Oesophagostomum bifurcum infection in man. A
study on the taxonomy, diagnosis, epidemiology
Krepel, H.P.Citation
Krepel, H. P. (1994, June 28). Oesophagostomum bifurcum infection in man. A study on the taxonomy, diagnosis, epidemiology. Retrieved from https://hdl.handle.net/1887/13885
Version: Corrected Publisher’s Version
License: Licence agreement concerning inclusion ofdoctoral thesis in the Institutional Repository of the University of Leiden
Downloaded from: https://hdl.handle.net/1887/13885
Note: To cite this publication please use the final published version
Chapter 3
HUMAN OESOPHAGOSTOMUM INFECTION IN NORTHERN TOGO AND GHANA: EPIDEMIOLOGICAL ASPECTS
H.P. Krepel, S. Baeta and A.M. Polderman
30
Summary
Recently, it has been established that human infection with Oesophagostomum bijurcum is common in northern Togo and northeastern Ghana. Two surveys were conducted in this area. In a regional survey, O. bijurcum infection appeared to occur in 38 of 43 villages. The highest prevalences (up to 59%) occurred mostly in small isolated villages and were usually associated with high hookworm infection rates. The infection was relatively rare in children under five years of age (7% infected). In older individuals, females showed higher preva-lences than males (30% v. 24%).
In a second survey, the entire population of two high-prevalence villages was examined. Infection rates were low in children under three years of age, but rose quickly thereafter, suggesting intense transmission. A stable level of infection was reached by 10 years of age.
Oesophagostomum larvae were found more frequently in hookworm-positive than in
Epidemiological aspects 31
Introduction
Oesophagostomum species are well-known parasites of goats, pigs, sheep, cattle and monkeys [1]. They are often referred to as 'nodular worms', because typically, the intestines of infected animals are covered with small, nodule-like abscesses. These abscesses are caused by Oesophagostomum larvae which penetrate into the intestinal wall and develop into young adult worms. These immature worms re-enter the intestinal lumen to start egg production. Outside the host, the eggs develop into third-stage larvae, and the cycle is completed when they are ingested by the host.
Oesophagostomum infection in man has been reported only on a few occasions, usually as
abscesses with larval stages [2,3]. Adult worms have been reported only twice in man [4,5]. Consequently, man has hitherto been considered as an incidental and abnormal host, in which the life cycle is normally not completed [6,7]. However, unusually large numbers of cases were reported from northern Togo and northeastern Ghana [8,9]. Although it was thought that man was probably more than an incidental host in these regions, no proof was given for the completion of the life cycle in man. Recently, a classical coproculture method was introduced to verify wether all 'hookworm' eggs excreted by the population in northern Togo and Ghana were indeed eggs of Ancylostoma duodenale or Necator Americanus [10]. In this survey 20-30% of the population was found to be infected with what appeared to be
Oesophagostomum bifurcum, a common parasite of monkeys.
It was the aim of the present study to examine epidemiological aspects of human
Oesophagostomum infection in northern Togo and northeastern Ghana. Two surveys were
carried out. Firstly, the occurence of Oesophagostomum infection was investigated in 43 villages throughout the region and the influence of size and location of the village, tribe, religion and profession was analysed. A second survey was then undertaken to examine the relationship between age, sex and hookworm infection in a homogeneous population, using data collected from almost the entire population of two villages with high prevalences.
Materials and methods Study area
0 • 0 % 1 - 1 0 % 1 1 - 3 0 % > 3 0 %
HP
2 0 km GAME PARK country border roadEpidemiological aspects 33
The Savannah Region, with Dapaong as the main town, measures 3700 square km, and has a population of 250 000. The 3000 km2 of the Bawku District has 330 000 inhabitants. The main tribes are Gourma (Togo), Kumasi (Ghana), Moba and the Peulh nomads (both Togo and Ghana). The inhabitants live in small gatherings of clay huts called 'soukoulas'. The main crops are millet, maize and cotton and cattle, goats, sheep and pigs are raised in large numbers. In Ghana, monkeys (Cercopithecus and Papio species) are seen both in the wild and in captivity, whereas in Togo they mainly occur in the game parks.
Public health care in the Savannah Region consists of one State Hospital of 210 beds in Dapaong and 33 health stations. In the Bawku district there is one District Hospital (Bawku) and 25 health stations. Apart from one good tar road in Togo, leading to Burkina Faso, all roads in the area are of dirt.
