Chapter 5

OBSERVATIONS ON THE MORPHOLOGY OF ADULTS AND LARVAL STAGES

OF OESOPHAGOSTOMUM SP. ISOLATED FROM MAN IN NORTHERN TOGO
AND GHANA

J. Blotkamp, H.P. Krepel, V. Kumar, S. Baeta,

J.M. van't Noordende and A.M. Polderman

Published in the Journal of Helminthology 1993;67:49-61

58

Abstract

Infection with Oesophagostomum sp. appears to be extremely common in man in northern

Togo and Ghana. Adult specimens were recovered from the intestinal lumen by treatment
with pyrantel pamoate and the morphological characteristics of oesophagostomes of man
could for the first time be compared with information available on the morphology of
oesophagostomes of monkeys. The observations and measurements demonstrated that the
species involved is Oesophagostomum bifurcum and that the eggs of this species cannot be
differentiated from those of Necator americanus. Both infections occur simultaneously in the
population involved. The LI larvae, too, cannot be differentiated from hookworm LI larvae.
The L3 larvae, however, are characteristic. Diagnosis of human Oesophagostomum infections
is based on the detection of these larvae in coprocultures. In the present paper, the eggs, the
LI and L3 larval stages and the adults, are carefully described and photos are given.
Morphology 59

Introduction

Several species of Oesophagostomum (Nematoda, Chabertiidae) infect primates [1] and other
animals around the world. In man, infections with Oesophagostomum sp. have been
considered as accidental infections for a long time. However, the finding of nine cases of
oesophagostomiasis in man in north-eastern Ghana [2] and, more recently of 51 clinical cases
within a period of 45 months in north-western Togo [3], suggests that quite intense
transmission of the nematode takes place in these areas. The taxonomie status of the
nematode responsible for the pathology in the clinical cases described so far, remains vague
as mature specimens have not been found since the first observations by Leiper [4] and
Henry and Joyeux [5]. In all later cases, only immature worms were described.

In 1987, a research project was started in Dapaong in northern Togo and just across the
border in Bawku in Ghana, the two areas from where Gigase and others [3] and Haaf and
van Soest [2] reported the cases of human oesophagostomiasis. The project objective was to
study different aspects of the infection in man. Recently Polderman and others successfully
isolated the third stage (L3) larvae of Oesophagostomum sp. from human faeces through
coproculture [6]. These larvae could easily be differentiated from those of hookworm. After
treatment mature worms of Oesophagostomum were recovered from the faeces.

In this paper we report on our observations on the morphology of various stages of the
isolated Oesophagostomum species recovered from human faeces as well as on their
developmental stages such as the eggs and L3 larvae harvested from the coproculture, and
the LI and L3 larvae grown from the eggs obtained from individual gravid females. For
differential diagnosis the morphological details of the eggs and larval stages are compared
with those of Necator americanus. Some observations are included on larvae cultured from
faeces of a locally obtained monkey (Erythrocebus patas) which carried a natural infection
and on the adult worms that were recovered after treatment. Finally we were able to examine
a few specimens of O. aculeatum from a monkey (Macacus irus) from Indonesia.

Materials and methods.

All parasitic material used in this study was obtained from volunteers who participated in
surveys and treatment trials in the area. Details on the population and the area involved are
given elsewhere [6,7]. The stages isolated from stool samples are described, followed by a
description is given of the mature worms and the larvae cultured from eggs isolated from
these gravid worms.
60

11 11
rlis ïi
la
ill
il
Bil II
length length

length

Figure 1. Frequency distributions of lengths and widths of eggs. A.Eggs in stool samples of four
patients with mixed infections (Oesophagostomum and hookworm) (sizes in microns). B.Eggs freshly
laid by an adult Oesophagostomum.
Morphology 61

Table 1. Characteristics ofL-3 larvae.

