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Pathology of lesions observed in whales flensed at Saldanha Bay, South Africa
J. COMP. PATH.
1966.
VOL.
PATHOLOGY FLENSED
OF AT
407
76.
LESIONS
OBSERVED
SALDANHA
BAY,
SOUTH
IN
WHALES AFRICA
BY
C. J. UYS Department of PatholoD, University of Cape Town Medical School, Observatory, C.P., South Africa and
P. B. BEST Division of Sea Fisheries, Cape Town, South Africa INTRODUCTION
are few reports on the pathology of lesions in the Cetacea, and the majority of studies have utilised material collected from whales killed on whaling expeditions.
There
It is of interest that neoplasms are listed quite frequently among lesions described, and include the following benign tumours : 3 granulosa-cell tumours and 1 mutinous cystadenoma of the ovary (Rewell and Willis, 1949); fibromyomata of the uterus (Rewell and Willis, 1949; Stolk, 1950); ganglion neuroma (Rewell and Willis, 1950); multiple fibromata of the skin and lower jaw (Rewell and Willis, 1950; Stolk, 1952, 1953b; Clarke, 1956); verruca of the skin (Stolk, 1953b); haemangioma and adenoma of the liver (Stolk, 195313); and several lipomatous tumours (Cockrill, 1960). A carcinoma of the ovary and a case of Hodgkin’s disease, both described by Stolk (1950, 1962) are the only records of malignant tumours. The non-neoplastic lesions described include inflammations such as abscesses,mastitis, tonsilitis, colitis, inflammation of muscle (Clarke, 1956; Stolk, 1953a); 4 instances of hepatic cirrhosis (Cockrill, 1960; Stolk, 1953c, 1954); 1 instance of myocardial infarction associated with atherosclerosis of the coronary arteries (Truex, Nolan and Truex, 1961) ; arteriosclerosis (Roberts et al., 1963); and multiple instances of fibromatous “husks” (Cockrill, 1960).
We thus feel it is desirable to record and describe lesions discovered during the examination of over 2,000 carcasesby one of us (P.B.B.) as part of a biological investigation into whales landed at Saldanha Whaling Station, Saldanha Bay (33”S., 18”E.). These details are summarised in Table 1. MATERIALS
AND
METHODS
Formol-fixed and paraffin-embedded tissues were sectioned and stained with haematoxylin and eosin in all cases. In addition, where indicated, further sections were stained with van Gieson’s method for collagen, Wilder’s method for reticulin, the periodic acid Schiff method (P.A.S.) and Perl’s method for haemosiderin. Lipids were demonstrated in frozen sections by Sudan III. In calculating the age of individual whales two methods have been used. For female sei and Bryde whales the annual accumulation of ovarian corpora has been assumed to be comparable to that of the fin whale (0.5 per year) and the age at sexual maturity taken as 10 years. In the interpretation of the laminations in male baleen whale ear plugs and sperm whale teeth a production rate of 1 per year has
PATHOLOGY
408
been assumed. These calculations individual ages.
OF WHALE
LESIONS
are thus only very approximate
estimates of
RESULTS
Neoplastic Lesions Only 2 neoplasms, both benign, were found comprising multiple fibromyomata in 1 whale and a melanotic tumour of the lip in another. Fibromyomata of uterus. These were from a 35 ft. (10.7 m.) female sperm whale (Physetcr catodon), approximately 19 years old, and presented as a mass weighing 1,121 g. and measuring 13 x 12 x 8.5 cm. in the wall of the right uterine cornu, and as a smaller, but similar growth, in the left uterine cornu. When sectioned they were firm and fibrous in consistency and their cut surfaces had the typical whorled appearance of a fibromyoma (Fig. 1). No degenerative changes were noted. Histologically, these masses were composed of wellTABLE LESIONS
OBSERVED
Nature of hion Multiple fibromyomata Benign melanotic tumour
IN
2,000
WHALES
1 FLENSED
AT SALDANM
Site Uterus Upper lip
BAY,
S.A.
