NationalLibraryOfScotland/medical-history-of-british-india huggingface dataset:
ON THE IDENTITY OF THE SCHISTOSOME FOUND IN CASES
OF BOVINE NASAL GRANULOMA AND SOME
OBSERVATIONS ON A FEW OTHER
MEMBERS OF THE
SCHISTOSOMIDÆ
BY
G. D. BHALERAO, M.Sc.,
Helminthologist, Imperial Institute of Veterinary Research, Muktesar.
(Received for publication on the 11th October 1932.)
(With Plates XXVI to XXXII,)
There exists in India a peculiar " snoring disease " of cattle known as nasal
granuloma. Up to the present time it has been known to occur in the United
Provinces, Assam, Bengal, Bihar, Bombay, Orissa, the Central Provinces, Madras,
Mysore and probably Sind. The etiology of this disease has baffled veterinary
workers in India for some time in the past. Krishnamurti Iyer [1922] was the first to
declare that the disease was a form of actinomycosis, since he regarded the rosette-
like bodies found in histological sections of the tissue as characteristic of the " Ray-
fungus ". Later, Krishnamurti Iyer [1927] detected cases of a similar condition
in cattle which were definitely due to the protozoon parasite, Rhinosporidium.
Very recently Datta [1932] has recorded the presence of Schistosome worms in nasal
granuloma tissue, and soon after his discovery his findings were confirmed by
Malkani [1932] and a few other workers in India.
The clinical, pathological and other aspects of the disease have been dealt with
by previous workers. The object of the present communication is to deal with the
morphological and taxonomical side of the schistosome found in bovine nasal
granuloma tissue and offer some remarks on a few other Schistosomes that are
at present in the possession of this Institute.
THE SCHISTOSOME FOUND IN BOVINE NASAL GRANULOMA TISSUE.
(Plate XXVI, figs. 1—4 ; Plate XXVII, figs. 1 and 2.)
Approximately three dozen males and one dozen female specimens collected
from the nasal granuloma tissue of two bulls and one cow imported here from Bihar
were available for study. Among these specimens there were ten pairs. In addition
to these specimens there were also many others of the same type obtained in one
instance from the portal circulation of a bull.
The specimens were in all instances fixed in bouin and later stained in acetic
alum-carmine. All the measurements given in this paper refer to these toto¬
preparations.
MORPHOLOGY.
Male.—The males are whitish in colour and do not exhibit any appreciable
degree of movement in the living condition. The anterior portion of the body is
( 338 )
IDENTITY OF SCHISTOSOME IN BOVINE NASAL GRANULOMA.
339
almost straight and carries two suckers. It is spindle-shaped, being thickest at the
site of the ventral sucker and thinnest at the oral sucker and its junction with the
rest of the body. The posterior part of the body is folded up, forming a groove
along its whole length, the gynæcophoric canal, in which the female is lodged during
copulation. This portion of the body has usually a spiral shape, but occasionally
specimens are found with a shape of the English letter C. The males measure
6.3—11* in length and the maximum dorso-ventral thickness is 0.335—0.55. The
body is covered with cuticular tubercles from the commencement of the gynæco¬
phoric canal. The anterior portion of the body is free from these tubercles.
The tubercles are somewhat; larger on the dorsal than on the ventral aspect and
those on the extreme posterior end are very inconspicuous. The gyanæcophoric
canal is covered entirely with fine spines.
The oral sucker is obliquely placed, its anterior tip projecting more forwards
than the posterior one. It measures 0.22—0.255 × 0.19—0.23. Its walls are very
thick and its lumen is funnel-shaped, which terminates at the commencement of the
alimentary canal. The union of this sucker with the rest of the body is sharply
demarcated. It is covered with fine spines. The ventral sucker measuring
0.22—0.335 in diameter, is larger than the oral sucker. It is borne on a very large
peduncle and is also covered with spiny processes.
The alimentary canal commences at the bottom of the funnel-shaped depression
of the oral sucker. The pharynx is absent. The œsophagus is a thin-walled tube
about 0.66 wide, but its outline appears to be usually irregular, probably on account
of the food matter contained in it. It is surrounded by the œsophageal glands,
special aggregations of which are noticed at its anterior and posterior ends where
it is also somewhat dilated. The aggregation of the œsophageal glands at the
posterior end is more prominent. It is 0.317—0.51 long and ends immediately
anterior to the ventral sucker where it bifurcates into two intestinal cæca. These
latter pass on either side of the body of the worm, close under the cuticle and have
an irregularly straight course. They join near the posterior end of the worm and
this point of the commencement of the common cæcum is found between a sixth and
a fourth of the entire length of the worm from its posterior extremity. As a rule
the intestinal cæcum does not divide, but in one instance only it was observed to
divide and unite again. It usually ends 0.6—0.7 from the posterior extremity of
the body.