Anus to
Length tip of Anus
Max oeso- tail of to end of
Length width phagus larva sheath

L3- Oesophagostomum 820.7 31.1 146.6 62.1 204.6

(from coproculture man)(n=29) 712-950 26-42 131-164 47-88 165-248
L3- Oesophagostomum 843.6 30.0 137.6 62.8 215
(from uterus female)(n=22) 780-900 28-33 125-153 45-85 183-250
L3- Oesophagostomum 822.7 27.8 148.2 64.0 223.3
(from coproculture monkey)(n=6) 702-903 23-30 131-154 56-70 183-253
L3- Necator 662.9 29.7 158.1 53.8 126.4
(from coproculture man)(n= 10) 606-713 27-33 140-173 42-61 117-136

Means and ranges in iim.

Eggs
From formalin preserved stool samples of four patients who carried a mixed infection of
Oesophagostomum sp. and N. americanus, as earlier confirmed by coproculture, eggs were
measured carefully. Eggs laid by an individual gravid female Oesophagostomum were also
measured.

L3 filariform larvae cultured from faeces

The L3 larvae of Oesophagostomum sp and N. americanus were obtained through a
coproculture procedure described previously [6]. For their measurement the larvae were
immobilized either by gentle heat or in a diluted iodine solution (0.06 g KI and 0.04 gr I/100
ml). The L3-larvae of monkey origin were processed in the same manner.

Adult worms
Following treatment with pyrantel pamoate, stool samples were collected and washed through
a set of sieves with pore sizes from 1000-100 /xm. The recovered worms were washed clean
of faecal material. Worms were fixed immediately for later examination by light microscopy
or scanning electron microscopy (SEM). For light microscopic examination worms were
fixed in 10% hot formalin (80 °C). The fixed worms were cleared in a drop of lactophenol
to make internal structures visible. For SEM the worms were fixed and postfixed in 1 %
Os04 in 0.1 % cacodylate buffer (pH 7.4). Next the specimens were dehydrated in an alcohol
series and critical point dried under carbon dioxide. The dried specimens were covered with
62

Figure 2. Egg and larval stages of 0.bifurcum. a: Egg of 0. bifurcum, recovered from human stool sample
(from this sample no hookworm and many Oesophagostomum larvae were cultured) (Magnification 400x). b:
Ll-larva of O. bifurcum cultured from eggs that were recovered from the uterus of a gravid female (200x). c:
L3 larva of O. bifurcum cultured from a human stool sample (200x). d: Detail of Fig. 2c showing the prominent
intestinal cells (SOOx). e: Characteristically coiled L3 larva showing the transverse striation of the sheath (150x).
f: Detail of the anterior end of the L3 larva. The buccal area is characteristically different from the mouth of
hookworm larvae, g: Detail of the posterior end with the finely tapered tail of sheath.
Morphology 63

a layer of gold, about 6 nm thick, and examined in a Cambridge S-180 scanning electron
microscope (accelerating voltage of 15 KV and tilting angle of 70% relative to the electron
beam).

LI rhabditiform larvae cultured from gravid females

LI larvae developed within 24 h from eggs which were recovered by keeping female worms
in saline at room temperature (approximately 30°C at that time) or from the eggs which were
teased from the uteri of gravid females directly into saline.

L3 filariform larvae cultured from gravid females

Eggs taken from individual worms as described above were kept in saline at room tempera-
ture for 24 h to embryonate. They were then added to a mixture of sterilized faeces and
charcoal and the larvae were allowed to grow at ambient temperatures to the L3 stage.

Results

Eggs
In Figures la and lb length and width are given of 25 eggs from each of four faecal samples
with mixed infection of Oesophagostomum sp. and N. americanus and of 25 eggs laid by a
female Oesophagostomum.