species Sperm Sei
“vo.of w?K?L?s :
Non-neoplastic Focal muscle and fat necrosis with replacement fibrosis Necrotic renal mass Necrotic endometrial mass Caseous necrosis associated with a tuberculoid inflammatory reaction Ductal obstruction with ectasia Moderate siderosis + fatty change Anal tonsil
Muscle back and jaw; adipose tissue around lungs and viscera Inside kidney Left uterine comu Right testis and epididymis
Sei (11) and W-de (1) Bryde Sei Blue
Right mammary gland Liver Peri-anal skin
Sei Sei Sperm
12 2 : t 1
differentiated smooth muscle and connective tissue fibres arranged in fasciculated bundles (Fig. 2). These diagnostic appearances very closely simulated those of the human fibromyoma. Benign melanotic tumour. The lesion appeared as a rounded dark nodule, 1.5 cm. in diameter, on the lip of a female sei whale (Bdaenoptera borealis) 51 ft. (15.5 m.) in length and approximately 48 years old. The cut surface had a jetblack featureless appearance (Fig. 3). Histologically, the nodule was composed of sheets of cells heavily packed with melanin granules which obscured all cytological detail (Fig. 4). Another feature was the number of well-formed arteries and arterioles in the stroma of the nodule. After bleaching the melanin with hydrogen peroxide, the cells were noted to have the vesicular nuclei and prominent nucleoli of melanocytes, but on the whole more cytoplasm. While the surface epithelium covering the nodule contained abundant melanin, no junctional activity could be demonstrated at the epidermal-dermal junction. The overall
C. J. UYS
AND
P. B. BEST
appearances of this growth suggested a hamartomatous proliferation melanocytes and arterial-type blood vessels. Tissue Necrosis with Formation
of Tumour-like
409 involving
Masses
Focal tissue necrosis, occurring at a variety of sites and presenting as a tumourlike mass showing various degrees of fibrous replacement, was the commonest non-neoplastic lesion. Taking into consideration the appearances and location of these massesthey are described under the following headings. Necrosis of muscle or fat with replacement fibrosis. These masses, found in 13 whales (12 sei and 1 Bryde, Balaenoptera edenzJ one of which was less than 10 years and the other about 14 years old, usually occurred in the back muscles grouped together in fibrous-walled pockets measuring 30 to 60 cm. in length by 7 to 10 cm. in width, each pocket containing up to 6 separate masses.However, in 1 whale the masses occurred in muscle near the articular surface of the mandible. Another whale, as well as having the muscular masses,showed similar ones on the pleural and peritoneal surfaces of the viscera, and in another, approximately 20 years old, a mass was found in the mammary gland. In 2 others, one a Bryde whale about 13 and the other a sei whale about 17 years old, the masseswere confined to the fat bodies on the surface of the lungs, while 3 whales also had similar massesin the peritoneal fat of the inguinal region. Individually these masses were flattened and oval, had smooth glistening external surfaces and measured up to 6 cm. in diameter (Figs. 5 and 6). When sectioned they were composed of rubbery, yellowish translucent tissue in which were obvious gritty foci of calcification with a putty-like appearance on the cut surface. Histologically the appearances were those of muscle and fat necrosis of varying duration and associated replacement fibrosis. Striated muscle was observed in the earliest lesions, in which not only the fibres but all stromal elements including vessels showed complete necrosis as in infarction. The necrotic fibres retained their outlines, but had lost their normal nuclear and cytoplasmic staining. Signs of an accompanying reactive acute inflammatory response were minimal (Fig. 7). In the older lesions the necrotic muscle fibres were barely recognisable and prrsented as distorted shrunken cells or as eosinophilic granular debris showing hasophilic foci of calcification. The necrotic tissue was encapsulated and replaced to varying degrees by dense, relatively acellular collagen in which scanty aggregates of pigment and lipid-laden macrophages occurred. Some of the pigment proved to be haemosiderin, but most of it resembled lipofuscin and except for being Schiff-positive gave negative staining reactions. In the smaller lesions, particularly those around the lungs, and in those of longest duration, fibrous replacement was complete (Fig. 8). As expected where the necrosis involved adipose tissue, larger numbers of lipid-filled phagocytes were demonstrated (Fig. 9). No parasitic remnants or any other causative factors could be demonstrated in any of these lesions. 1\‘ecrotic renal and endometrial masses. In 2 Bryde whales, approximately 8 and 14 years old, solitary pale masseswere seen inside the kidney. Histologically both lesions were similar and consisted of very autolysed, completely necrotic tissue, in which moderate numbers of disintegrating polymorphonuclears were
410
PATHOLOGY
OF
WHALE
LESIONS
recognisable. The tissue could not be identified, but at the edge of one mass a little viable tissue remained which was composed predominantly of smooth muscle. If this tissue is a reflection of the structure of the entire mass, then it may well be a necrotic leiomyoma. Neither mass showed evidence of replacement fibrosis. Remnants of parasites were carefully sought for, but not demonstrated. In 1 sei whale, approximately 40 years old, a structure (1 x 1.5 cm. in size) found lying free in the left uterine comu proved to be necrotic endometrium surrounded by a fibrous capsule. Gaseous Necrosis of Epididymis
and Testis
