the grassland and the same species of mosquitoes are obtained here.

Health Services and Conditions

Services.

Medical care in Ghana is socialized. It is fully subsidized by the government and administered through the Ministry of Health. The ministry maintains an office in each of the nine regions headed by a Regional Medi¬ cal Officer of Health who is responsible for the supervision and coordina¬ tion of all public health activities involving hospitals, health centers, health posts, health inspectorates, health education, control of communi¬ cable diseases, maternal and child welfare and nutrition. There are 43 government hospitals, 12 government affiliated hospitals and 34 mission hospitals. In addition there are 12 hospitals run by mine companies for their employees and 17 private hospitals.

Conditions.

As in most developing countries, communicable and infectious diseases are the leading cause of ill-health in Ghana. They are responsible for approximately 60% of attendance in hospitals and 20% of the certified deaths.

(Report of the health situation in Ghana 1965-1970).

Some of the most important communicable diseases are:

Malaria: This disease which is hyper-endemic to holoendemic is the

leading cause of illness in Ghana. At this time control is limited to anti¬ mosquito activities in cities and major towns, and administration of anti-

malarial drugs.

-19-

Schistosomiasis: The prevalence of schistosomiasis is estimated at

1% of the population. Although its distribution has been focal, the con¬ struction of dams for irrigation and industrial purposes has extended the area of endemicity and the incidence of the disease has been increasing.

Control measures are directed to snail eradication, health education, in¬ stallation of latrines and safe water supplies.

Trypanosomiasis: By the 1970 trypanosomiasis has been restricted to

10 endemic foci along the Volta River and its tributaries. One hundred and seventy cases were reported in 1969 as compared to 99 cases reported in 1970. Measures have been instituted to control the vector, tsetse-fly, by clearing riverine vegetation near human settlements in endemic areas.

Onchocerciasis: Increasingly it is becoming clear that onchocerciasis is prevalent over most of Ghana and it is especially high in the Volta

River basin where a correspondingly high incidence of blindness is seen.

Tuberculosis: This disease has been and continues to be a serious health problem. In 1969 and 1970 the report of new cases was 54.6 and

55.2 per 100,000 population. The standard control measure has been to find cases and to treat them within their communities. This, of course, means others in the population will become exposed to tuberculosis.

Ghana is receiving help from UNICEF for a mass BCG vaccination program.

Yellow fever: Sporadic cases of yellow fever continue to be reported and it is possible that foci of sylvan yellow fever persist in the country.

There were 303 suspected cases in 1969 and 12 confirmed cases in 1970. A mass yellow fever immunization program has been started in 1969 and it is hoped that in the next several years a majority of the population would be vaccinated. Such a program, of course, requires continuing updating. Con¬

currently there have been attempts to control the vector Aedes aegypti, in

their urban breeding places.

-20-

Smallpox: Due to the aggressive vaccination program against smallpox initiated in 1959, greater than 50% of the population has been vaccinated

10 years later. There has been no reported cases since 1969.

Yaws: By 1970 yaws had adequately been controlled but there are signs that the disease is re-emerging and control measures have been tightened.

Other diseases: The situation with several other diseases of public health interest, especially venereal disease, is not adequately understood because of the lack of laboratory facilities for the diagnosis of these diseases. Some authorities suggest that syphilis may not ordinarily occur in this country due to the immunity that develops with yaws infection and partially protects against the Treponema pallidum. With the continued control of yaws there will be an increasing number of people with no pro¬ tecting antibodies who will be susceptible to syphilis. It will be sad if such a situation were to occur in Ghana.

-21-

REVIEW OF LITERATURE

Arboviruses

The arboviruses (Arthropod-Borne Viruses) are viruses that multiply in vertebrates and arthropods. The former serve as res¬

ervoirs in the cycle of transmission with the arthropods as vectors.

Certain of these viruses cause disease in the vertebrate host but, with rare exceptions, do not affect the arthropod vector.

Some of the arboviruses are classified in groups A (alphaviruses)

and B (flaviviruses) on basis of serological reactions as well as

size, morphology and intracellular growth characteristics. Members within a group show varying degrees of cross-activity with each other

often in several serological testing methods, but not with arboviruses

of other groups. (Casals and Brown, 1954). Some arboviruses belong

to the supergroup Bunyamwera (bunyaviruses). They are grouped mainly

by complement-fixation studies which reveal greater cross-reactivity

among members of the group than do hemagglutination-inhibition tests.

(Casals and Whitman, 1960). Apart from these three major groupings,

there are other groups of arboviruses defined by combinations of

morphology, biophysical properties, and serological relationships.

(Theiler and Downs, 1973). There remain several dozen ungrouped viruses

which show no serological relationship to any other virus.

Identification of the virus within a group is accomplished by

neutralization with standard immune sera when other serological tests

fail to make an adequate differentiation. (Theiler and Downs, 1973).

-22-

Alphaviruses

This group consists of twenty distinct agents. (Theiler and Downs,

1973). Of the twenty viruses only chikungunya, Middelburg, Ndumu, o'nyong-nyong, Semliki Forest and Sindbis exist in Africa. (Theiler and

Downs, 1973; Berge, 1975). With the exception of Ndumu and Sindbis, all have been isolated from West Africa (Theiler and Downs, 1973). Actual virus isolations from man have been obtained for chikungunya, o'nyong- nyong and Sindbis (Berge, 1975). Further, there is evidence from anti¬ body studies that Ndumu and Semliki Forest may also cause human disease

(Berge, 1975). All these agents are transmitted by mosquitoes (Theiler and Downs, 1973).

Chikungunya

Chikungunya is an alphavirus. First isolated by Ross in 1953

(Ross, 1956) from the serum of a febrile man in the Newala district,

Tanzania. Strains of chikungunya have since then been isolated from man in Uganda (Weinbren e_t a_l, 1958; East African Virus Research In¬ stitute (EAVRI) Ann. Rep., 1958-63), Zaire (Osterrieth, e_t a_l, 1960),

Nigeria (Causey, et al, 1969), and Senegal (Hannoun and Echalier, 1971).

In addition, numerous strains of chikungunya have been isolated

from a variety of mosquitoes other than its classical vector, Aedes

aegypti. These include strains of virus from A. africanus, Mansonia

fuscopennata, M. africana and M. uniformis in Uganda (EAVRI Ann. Rep.,

1955-1956, 1960-1961, 1961-1962). In Nigeria virus strains have been

isolated from M. africana (McIntosh et al, 1964; Boorman and Draper,

1968). Isolations of chikungunya have also been achieved from bats in

-23-

Senegal (EAVRI Ann. Rep., 1958-1963), from birds and sentinel mouse in

Nigeria (Causey et al, 1969). McIntosh et_ £l (1964) also found antibodies

to chikungunya in wild monkeys. These findings suggest that monkeys may

play a part in the natural cycle of the virus.

Serological studies on HI antibodies of sera from man in Africa,

have shown that infection with chikungunya may be widespread. In West

Africa HI antibody levels of this virus in man are generally very high,

and the presumed presence of the infection of the virus has been shown

in Senegal (Bres, et al, 1963), Mali (Bres 1970), Upper Volta (Brbs,et al,

1965) Ivory Coast (Robin _et_ al, 1968), Togoland (Bres, 1970) and Nigeria

(RFVL-NY Ann. Rep. 1961; Casals, 1966; Monath et al, 1973; Lee et al.1974;

Monath et_ afL, 1974; Fagbami and Fabiyi, 1975). In Ghana HI studies on

sixty sera by RFVL-NY (1961) have indicated that the virus might be pre¬

sent here.

The virus has been responsible for huge epidemics in East Africa

(Ross, 1956). It appears to have a pattern of an endemic infection in

West Africa although small epidemics have been reported (Tomori,1976).

Sindbis

Sindbis virus, first isolated from Culex univittatus caught in Sind¬

bis, a village of the Nile Delta, Egypt (Taylor ejt al, 1955) is an alpha-

virus .

Strains of Sindbis have subsequently been isolated from man in Uganda

(EAVRI Ann. Rep., 1961-1962) and South Africa (Malherbe and Strickland-

Chomley, 1963) and from a variety of animals including sentinel mice in

Ibadan, Nigeria(Univ. of Ibadan Arbo-Virus Research Project (UIARP) Ann.

Rep., 1971-1972). However, mosquitoes continue to be the chief source of

-24-

isolation of this virus, and Sindbis has been isolated from (2. antennatus

and Anopheles pharoensis in Egypt, Culex univittatus, C. pipiens, C. theileri,

Aedes circumluteolus and M. africana in South Africa, and Mansonia fuscopennata

in Uganda (EAVRI Ann. Rep., 1962).

The possibility that birds may play a part in the virus cycle in nature

has been suggested by isolation of Sindbis from a hooded crow, Corvus coroae

sardonicus in the Nile Delta (Taylor et_ al, 1955) , and by the occurrence of

antibodies to this virus among wild birds in South Africa (Malherbe and

Strickland-Chomley, 1963).

In West Africa immunity surveys using HI techniques have shown either

no antibodies or very low levels of antibodies to this virus in man and in

animals (Bres, et: al, 1963, 1965; Casals, 1966; Monath et al, 1974; Fagbami

and Fabiyi, 1975). The inference that can be made here then is that infec¬

tions caused by this virus may occur only rarely in this area.

Flaviviruses

There are fifty-seven flaviviruses}and seventeen of these exist in

Africa. (Berge, 1975). This group can be divided into three subgroups de¬

pending on whether the mode of transmission is by a mosquito, a tick, or is

unknown. (Theiler and Downs, 1973).

The largest of these subgroups comprises the viruses transmitted by

mosquitoes. Twenty-six of these viruses are known and most can cause

disease in man (Theiler and Downs, 1973; Berge, 1975). The African members

of this subgroup are Banzi, Bouboui, dengue 1, dengue 2, Ntaya, Spondweni,

Uganda S, Usutu, Wesselsbron, West Nile, yellow fever, and Zika (Berge,1975).

All these viruses, with the exception of Bouboui, Ntaya, Uganda S and Usutu,

have been isolated from man. There are no reported results that Usutu causes

-25-

disease in man. Of the group of viruses isolated in Africa, Banzi and

Ntaya do not occur in West Africa (Berge, 1975).

Ticks serve as vectors for the next subgroup. The only virus iso¬

lated in Africa that belongs to this group is Kadam (Berge, 1975). The

virus has not been isolated from vertebrates (Berge, 1975).

For the third subgroup no arthropod vectors are known. Dakar Bat,

Entebbe Bat, Koutango and Saboya are the only viruses of this subgroup

that have been isolated in Africa, (Berge, 1975). None of these iso¬

lations came from man, but positive serological reactions have been re¬

ported in man to the Dakar Bat virus in Senegal and Saboya virus in Sierra

Leone (Berge, 1975).

Dengue

The four recognized dengue viruses: dengue 1, 2, 3, and 4, belong to

the flaviviruses. All four types have been isolated from man (Theiler and

Downs, 1973).

According to Theiler and Downs (1973) the first epidemics of dengue

were described by Hirsch in 1779 in Batavia (now Netherlands) and in 1780

in Philadelphia, USA. Since then dengue infections have been reported in

a variety of places, especially the tropics, including Hawaii, New Guinea,

Trinidad, Indies and Puerto Rico (Theiler and Downs, 1973). The first

African epidemic of dengue may have been in Durban in South Africa in 1927

Kokernot,e_t aJL (1956) in neutralization tests using sera from people who

were alive at the time of the Durban epidemic reported that some of these

individuals neutralized the dengue virus. By contrast individuals born

after the epidemic were devoid of antibodies.