The observations given in Figure la indicate that the dimensions of all eggs measured are
not only within the range of sizes of hookworm eggs (58.2-68.6 x 38.8-46.8 /xm)[8] but in
mixed infections no sign of a biphasic frequency distribution of sizes can be recognized.
Instead, the length and width of the eggs do vary from one patient to the other.Measurements
on eggs laid by individual gravid females demonstrate that these freshly laid eggs have not
attained their definitive shape yet and their sizes are much more variable (Fig. lb). These
observations cannot be used to differentiate between eggs of Oesophagostomum and
hookworm.

L3 larvae
At ambient temperatures the L3 larvae of Oesophagostomum can be found in the coprocul-
tures as from the fourth day of culture. The cultures are usually harvested on day seven.
Characteristic features of these larvae are the triangular intestinal cells (Fig. 2d), the very
long and finely tapered tail of sheath (Fig. 2g) and the prominent transverse striation of the
sheath (Fig. 2d, 2e). The slightly thickened cuticle of the anterior end of the oesophagus
together with the lining of the buccal capsule give the shape of an inverted "Y". By these
characteristics they are easily differentiated from L3 larvae of Necator.
64

Figure 3. Adult worms, male and female, a: Anterior end of adult worm (light microscopy). Note the ventral
groove (vg) (150x). b: Antgerior end of adult (SEM). Note the terminally positoned mouth, the ventral groove
(vg) and the cervical papillae (cp) (325x). c: Bursa copulatrix of a male with arrangement of the rays
characteristic of the genus (125x). d: Detail of the cloaca (SEM) showing protruding spicules (s), and the genital
cone with a ventral (O) and two subventral (s) paillae. Dorsal to the cloaca the raylets (7)of the cloacal nerves
are visible (400x). e: Posterior end of adult female (SEM) showing the straight and pinted tail, the anus (a) and
the vulva (v) (200x). f: Ventral view of the posterior end of adult female with kidney shaped ovejector (125x).
Morphology 65

Figure 4. Anterior end of adult O. bifurcum. a: Overview of the broad cup shaped mouth beaker. Two of the
three denticular projections (see 4b) are in focus (dp) (650x). b: Frontal view (SEM) of the mouth, showing
the external leaves (el), three denticular projections (dp) and the valve-like structure (v). The mouth is
surrounded by 4 papillae (p) and 2 laterla amphids (la)(1000x). c: View (SEM) of the external (ec)- and
internal leafcrown (ic) with a perioral groove (pg) at its base (lOOOx). d: As in Figure 4c, but with the position
of the dorsal denticular projection (dp) in connection with the perioral groove (pg) and the valve-like structure
(v)(1500x). e,f,g: An example of the variation in the numbers of leaves of the external crown (10,11,12 leaves)
(approximately 250x).
Table 2. Characteristics of adult female and male worms

Number Ventral Cervical

leaves Length groove to papillae Vulva Anus
external oeso- anterior to anterior to tip to tip Length
Length Width crown phagus body end body end of tail of tail spicules

Female Oesophagostomum
from humans (Togo/Ghana) 14.4 0.50 10-13 0.63 0.25 0.45 0.48 0.22
(present research, n=30) 11.0-16.8 0.31-0.68 0.52-0.74 0.20-0.30 0.32-0.56 0.36-0.62 0.17-0.26
from monkey (Ghana) 16.6 0.37 10(?) 0.67 0.23 0.58 0.45 0.20
(present research, n=10) 14.7-17.8 0.33-0.43 0.60-0.70 0.17-0.26 0.41-0.73 0.42-0.47 0.18-0.23
O. bifurcum (Creplin,1849)[27]
monkeys (origin unknown) 11.5-14.1 0.38-0.54 10 0.44-0.58 0.16-0.22 0.33-0.44 0.38-0.61 0.15-0.28
O. aculeatum (Linstow, 1879)[27]
monkeys (origin unknown) 13.0-19.0 0.44-0.48 10 0.55-0.67 0.21-0.28 ? 0.36-0.47 0.17-0.20