In a blue whale (Balaenoptera musculus), length 66 ft. (20.1 m.), the right testis was enlarged (42,620 g.) and fi rm, and when sectioned had a fibrous consistency. The epididymis appeared prominent and showed ducts containing solid yellow material. The contralateral testis was normal in size (8,440 g.) and appearance. Histologically, no normal epididymis was recognisable. The tissue was replaced by foci of caseous necrosis which were surrounded by epithelioid cells, lymphocytes, plasma cells and occasional eosinophiles. In the body of the testis similar changes were noted except that caseation was more extensive and acute in appearance (Fig. lo), the overall picture being that of a tuberculoid lesion which in many ways resembled that of human tuberculosis. No acid-fast bacilli were demonstrated by Ziehl-Neelsen stain and no other organisms noted. Duct Obstruction
of Right
Mammary
Gland
The right mammary gland of a 51 ft. (15.5 m.), pregnant sei whale approximately 36 years old, showed very wide and ectatic ducts. The corresponding nipple was deformed and no external opening could be demonstrated. Microscopically the gland showed the lobular proliferation of a prelactating breast. A notable feature was the degree of ductular and ductal dilatation throughout the gland tissue with retention of an amorphous eosinophilic substance in the lumina. The acinar lining cells showed some atrophy. These changes conform with those of duct obstruction of some duration, and their diffuse distribution suggests obstruction of the major ducts as would occur in a lesion of the nipple. Siderosis and Fatty Change of the Liver The liver of a 50 ft. (15.2 m.) pregnant sei whale, approximately 16 years old, showed brown patches. Microscopically these areas revealed diffuse siderosis with haemosiderin appearing in the cytoplasm of the liver cells and in enlarged Kupffer cells. The cells in the periportal zones of the lobule contained more haemosiderin than those in the central areas. In addition, there were sharplyoutlined foci, cornposed of several lobules at a time, of diffuse fatty change of the liver cells (Fig. 11). Anal ccTonsilS)
Six sperm whales showed numerous lumps externally around the anal opening.
C.
J.
UYS
AND
P.
B.
BEST
411
One measured 4.5 cm. in diameter, and consisted of a rounded pale maSS covered by skin which had multiple pits on the external surface (Fig. 12); the tissue was soft and the cut surface had a greyish appearance. Histologically the mass consisted of well-differentiated lymphoid tissue covered by squamous epithelium. Epithelial-lined crypts extended from the surface into the lymphoid tissue as in mammalian faucial tonsils. A degree of follicular hyperplasia was apparent, and the crypts contained an acute inflammatory cellular infiltrate of polymorphonuclears, which also extended into the lining epithelium. Plasma cells were abundant in lymphoid tissue. Similar lumps were found at the base of the tongue in 2 sperm whales. DISCUSSION
To the list of known neoplasms recorded in Cetacea these findings add a further instance of multiple uterine fibromyomata and of a benign melanotic tumour of the lip, a neoplasm previously not recorded. The appearances of both tumours closely simulate those of related lesions found in other mammalian species. Other lesions, hitherto undescribed in whales and of interest, are siderosis and fatty change of the liver and caseous necrosis of the testis, the latter being histologically similar to tuberculosis of the testis. Although no acid-fast bacilli were demonstrated the possibility that a species of Mycobucterium was responsible for the lesion cannot be excluded. As the nature of the lesion was not suspected initially no unfixed tissues were available for further investigation. Besides these new records, which are not surprising considering the small amount of material so far examined by pathologists, the present report represents the first collection of lesions from sei and Bryde whales. It is significant that as with other reports on the lesions of baleen whale species, tumour-like masses, particularly of dorsal muscles and of adipose tissue around the viscera, constitute the most frequent finding. These masses are referred to colloquially among whalermen, as “husks”, and their occurrence is well-known, though their aetiology remains unexplained. Cockrill (1960) considers they may be parasitic in origin. Our findings indicate that these lesions are essentially focal areas of infarct-like tissue necrosis. In late lesions the necrotic tissues undergo fibrous encapsulation and may be completely or partially replaced by fibrous tissue. The aetiology of the necrosis is not obvious, but there is no evidence of parasitic infestation. The mild inflammatory signs observed are not to be interpreted as an indication of underlying infection and constitute a reaction to tissue necrosis. While trauma cannot be completely excluded as a mechanism of the necrosis, the location of some lesions is against this explanation. Whereas the lesions of the jaw and back muscles are at sites which may be more prone to trauma in a whale, this hardly can be said of pleural and peritoneal fat which are the sites involved next in frequency. Finally, gaseous emboli are known to produce ischaemia and tissue necrosis, and one wonders whether a similar mechanism may be responsible for the initial tissue necrosis in the whale whose marine environment and mode of existence must subject it to decompression stresses. NO doubt under normal conditions physiological adaptations enable this mammal to compensate for the phenomenon, but this doa not rule out the possibility that under abnormal conditions air embolism ma)r sometimes occur.