Recently, dengue type 1 and 2 isolates have been made from febrile

-26-

patients presenting at the University Hospital in Ibadan, Nigeria (Carey, et al, 1971), and several reports of dengue-like illness have been re¬ ported in humans in Nigeria (Lee, 1969). HI investigations have revealed the presence of antibodies to dengue in Nigeria (Monath and Kemp, 1973;

Monath, et_ a_l, 1973^;Monath, ejt al, 1974; Fagbami and Fabiyi, 1975), and

Cameroun (Salaun and Brottes, 1967). These antibodies have been to either type 1 or type 2. Additional information regarding the presence of dengue in West Africa has been given by results of neutralization tests in Nigeria by Macnamara, _et_ al, (1959). In Ghana HI tests on a limited sera has re¬ vealed presence of antibodies to dengue. (RFVL-NY, 1961; Fabiyi, 1961).

Dengue is transmitted by the bite of a mosquito (Theiler and Downs,

1973). Studies have shown that the usual vector is Aedes aegypti, however, other mosquitoes notably Aedes albopictus can transmit the virus (Rudnick and Chan, 1965).

An important complication of dengue virus infection is dengue hemor¬ rhagic fever, which is thus far localized to southeast Asia, with possibly cases in Oceania and the West Indies. No cases of dengue hemorrhagic fever have been recognized in Africa, (Suchitra,ejt al, 1969; Halstead, 1970).

Uganda S

Uganda S is another member of the flaviviruses. The virus was initially

isolated from a pool of Aedes spp. in Uganda in 1947 (Dick and Haddow,1952),

Since then there had been, supposedly, another isolation from a febrile

patient from Makonde, Uganda, (Spence and Thomas, 1950) but this was never

confirmed (Theiler and Downs, 1973).

In West Africa antibodies capable of neutralizing the Uganda S virus

have been demonstrated in human sera from Nigeria (Macnamara, et al, 1959)

-27-

and Senegal (Bres, _et al, 1963). However, Theiler and Downs (1973) suggest that most of the positive neutralizations do not reflect Uganda S infection. Serological surveys utilizing HI techniques have revealed the presence of antibodies to the Uganda S virus in many West African countries including Senegal (Bres, ejL _al, 1963), Upper Volta (Bres et_ a]^, 1965),

Ivory Coast (Robin et al, 1968),Togoland (Bres, 1970) and Nigeria (Bres,

1970).

Causey j2t al, in 1969 reported of isolation of Uganda S virus from a sentinel mouse in Nigeria. To date no isolation of the virus had been made from sera of humans in West Africa.

Wesselsbron

Wesselsbron is another member of the flaviviruses. The virus was first isolated by Weiss et al_, 1956 from a lamb during an epidemic in the Wessels¬ bron district of South Africa. In 1957 Smithburn at a_l, reported an isola¬ tion of a strain of the Wesselsbron virus from a febrile man in Tongaland,

South Africa. Serological surveys for the presence of neutralizing anti¬ bodies in human sera indicate that the virus might be prevalent in Botswana,

Caprivi and Angola (Kokernot et al, 1965a, 1965b). Surveys among humans using

the HI techniques reveal the presence of antibodies to Wesselsbron in Senegal

(Brfes, 1970) and Nigeria (Casals, 1966) but in very low proportions.

However, the virus is present in West Africa and has been isolated from

a camel in Nigeria, and from several mosquito species in the Cameroun (Salaun

et al, 1969).

West Nile

West Nile virus, a member of the flaviviruses, was first isolated in

1937 from the blood of a febrile woman in the West Nile District of Uganda

-28-

(Smithburn ert al, 1940). In addition there had been other isolations from humans in South Africa (Kokernot and McIntosh, 1959), Egypt (Mel- nick et^ al, 1951), Zaire (Lucasse, 1963).

Neutralization studies have also indicated a high proportion of sera with antibodies to West Nile virus in Africa (Smithburn and Jacobs,

1942; Kokernot eL al, 1956). In Nigeria Macnamara jit al, (1959) and

Boorman and Draper (1968) have reported on presence of antibodies to

West Nile virus among humans by neutralization tests. Other serological surveys using HI techniques have also suggested that antibodies to this virus are widespread in Senegal (Bres ejt al, 1963), Mali (Brbs, 1970),

Upper Volta (Bres ert al, 1965), Ivory Coast (Robin ejt al, 1968), Togo- land (Bres, 1970) and Nigeria (RFVL-NY, Ann. Rep., 1961; Casals, 1966;

Monath ejt al, 1974; Fagbami and Fabiyi, 1975). Fabiyi (1961) reported a prevalence of complement-fixation antibodies to West Nile virus in Tema,

Ghana and found the same proportion of positives as in the other West

African countries. HI tests done on sera sent to the RFVL-NY (1961) also revealed the possible presence of antibodies to this virus in Ghana.

In a study carried out by Taylor ejt al (1951) in Egypt the main vec¬ tor of West Nile was found to be the mosquito CL univittatus which is pre¬ sumably a bird feeder. This finding from Egypt plus the fact that virus

isolations have been obtained from birds in Nigeria (Causey et_ jrl, 1969) and South Africa (Kokernot and McIntosh, 1959) suggests that birds may be of importance in maintaining virus cycles in nature.

Other isolations of West Nile have been obtained in Nigeria from

sentinel mice (Causey et al, 1969). Neutralization tests have also re¬ vealed that the virus may prevail among wild animals in Nigeria (Causey

et al, 1969).

-29-

Yellow Fever

Yellow fever virus, the causative agent of yellow fever is a flavivirus.

Although the disease has been reported for several centuries in

West Africa, its epidemiology remained obscure until 1881 when Carlos

Finlay, a Cuban, speculated in a paper that the disease was probably transmitted by the mosquito (Haddow, 1968). It was not, however,till the investigations carried out by the United States Army Yellow Fever

Commission in 1900 in Cuba that such a vector was found. The mosquito,

Aedes aegypti, was involved in a man-mosquito-man cycle.(Reed et_ al,

1900). Many years later several workers in Africa, notably Bauer (1928), and Kerr (1932) showed that under laboratory conditions a substantial number of African mosquitoes other than A. aegypti could transmit the virus by bite. This finding suggested a more complex epidemiology than the simple man - A. aegypti - man cycle (Strode, 1951). However, in West Africa the position of this mosquito in yellow fever epidemiology was the more emphasized by virus isolations from A. aegypti captured at

Ife, Nigeria (Beeuwkes and Haynes, 1931) and at Ogbomosho, Nigeria (Taylor,

1951). Further eludication of the epidemiology of yellow fever came from

East Africa where much of the work was concentrated following the estab¬

lishment by the Rockefeller Foundation of the Yellow Fever Research In¬

stitute (later the East African Virus Research Institute) in 1936. Through

the diligent work of the Institute, an isolation of a strain of yellow

fever virus was obtained from Aedes simpsoni captured from Bwamba County

in Uganda (Mahaffy _et _al, 1942). Subsequent studies revealed that A.

simpsoni was involved in transmission of the virus from monkey to man.

Thus, the existence of a vector distinct from A. aegypti was established.

-30-

Work done at the same time revealed a widespread immunity to the yellow fever virus among monkeys found in Semliki Forest, Uganda. This finding raised the question of a sylvan vector. (Haddow et_ aJ, 1947). In 1949

Smithburn _et_ al,were able to isolate a strain of yellow fever virus from

Aedes africanus caught in Semliki Forest during an outbreak of sylvan yellow fever, and to prove A. africanus as a principal vector. Also A. africanus was also found to form a link between the infections of animals and birds of the forest's canopy and those species, including man, which frequent the forest floor (Haddow and Ssenkubuge, 1965).

Two epidemiological patterns of yellow fever emerge in Africa:

There is an urban, man-mosquito-man cycle usually involving Aedes aegyptiy and jungle or sylvan, involving forest vertebrates, usually if not exclu¬ sively primates, and Aedes africanus. Man may be tangentially infected from the sylvan cycle. Aedes simpsoni^common in plantation areas^is im¬ portant in bridging the gap between the jungle and the city.

The first isolation of the virus was achieved by Stokes et al (1928) from the sera of a man, called Asibi, who was bled in the field at ,

Ghana, by Mahaffy. Subsequent surveys by Beeuwkes et_ al (1930) using rhesus monkey protection tests and Beeuwkes and Mahaffy (1934) using mouse protection tests, showed a high proportion of people with antibodies to yellow fever virus in Nigeria, Ghana, Sierra Leone, Gambia, Liberia,

Dahomey, Niger and Sudan.

Since these surveys, intensive immunization programs, especially in the Francophone countries, have decreased the incidence of yellow fever in

these locations. The disease, however, persists, and sylvan yellow fever

is reported almost every year in West Africa (Table 2). "There is no

doubt that cases of jungle yellow fever occur more frequently than are

Yellow Fever Cases Notified During Period 1960-1975, West Africa M 3 O 3 4-1 Ov X o cx 33 'S 3 60 3 33 3 e e O Pi C 3 3 m 3 u 3 O o 6 3 3 rH 3 1^. Or rH 3 • H • r* • 3 • CO • r-~ • (T> •> CO • 03 r-r to w rH I Eh HlcTv •> rr. -cr < Pi M 3 3 CX CX O 3 3 3 3 T—I hl rH J-4 60 u 3 Eh 3 > 3 o 3 Eh > 3 3 3 3 3 X 33 ■H X 4-> Jh 60 3 3 S 3 3 3 3

-32-

diagnosed and the risk of epidemics is fairly large." (Wkly. Epidem.

Rec. 1973). So occasionally where the conditions are optimal, that is,

a monkey population large enough to support the transmission of the

virus, a susceptible human population and a suitable vector, there

have been yellow fever epidemics. Such an epidemic has been reported

for Ethiopia where from 1960 to 1962, the largest epidemic ever re¬

corded in Africa occurred. The number of cases were estimated to be

over 200,000 with 30,000 deaths (Berdonneau et^ a_l, 1961; Sdrid et_ al,

1964). In West Africa there was an epidemic in Senegal during 1965

and the number of cases were variously estimated at 2,000-20,000 with

15% mortality (Bres, 1966; Chambon et al, 1967). A moderately large

outbreak of yellow fever occurred in 1969 in the Upper Volta, 87 cases were reported and out of these there were 44 deaths (Wld. Hlth. Org.

Rep. Ser. No. 479,1971). A second epidemic was reported that year

from the Jos Plateau in Nigeria. There were 55 cases confirmed and

in 15 of these the virus was isolated (Carey et al, 1972). In 1970

an outbreak was reported from the Okwoga District, Benue Plateau

States, Nigeria, where there was an estimated 786 cases with 15-40

deaths (Monath ej: al, 1973a, 1973b).

In Ghana, recent yellow fever vaccination statistics (Table 3)

reveal that a large number of the population remain unvaccinated(Ghana

Monthly Epidem. Bull., March 1971). Several outbreaks of the disease

have been reported. One epidemic occurred at Pong-Tamale in the Upper

Region during 1969, and involved 303 people; 12 of these cases were

confirmed by laboratory investigations. Overall there were 72 deaths.

A smaller outbreak involving 12 cases was reported from the Eastern

Region in 1970. All the cases were confirmed and there were 7 deaths

(Ghana Monthly Epidem. Bull., March 1971).

Yellow Fever Vaccination In Ghana, 1969-1970 -3

1970 Population Census. Adapted from Ghana Monthly Epidem. Bull. March, 1971.

-34-

Interestingly,the outbreak in Senegal and the Upper Volta occurred despite the high level, 86% and 75% respectively, of immunity to yellow fever that has been reported for these countries (Bres et_ aJL, 1963; 1965).