Male Oesophagostomum
from humans (Togo/Ghana) 11.5 0.38 10-13 0.58 0.23 0.41 1.02
(present research, n=20) 8.6-15.1 0.19-0.53 0.42-0.68 0.18-0.29 0.32-0.59 0.84-1.11
from monkey (Ghana) 12.3 0.30 10 (?) 0.62 0.22 0.54 0.96
(present research, n = 5) 11.1-13.3 0.27-0.33 0.60-0.65 0.21-0.23 0.49-0.59 0.92-0.97
O. bifurcum (Creplin,1849)[27]
monkeys (origin unknown) 8.0-13.0 0.31-0.41 10 0.16-0.22 0.33-0.44 0.84-1.14
O. aculeatum (Linstow, 1879)[27]
monkeys (origin unknown) 11.0-13.0 0.34-0.41 10 0.57-0.66 0.23-0.26 0.34-0.40 1.17-1.37

Means and ranges in mm.

Morphology 67

The intestinal cells of hookworm L3 larvae are not triangular and hardly visible. In Table
1 detailed measurements of L3 larvae of Oesophagostomum, cultured from human faeces are
compared with L3 larvae originating from female Oesophagostomum worms and with L3
larvae from coproculture of monkey faeces. Also shown are data on L3 larvae of N. america-
nus.

We noted a remarkable variation in the number of intestinal cells, varying from 16-32. Most
frequently 28-32 cells are seen but approximately 20 intestinal cells are also fairly commonly
seen. The same variation in numbers of intestinal cells is seen when larvae are grown from
eggs obtained from a single adult female.

The L3 larvae appear remarkably resistant to desiccation.

Adult worms
The adult worms are straight roundworms, 8-17 mm long, tapering at both ends with a
transversally striated cuticle. The mouth is terminal and surrounded by an oral collar. The
cephalic end bears a cuticular vesicle terminating ventrally in a deep groove which gradually
smoothens down on the dorsal surface (Fig. 3a,3b). There is an excretory pore at level with
the ventral groove. The mouth has a ring-like projection leading to a small buccal capsule,
surrounded by 10-12 leaves which constitute the external leafcrown (Fig. 4a-4g). At the base
of the external leafcrown there is an internal crown with 20-24 small petals (Fig. 4c,4d). The
mouth is surrounded by papillae and the openings of two lateral amphids which stand out
distinctly (Fig. 4b). The cup-shaped oesophageal funnel is closed by a valve-like structure
of three sclerotized plates (Fig. 4b), each with a prominent denticle that projects into the
buccal capsule (Fig. 4b). A dorsal gutter projects into the buccal cavity. This gutter forms
a dorsal cone which carries the ducts of the dorsal gland. Sharply pointed, laterally situated
cervical papillae protrude through the cuticle (Fig. 3b), of the anterior end of the baton-
shaped oesophagus. On average, their position is at 71% of the oesophagus' length (range
53-105 %; n=50).

Male. The bodylength of the male is 8.6 - 15.1 mm (n=20). The caudal bursa (Fig. 3c) is
broad and trilobate, the dorsal lobe is small, the lateral lobes are ventrally united though
spatially separated by a deep incision. The bursa copulatrix presents all features characteristic
of the genus Oesophagostomum. The gubernaculum is present and prebursal papillae are at
level with the anterior end of the gubernaculum. The genital cone is slightly convex. The
opening of the cloaca is surrounded by a ventral triangular papilla and two smaller subventral
papillae. Dorsal to the cloaca the raylets of the cloacal nerves protrude. The spicules are of
equal length, long, thin and finely striated. Lateral alae extend along almost the entire length
of the spicules. The distal ends are not united.
68

Table 3. Oesophagostomum females of man in Togo/Ghana, compared with those of primates.