Stool samples
Stool sampling methods were different in the two surveys. In the first, area-wide survey, 43 villages were visited to introduce the project and invite the population to participate. In Togo, 25 village health stations were visited on several occasions so that outpatients could be asked to give stool samples. In Ghana, 16 villages were visited and volunteers that were present on the day of the visit were asked for stool samples. Name, sex, age, village of origin, tribe, religion and profession were registered.
In the second village survey the populations of Pana and Dassoute (see Table 1 and Fig. 1) were examined. In these villages many cases of Oesophagostomum infection had been found during the regional survey, and in both villages cooperation was assured. All houses were numbered and the name, age, sex and house number of each villager were registered.
Stool specimens were cultured on the same or the next day using the classical coproculture procedure following Polderman et al [10]. The larvae were identified with the help of a key for filariform larvae given by Little [11].
Statistical methods
three-Table 1 Overview of the results in all participating villages.
M + F < 5 M S 5 F ^ 5 M + F è 5
Village clv clr n oe% n oe% n oe% hw% oec,
Ghana 28. Bawku 29.Bimbagu 30.Binaba 31.Bunkpurgu 32.Garu 33.Gowrie 34.Kuka\Zuli 35. M issiga\ Pussiga 36.Nafkoliga 37.Nakpandouri 38.Nangoudi 39. Tubong\Tempane 40.Widana 41.Widnaba 42.Yalugu 43. Zawse\Magnory Total
Legend: n = number of persons examined; M = males; F = females; hw% = prevalence of hookworm infection; Oe% = prevalence of infection with Oesophagostomum.
clv = class of village: clr = class of road:
1 = > 10.000 inhabitants 1 = tar road 2 = 5.000 - 10.000 " 2 = main dirt road 3 = 2.000 - 5.000 " 3 = secondary dirt road 4 = 1.000 - 2.000 " 4 = small dirt road
5 = < 1.000
(Source: Direction de la Cartographie Nationale et du Cadastre, Lomé 1984; Bawku Rural Health Service, Annual Report 1986)
36
four, five-nine, 10-19, 20-29 and more than 29 years of age. Daily and social activities were comparable within these groups. The associations between Oesophagostomum infection and sex, age and hookworm infection were tested with the Chi-squared test.
Results Regional survey
Village-specific prevalences
Cases of Oesophagostomum infection were detected in all but five villages: Mandouri, Bawku, Gowrie, Nangoudi and Zawse/Magnory (Figure 1 and Table 1). The highest prevalence of Oesophagostomum infection (59%) was observed in Naki-Est.
Villages were classified according to their road communications ('clr' in Table 1) and size ('civ'). Villages alongside the main tar road (clr 1), showed Oesophagostomum prevalences of less than 20% (Table 2), whereas prevalences in villages alongside small dirt roads (clr 4) were all higher than 10% and mostly higher than 30%. In towns (civ 1) and larger villages (civ 2) high prevalences were rarely seen. The highest prevalences were seen in the smallest villages (civ 4 and 5, Table 2).
No relationship was observed between Oesophagostomum infection and tribe, religion or profession.
Table 2. Numbers of villages classified by size and road communications and prevalence of Oesophagostomum infection Oesophagostomum infection rate (%) 0-10 10-19 20-29 S>30 / 3 2 -Class 2 4 4 1 3 of roacC 3 5 4 1 3 4 . 1 4 8 1 1 1 -Class 2 3 2 1 -of village' 3 5 1 2 2 4 2 7 1 8 5 1 -2 4
Epidemiological aspects 37
Age- and sex-specific prevalences
In Togo, results were obtained from 3820 individuals [1926 males (M) and 1894 females (F)]. Third-stage larvae of Oesophagostomum and hookworm were detected in 1057 (27.6%) and 2746 (71.9%) of cases, respectively. Strongyloides stercoralis larvae were seen in only 41 cultures (1.1%).
In Ghana, stool cultures from 1313 individuals (658 M, 655 F) were examined. Of these, 157 (12%) were positive for Oesophagostomum, 684 (52%) for hookworm and 53 (4%) for
Strongyloides stercoralis.