It is possible that in Diourbel, Senegal, and the South East Central part of Upper Volta where the epidemics took place the proportion of population vaccinated was low. Elsewhere in West Africa pre-existing flavivirus immunity does not seem to protect against yellow fever:

Monath e£ aj. (1973c) worked on sera collected from Okwoga District,

Nigeria, before the 1970 epidemic, and found that flaviviruses, especially dengue and Zika, were very active prior to the outbreak.

HI studies show that most of the Francophone countries of West

Africa (Mali, Upper Volta, Ivory Coast, Dahomey, Togoland, and the

Camerouns) have a high level of antibodies to yellow fever (Bres e_t al,

1963; 1965; Robin jat a_l, 1968; Br^s, 1970; Boche e_t al, 1974). Similarly, in Nigeria several studies done on HI antibodies revealed a high percent¬ age of positives to the yellow fever virus among people in the Jos

Plateau (Monath ejt aJ., 1973a, 1973b), Benue Plateau (Carey et_ al, 1972) and the Nupeko Forest (Monath aJL, 1974). It must be stressed that studies done in Jos and Benue Plateaus were executed on sera collected after outbreaks of yellow fever in 1969 and 1970 respectively, and may not give an accurate immunity status of the whole of Nigeria.

Zika

This virus is a flavivirus. It was first isolated' in 1947 from the

sera of a sentinel monkey in the Zika Forest, Uganda (Dick et^ aJ, 1952).

Since then several isolations of the virus have been obtained from the mosquito Aedes africanus caught in Zika Forest (Haddow et_ ajL, 1962).

-35-

Elsewhere in Africa the virus has been isolated from A. luteocephalus

and other Aedes species (UIARP Ann. Rep. 1969).

Neutralization studies in Uganda (Dick ej^ al, 1952; Smithburn,

1952), Tanzania (Smithburn, 1952) and Nigeria (Macnamara et al,1959)

suggested that the virus may cause disease in man. Confirmation that

this indeed is the case have been obtained with the isolation of the

virus from man in Senegal (Simpson, 1964), Uganda (Simpson, 1964) and

Nigeria (UIARP Ann. Rep., 1969).The results of serological surveys

using HI techniques in Senegal (Bres et al, 1963),Upper Volta (Bres

et^ al., 1965), Ivory Coast (Robin et_ al, 1968), Ghana (RFVL-NY Ann.Rep.,

1961), Nigeria (RFVL-NY, Ann. Rep.,1961; Casals, 1966; Monath et al,

1973a, 1974), and Camerouns (RFVL-NY, Ann. Rep., 1961; Boche et al,

1974) indicate that Zika may cause disease in humans in many countries

in West Africa.

Perhaps, also, the fact that Zika infects monkeys (Dick et al,

1952; Bres, 1970) and shares a common vector, A. africanus with yellow

fever (Smithburn e_t al, 1949; Haddow, 1962) may mean that the respective

epidemiologies of these viruses in the forest share similarities.

Bunyaviruses

Members of this group are characterized predominantly by similari¬

ties during Complement-Fixation (CF) studies. (Casals and Whitman,1960).

Four of the viruses from this group: Birao, bunyamwera, Germiston and

Ilesha are found in Africa and have all been isolated from mosquitoes

(Theiler and Downs, 1973). Furthermore, human infections confirmed by

virus isolation, have been reported for bunyamwera and Ilesha.(Berge,

1975).

-36-

Bunyamwera

The first isolation of this virus was achieved by Smithburn _et_ _al

(1946) from a mixed pool of Aedes mosquitoes captured in Semliki Forest,

Uganda. Subsequently, a second strain was isolated from Aedes circum-

luteolus caught in Tongaland, South Africa in 1955. (Kokernot et_ al,

1957). Since then several isolations of bunyamwera from various mos¬ quito-species have been made from Aedes species in the Cameroun (Brottes ejt a_l, 1966), from Culex species in Central African Republic (Inst.

Pasteur-Bangui, Ann. Report, 1969) from Mansonia africana in Nigeria

(Boorman and Draper, 1968) and M. uniformis in Kenya (EAVRI, Ann. Rep.

1971).

In 1958 Kokernot et al reported the first isolation of the virus

from a naturally infected human in Tongaland, South Africa. Five years

later Bearcroft jet ail (1963) reported the isolation of strain of bunyam¬ wera in Nigeria, from the sera of an adult male with mild febrile illness

at Yaba near Lagos.

Serological surveys have indicated that antibodies to this virus are widespread in human populations in Africa. Antibodies in human sera cap¬

able of neutralizing the virus have been found in Uganda (Smithburn et_ al,

1946), South Africa (Kokernot et al, 1958), and Nigeria (Macnamara et al,

1959).

In West Africa serological surveys utilizing HI techniques have re¬

vealed a high proportion of sera with antibodies to bunyamwera virus in

the populations of the various countries: HI antibodies have been re¬

ported in Senegal (Bres _et_ al, 1965) . Ivory Coast (Robin et_ al, 1968) ,

Togoland (Bres, 1970) and Nigeria (RFVL-NY, 1961).

-37-

Very little is known of the epidemiology of this virus and it is unclear how the virus is maintained in nature (Theiler and Downs, 1973).

The possibility of involvement of monkeys in such a maintenance is offered by the report of workers at Inst. Pasteur-Bangui (1961) of pre¬ sence of neutralizing antibodies for bunyamwera virus among chimpanzees in the Congo.

Ilesha

In 1957 a virus was isolated from the sera of a nine year old febrile girl by Morley at Yaba, Nigeria (West African Council for

Medical Research, Ann. Rep. 1957). This virus was subsequently shown to be belong to the Bunyaviruses through work of Okuno

(1961). The virus, Ilesha, has since been isolated from man in Uganda

(EAVRI Report, 1961-1962), Cameroun (Salaun et^ ai, 1968), Central

African Republic (Inst. Pasteur-Bangui, Ann. Rep.,1969-1970) and

Senegal (Inst. Pasteur-Dakar, Ann. Rep., 1969-1970). An isolation of the virus has been achieved from the mosquito. Anopheles gambiae, captured in the Central African Republic (Inst. Pasteur-Bangui Ann.

Rep., 1969-1970) .

From the results of HI studies, infections of man by Ilesha may be presumed to occur in Liberia (RFVL-NY Ann. Rep., 1961), Ghana

(RFVL-NY Ann. Rep., 1961) and in Nigeria (RFVL-NY Ann. Rep., 1961;

Casals, 1966). Further support for the possibility of infection in man of this virus in Ghana has been given with a serological survey using

CF techniques on sera from Tema, Ghana (Fabiyi, 1961).

-38-

MATERIAL AND METHODS

Field Methods.

The months of June, July and August, 1975 were spent collecting blood samples from various towns in Ghana.

Areas included in the survey were chosen randomly to represent not only vegetational, climatic and population size variations but also administrative regions and indeed most representative parts of

the country were sampled. The only limitation was the availability

of a hospital or health center in the survey locality. Human blood

specimen were obtained by venipuncture from patients presenting at

out-patients department of government hospitals, mission hospitals

and government health centers. As was expected permission from sub¬

jects to be bled was difficult to get. This problem was circumvented

by allowing the surveyor to act as a member of the medical team in

some of the localities he visited. In this manner individuals were

bled as part of their medical work-up.

The blood samples were allowed to stand at room temperature for

two hours and then stored in insulated styrofoam boxes, cooled by

frozen "cold dog" cans, overnight. Next morning the sera were pipetted

into culture tubes and the tubes were stored back in the styrofoam

boxes. In the majority of cases the sera were put into freezers at -20°C

three to four days after they were taken. The entire collection was kept

at ~20°C until an hour before it was flown to the United States of America

in well insulated styrofoam boxes without added ice. At Kennedy Airport,

New York, the sera were refrigerated until delivered to Yale Arbovirus

Research Unit four days after their arrival in New York.

-39-

Characteristics of Sample

Geographic Distribution.

Figure 7 is a map of Ghana with boxed towns indicating locations where sera were obtained and the number of samples collected at each

location are shown in Table 4. Distribution of the collections by

population size is given in Table 5. Since population size does not

always indicate the urban or rural nature of a town in Ghana, this

distinction has been omitted. However, "semi--rural" would probably be

a fair characterization of the majority of locations; most distinctions would be between "semi-rural" and "rural" rather than between "semi-

rural" and "urban." In all cases attempt was made to bleed individuals who have resided in a locality for more than five years.

Age Distribution.

Overall 1439 subjects ranging from age 10 to 79 years were bled.

Children below the age of 10 were excluded because venipuncture needles

and tubes used in the study were deemed inappropriate for blood collec¬

tion in this age group. The distribution of samples collected by age

group is shown in Table 6. The age range 20 to 29 was the largest

single group with 535 (37%) of the total collection.

Sex Distribution.

Seven hundred and forty-five (51%) of the 1439 subjects were males.

Vaccination Status.

Subjects usually could not give history of yellow fever vaccinations.

However, Table 3 gives a picture of yellow fever vaccination in Ghana at

40

Figure 7

RfEMfNCE

’■ ' I R«|k>««J H«»dqu«Man Dt»tr.ci A Sub-0ct

«lWl oVonf\. In -

NO I €

[oAdoyirf o^* Sr> _ jyi f4 SoT.T^i LurjNj"g

twm-

[lO'Ofcor <*Nufton Koglfn»

Mtfndc' [Crp-.s.

ToieniipeV _ Wa^gov '•Plompo/ -<»doJkp*- ,Mpa)vl SAC'T’bj^

’/ Su,nf KponnoJ

Taoficnc

aN(W'

, A/X>*^3■.Ol'lluo Trooar<$ KertyOM Nlotrtnoo} ju^rono'1 \Mun« Hi m non j

^‘urcaio ^ibwni Ax/J1 A/’Ktrr?,

rObuaji Ju inro**bfa

Asar^jni

GHANA

2 000

-41-

Table 4

Geographic Distribution of Human Sera Collected from Ghana,

June - September, 1975

Region Town No. of sera collected

Eastern Koforidua (KOF) 30 Nkawkaw (NKK) 30 Akim - Oda (A-0) 40 Akuse (AKU) 40

Western Ainyinase (AIN) 20 Tarkwa (TWA) 40 Wassa-Akropong (W-A) 24 Asankrangwa (ASA) 35 Sefwi- (S-W) 39

Brong-Ahafo Sunyani (SUN) 30 Dormaa-Ahenkro (D-A) 40 (GSO) 48 (ATE) 35 Kintampo (KIN) 48

Ashanti (NYI) 25 Ofinso (OFI) 32 Agogo (AGO) 47 Ashanti-Mampong (AS-MA) 45 Ejura (EJA) 35 (BEK) 47

Northern (SAL) 32 Savelugu (SGU) 35 Yendi (YEN) 42 (NAL) 48

Upper (DAM) 30 Bawku (BAW) 40 Navrongo (NAV) 48 Tumu (TUM) 30 Jirapa (JIR) 48 Wa (WA ) 32

Central Dunkwa-On-Ofin (DKA) 44 Cape Coast (C-C) 48 Winneba (WIN) 40

Volta Ho (HO ) 48 Hohoe (HOH) 48 Worawora (WOR) 48 (ADI) 48

TOTALS 1439

-42-

Table 5

Distribution of Sera according to population size of sampling towns

Population of sampling Towns Samples

No. Percent

<5,000 354 25

5,000 - 10,000 390 27

10,000 - 20,000 306 22

>20,000 380 26

-43-

Table 6

Age distribution of samples of Ghanaian population

Age No. in group Percent

10 - 19 348 24

20 - 29 535 37

30 - 39 312 22

40 - 49 173 12

>50 65 5

-44-

the immediate past. Seven percent of the population were vaccinated

by 1970, and these were concentrated solely in Accra, Eastern, Northern,

and Upper Regions. There have been prior yellow fever vaccination cam¬

paigns in Ghana but data were not available. Due to aggressive vacci¬

nation programs over the past years, the majority of the Ghanaian pop¬

ulation have been vaccinated against small pox. Measles vaccination

programs have been instituted and is at the moment concentrated on the

children population. Polio vaccination is also in progress, and avail¬

able data indicate that only a small fraction of the population is vac¬

cinated.