The excretory system, as far as could be made out, consists of a bladder opening
at the posterior end, which bifurcates into two arms passing anteriorly along the
* All measurements in millimeters.
340 THE INDIAN JOURNAL OF VETERINARY SCIENCE AND ANIMAL HUSBANDRY [II, IV
sides of the body. The point of bifurcation lies at a distance of 0.09 from the
posterior extremity.
Out of the ten toto preparations of males that were studied, two had three
testes, five had four, two had five and only one had six. They lie just beneath the
cuticle, in one row, on the dorsal aspect, posterior to the union of the anterior
portion of the worm with the rest of the body. Their shape and size varies very
much. They may be round, oval or somewhat irregular. The smallest of them
measured 0.033 × 0.021 and the largest 0.14 × 0.076. In the majority of the
specimens it was found that the anteriormost testis was the largest in size. They
may lie side by side, overlap each other or may in some cases be separated from one
another by some distance. Immediately anterior to the first testis is the vesicula
seminalis which in preserved specimens appears oval, elliptical or pear-shaped. It
measures 0.032 — 0.038 × 0.02 - 0.03. In the majority of instances it was found
filled with sperms. From this proceeds a fine canal known as the ejaculatory duct
which opens on the ventral surface almost at the commencement of the ventral
groove. It measures 0.082 — 0.088 in length. The muscular cirrus found in other
trematodes is absent.
Female.—The female is cylindrical, more or less like a whip, the posterior
portion being thicker than the anterior. Both the extremities are tapering. The
posterior portion of the body appears to be somewhat dark on account of the black
intestinal contents and the development of the vitellaria. It lodges in the gynæco¬
phoric canal of the male worm during copulation and is seen with some parts
projecting externally on account of its greater length. It measures 8.25 — 11 in
length and the maximum thickness attained in the region of the common intestinal
cæcum is 0.103 — 0.203.
The cuticle of the body is smooth except the posterior end which bears small
spines.
The oral sucker is oblique and is not so distinct as in the case of the male. It
is small, spiny and less muscular and measures 0.05 - 0.1 × 0.037 - 0.048. The
ventral sucker in the majority of cases is not visible externally, but can be seen
retracted within the body. In one instance only, out of seven stained preparations
examined, could it be seen outside the body. It is circular and measures 0.038 -
0.041 in diameter.
The oral sucker is immediately followed by the œsophagus, the pharynx being
absent. It measures 0.106- 0.18 in length. No great development of the œsopha-
geal glands around it is seen, as in the case of the male. It bifurcates into two
intestinal cæca which pass posteriorly along the sides of the body for a distance of
4.42 - 6.3 and unite to form a common intestinal cæcum. This latter passes
IDENTITY OF SCHISTOSOME IN BOVINE NASAL GRANULOMA.
341
straight posteriorly and ends at a distance of 0.106 — 0.3 from the posterior end.
The length of this cæcum is 4.28 — 5.23.
The ovary is an oval body measuring 0.184 — 0.27 × 0.078 — 0.146. In pre-
served specimens its shape is invariably disfigured. It is situated slightly in front
of the union of the intestinal cæca. The oviduct arises from its posterior aspect
and after a short course passes anteriorly. In front of the ovary it is surrounded
by a small shell gland. The uterus is seen in front of the ovary as a thin zigzag
duct, which later takes a straight course in the intercæcal region and opens to the
exterior immediately posterior to the ventral sucker.
The vitelline follicles are seen in the region of the common intestinal cæcum
arranged in one row on either side of it throughout its length. Occasionally a few
follicles may extend beyond the posterior extremity of the cæcum or they may stop
short of it by a few of them on one side or the other or both.
The majority of the specimens obtained from the nasal granuloma tissue did
not contain any ova in their uterus. These were seen only in a few instances and
in no case was more than a single ovum seen in the uterus. The egg from the
uterus measured 0.300 × 0.043 and those from the tissue or nasal discharge in
which the embryo was developing measured 0.336 — 0.41 × 0.038 — 0.073. They
are assymetrical with a bulging on one side, called for convenience of description
the upper side, and assume different shapes. The eggs present in the uterus (Plate
XXVI, fig. 4) have usually the lower side almost straight as is shown in Mont-
gomery's [ 1906 ] figure of S. spindalis, but this is not the rule; some of the eggs in
the nasal discharge or those liberated in the tissue have also a straight lower side
(Plate XXVII, fig. 2a). Usually the lower side shows a more or less degree of curva-
ture. In extreme cases they are much curved and appear like a " boomerang " or
a " Napolean's hat" (Plate XXVII, fig. 26). In cases in which the embryo is fully
developed inside they have a very large bulging centrally on the dorsal side (Plate
XXVII, fig. 2c), which corresponds probably to some organ of the developing
embryo. In many cases it was noticed that the same egg presents different
appearances when viewed in different positions (Plate XXVII, figs. 2a and. d).