The infection rate of Oesophagostomum in the group of young children was lower than for the older age groups in both Togo (10% v. 31 %) and Ghana (1 % v. 15%). In the two older groups, that of females had a higher prevalence than that of males, both in Togo (35% v. 28%) and in Ghana (18% v. 12%). Oesophagostomum 1 0 0 % 8 0 % 6 0 % 4 0 % 2 0 % 4 0 % 6 0 % Hookworm 8 0 % 1 0 0 %
38 Pana, Oesophagostomum (A) N = 31 24 18 28 40 52 58 42 26 39 38 85 100% 80% 60% 40% 20% 0% 0-2 3-4 5-9 10-19 20-29 >30 Years Pana, hookworm (B) N = 31 24 18 28 40 52 58 42 26 39 38 85 100% 80% 60% 40% 20% 0% 0-2 3-4 5-9 10-19 20-29 >30 Years • Males Q f e m a l e s
tffïfl
Figure 3 (a-d). Prevalences with Oesophagostomum (A,C) and hookworm (B,D) in the villages of
40
Association with hookworm
Oesophagostomum and hookworm infection were associated both at the individual and at the
village level. In villages with high prevalence of Oesophagostomum, the prevalence of hookworm infection was also high; infection with Oesophagostomum was never common in villages with low hookworm prevalences (Table 1 and Fig. 2).
At the individual level, larvae of Oesophagostomum were found more frequently in hookworm positive than in hookworm-negative cultures (P<0.01). This association was observed in almost all age groups and in both sexes.
Village survey
In Pana and Dassoute, 992 subjects were examined, covering 96% and 85% of the population, respectively. The number of inhabitants and percentages of participation for each of the villages are given in detail in Table 3.
r
Table 3. Participation in the village surveys at Pana and Dassoute.
Sex and age (years) males 0 - 4 5 - 19 2:20 females 0 - 4 5 - 19 ;>20 No. of inhabitants 53 102 81 56 99 126 Pana No. of participants 49 98 76 52 94 125 Participation (%) (94) (96) (94) (93) (95) (99) No. of inhabitants 52 147 57 70 109 139 Dassoute No. of Participation participants 47 129 42 61 96 119 (%) (90) (88) (74) (87) (88) (86)
Age- and sex specific prevalences
Epidemiological aspects 41
Hookworm prevalences were higher than Oesophagostomum prevalences in all age groups and in both villages. Infection rates increased with age; no significant difference was observed between males and females aged five years or older.
Association with hookworm
When screening the coprocultures, there were four possible outcomes: detection of
Oesophagostomum larvae or hookworm larvae, or both types of larvae, or no larvae. Table
4 shows the frequencies of each outcome for all the cultures from Pana and Dassoute.
Table 4. Crosstables demonstrating the association between the presence of Oesophagostomum and
hookworm larvae in coprocultures in two groups (males and females of 5-19 years in Dassoute). The numbers in brackets are the expected numbers in a random distribution.
Pana (X2 = 63.6, P<0.01) Dassoute (X2 = 52.8, P<0.01) Oesophagostomum Negative 136 (100) 184 (220) Positive 18 (54) 156 (120) Totals 154 340 Oesophagostomum Negative 109 (69) 133 (173) Positive 31 (71) 221 (180) Totals 140 354 Hookworm negative Hookworm positive Totals 320 174 494 242 252 494
The numbers of cultures with both types of larvae or with none were higher than would be expected in a random distribution of Oesophagostomum and hookworm larvae. This association of hookworm and Oesophagostomum persisted in smaller, homogeneous groups and it was statistically significant in 11 of 24 groups (Table 5) and highly significant for the totals for all the groups.
Discussion
42
Table 5. Levels of signiftcane of the association between the presence of Oesophagostomum and
hookworm larvae among various subgroups of the population of Pana and Dassoute.
Pana Dassoute Males Females Males Females
Age (years) 0-2 3-4 5-9 10-19 20-29 ^ 3 0 Total N 31 18 40 58 25 51 P' N.S. <0.05 N.S. N.S. N.S. <0.10 223 < 0.001 N 24 28 52 42 39 86 271 P N.S. <0.10 N.S. <0.10 N.S. <0.05 <0.01 N 10 37 81 48 16 26 218 P <0.10 N.S. <0.01 N.S. N.S. N.S. <0.001 N 16 45 62 34 40 79 276 P N.S. <0.01 <0.10 <0.01 <0.01 N.S. <0.001
* Results of X2 tests. N.S., not significant.
villages. There are many traders who have dwelt in these villages for only a few years, and their homes and compounds differ markedly from the traditional soukoulas of the autochtonous population. Sanitary conditions are generally better and drugs like anthelminthics are more readily available.
Although Oesophagostomum infection rates were relatively low in young children, in both regional and village surveys, infections were found in children less than three years old. The rapid increase in prevalences in children between their second and 10th year, observed in the village survey (Fig. 3), indicates that transmission is intense.