Laboratory Methods.

For this initial serological survey of Ghana 216 (40%) of the

samples from the age range 20 to 29 were tested. The 216 sera was made up of representative samples from every locality included in the

survey. This age range was chosen because it was felt that they would

have had to considerable "exposure" to arboviruses and adequately serve

to give some indication of the prevalence of antibodies to the arbo¬

viruses in the Ghanaian population.

Hemagglutination-inhibition (HI) tests were carried out on the 216

sera by the methods of Clarke and Casals (1958). As a screening pro¬

cedure all sera were first tested in dilution of 1:10 and 1:20 against

antigens of various members of the arboviruses. Sera that inhibited

agglutination of these dilutions were then tested at a dilution of 1:40

and 1:80. The antigens used in dilutions equivalent to four to eight

units as listed in Table 7.

Virus antigens used in HI testing: Serological Survey, Ghana, 1975 <44 X d 4-1 x o O o d X cO d d X O a, 5-4 m 3 3 0s** -H X X X X X CO d * 3 d 3 X, CO 3 • • X *H •H •H z X rH X X >4-4 4-1 rH )-i cn cn ON 1-t X 00 CO 0) c 4-1 CO d r—1 •H w o co cr o 0) a 3 X •H < -d W 4J 3 co d X X cn a CJ 4J co 0) d o 5-4 o a d • #» CO o cO o d 54 00 On CO (4 00 a CO CO • X > 3 CO a • • X •H X cn *H X X z X rH X X X X 4-1 oo cO X co *H X SC 54 (0 (U d CU 4J 00 d rH r—i X X CO d 0 Ph PC Q o a X cO CU c 54 9 * cO o cu CD co CO X CO CO CO s cO • > > 3 00 01 d 01 3 i -45 rH X cn *H •H X X z X X ■H 4-J X 00 CO rH X X cu X X CO G X •U 00 CO 0) X X X cu G •H o rH X o cu CO CO d X cn X d co X X 3 N • A CO 0) 3 o > • oo 3 3 > 3 3 G X rH •H X X X •H •H X X z X •H X u o <-3 o CO rH X X X 4-1 *H X o o d r^. X O a rH -d < • r\ CO 13 cn d •H x cn 3 o cu PC PH rH X cn oo X 3 d rH X 0) X 3 e • o d z X • a cu 3 3 > 3 3 3 c 3 3 3 3 • • X o 3 X 3 > 3 X 3 3 rH X Z 3 -d X X P3 X X 00 3 3 • « O 3 d o 3 C a 3 3 00 3 3 c 3 C • cn rH X rH pH X >4 Ph X X 33 rH X 3 X > M-) d c •H > 3 > 3 3 o s 3 3 3 X X s X X e> -d X 3 X O 3 • « X 3 3 3 a d 5 3 3 3 d 3 • X rH *H •H X Ph Xi N X rH X cn X 3 X 3 > > •H 3 3 •H rH X z X -d X X 00 3 u 3 3 3 OO X 3 d d 3 3 d • »\ 3 o d 3 o 3 e 3 d oo 3 3 d • rH X X X o w PQ X 3 X 3 oo d X 3 >N 3 > 3 a d 3 •H d On 3 3 •H *H 3 X X z X X X X X oo 3 • A 3 3 d 3 o 3 oo 3 3 c • — rH X CN cn X o X z CJ rH X PQ rH •H H X •H -d X •H 00 3 3 z X X O 3 3 d 3 X 3 X a 3 d d tn > 3 o a 3 3 c X 3 3 3 3 o 3 o 3 3 d • f> X a 3 d 00 X 3 o 3 3 3 •

-46-

RESULTS

Of 216 sera tested against 11 viruses in group alphavirus, flavi- virus and bunyavirus, 176 (81%) were positive for one of more of the viruses, and 40 (19%) did not show positive reaction to any of the viruses (Table 8).

The positive sera were further interpreted on the basis of the

following criteria. Within each of the three antigenic groups a posi¬

tive serum was reported as giving one of three types of reaction.

i. Specific: A reaction was considered specific for an antigen when

the titer of the serum against this antigen was fourfold, or more,

greater than against any of the other antigens of the group included

in the survey.

ii. Superinfection: This type of reaction obtains when the titers

of a serum were the same with two or more antigens of a group (or the

difference in titer was no greater than two-fold) and these titers

were 1:40 or higher.

iii. Undiagnosable: A reaction was considered undiagnosable when the

serum reacted with one antigen only but with a titer of 1:10; or with

more than one antigen with a maximum titer of 1:20.

The above criteria does not necessarily indicate infection with

the designated viruses, it is possible that a related virus, known or

unknown, not included in the survey may have infected the individual.

Alphaviruses.

Chikungunya and Sindbis are the two members of this group against

which sera were tested in this study.

-47-

3 3 • 3 > i—i a •H w 43 •H 44 M •H <4-4 •H CO iH 3 X 3 CJ O •H 3 o 3 CN i—l i—i CN CN cn 00 CN CO Cu 33 0) cu Cu T—i 3 S CO co 1—1 O 3 o 3 N—' rH CU 5 u Cu CO 3 < T3 3 3 •H '—x 3 rH •H cO 3 cu cO 43 33 >N o > 3 3 cO 0 3 3 CU cu 3 3 • 3 43 43 3 i—! 43 I—1 pH 3 CO 3 Q) O •H 00 CO 1 CO •H 3 3 3 s 3 4-1 3 •H 0) i—l Z 3 g 3 3 > CU 3 3 43 3 a) o 3 43 •H c CO 4* 33 00 CO 44 1—1 3 >. 3 > 44 cO CO •H C 3 CO CO 1—1 44 3 cU 3 •H •H 3 3 43 •H 3 CU CU 3 3 i-H >1 3 CO 3 o U co Q 13 3 >-< CN m M 3 O 3 •H >4-1 3 Oh cO > pa 4= l—1 O 33 CN 3 no cn cn 00 NO 3 3 3 3 3 3 3 3 3 H <4-4 a m-i O o 4-4 O o <4-1 O 3 Ih’I O •H C 3 •H 3 3 •H 3 3 > 3 C <4-4 -H oo <4-4 •H oo 4-4 •H 00 •H 3 o on 3 •H 3 3 •H 3 3 •H 3 3 44 PC •H CN a CJ 3 •H 3 3 •H 3 3 •H •H W I >-> 3 0- 33 3 CU 33 3 cu 33 CO -a 00 •H O H Cu 3 3 CU 3 3 CU 3 3 o 3 JO cn CO CO 33 CO CO 3) CO CO 33 cu 3 0) •H 1 1—1 43 CO o •H 42 3 a) ON > cO M 00 3 H 3 3 t-H •H o 3 -H s a 3 3 3 > •H > > O •H 3 3 •H 3 > 3 CO O 43 > 3 O 3 a 3 3 •H cu 3 rH rH 3 •H < PH PQ 3 NO > 3 O 3 3 43 5 •H 3 < 3 3 3 3 <4H 3 3 O 3 3 3 3 CO •H •H > > •H 3 3 > >N CO cO 3 3 3 a i—1 3 ed cO O PH PC a) > 1 1 •H 3 •H 4-1 43 > iH CO cu 3 CO 00 r—1 i—1 o 3 < pH 34 2 cO

-48-

One hundred and fifty-four (71%) of the 216 sera were positive for

the alphaviruses. There were 113 specific reactions of which 112 were

due to chikungunya and one to Sindbis.

Analysis of the alphavirus positive reactors by population size

annual rainfall and vegetation are shown in Tables 9, 10, and 11 re¬

spectively. While there existed no clear relationship between population

size and alphavirus positive reactors, the savannah had a higher propor¬

tion (83%) of reactors than the forest (60%), and areas with rainfall below 50 inches showed greater number of positives than the areas with

precipitation above 50 inches. Table 12 shows the geographic distribu¬

tions of positive reactors and indicates that prevalence of antibodies

to alphaviruses is highest in the Northern region which is also the

driest. All the 30 sera tested from this region were positive.

Flaviviruses.

The flaviviruses dengue-1, Uganda S, Wesselsbron, West Nile, yellow

fever and Zika were the antigens used from this group.

Fewer number of sera were positive to the flaviviruses than to the

alphaviruses. One hundred and twenty-four (57%) of the original 216

sera were positive to antigens to this group. Of the 124 positive

reactors, eight gave specific reaction with Zika, three with yellow

fever, two each with West Nile and Wesselsbron, and one with dengue-1.

As in the case with the alphaviruses, flavivirus positive reactors

prevail in the savannah (80%) over the forest (32%) areas and regions

with annual precipitation below 50 inches shows more positive reactors

(81%) as compared to areas above 50 inches (22-44%). There was no cor¬

relation between positives and population size and the Upper Region had

a higher proportion (87%) of flavivirus reactors.

-49-

Table 9

Arbovirus HI reactors by population of towns

| Population of No. Positives | Sampling towns Tested Alphav iruses Flaviviruses Bunyaviruses i

No. % No. % No. %

<5,000 53 44 83 33 62 16 30

5,000-10,000 61 46 75 37 61 9 15

10,000-20,000 42 24 57 12 29 13 31

<20,000 60 40 67 34 57 9 15

— ■

Table 10

Arbovirus HI reactors by annual rainfall

Annual No. Positives rainfall Tested Alphaviruses Flaviviruses Bunyaviruses | (in inches) 1

No. % No. % No. % 1 17 <50 84 71 84 68 81 14

50 - 60 83 52 62 37 44 22 26

60 49 29 59 13 22 12 24

-50-

Table 11

Arbovirus HI reactors by vegetation zone

Positives Vegetation No. _ zone Tested Alphaviruses Flaviviruses Bunyaviruses

No. % | No. % No. 7 ■ i 00 U) 00 Savannah 102 85 o 78 14 14 woodland

High 114 69 60 37 32 31 27 Forest i

-51-

Table 12 Geographical Distribution of HI arbovirus reactors

Positives No. Regions Tested I ! Alphaviruses Flaviviruses Bunyaviruses _ No. % No. % No. %

Ashanti 35 23 66 10 28 11 31

Brong-Ahafo 30 17 57 13 43 6 20

Central 18 9 50 7 39 3 17

Eastern 24 16 67 9 37 3 13

Northern 30 30 100 26 87 3 10

Upper 30 26 87 29 98 6 20

19 79 17 70 8 33 Volta 24 !

Western 25 14 56 8 32 7 28 j |

Bunyaviruses.

This group had the lowest number of positive reactors. Forty-seven

(22%) of 216 sera reacted to group antigens and eight of these gave specific reactions to Ilesha and two to bunyamwera. A greater proportion of undiagnosable reactions were obtained in this group.

Unlike the two previous groups there were more positive reactors to bunyavirus antigens in the forest (31%) than in the savannah (14%), and in areas of high annual rainfall than those of low rainfall. There was no trend evident in relating positives to population group size. Most of the positives to this group came from the Ashanti and Volta Regions.

Appendix I summarizes the results by administrative regions, towns, population size, annual rainfall and vegetation type.

DISCUSSION

The findings in this serological survey of Ghana suggest that there is considerable alphavirus, flavivirus and bunyavirus activity in this country.

Alphaviruses.

One hundred and fifty four (71%) of the 216 sera in this investigation revealed positive reaction to the alphavirus. Similar findings were re¬ ported by the RFVL-NY in 1961. Working on 60 sera collected from Sekondi,

Kintampo and Tamale they found 73% positive reactors to the alphaviruses.