Ventral
Number Length groove to Vulva Anus to
of oeso- anterior to tip tip of
Length Width leaves phagus body end of tail tail

Oesophagostomum sp. 11.0-16.8 0.31-0.68 10-13 0.52-0.74 0.20-0.30 0.36-0.62 0.17-0.26

(Dapaong/Bawku)
(from humans)
O. bifurcum 11.5-14.1 0.38-054 10 0.44-0.58 0.16-0.22 0.38-0.61 0.15-0.28
(Creplin, 1849)
O. aculeatum 13.0-19.0 0.44-0.48 10 0.55-0.67 0.21-0.28 0.36-0.47 0.17-0.20
(Linstow, 1879)
O. blanchardi 17.0-20.0 0.57-0.71 10 0.70-0.90 0.22-0.30 0.37-0.48 0.18-0.24
(Railliet & Henry, 1912)
(from monkeys)
O. stephanostomum 18.0-30.0 0.74-0.90 30-38 0.47-0.50 0.32-0.50 0.35-0.48 0.17-0.20
(Stossich, 1904)

Ranges in mm.

Female. The bodylength of the female is 11.0 - 16.8 mm (n=30). The posterior end tapers
gradually towards a thin, straight and pointed tail. The vulva is slightly protruding and is
situated 0.19-0.36 mm anterior to the anus. The vagina is fairly long, oblique, and leads to
a kidney-shaped, thick-walled ovejector which is placed somewhat anterior to the vulval
opening. The ovejector has a mean length of 0.25 mm. It corresponds to Type II of the
description of Lichten fels [9].

Table 2 gives detailed measurements of adult Oesophagostomum worms isolated in our

project from man. In Table 3 our data on female worms are brought together with those of
four species of Oesophagostomum parasites of primates [10].

LI larvae
The two features which are generally used to differentiate first stage larvae of hookworm and
Strongyloides are the length of the buccal canal and the size of the genital primordium. The
LI larvae of Oesophagostomum have a long buccal canal and a small, inconspicious genital
primordium. They closely resemble LI larvae of Necator and they cannot be differentiated
reliably on morphological grounds. Only the tail of LI larvae of Oesophagostomum would
seem to be slightly longer (26.7 vs 23.1 % of the total larval body length).
Morphology 69

Table 4. Characteristics ofL-1 larvae.

Length Length Anus to tip

Maximum oeso- buccal of tail (% of
Length width phagus canal total length)

L1 -Oesophagostomum 354.5 19.8 97.5 15.2 94.1 (26.7%)

(n=25) 300-430 17-20 72-117 12-18 75-108(21-31%)
LI -Necator 316.7 20.0 91.9 14.5 71.3(23.1%)
(n=10) 253-398 19-23 84-103 12-16 61-80(19-29%)
L1 -Strongyloides 320.2 17.6 88.6 5.2 51.6(16.4%)
(n-10) 294-380 16-19 82-94 3.4-9.4 41-61 (14-19%)

Means and ranges in \im.

Table 4 shows measurements of LI larvae of Oesophagostomum compared with those of

Necator and Strongyloides.

Discussion

Since the first report on oesophagostomiasis in man in 1905 [11], a number of cases of
human infections have been described by workers in Africa [2-5,12-24] in South-America
[25] and in Asia [26]. In almost all these cases, species determination was done on worms
obtained through surgery or at post mortem examination and concerned mainly immature
worms found in abdominal abscesses. In fact, it was suggested by some workers that in man
the parasite could not develop beyond the encysted stages. Anthony and McAdam concluded:
"man is an accidental host and seems an abnormal one" [19], and Barrowclough and Crome:
"man is an unsatisfactory host and the larvae fail to return to the bowel lumen after their
histotropic phase" [21]. Haaf & van Soest, however, cautioned that: "the possibility that man
himself may act as a source of infection cannot yet be discarded", but they failed to prove
through coproculture the presence of Oesophagostomum eggs in the faeces of their patients
[2]. Polderman and others [6] and Krepel and others [7] showed that in the study area of
North Togo and Ghana Oesophagostomum is a common parasite of man. For the first time
was it possible to obtain both larval and adult stages from man and thus it became possible
to give a complete description of the morphological characteristics, the adult worms included.