Oesophagostomum prevalences were lower than those of hookworm. The numbers of larvae
found in samples from Oesophagostomum-positive subjects, however, were lower than those in samples from hookworm patients, and the diagnosis of Oesophagostomum infection was rarely based on the finding of a single larva. It is likely, therefore, that a larger underestimation was made of the prevalence of Oesophagostomum infections than of hookworm infections. The comparatively low numbers of Oesophagostomum larvae found in many stool cultures may not only represent low intensities of infection but also low egg-production of the adult females. It has recently been shown, however, that the egg egg-production of Oesophagostomum is similar to that of hookworm [12].
Epidemiological aspects 43
than for the selected and homogeneous groups of Table 5. It is remarkable, though, that a statistical association is present even within these subgroups, and there are three possible explanantions.
The most obvious explanation is a similarity in transmission. This is unlikely, since Necator americanus is the predominant hookworm species and hookworm transmisssion occurs mainly
via the percutaneous route. Although percutaneous transmission cannot be ruled out in human oesophagastomiasis, oral transmission would seem more likely: Oesophagostomum infections of veterinary importance follow the oral route of infection, and third stage infectious larvae applied to the intact skin of one of us (A.M.P.) failed to penetrate.
A second explanation is based upon the assumption that similar risk factors are present. Are the smaller, isolated communities more infected because of different customs related to hygiene, agricultural practices or the relative lack of potable water? (This could also explain why women are more often infected than men, as their daily activities are widely different.) Or are there climatological, geological or perhaps other factors which determine the peculiar geographical distribution and which may have some, but much less, impact on the transmission of hookworm infection? It is notable that the infection seems to occur mostly in a well-defined area (Fig. 1) concentrated in several foci, and with decreasing prevalences at the periphery. Although no systematic research has been carried out there, human oesophagostome infection appears to be rare south of the present study area.
A third explanation is methodological error; if mixed coprocultures are relatively more successful an apparent association will result. More information is needed to decide which of the explanations is correct.
44
Acknowledgements
The research in Togo was supported and assisted by the Minister of Health, Dr. A. Agbetra, and the Minister of Education, Dr. T.K. Tchalim. The valuable advice and assistance of Mr. K.D. Amouzou, Administrative Director of Dapaong Hospital, and of Mr. Tiem, Chef-Kanton of Pana, are much appreciated. The fieldwork of Mss A.N. Hiemstra, A. Rietveld, F. Stelma and other students, as well as the laboratory assistance of Ms A. Lamboni, have been of great value. The technical advice of Ms J.Blotkamp were essential for the research.
Epidemiological aspects 45
References
1. Levine ND, 1968. Nodular worms, bowel worms, gapeworms and kidney worms. In
Nematode parasites of Domestic Animals and of Man. Burgess, 115-125.
2. Railliet A, Henry A, 1905. Encore un nouveau sclérostomien (Oesophagostomum brumpti nov.sp.) parasite de 1'homme. Comptes Rendues des Séances de la Société de Biologie 58:643-645.
3. Barrowclough H, Crome L, 1979. Oesophagostomiasis in man. Tropical and Geographical
Medicine, 57:133-138.
4. Leiper RT, 1911. The occurence of Oesophagostomum apiostomum as an intestinal parasite of man in Nigeria. Journal of Tropical Medicine and Hygiene 74:116-118.
5. Henry A, Joyeux CH, 1920. Contribution a la faune helminthologique de la Haute Guinee francaise. Bulletin de la Société de Pathologie Exotique 75:176-182.
6. Elmes BGT, McAdam IWJ, 1954. Helminthic abscess, a surgical complication of Oesophagostomes and hookworms. Annals of Tropical Medicine and Parasitology, 48:1-7.
7. Chabaud AG, Larivière M, 1958. Sur les Oesophagostomes parasites de 1'homme. Bulletin
de la Société de Pathologie Exotique, 57:384-393.
8. Gigase P, Baeta S, Kumar V, Brandt J, 1987. Frequency of symptomatic human oesophagostomiasis (helminthoma) in Northern Togo, in Geerts and others, eds., 1987.
Helminth Zoonoses. :228-236.
9. Haaf E, van Soest AH, 1964. Oesophagostomiasis in North Ghana. Tropical and
Geographical Medicine 70:49-53.
10. Polderman AM, Krepel HP, Baeta S, Blotkamp J, Gigase P, 1991. Oesophagostomiasis, a common infection of man in Northern Togo and Ghana. American Journal of Tropical
Medicine and Hygiene 44:336-344.
46
12. Krepel HP, Polderman AM, 1992. Egg production of Oesophagostomum bifurcum, a common parasite of humans in Togo. American Journal of Tropical Medicine and Hygiene