Casals (1966) reported a 90% HI positive reactors to the alphaviruses

among 351 sera from the Benue-Plateau State, Nigeria. Another study re¬

ported from Nigeria by Monath e_t aT (1974) gives 74% alphavirus positives

in their investigation of human hosts in Nupeko Forest.

-53-

In this present study there were 112 (52%) specific reactions to chikungunya and one to Sindbis. Chikungunya was first isolated during an outbreak of febrile illness at Newala district, Tanzania in 1952

(Ross, 1956). In West Africa this virus has been isolated in Ibadan,

Nigeria, from sera collected from patients seen during another febrile epidemic in 1969 (Moore _et a_l, 1974). Although no isolation has been made in Ghana, chikungunya infections are known to be frequent in the eastern and western sections of Nigeria (Boorman e_t a_l, 1968) . Tomori

(1976) have described a 1974 outbreak of chikungunya among children in

Ibadan during which ckikungunya isolations were made and concluded after examination of the characteristics of this and other outbreaks that chikungunya epidemics occur in five year cycles. The areas just mentioned in Nigeria share identical geographical, vegetational and climatic conditions with Ghana. As was indicated previously in the presentation of the results of this study, there is no absolute cer¬ tainty that the alphavirus infections were specifically caused by chikungunya. Further, the work of Casals in Nigeria revealed that there were only 2% specific reactions due to chikungunya as compared to 70% specific reactions to o’nyong-nyong. This finding underscores the fact that other alphaviruses not included in this present study may be in¬ volved. However, of the alphaviruses only three, chikungunya, o’nyong- nyong and Sindbis have been isolated from man in Africa (Theiler and

Downs, 1973; Berge, 1975). With regard to the Casals’ findings, chikun¬

gunya and o’nyong-nyong are very closely related and HI studies may give

identical results for both viruses (Bres et 1965). Since o'nyong- nyong has not been isolated as yet in West Africa and seems up to this

time to be restricted to East Africa, it can be speculated that the

-54-

chikungunya specific reactions in this study may well be caused by this virus. However, an emphatic statement on this point cannot be made.

And indeed Davis in a thesis presented to the Yale University School of

Medicine (1971) indicated that another virus isolated from Nigeria,

Igbo-Ora, is closely related to chikungunya. He suggested that o'nyong- nyong and Igbo-Ora may be substrains of chikungunya.

Sindbis is the other virus studied from the alphavirus group. This virus was first isolated in Egypt from a mosquito (Taylor e_t aJL, 1955).

Isolations from man have been obtained in Uganda (EAVRI Ann. Rep. 1961-

1962) and South Africa (Strickland-Chomley, 1963). The only West

African isolation has been from a sentinel mouse in Nigeria. Serologi¬

cal studies have disclosed comparatively low level prevalence of HI

antibodies in West Africa (Bres e_t

Monath el: _al, 1974; Fagbami and Fabiyi, 1975). This present investiga¬

tion reveals only one specific reaction to Sindbis of 216 sera. Generally,

this virus was involved in only a limited number of the alphavirus posi¬

tive reactors.

Flaviviruses.

The six flaviviruses used in this study were dengue-1, Uganda S,

Wesselsbron, West Nile, yellow fever and Zika. There were less HI posi¬

tive reactors to this group than to the alphaviruses. Of the 216 sera,

124 (57%) were positive to the flavivirus antigens as compared to 154

of 216 (81%) to the alphaviruses. Results from other West African

surveys are similar to those results for flaviviruses in this study.

Casals (1966) in his study of 351 sera from the Benue-Plateau State,

Nigeria, found 56% positive HI reactions to flaviviruses. A somewhat

-55-

larger proportion (84%) flavivirus positives was obtained by Monath and his associates (1974) during the investigation carried out in

Nupeko Forest. Similar proportions of flavivirus positives have been reported in Senegal (Bres £t ad., 1963), Ivory Coast (Robin

Upper Volta (Br\s ej: ad, 1965) and Togoland (Bres, 1970).

The remarkable characteristic of the flavivirus reactors is the high proportion of superinfection (76%) among those positive. Using identical criteria to analyze the results of his Nigerian studies as used in this investigation, Casals (1966) reported a 42% superinfection among the adult group. Superinfection can be caused by one virus in¬ fecting an individual more than once or by several viruses within a group at different times. This implication of superinfection coupled with the high incidence cross-reactivity within the flavivirus group make the interpretation of these superinfection results difficult. A safe conjecture in view of the multiplicity of the different flavivirus isolated in West Africa, is that those individuals showing superinfection type of reaction were generally infected by different viruses within the

flavivirus group. It should be stressed here that Zika was found to be

involved in most of the superinfections. Thus, as suggested by Macnamara

et ad (1959) Zika antibodies may have wider overlap in their antibody

than other agents and their antibodies.

Somewhat more definate statement can be made for sera specific for

particular viruses. Overall there were 16 sera for the flaviviruses,

eight for Zika, three for yellow fever, two for Wesselsbron, two for

West Nile and one for dengue-1.

Zika was first isolated in Uganda, East Africa. In West Africa the

virus has been isolated from man in Senegal (Simpson, 1964) and Nigeria

-56-

(UIARP Ann. Rep., 1969). Other serological evidence using neutralization tests in Nigeria (Macnamara e_t al_, 1959). HI techniques in Senegal (Br^s et aT, 1963), Ivory Coast (Robin et al, 1965), Upper Volta (Bres et al,

1965), Togoland (Br^s, 1970) and Ghana (RFVL-NY Ann. Rep., 1961) indicate that antibodies to this virus may be widespread.

The results quoted previously for specific Zika HI positive reactors in this survey is similar to that reported by Casals in his study of

Nigerian sera. In his investigation the majority of the specific infec¬ tions, 35 of 49 (71%), among the adult population were to Zika.

The next antigen with most specific reactors was yellow fever with three of 16 specific reactors. Theiler and Downs (1973) conclude on work done on sera from West Africa at the RFVL-NY, that only in rela¬ tively few cases could they make a diagnosis of a specific infecting virus from the HI pattern. Most specific infections came from children or from adults in places where the overall flavivirus incidence was low.

The results of this study underscores this contention.

The first isolation of the yellow fever virus from man came from the blood of a Ghanaian, Asibi, at Kpeve, Ghana (Stoke et_ aT, 1928).

Antibodies to the viruswere shown subsequently to be prevalent in West

Africa through the work of Beeuwkes et^ al (1930) and Beeuwkes and Mahaffy

(1934). With the introduction of the yellow fever vaccine, perfected largely through the work of Theiler and Smith (Theiler, 1951), some of

the populations in West Africa were vaccinated during the 1940's and

1950's. The lack of followup of such vaccination programs after the

initial problem has been contained means than an increasing proportion

of the population which is being born remain unvaccinated and therefore

susceptible to the disease. Recent reports of epidemics from West Africa

-57-

indicate that this may indeed be the case. In their investigation of the epidemic at Diourbel in 1961, Bres and his co-workers (1965) found a large proportion of the inhabitants of the Diourbel region were unvaccinated and thus did not posses protecting antibodies to yellow fever.

In the past there were few fatal cases reported among Africans from West Africa (Theiler and Downs, 1973). The speculation was that the high incidence of antibodies against the flaviviruses in the West

African population was responsible for this salutary state of affairs.

However, recent reports from Nigeria by Monath et^ al (1973c) indicate

that the 1970 epidemic in Okwoga, in which there were many fatali-

ties> had occurred even though there had been a high dengue, Zika and

Wesselsbron activity prior to this outbreak. They suggested that

flavivirus antibodies may not protect against yellow fever infections.

These divergent conclusions with regard to yellow fever outbreaks

and the prior presence of flavivirus antibodies could possibly be re¬

conciled by consideration of the sequence and type of flavivirus super¬

infection. Various workers have shown that monkeys immunized with

certain flaviviruses will give varying degrees of protection against

yellow fever: Macnamara (1953) found that monkeys immunized with

Uganda S were protected against a subsequent challenge with yellow

fever Asibi strain. In a similar experiment but using Zika to immunize

instead of Uganda S, Bearcroft (1957) showed that monkeys survived con¬

siderably longer than control monkeys when challenged with yellow fever

virus. Similar results were obtained by Theiler and Anderson (1975)

immunizing with dengue. Immunizing with West Nile, Wesselsbron, Zika,

Banzi and yellow fever, Henderson e_t aT (1970) found the yellow fever

-58-

viremia levels to be lower in Zika immune monkeys and protection against secondary infection with yellow fever virus was present in

Wesselsbron immune monkeys. The existence of cross-protection offered by dengue, Uganda S, Wesselsbron and Zika may influence the epidemiology of yellow fever.

In Ghana sporadic cases of yellow fever have been reported in the past five years in the Northern, the Upper, the Eastern and the

Brong-Ahafo Regions (Ghana Monthly Epid. Bull. March, 1971; Inst.

Pasteur-Dakar, Rapport Annuel, 1974). This may indicate that foci of sylvan yellow fever still exist in Ghana. The awareness of this problem has lead to the institution of a new yellow fever vaccination campaign.

In conclusion, yellow fever remains endemic in Ghana and even though the prevailing flavivirus antibodies may offer protection, fatal yellow fever cases still occur.

There were two specific reactions to West Nile. This virus which was initially isolated from a febrile woman in Uganda (Smithburn et al,

1940), has subsequently been isolated in Nigeria. Serological studies by various investigators (Macnamara et al, 1959; Boorman and Draper,

1968; Bres et al, 1963, 1965; Casals, 1966; Robin e_t a_l, 1968; Monath et al, 1974; Fagbami and Fabiyi, 1975) have shown, that antibodies to this virus are widespread in West Africa. This study presents similar findings for Ghana.

Wesselsbron was the other virus with two specific reactors. First isolated from a lamb in South Africa (Weiss et^ al, 1965) , the only West

African isolate had come from a camel in Nigeria (UIARP Ann. Rep., 1971-

1972). The close association of humans and livestock in Nigeria and

-59-

elsewhere in West Africa suggests the possibility of Wesselsbron infections in man. Serological surveys have indicated that this may well be the case (Casals, 1966; Bres, 1970), but that the proportion of the population involved may be small. In Ghana antibodies to

Wesselsbron were in comparable proportions to what was found for the other West African countries.

Dengue-1 had one specific reactor. For a long time dengue was thought not to be present in West Africa. However, Lee in 1969 re¬ ported several dengue-like illness in Nigeria. Since then dengue-1 and dengue-2 isolates have been made from patients presenting at the

University Hospital in Ibadan, Nigeria (Carey et_ al, 1971). Interest¬ ingly, the important complication of dengue virus infection, dengue hemorrhagic fever, which is common in South East Asia was not re¬ ported in any of these cases. Hemagglutination-inhibition studies, carried out in most cases in Nigeria, have shown the antibodies of the virus to be prevalent (Monath and Kemp, 1973; Monath et^ al, 1974;

Fagbami and Fabiyi, 1975), with interpretation complicated by flavi- virus cross-reacting antibody considerations.

The only flavivirus in this study with no specific reactor is the

Uganda S virus. This virus was isolated from Aedes species in Uganda

(Dick and Haddow, 1952). A human isolation has probably been obtained

in Uganda but not confirmed (Theiler and Downs, 1973). Antibodies

capable of neutralizing Uganda S have been found in human sera in

Nigeria (Macnamara et al, 1959) and in Senegal (Bres et al, 1963). These

positive neutralizations according to Theiler and Downs (1973) may not

reflect Uganda S infection. However, HI antibodies have been obtained

in this study and in investigations carried out in other West African

-60-

countries including Ghana's neighbors. Upper Volta (Bres e_t al, 1965),

Ivory Coast (Robin e_t al, 1968), and Togoland (Bres, 1970). Because of the inherent properties of this virus group, these antibodies may be cross-reacting to Uganda S.