Both the ends of the eggs are drawn out. At one end is a spine measuring
0.010 — 0.015 in length and the other end is blunt. In addition to these charac-
teristic eggs various other forms of eggs are often seen in the nasal discharge
(Plate XXVII, fig. 1). These varying forms as described by Datta [ 1932 ] are (a)
a non-spined globular egg, (b) a rounded or ovoid egg with a single terminal spine
which may be short or long; slender throughout the length or broad at the base
and (c) an ovoid elongated egg with double terminal spine. An explanation to the
production of many different kinds of ova by the same species of Schistosomes has
342 THE INDIAN JOURNAL OF VETERINARY SCIENCE AND ANIMAL HUSBANDRY [II, IV
been offered very recently by MacHattie and Chadwick [ 1932 ] who attribute it to
the action of the sphincter which is present at the opening of the duct of the shell
gland into the ootype. They have also given actual figures of various novel forms
of eggs thus produced in the case of schistosoma bovis [ Sonsino, 1876]. The appear
ance of the hæmatobium-like eggs in the species S. mattheei Veglia and Le Roux, 1929,
which is considered as a synonym of S. bovis has also been explained on the same
hypothesis.
Identity.—Before offering any remarks on the identity of this parasite it will
be instructive to compare in a tabular form some important features of this parasite
with those of S. spindalis Montgomery, 1906. It is rather surprising to find that
although many workers in India, e.g., Soparkar [ 1921 ], Liston and Soparkar [1918]
and Fairley and Jasudasan [ 1927 ], Fairley and Mackie [1925] have worked on the
other aspects of the species S. spindalis Montgomery, 1906, nobody since the origi
nal author has touched the morphological side of the parasite which presents, as
will be seen later, such interesting features. The only detailed description of the
species obtainable at present is that of Montgomery himself [ 1906, 2 ]. Vryburg
[ 1907 ] also gave a description of the parasite from the specimens that he had
obtained in Sumatra, but it is restricted to some external features and the measure
ments of the eggs only. Porter [ 1926 ] recorded a new variety which differs from
the original species only in respect of the dimensions of the eggs and the cercaria
which were smaller than in the Indian forms.
_
♂
Cuticle .
Length .
Width .
Oral sucker
Ventral sucker . .
Testes
♀
Length .
Thickness
Oral sucker
Ventral sucker .
Length of paired in
testine
Length of intestinal
cæcum
Ovary . . .
. .
Eggs
S. spindalis, Montgomery,
1906
Tuberculate . . . .
4.5 —12.2 .
0.25 — 0.667
Spiny, 0.3 — 0.306 ×
0.25
Spiny,
pedunculated,
0.267 — 0.357 dia.
6 — 7, 0.085 dia. .
7.17 —14.1 .
0.1 — 0.2 .
0.068 dia. .
Not given
7.702 .
.
.
.
6 . . . .
Post equatorial
Spindleshaped, asymmet
rical.
0.284— 0.400 × 0.044
— 0.072
S. spindalis var.
africana, Porter,
1926
....
....
....
....
....
....
....
....
....
....
....
....
....
....
0.163 — 0.258 ×
0.046 — 0.070
Schistosome found in
nasal granuloma
Tuberculate
6.3 — 11
0.335 — 0.550
Spiny, 0.22 — 0.255 × 0.19
— 0.23
Spiny, pedunculated, 0.22 —
0.335 dia.
3 — 6, 0.33 — 0.14 × 0.021
— 0.076
8.25 —11
0.103 — 0.203
0.05 — 0.1 × 0.037 — 0.048
0.038 — 0.041 dia.
4.42 — 6.3
4.28 — 5.23
Post equatorial
Spindleshaped, asymmetri
cal
0.3 — 0.41 × 0.036 —0.073
IDENTITY OF SCHISTOSOME IN BOVINE NASAL GRANULOMA.
343
It will be noticed from this table of comparison that the schistosomes found in
cases of nasal granuloma agree in almost all respects with S. spindalis, Montgomery,
1906. A very slight difference is, however, noticed in the dimensions of the body.
The schistosomes of nasal granuloma fail to reach the maximum size attained by
the other schistosomes. This is governed, in all probability by the site of infection.