Diagnosis of infection with Oesophagostomum in man is greatly hampered by the fact that
the eggs closely resemble true hookworm eggs. Eggs of other species of Oesophagostomum
are larger than hookworm eggs. Therefore, it was hoped it would be possible to distinguish
between eggs of Oesophagostomum from man and those of hookworms on the basis of
70

comparing length and width of the eggs. The measurements of eggs of four mixed infections
of Oesophagostomum and hookworm, as given in Fig. 1, demonstrates that the eggs cannot
indeed be differentiated on morphological grounds: length and width are within the range
given for hookworm [8]. Even if there were differences in size, there is at least a very wide
overlap in the dimensions of the eggs of both species. Freshly laid eggs of Oesophagostomum
may have more blastomeres but the degree of development of the embryo is not a reliable
diagnostic character for the identification of the eggs. Therefore, on the basis of stool
examination alone, it can not be concluded whether a person is infected with hookworm or
Oesophagostomum. The eggs are so similar that the microscopist will not even be suspiscious
when finding "hookworm" eggs. It is quite likely that in other areas, too, infections with
Oesophagostomum are erroneously identified as those of hookworm.

As shown in table 4, the LI larvae are an unsatisfactory stage to differentiate between

Oesophagostomum and hookworm: the length, width, shape of the mouth as well as the tiny
G-cell, are all morphologically identical to those of N. americanus. L2 larvae show characte-
ristics of both LI and L3 larvae; this stage is less well defined in its morphology.

Only when hookworm-like eggs are grown to the L3 stage is the identification of the genus
Oesophagostomum possible. At this stage the larvae have distinct and easily recognizable
features: they are longer than hookworm and Strongyloides larvae, they have a long
"hairlike" tail of sheath, the transverse striation of the sheath and the triangular intestinal
cells are prominent. These features were identical for larvae obtained from cultures of human
stools, monkey dung and of larvae grown from eggs which we collected from gravid females
of Oesophagostomum sp. It puzzled us that the numbers of intestinal cells varied from 16-32.
The larvae with few intestinal cells are, on the average, somewhat smaller than those which
have as many as 30 intestinal cells. Since variable numbers were found in the progeny of
single worms, the number of intestinal cells appears to be an unstable characteristic.

The taxonomie classification of the specimens found in the study area depends first of all on
the characteristics of the adults. A correct assessment of the species involved is troubled by
the confusion in the nomenclature of the genus Oesophagostomum. Old names have been
used long after the publication of the very careful analysis of the validity of the species by
Travassos & Vogelsang [27]. Their systematics have been largely followed by more recent
authors: Chabaud and Larivière, who summarized their studies and made them generally
accepted [14], and by Glen and Brooks on quantitative taxonomy and shifting of hosts [28].

Eight species are presently recognized to occur in monkeys: O. blanchardi, O. aculeatum,

O. bifurcum, O. ovatum, O. pachycephalum, O. raillieti, O. zukowskyi, and O.
stephanostomum. In O. pachycephalum and O. stephanostomum there are 30-40 external
Morphology 71

leaves around the buccal capsule while in all others their number varies between 10 and 14.
O. zukowskyi is definitely smaller (males < 6 mm, females < 7 mm) than all others. In
contrast to the other species, O. pachycephalum, O. stephanostomum, and O. raillieti are all
characterized by very long spicules ( > 1.25 mm) and a wide buccal capsule ( > 80 pm). O.
ovatum has a buccal capsule that is much wider than observed in the worms described here
and O. blanchardi has spicules that are significantly larger.

The specimens described by us share most characteristics with O. bifurcum and O. aculea-
tum. Although the length of the spicules is not used by Glen and Brooks to differentiate these
species [28], the original data of Travassos and Vogelsang indicate that the spicules of O.
aculeatum are significantly longer than those of O. bifurcum (1172-1336 vs 843-1144 /xm)
[27]. Chabaud and Larivière use this criterion to show that the "O. bijurcus" found in
Indonesia by Lie Kian Joe [26], was in fact O. aculeatum [14].