Bunyaviruses.

This group showed the least number of positive reactors of the three groups in this study. Forty-seven (21%) of the 216 sera showed positive reactions to the two antigens, bunyamwera and Ilesha. Casals' study utilized two antigens from the bunyaviruses: Bwamba from the

Bwamba group and Ilesha from the Bunyamwera group. The overall HI positives obtained was 68%. However, only 21% of the sera had anti¬ bodies to Ilesha. A similar result for Ilesha was reported by Monath et al (1974) in their studies of humans in Nupeko Forest, Nigeria.

Other workers using bunyamwera antigen have obtained 19% of positives in Senegal (Bres et al, 1963), 17% in the Upper Volta (Bres et_ al, 1965) and 14% in the Ivory Coast (Robin e_t aJL, 1968). There were 10 specific reactions, two bunyamwera and eight Ilesha found in this study.

Bunyamwera HI antibodies, as previously mentioned, are widespread in human populations in West Africa. The virus was first isolated from

Aedes mosquitoes in Uganda (Smithburn

the virus is an inhabitant of West Africa and presumably in Ghana as shown in this study.

Another member of the bunyaviruses Ilesha was initially isolated in

Nigeria from a febrile patient (West African Council for Medical Research

Ann. Report, 1957). Other human isolations have been obtained in the

-61-

ft Cameroun (Salaun et al, 1968) and Senegal (Inst. Pasteur-Dakar, Ann.

Rep., 1969-1970). This study revealed eight specific or diagnostic reactions for Ilesha. This is not a conclusive evidence of the ex¬ istence of the virus in Ghana. Neutralization tests of these specific reactors of HI if positive may give a more reliable information. How¬ ever, isolation from human beings is necessary to provide incontrover¬ tible evidence.

Arboviruses, Administrative Regions, Population size. Annual Rainfall and Vegetation.

The arbovirus HI positive reactors for each group were analyzed by administrative regions, population group size, annual rainfall and vegetation of the localities where the samples were obtained.

The results indicate that there is greater prevalence of antibodies to the flaviviruses in the savannah zone than the rain forest zone. There were 80 of 102 (78%) flavivirus reactors from the savannah compared to only 37 of 114 (32%) from the rain forest. This result is different

from the one obtained by Macnamara ejt al (1959) in Nigeria. These workers suggested that the low occurrence of diagnosable yellow fever in the forest belt in Ghana and Nigeria was due to the fact that there was a high inci¬ dence of serologically-related viruses particularly Zika and Uganda S in

the forest belt with subsequent partial or complete suppression of overt yellow fever, whereas in the savannah belt infections with flaviviruses were less common and their lower incidence allowed yellow fever to occur

in epidemic forms. Recent reports from West Africa, notably Ghana and

Nigeria, reveal that the frequency of yellow fever cases are similar in

the forest and savannah zones. The outbreak of yellow fever reported by

Monath et_ aJL (1970) occurred at Okwoga in the savannah region but the

most recent outbreak of yellow fever took place at Uyo in the forest re-

-62-

gion (Institute Pasteur-Dakar Rapport Annuel, 1974). In Ghana reports of yellow fever outbreak are seemingly evenly scattered over the country (Ghana Monthly Epid. Bull., March 1971; Inst. Pasteur-

Dakar, Rapport Annuel, 1974).

Surveys that have been carried out in Nigeria for arboviruses other than the alpha - and flaviviruses indicated that the highest occurrence of antibodies were in the savannah zone. Fagbami et_ al,

(1972) studied the sera of humans taken from three ecological zones for antibodies to Tataguine by neutralization test and reported that the highest prevalence of antibodies to Tataguine was found in the savannah (61%) compared to 43% in the forest. Tomori and his associ¬ ates (1974) reported similar findings when they surveyed the human population of Nigeria for antibodies to Bwamba. The prevalence of neutralization antibodies was lower in the forest than in the savannah.

When the results of this study were analyzed by the amount of rainfall in the survey localities, there was a higher proportion of

flavivirus positives in the areas with less than 50 inches of rainfall annually (84%) to those areas with rainfall above 50 inches (59%). A similar result was obtained for the alphaviruses. These results were not unexpected as the savannah area generally has annual rainfall below

50 inches whereas the forest zone has annual rainfall above 50 inches.

Some may argue that the samples from the forest zone may have been

drawn from predominantly urban centers. As was mentioned earlier most

people in Ghana live in what might be termed rural to semi-rural setting,

and the majority of the samples from the high forest were in locations

with less than 10,000 inhabitants. Further, analyzing the results of

positive reactors by population size indicate that these reactors were

-63-

divided almost equally among the population group sizes as shown in

Table 9.

For administrative purposes, the positive reactors were analyzed by administrative regions and not unexpectedly the drier regions of the country, the Northern and Upper Regions, showed the most positive reactors.

This study and those by Fagbami e_t a1 (1972) and Tomori e_t al_

(1974) show contrary findings to those of Macnamara and his co-workers

(1959) with regard to the prevalence of arbovirus antibodies in the savannah and the forest. The changes of arboviral antibody distribu¬ tion that have taken place since the Macnamara ej; al studies in 1959 might be explained by changes in ecology, environment and human acti¬ vity. Occurrence of a virus in a certain region depends on conditions favorable to its propagation. With regard to the arboviruses this implies the presence of a vector, suitable hosts and the environmental conditions adequate for these to breed in. A change in the vector, host population or the environment in a locality will lead to disap¬ pearance of a virus depending on them for survival. In Ghana much of the activity to eradicate a vector such as the mosquito have been con¬ centrated in the more populous areas of the south and the rain forest.

Furthermore, increasing human populations in the south has also nec- cessitated clearing of forests for human habitation or agriculture, so that suitable habitats for vertebrate hosts such as monkeys which are important in maintenance of the yellow fever virus are subsequently destroyed.

There has not been such marked changes evident in human activity

in the north and the savannah regions. Large tracts of land remain un-

-64-

inhabited, and wild animals such as monkeys roam free. Mosquito popu¬ lations breed along water courses which in the dry season serve as watering holes for wild animals in the savannah. In such circumstances a virus can be maintained and circulated. Human practices may help to introduce a virus into the human population and propagate it among them.

The majority of the population in the savannah are farmers and hunters and frequently come into an environment where a virus is circulating among vectors and wild hosts, and become tangentially involved in this cycle. Propagation of such a virus in humans may be achieved through domestic vectors which abound around human dwellings in the savannah.

In the case of a vector such as Aedes aegypti existence in human dwel¬ ling is aided by water storage practices of the human population. Be¬ cause of the dryness of the savannah, water is conserved in pots around huts which become breeding spots for mosquitoes. Since most of the mosquitoes are man-biting Aedes species a virus can be transmitted from man to man and to domestic animals, such as cattle, that are kept by him.

On the serological evidence given by the tests described it can be concluded that a number of arboviruses have been active in the population surveyed. The principal of these viruses were chikungunya, Zika, yellow fever and Ilesha, or other viruses not included in this survey that are serologically related. Their activity appears to be more concentrated in the drier savannah areas of the Northern and Upper .

Limitation to this investigation.

The foremost limitations to this study are the inherent limitations of the HI test with regard to the arbovirus. As mentioned previously, it is hard to interprets the results of the HI test when a superinfection

-65-

or an undiagnosable pattern emerges. A specific or primary infection picture even though it would give some indication of the virus involved,

does not rule out the possibility of other viruses not included in the

study or as yet unknown. Neutralization tests will serve to give a more

exclusive result of the virus involved. But then some viruses do cross-

react in the neutralization tests with antibodies formed to other viruses within the same group. For an unequivocal diagnosis, a virus isolation

is needed.

With a serum collection that excludes children below the age of 10

years, it is not possible to make an age group comparison. Analysis of

the results of HI tests will give some indication as to how an individual

arboviral antibody composition changes with age. Hemagglutination-inhi¬

bition pattern in the age group below 10 will often give specific or

diagnostic pattern and thus make the interpretation of this test easier

and more fruitful.

The choice of the age range 20-29 years in this investigation re¬

veals only the antibody pattern for this age group. Extrapolation of

the results to any other age group is tenuous . Furthermore, because

mobility is greater in this age group, the results will not always in¬

dicate that an infection had taken place in the locality where the

sera were collected. Comparison of the HI test results by locality,

rainfall, vegetation zone and population group sizes of the locality

where the sera had been originally obtained will be biased by the

mobility factor.

Another bias might be the fact that the collection dealt with

hospital out-patient population, therefore, only the group who were

incapacitated in some way were sampled. However, it is not felt that

-66-

this population would differ particularly from the population at large.

The number of sera used in this study was small, and any conclusions can only be applied to this limited number and not to the whole popula¬

tion.

Finally, the sera were not gathered and treated under the most optimal of conditions. However, it is not felt that serological tests used would be seriously affected.

Perspectives for the future.

Given the limitations cited above, some more work is indicated.

For instance, neutralization tests on chikungunya and Ilesha specific

reactors found in this study will help to further indicate the pre¬

sence of these viruses in Ghana. But more importantly, there is need

to collect sera for the purpose of isolation of viruses. In addition

to human viral isolations, studies to elucidate vectors and vertebrate hosts of arboviruses and their characteristics are sorely needed. With

respect to this survey, further serological work on the remaining sera will offer a better indication of arboviral antibody characteristics

of the Ghanaian population and the possible arboviruses involved in

these infections. Additional serum collections might be planned to ex¬

plore further some of the interesting disease distributional findings

already obtained.

Downs (1975) discussed the problems involved with the diagnosis

of malaria in Africa. Often patients are diagnosed as having malaria

who actually have febrile illness caused by a virus or bacteria; at

other times malaria may be present and demonstrable on blood examina¬

tion whereas the incitant agent of the immediate illness might be a

-67-

virus or bacteria. It is desirable that accurate diagnosis be made in

these cases. An investigation that might go some way to help solve

these problems, in view of inadequate laboratory facilities, will be

to gather sera from febrile patients presenting at hospitals in Ghana and to put these sera through various diagnostic tests to determine

the etiology of the febrile illness. The results obtained from such a study will help doctors working in Ghana to get some feel for the differential diagnosis involved in febrile cases and to treat these accordingly.