It is but natural to expect the worms growing in a tough tissue like the nasal
septum do not get so much scope for developing as they do in the portal system or
mesenteric veins. Apart from this the question of the age of the parasites cannot
altogether be ignored.
Another noticeable point of difference is the number of testes. In Montgo-
mery's specimens they are described as varying from 6—7, while in the nasal
granuloma specimens their number varies from 3—6. It may be possible that
Montgomery's observations were confined to the examination of very few specimens
so that he would not notice such a range of variation in this respect, or perhaps all
the specimens that he happened to examine had coincidentally 6 or 7 testes. It is,
moreover, a significant fact that the number of testes in this genus shows a large
degree of variations. The following statement regarding the number of testes in the
existing species of the genus may be instructive :—
Species.
S. hæmatobium . . . . . .
S. mansoni . . . . . .
S. japonicum . . . . . .
S. bovis .
.
.
.
.
.
.
S. indicum . . . . . .
S. rodhaini . . . . . .
No. of testes.
4—5
8—9
6—8
3—6
5—12 (See description of
this species below.)
6—8
It will be evident from this that to the question of the number of testes cannot
be attached much importance; moreover, in the specimens in question the degree of
variation is not so great as is found in the case of S. indicum. As a matter of fact
S. bovis shows the same range variation in respect of the testes.
No other point of difference can be made out between the species S. spindalis
and the Schistosome found in nasal granuloma tissue. It may therefore be concluded
that the schistosome found in the tissue of bovine naeal granuloma in India belongs
to the species S. spindalis, Montgomery, 1906.
344 THE INDIAN JOURNAL OF VETERINARY SCIENCE AND ANIMAL HUSBANDRY [II, IV
The infection of S. spindalis was first discovered in cattle by Montgomery
[1906] at Muktesar. Liston and Soparkar [1918] elucidated their life-history and
discovered that the intermediate host involved in transmitting the parasite was
Indoplanorbis exustus. Starting on the knowledge of the water-inhabiting propen-
sities of buffaloes and their close association with the intermediate host in this
habitat, Fairley and Jasudasan [1927] stated that the water-buffalo was the defini-
tive host of this parasite, but it has since been found that goats are also capable of
being infected with this parasite, and a case of natural infection of sheep due to this
parasite is also known to the writer. In view of these facts the immunity of other
animals, particularly buffaloes, to nasal granuloma is difficult to explain, but it is
possible that the secretions from the nose of other animals than cattle are inimical
to the development of this parasite in this location.
SOME VARIATIONS OCCURRING IN THE SPECIES SCHISTOSOMA SPIND
(Plate XXVIII, figs. 1—4.)
A large number of parasites were obtained from the portal and mesenteric
veins of the same two plains bulls, from which the nasal granuloma parasites were
collected. Another lot of these parasites from a sheep collected in Madras were
kindly handed over to the writer by Mr. F. Ware, the Director of this Institute.
An examination of these parasites revealed that they belong to the species S. spin¬
dalis : the females showing typical asymmetrical, spindle-shaped ova with a terminal
spine. These parasites, however, show some interesting variations, particularly in
respect of the form of the body, in the development of the tubercles on the cuticle
and the size of the eggs.
These parasites are either straight or bent like the English letter C. They
were in no case coiled like the parasites of nasal granuloma. In size also they were
somewhat larger than the latter parasites.
The cuticle of the parasites from the portal and mesenteric veins had no deve-
lopment of any tubercles on it, and it was absolutely smooth. The specimens
obtained from a sheep were no doubt tuberculated, but. the tubercles were not so
conspicuous and large as in the case of the nasal granuloma parasite. It therefore
transpires from this that the same species of schistosome may show variation in the
development of the tubercles on the cuticle, and it may even be completely devoid
of them. The same phenomenon was observed in the case of S. turkestanicum
obtained from goats in Irak. One fact, however, was found to be constant in both
the species that the tuberculated specimens were somewhat smaller in size and had a
tendency to coil, while the non-tuberculated forms were more elongated, slender
and straight. It would be an interesting point to investigate whether such varia-
tions of forms and cuticle occur in other species of schistosomes besides these two.
IDENTITY OF SCHISTOSOME IN BOVINE NASAL GRANULOMA.
345
Among the specimens of S. indicum from various sources I was able to find a large
number of individuals showing moderately developed tubercles, but a few of them
had only a very slight development of these.
In this connection it may be remarked that the tuberculate or non-tuberculate
nature of the cuticle should not be considered as of any value in distinguishing one
species of schistosome from another.