We had the occasion of examining a few identified specimens of O. aculeatum (originating

from a Macacus iris from Indonesia, obtained from Dr. J.J. Jansen, Utrecht). The spiculae
of a single male specimen measured 1200 /*m, i.e. longer than those of any of our
specimens. The most pronounced morphological differences between O. aculeatum and those
collected by us are seen in the buccal region. The buccal capsule was more funnel-shaped
in O. aculeatum and convincingly cup-shaped in our specimens. Although both have a dorsal
gutter, the dorsal cone is comparatively inconspicious in O. aculeatum. and the three
denticles are much smaller.

Furthermore, O. aculeatum is considered to have its distribution in south-east Asia while O.

bifurcum occurs both in Africa and Asia. On the basis of these arguments, the adults
described here show most similarity with O. bifurcum Creplin, 1847.

Two features, however, obscure a straightforward classification. Firstly the number of leaves
of the external crown varied from 10-13 with 10 and 12 most often seen. In no other way
did these worms differ and there was no relation with the variation seen in the numbers of
intestinal cells of the L3 larvae. Secondly the female worms are longer than described so far
for the primate infecting species in Africa. Sixty percent of the females found by us are
longer than the maximum length of the adult females of O. bifurcum described so far. Even
the mean length of our females (14.4 mm) is longer than the maximum length of 14.0 mm
described by Popova [10] and by Travassos and Vogelsang [27]. The extravagant length of
the female worms could possibly be explained by host or geographical factors. Most worms
described by earlier authors originated from monkeys, while those described by us were
collected from the human host. Moreover, it has not been clearly indicated in the older
72

literature whether the worms described were fully developed stages obtained from the
intestinal lumen or young adults recovered from the nodules in the intestinal wall. In this
context it is remarkable that the females described by us are much bigger than those
described earlier while the males are of the same length. The explanation of a predominant
influence of host factors is not supported by the only other observation on six adults of O.
apiostomum (syn. O. bifurcum) from the intestinal lumen: the biggest female found by Leiper
was 11 mm; the longest male 8 mm [4]. The same holds true for the adult worms recovered
from the monkey: the adult females isolated from a naturally infected monkey were signifi-
cantly bigger (15.2-17.7; mean 16.5 mm; n= 10) than described earlier while the adult males
recovered from the monkey are within the normal range of sizes for O. bifurcum (11.1-13.3;
mean 12.3 mm; n=5). It is realized, however, that the size of adults is not normally
considered to be a very stable characteristic.

The species of Oesophagostomum that appeares to be so common in man, and quite important
from a public health point of view in northern Togo and Ghana, should therefore be
considered to be Oesophagostomum bifurcum.
Morphology 73

Acknowledgements

The research was supported by the Ministers of Health and Education in Lomé, Togo. The
involvement of the staff of the hospital in Dapaong, Togo, and the assistance of Ms Assibi
Lamboni have been essential for the field work. We thank the department of Infectious
Diseases and Immunology of the Faculty of Veterinary Medicine, Utrecht, for providing us
with specimens of oesophagostomes from primates. The critical reading of the manuscript
and the comments of Dr. L.M. Gibbons of the International Institute of Parasitology,
St. Albans, and of Dr. Y. Gutierrez of Case Western University, are greatly acknowledged.
The fieldwork component of the study was funded by the Netherlands Foundation for the
Advancement of Tropical Research (WOTRO).
74

References

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de Parasitologie 13:161-202.

2. Haaf E, van Soest AE, 1964. Oesophagostomiasis in man in north Ghana. Tropical and
Geographical Medicine 76:49-53.

3. Gigase P, Baeta S, Kumar V, Brandt J, 1987. Frequency of symptomatic human oesop-

hagostomiasis (helminthoma) in Northern Togo, in Geerts and others, ed., 1987. Helminth
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