Summary of Results by region, town, population, annual rainfall, and vegetation type 40 3 •H PC M •H Ph •H 44 rH <3 rH > •H •H Pd •H H Pi 3 Pd 44 44 O 3 > > 3 Alphav: CO 3 vD VOvO H CNCMvf X) to rH r—IO o m m M-l CO m 40 Pn sO T3 <3“ CN •H m SC •H W £*d •u 44 3 toO o 3 3 o O (1) CO CO 3 3 3 3 3 l 3/6 XD 00 CO o o CN rH OS fH 44 CN m 44 •H 40 Z 00 >-l & 00 o cu CO CO cO 3 1 sO m sO sO o in o CN OS r^v pH m •H 40 44 •H 33 00 <3 o T ■u 3 CO toO o cu e cO 1 X) m o m 3) rH T3 cn OS rH 40 <3 44 CO O cO > CO e 3 CO 3 O 3 C CO 0) 3 i -68 \D v£>XN CN mHiH sO H CMrH> 3 toO O 3 3 3 3 3 3 l 1 2/6 sO X> m m o rH 40 44 oo CTc m Ph on •H 40 a < OC 44 3 3 o too 3 o e 3 3 3 3 O 3 3 i 1

cn X> sO sO LO in o o 1—1 o *H 40 Ph O OC

■u 3 toO O 3 3 O 3 o 3 1

in 9/9 SO SO CO m o m 33 rH TO < o 40 40 40 CO H 3 3 O O 3 3 3 > 3 3 3 3 3 3 l SO 33 rH 3 3 3 3 £ O 1 5/6 s <44 3 3 1 5/5 m sO o •H CN o rH sO m •H Ph o 40 PC 4-J 3 3 o O 3 3 3 toO 1 5/6 sO O m in o <3 rH rH •H Ph 40 OC 44 GO toO o o too 3 O 3 3 1 3/6 X) sO o sO rH 40 rH cn 00 os in < •H s m •H 40 Oh PE H 4-J 3 03 toO 3 3 3 6 0- O too O 3 3 3 i i CO SO o •r—j rH SO m in rH 33 o 40 33 w 131 3 03 3 03 O O 3 3 3 3 > 3 3 3

1 3/6

CO 9/9 44 CN CO o o H rH pH PC *H 40 so 4-J 3 3 3 s toO O 3 3 1

cont

Summary of results by region, town, population, annual rainfall, and vegetation type XI •H X rH X X 4-4 4-1 X H o pi X CO c0 PC 01 CO 3 3 C 3 0) 3 3 o a o 3 3 1 PC o 3 3 'w' 4-1 rH rH •H X 4-1 CO o. 01 ca a 3 3 X X 3 co 3. CO > 3 >£) vC^lO 3 3 3 X 3 3 3 PC 3 1 3 O 3 X x 3 3 3 O 3 3 3 3 PC > 3 3 3 3 i X rH X 04 04 -3- O X o 04 in m 03 X X >-i 3 3 3 o o 3 3 > 3 3 3 3 3 l rH X 3 3 3 3 3 3 -69“ 3 PC 3 3 3 i rH <1* X X X o m X o 03 a 3 3 3 3 3 0 o 3 > 3 3 PC e O O 3 3 1 N OH X x v,O vOX X \0 X CO 3 3 3 3 3 3 a a 3 3 3 i ^ lO 1-1 X X vf m X 00 ON o 03 n Z o o 3 3 3 3 3 > 3 3 3 3 PC 3 > O O 3 l X 1- X 3 3 3 3 3 B 3 3 i X X CH 3 3 3 C3 3 3 i X X 1—\ m X X 04 rH o 03 2 3 3 > 3 o o 3 3 3 3 3 3 i X XX iO \DlO XXX H O(M cn 04 rH ON X 4-4 X 3 3 o pc 3 3 O O i r^. X •H PH X i—l r-'* n m m o X X X 4-4 3 PC O 3 O 3 o 3 1 3 3 3 1 CO co cn o 0) 3 1970 Population 3 X on X O' •H o o

Distribution of Arbovirus Reactor and Non-reactors of Ghanaian sera, 1975 p-l o 03 Z 03 O Hi • 0) •H T3 OtJ H H 00 O 03 3 03 O C 3 •H Ph 03 43 tn rH <3 03 43 > rH *H <3 Z <-3 3 H 3 oo 03 > 03 -H > M CX 03 < > 03 > 03 C CX 3 03 I cn 03 *H Pn 3 03 a o! 3 -H C H CX H 03 i 03 I 03 • > • > • H H S-i 03 03 03 03 03 3 03 03 03 o cmcoi—i O rHo o i—I MCMOH rH CMOCOCNI O rH O i—ICMrH lO vOvD •H on orH>h 43 < H 03 03 C rH o|<30(3 O

cont

Distribution of Arbovirus Reactor and Non-reactors of Ghanaian sera, 1975 3 to > 0) O -U • 3 33 Eh E-t 3 3 o o r—( O rH O ; o 1 o rH i c O i bC >, 3 'c ’’ O G 3 >> C ! C S G i c Region >. I •—I 3 X pH *H rH H ■-3 < PQ •H CO Pl CQ >H 3 IH 3 <3 « T—i T—I CO 3= > ccJ 3 > CO <3 Ph CL C ffl > PL > CO 3 rH iH I < > ex c CO 3 I > rC 3 3 -H CL 3 H 3 ^ 3 3 G H 3 -H 3 H > 3 CL U 3 I 3 • > I 3 • > | 3 • H 3 to CD CO Cl) 3 3 3 3 ooooo O iHr—II—I OOOOO OOOOO m 'Ocnin ooooo ooooo rH OCN < Otd5 r4 OS3hJ2 c/3 >-iS3O ,C z HI H H 3 c O mO 71- H ONrl rH O OOOOO ooooo O rHo OOOOO < 5WC ^ >SPJ cD cOCO CQ 2;E-cO3 O H CL CL 3 in vt HI o 3 33 Pd r—I OrH O rH O o cn O CNrH vO cON O rH rH CNC3 C <3t£ 3 IC/3| H 12<3c/3 S ■U H c 3 3 3 O HCM CN O Eh <3 C/3 Eh h4

aindicate number of positives exclusive to each group singly or to groups in combination. t>Sera not reacting to any group.

-72-

BIBLIOGRAPHY

1* Bauer, J.H. 1928. Transmission of yellow fever by mosquitoes other than Aedes aegypti. Am. J. Trop. Med., j}: 261-282.

2. Bearcroft, W.G.C. 1957. The histopathology of the liver of yellow fever infected rhesus monkeys. J. Path. Bact., ]_b_: 295-303.

3. Bearcroft, W.G.C., Porterfield, J.S., and Sutton, R.N.P. 1963. The isolation of Ukauwa, A Bunyamwera group virus from Nigeria, Trans. Roy. Soc. Trop. Med. & Hyg. , 5_7: 308-312.

4* Beeuwkes, H., Bauer, J.H., and Mahaffy, A.F. 1930. Yellow fever endemicity in West Africa with special reference to protection tests. Am. J. Trop. Med. & Hyg., H): 305-333.

5. Beeuwkes, H., and Hayne, T.B. 1931. Experimental demonstration of infectivity with yellow fever virus of Aedes aegypti captured in an African town. Trans. Roy. Soc. Trop. Med. & Hyg., 25: 107-110.

6. Beeuwkes, H., and Mahaffy, A.F. 1934. The past incidence and distribu¬ tion of yellow fever in West Africa as indicated by protection test surveys. Trans. Roy. Soc. Trop. Med. & Hyg., 28^: 233-258.

7. Berdonnean, R., Serie^ C., Pantheir, R., Hannoun, C., Papaioannov, S.C., and Georgieff, P. 1961. Sur l'epidemie de fievre jaune de l'annee 1959 en Ethiopie. Bull. Soc. Path. Exot.,54_: 276.

8. Berge, T.O. [Ed.] 1975. International catalogue of arboviruses, 2nd ed. DHEW, Atlanta

9* Boateng, E.A. 1966. A geography of Ghana, University Press, Cambridge.

10. Boche, R., Millan, J., and Revisse, P. 1974. Surveillance epidemiologique de la fievre jaune au Cameroun. Med. Afri. Noire., 2^: 501-503.

11. Boorman, J.P.T., and Draper, C.C. 1968. Isolation of arboviruses in the Lagos area of Nigeria and a survey of antibodies to them in man and animals. Trans. Roy. Soc. Trop. Med. & Hyg., 6_2: 269-277.

12. Bres,P. 1970. Donnees recentes apportees par les enquetes serologiques sur les prevalence des arbovirus en Afrique, avec reference speciale a la fievre jaune. Bull. Wld. Hlth. Org. , 4_3: 223-267.

13. Bres, P., Causse, G., Robin, Y., Cornet, M., and Oudart, J.-L. 1966. Med. Trop., _26: 261.

14. Brfes, P., Lacan, A., Diop, I., Michel, R., Peretti, P., and Vidal, C. 1963. Les arbovirus en Senegal, Enquete Serologique. Bull. Soc. Path. Exot., _56: 384-402.

15. Bres, P. , Carrie,J., Desbois, A., Larfique, J.J., and Mace, G. 1965. Les arbovirus en Haute Volta. Ann. Inst. Pasteur, 108: 341-352.

-73-

BIBLIOGRAPHY

16. Brottes, H., Rickerbach, A., Bres, P., Williams, M.C., Salaun, J.J., and Ferrara, L. 1966. Les arbovirus au Cameroun. Isolements h partir des mostiques. Bull. Wld. Hlth. Org. , _35: 811-825.

17. Carey, D.E., Kemp, G.E., White, H.A., Troup, J.M., Smith, E.A., Addy, R.F., Fom, A.A.M.D., Pifer, J., Jones, E.M., Brhs, P., and Shope, R.E. 1972. Epidemiological aspects of the 1969 yellow fever epidemic in Nigeria. Bull. Wld. Hlth. Org., 4j3: 645-651.

18. Casals, J. 1966. Serological survey of Northern Nigeria by hemagglutination- inhibition test. Yale Arbovirus Research Unit, Ann. Rep. 1966.

19. Casals, J., and Brown, L.V. 1954. Hemagglutination with arthropod-borne viruses. J. Exp. Med., 99j 429-449.

20. Casals, J., and Whitman, L. 1960. A new antigenic group of arthropod-borne viruses. The Bunyamwera group. Am. J. Trop. Med. & Hyg. , 9_: 73-77.

21. Causey, O.R., Kemp, G.E., and LEE, V.H. 1969. Arbovirus surveillance in Nigeria, 1964-1967. Bull. Soc. Path. Exot., 6j2: 249-253.

22. Chambon, L., Wone, J., Bres, P., Cornet, M., Cire Ly., Michel, A., Lacan, A., Robin, Y., Hendersen, B.E., Williams, K.H., Camain, R., Lambert, D. , Rey, M., Diop, M.I., Oudart, J.-L., Causse, G., Ba, H., Martin, M., and Artus, J.C. 1967. Une epidemice de fievre jaune au Senegal en 1965. Bull. Wld. Hlth. Org., 36: 113.

23. Davis, J.L. 1971. Two o'nyong-nyong-like virus strains from Nigeria. Thesis. Yale University School of Medicine.

24. Dick, G.W.A., and Haddow, A.J. 1952. Uganda S virus. A hitherto unrecorded virus isolated from mosquitoes in Uganda. I. Isolation and patho- geneicity. Trans. Roy. Soc. Trop. Med. & Hyg., 4b: 600-618.

25. Dick, G.W.A., Kitchen, S.F., and Haddow, A.J. 1952. Zika virus. I. Iso¬ lation and Serological Specificity. Trans. Roy. Soc. Trop. Med. & Hyg., 46: 509-520.

26. Downs, W.G. 1975. Malaria: The great Umbrella. Bull. N.Y. Acad. Med., 51: 984-990.

27. East African Virus Research Institute. Ann. Rept., 1955-1956, 1958-1963.

28. Fabiyi, A. 1961. Yellow fever at Ghana. 1959. Serological survey by complement-fixation. Ann. Trop. Med. Parasit., 58:

29. Fagbami, A.H., and Fabiyi, A. 1975. Arbovirus Studies in two towns in Western State of Nigeria. Trop. Geogr. Med., 2_7: 59-62.

30. Fagbami, A.H., Monath, T.P., Tomori, 0., Lee, V.H., and Fabiyi, A. 1972. Studies in tataguine infection in Nigeria. Trop. Geogr. Med., 24; 298-302.

bibliography

31. Ghana Monthly Epidemiological Bull., March, 1971.

32. Ghana Government, Population Census, 1970.

33. Ghana Government, Portfolio of Ghana Maps, Survey of Ghana. 1969.

34. Haddow, A.J., Gillet, J.D., and Highton, R.B. 1947. The mosquitoes of Bwamba County, Uganda. V. The vertical distribution of biting- cycle of mosquitoes in Rain-forest, with further observations on microclimate. Bull. Ent. Res., 37_: 307-330.