The uterine eggs of these specimens are somewhat smaller in size than those
in the case of typical spindalis ova. They converge more towards the variety
africana Porter, 1926, in which case they measure 0.163—0.258×0.0464—0.070.
A few measurements made in the case of these parasites from the portal and
mesenteric vessels of a bull are given below :—
Male.—Length 5.6—13.5. Dorso-ventral thickness 0.171—0.326. Oral sucker
0.206—0.29×0.136—0.33. Ventral sucker 0.18—0.32×0.04—0.12. The distance
between the oral sucker and the ventral sucker is 0.29—0.44. Œsophagus 0.262—
0.37 long. Intestinal cæca 3.2—9.1 long. Common intestinal cæcum l.82—4 long.
The distance from the end of the cæcum to the posterior extremity is 0.11—0.151.
Number of testes 3—6. Dimensions of the testes 0.3—0.08×0.026—0.068. Vesi¬
cula seminalis 0.03—0.068. Ductus ejaculatorius 0.2 long. Stem of excretory
bladder 0.104.
Female.—Length 7.18—16.2. Width 0.095—0.143. Oral sucker 0.044—0.086 ×
0.023—0.043. Ventral sucker 0.037—0.048 × 0.016. The distance between the oral
and the ventral sucker 0.15—0.133. Œsophagus 0.112—0.156 long. Intestinal
cæca 2.8—8.8 long. Common intestinal cæcum 4.19—6.93. The end of cæcum
from the posterior extremity 0.7—0.27. Ovary 0.272—0.5×0.073—0.1. Eggs in
uterus 0.16—0.248×0.02—0.032.
Schistosoma indicum Montgomery, 1906.
Synonym. Bilharzia indica Montgomery, 1906 ; Hutyra and Marek, 1910.
(Plate XXIX, figs. 1—3.)
Up to the present time this species has been recorded only from the horse,
donkey, camel and sheep in India. The material at my disposal was obtained
from horses, goats, sheep and cattle at Muktesar, from plains cattle imported here
from Bihar, from sheep in Karachi and goats in Madras, the last named being
kindly given to me by Mr. F. Ware. It is an interesting fact to note here that
there exists up to the present time no record of the occurrence of this parasite in
cattle and goats, this forming therefore the first one of its kind.
Montgomery [1906, 1] gave quite a good account of this parasite, but there are
some points of interest which require re-examination, as a result of the study of the
diverse material at my disposal.
346 THE INDIAN JOURNAL OF VETERINARY SCIENCE AND ANIMAL HUSBANDRY [II, IV
Male.—Montgomery remarks that two types of specimens can be distinguished
as follows :—
(a) " Those tending to assume the straight position, larger, whiter in colour,
and the body much more transparent. The ventral sucker is distinctly
pedunculated and the testes easily seen. Usually there is a well defined
band of spines running along the outer surface of the lateral wall of the
gynæcophoric canal."
(b) " Those which are found considerably coiled and distorted, smaller in size,
of a dull cream colour and almost opaque. The ventral sucker is more
or less flattened against the body and the testes indistinguishable. The
spines on the body are more irregularly distributed over the surface. "
From a study of the specimens at my disposal I could corroborate only the
first point raised by Montgomery, viz., that some specimens are straight and some
are coiled, some, moreover, are much larger than others. I could not mark the
difference in colouration of the specimens since all the preserved specimens at my
disposal were white in colour. I could also verify the truth of Montgomery's state-
ment "It was rare to find both the kinds present in the same animal " Most of
the specimens from horses were coiled, only a few being straight. The specimens
from a bull were either straight, C-shaped or S-shaped. The specimens from the
sheep at Muktesar were almost straight and those from goats were straight, C-shaped
or slightly curved. In regard to the other three points raised by Montgomery I
could not find any constancy. The ventral sucker was seen pedunculated or almost
flat with the body both in coiled and straight specimens. The same thing was
true in regard to the band of spines. I examined about 30 stained preparations,
but in none of them was any relation between the clarity of the testes and the type
of the specimen noticed. In a few of my preparations the testes were indistinct,
but this could not be correlated with the type of the specimen.
Montgomery refers to the constrictions at varying points of the œsophagus.
This condition is accentuated by the development of the œsophageal glands
surrounding the œsophagus, greater development of which is seen at its anterior
and posterior end, particularly the latter. The area between these two ends has
poor development of the œsophageal glands and for this reason the oesophagus
appears constricted.
The length of the intestinal cæca is to eight times the length of the common
cæcum. I think this is true even of Montgomery's specimens although he makes no
mention of this.