35. Haddow, A.J., and Ssenkubuge, Y. 1965. Entomological Studies from a high steel tower in Zika Forest, Uganda. Part I. The biting activity of mosquitoes and tabanids as shown by 24 hr. catches. Trans. Roy. Ent. Soc. Lond., 117: 215-243.

36. Halstead, S.B. 1970. Observation related to pathogenesis of dengue hemorrhagic fever. VI. Hypothesis and Discussion. Yale Biol. Med., 42: 350-362.

37. Hannoun, C., and Echalier, A. 1971. Arbovirus multiplication in an established diploid cell line of Drosophila melanogaster. Current Topics Microbiol. Immunol., _55: 227.

38. Institut Pasteur-Bangui. Rapport Annuel, 1969.

39. Institut Pasteur - Dakar. Rapport Annuel, 1974.

40. Kerr, J.A. 1932. Studies on transmission of experimental yellow fever by Culex thalassius and Mansonia unifornis. Ann. Trop. Med. Parasit., 2jS: 119-127.

41. Kokernot, R.H., Heymann, C.S., Muspratt, J., and Wolstenholme, B. 1957. Study on arthropod-borne viruses of Tongoland. V. Isolation of Bunyamwera and Rift Valley Fever viruses from mosquitoes. S. Afr. J. Med. Sci., _22: 71-79.

42. Kokernot, R.H., and McIntosh, B.M. 1959. Isolation of West Nile from a naturally infected human being and from a bird Sylvietta rufescens (Vieillor). S. Afr. Med. J., 33: 987-989.

43. Kokernot, R.H., Smithburn, K.C., Meillon, B.de, and Paterson, H.E. 1958. Isolation of Bunyamwera virus from a naturally infected human being and further isolations from Aedes (Bankisinella) cireumlu- teocus Theo. Am. J. Trop. Med. & Hyg., _7: 579-584.

44. Kokernot, R.H., Casaca, V.M.R., Weinbren, M.P., and McIntosh, B.M. 1965a. Survey for antibodies against arthropod-borne viruses in the sera of indigenous residents of Angola. Trans. Roy. Soc. Trop. Med. & Hyg., 39: 563-570.

45. Kokernot, R.H., Szlamp, E.L., Levitt, J., and McIntosh, B.M. 1965b. Survey for antibodies against arthropod-borne virus in sera of indigenous residents of the Capivi strip and Bechuanaland and Protectorate. Trans. Roy. Soc. Trop. Med. & Hyg. ,39_: 553-562.

-75-

BIBLIOGRAPHY

46. Lee, V.H. 1969. Aedes aegypti surveillance in Ibadan. Bull. Ent. Soc. Nigeria, 2^: 87-88.

47. Lee, V.H., Monath, T.P., Tomori, 0., Fagbami, A., and Wilson, D.C. 1974. Arbovirus studies in Nupeko Forest, a possible natural focus of yellow fever in Nigeria. II. Entomological investigations and viruses isolated. Trans. Roy. Soc. Trop. Med. & Hyg. , 6J3: 39-43.

48. Lucasse, C. 1963. First isolation of West Nile in Central Africa. Bull. Soc. Path. Exot., _56: 156-161.

49. Macnamara, F.N. 1953. Uganda S and yellow fever viruses. A slight re¬ lationship shown by experiments in rhesus monkeys and white mice. Brit. J. Exp. Path., ^4: 392-399.

50. Macnamara, F.N., Horn, D.W., and Porterfield, J.S. 1959. Yellow fever and other arthropod-borne viruses. A consideration of two sero¬ logical surveys made in South Western Nigeria. Trans. Roy. Soc. Trop. Med. & Hyg., _53: 202-212.

51. Mahaffy, A.F., Smithburn, K.C., Jacobs, H.R., and Gillet, J.D. 1942. Yellow fever in Western Uganda. Trans. Roy. Soc. Trop. Med. & Hyg., 36: 9-20.

52. Malherbe, M., and Strickland-Chomley, M. 1963. Sindbis virus infection in man, S. Afr. Med. J., _3_7: 547.

53. McIntosh, B.M., Patterson, H.E., McGillivray, G., and Sousa, J.de. 1964. Further studies on the chikungunya outbreak in Southern Rhodesia in 1962. Ann. Trop. Med. Parasit., 5j3: 45-55.

54. Melnick, J.L., Paul, J.R., Riordan, J.F., Barnett, V.H.H., Goldblum, N., and Zabin, E. 1951. Isolation from human sera in Egypt of a virus apparently identical to West Nile virus. Proc. Soc. Exp. Biol. & Med., 11: 661-665.

55. Monath, T.P., and Kemp, G.E. 1973. Importance of non-human primates in yellow fever epidemics in Nigeria. Trop. Geogr. Med., 225: 28-38.

56. Monath, T.P., Wilson, D.C., Stroh, G., Lee, V.H., and Smith, E.A. 1973a. Immunity survey to determine geographic limits and origins of the epidemics. Bull. Wld. Hlth. Org., 49J 122-128.

57. Monath, T.P., Wilson, D.C., Lee, V.H., Stroh, G., Kuteyi, K., and Smith,E.A. 1973b. The 1970 yellow fever epidemic in Okwoga District. Benue Plateau State, Nigeria. I. Epidemiological observations. Bull. Wld. Hlth. Org., 4j): 113-121.

58. Monath, T.P., Wilson, D.C., and Casals, J. 1973c. The 1970 yellow fever epidemic in Okwoga District, Benue Plateau State, Nigeria. Sero¬ logical responses in persons without pre-existing heterologous group B immunity. Bull. Wld. Hlth. Org., 42^: 235-244.

-76-

BIBLIOGRAPHY

59. Monath, T.P., Lee, V.H., Wilson, D.C., Fagbami, A., and Tomori, 0. 1974. Arbovirus studies in Nupeko Forest, a possible natural focus of yellow fever in Nigeria. I. Description of the area and serological survey of humans and other vertebrate hosts. Trans. Roy. Soc. Trop. Med. & Hyg., 68: 30-38.

60. Okuno, T. 1961. Immunological studies relating two recently isolated viruses. Germiston virus from South Africa and Ilesha from West Africa to the Bunyamwera group. Am. J. Trop. Med. & Hyg., IjO: 223-226.

61. Osterrieth, P., Delaplanque-Liegeois, P., and Renoirte, P., 1960. Recherches sur le virus chikungunya au Congo-Beige. II. Enquete serologique. Ann. Soc. Beige Med. Trop., 4(): 205-214.

62. Reed, W., Carrol, J., Agramonte, A., and Lazear, J.W. 1900. Etiology of yellow fever; preliminary note, Phila. M.J., 6_: 790-796.

63. Report of the health situation in Ghana. 1965 - 1970.

64. Robin, Y., Bres, P., Lartique, J.-J., Gidel, R., Lefevre, M., Athawet, B., and Hery, G. 1968. Les arbovirus en Cote - d’Ivoire. Enquete Serologie aus la population humaine. Bull. Soc. Path. Exot., 61: 833-842.

65. Rockefeller Foundation Virus Laboratory - New York, Ann. Rep. 1961.

66. Ross, R.W. 1956. The Newala epidemic. III. The virus, isolation pathogenic properties, and relationship to epidemic. J. Hyg., 54: 177-191.

67. Rudnick, A., Chan, Y.G. 1965. Dengue type 2 virus in naturally infected Aedes albopictus mosquitoes in Singapore. Science, 149: 683-689.

If 68. Salaun, J.-J., and Brottes, H. 1967. Les arbovirus au Cameroun. Bull. Wld. Hlth.0rg., 37: 343-361.

If 69. Salaun, J.-J., Rickenbach, A., Brhs, P., Brottes, H., Germain, M., Eouzan, J.~P., and Ferrara, L. 1969. Les arbovirus isoles h partir de moustiques au Cameroun. Bull. Wld. Hlth. Org., 4T: 233-241.

70. Serie, C., Andral, L., Lindrec, A., and Neri, P. 1964. Epidemic de fievre jaune en Ethiopie (1960 - 1962). Bull Wld. Hlth. Org., 30: 299-342.

71. Smithburn, K.C., Hughes, T.P., Burke, A., and Paul, J.H. 1940. A neuro¬ tropic virus isolated from the blood of a native Uganda. Am. J. Trop. Med., 20: 471-480.

72. Smithburn, K.C., and Jacobs, H.R. 1942. Neutralization tests against neurotropic viruses with sera collected in Central Africa. J. Immunol., 44: 9-23.

-77-

BIBLIOGRAPHY

73. Smithburn, K.C., Haddow, A.J., and Mahaffy, A.F. 1946. Neurotropic virus isolated from Aedes mosquitoes caught in Semliki Forest. Am. J. Trop. Med. & Hyg. , _26: 189-208.

74. Smithburn, K.C., Haddow, A.J., and Lumsden, N.H.R. 1949. An outbreak of sylvan yellow fever in Uganda with Aedes (Stegomyia) africanus Theobald as principal vector and insect host of the virus. Ann. Trop Med. Parasit., 43: 74-89.

75. Smithburn, K.C. 1952. Neutralizing antibodies against certain recently isolated viruses in sera of human beings residing in East Africa. J. Immunol., 69_: 223-234.

76. Smithburn, K.C., Kokernot, R.H., Weinbren, M.P., and Meillon, B.de. 1957. Studies on arthropod-borne viruses in Tongaland IX. Isolation of Wesselsbron virus from a naturally infected human being from Aedes (Banksinella) circuluteolus Theo. S. Afr. Med. J., 3E3: 555-561.

77. Spence, L., and Thomas, L. 1959. Application of hemagglutination and complement-fixation to the identification and serological classifica¬ tions of arthropod-borne viruses. Studies on chikungunya and Makonde viruses. Trans. Roy. Soc. Trop. Med. & Hyg. 5_3: 248-255.

78. Stokes, A., Bauer, J.H., and Hudson, N.P. 1928. Experimental transmission of yellow fever to laboratory animals. Am. J. Trop. Med., 8^:103-164.

79. Strode, G.K. (Ed.). 1951. Yellow fever. McGraw-Hill, New York and London.

80. Suchitra, N., Halstead, S.B., Cohen, S.N., Margiotta, M.R. 1969. Dengue and chikungunya virus infection in man in Thailand, 1962-1964. Am. J. Trop. Med. & Hyg., 18: 954-1033.

81. Taylor, R.M. 1951. Yellow fever: Epidemiology. In yellow fever (G.K. Strode, Ed.). McGraw-Hill, New York and London.

82. Taylor, R.M., Hurlburt, H.S., Work, T.H., Kingston, J.R., and Frothingham, T.E. 1955. Sindbis virus: A newly recognized arthropod-transmitted virus. Am. J. Trop. Med. & Hyg., 4-: 844-862.

83. Theiler, M. 1951. Yellow Fever: The virus. In Yellow fever (G.K. Strode Ed.), McGraw-Hill, New York and London.

84. Theiler, M., and Downs, W.G. 1973. The arthropod-borne viruses of verte¬ brates, Yale University Press, New Haven.

85. Theiler, M., and Anderson, C.R. 1975. The relative resistance of dengue- immune monkeys to yellow fever virus. Am. J. Trop. Med. & Hyg., 24: 115-117.

86. Tomori, 0. 1976. Personal communication.

-78-

BIBLIOGRAPHY

87. University of Ibadan Arbovirus Research Project, Ann. Rep. 1969-1972.

88. Weekly Epidemiological Record. 1971 (46); 1972 (47); 1973 (48); 1974 (49).

89. Weiss, K.E., Haig, D.A., and Alexander, R.A. 1956. Wesselsbron virus - a virus not previously described associated with abortion in domestic animals. Onderstepoort J., 27_: 183-195.

90. West African Council for Medical Research. Ann. Rep., 1957.

91. World Health Organization Technical Report Series No. 479, 1971.

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