F
412
PATHOLOGY
OF
WHALE
LESIONS
CONCLUSIONS
The lesions observed in 2,000 whales flensed at Saldanha Whaling
Station in
South Africa are described. Significant amongst these were two benign neoplasms, consisting of multiple uterine fibromyomata, a benign melanotic tumour of the lip in a sperm and sei whale respectively, multiple fibromatous masses (husks) of skeletal muscle and adipose tissue in sei and Bryde whales. The last appear to be the result of spontaneous tissue necrosis with subsequent fibrous replacement or encapsulation of the necrotic tissue. The mechanism of necrosis is not obvious, but possible causes are discussed. REFERENCES
Clarke, R. (1956). Discovery Rep., 28, 237. Cocknll, W. Ross (1960). Bit. vet. I., 116, 113, 175. Rewell, R. E., and Willis, R. A. (1949). J. Path. Bact., 61, 454; (1950). Ibid., 62,450. Roberts, J. C. (Jnr.), Brown, D. H., and Brice, R. C. (1963). Circulufion, 2%, 670. Stolk, A. (1950). Amsterdam Naturalist, 1, 1; (1952). Proc. Kon. Ned. Akud., v. Wetensch., SC, 275; (1953a). Ibid., SC, 364; (195313).Ibid., 369; (1953c). Ibid., 375; (1954). Ibid., 57C, 258; (1962). Ibid., 65C, 250. Truex, R. C., Nolan, F. G., and Truex, R. C. (Jnr.) (1961). Anut. Rec., 141, 325. [Received
for
publication,
LEGENDS
TO
December
8th, 19651
ILLUSTRATIONS
Fig. 1. Slices of uterine fibromyoma of sperm whale showing the typically whorled cut surface Scale in cm. Fig. 2. Fibromyoma showing bundles of spindle-celled smooth muscle fibres with little connective tissue interspersed. H. & E. x 72. Fig. 3. Benign melanotic tumour of sei whale. Scale in cm. Fig. 4. Benign subepidermal melanoma showing closely-packed masses of melanin-packed cells. The profusion of vascular channels is also obvious. H. & E. x 72. Figs. 5 and 6. Masses of necrotic muscle which have been encapsulated and partially replaced by fibrous tissue. Fig. 7. Recent necrosis of voluntary muscle. The nuclear staining of sarcolemmal sheaths has been almost lost. H.&E. x 72. Fig. 8. Long-standing necrosis of muscle. Necrotic muscle fibres have disintegrated and are replaced eripherally by collagenous fibrous tissue. H. & E. x 72. Fig. 9. % ng-standing fat necrosis. Necrotic fat cells are replaced by lipid-laden macrophages and fibrous tissue. x 72. Fig. 10. An area of caseous necrosis of the testis demarcated by proliferating epithelioid cells and fibroblasts. H. & E. x 72. Fig. 11. Fatty change of liver cells. H. & E. x 36. Fig. 12. Anal “tonsils”. The openings of the crypts can be seen on the external surface (left). Scale in cm.
C.
1IIiii]fIi
J.
I/‘:(
i6
UYS
AND
!I!!,
I7
P.
B.
BEST
‘,’
8
9
PATHOLOGY
OF
WHALE
LESIONS
C.
J.
UYS
AND
P.
B.
BEST
PATHOLOGY,OF
WHALE
LESIONS
1966.
VOL.
PATHOLOGY FLENSED
OF AT
407
76.
LESIONS
OBSERVED
SALDANHA
BAY,
SOUTH
IN
WHALES AFRICA
BY
C. J. UYS Department of PatholoD, University of Cape Town Medical School, Observatory, C.P., South Africa and
P. B. BEST Division of Sea Fisheries, Cape Town, South Africa INTRODUCTION
are few reports on the pathology of lesions in the Cetacea, and the majority of studies have utilised material collected from whales killed on whaling expeditions.
There
It is of interest that neoplasms are listed quite frequently among lesions described, and include the following benign tumours : 3 granulosa-cell tumours and 1 mutinous cystadenoma of the ovary (Rewell and Willis, 1949); fibromyomata of the uterus (Rewell and Willis, 1949; Stolk, 1950); ganglion neuroma (Rewell and Willis, 1950); multiple fibromata of the skin and lower jaw (Rewell and Willis, 1950; Stolk, 1952, 1953b; Clarke, 1956); verruca of the skin (Stolk, 1953b); haemangioma and adenoma of the liver (Stolk, 195313); and several lipomatous tumours (Cockrill, 1960). A carcinoma of the ovary and a case of Hodgkin’s disease, both described by Stolk (1950, 1962) are the only records of malignant tumours. The non-neoplastic lesions described include inflammations such as abscesses,mastitis, tonsilitis, colitis, inflammation of muscle (Clarke, 1956; Stolk, 1953a); 4 instances of hepatic cirrhosis (Cockrill, 1960; Stolk, 1953c, 1954); 1 instance of myocardial infarction associated with atherosclerosis of the coronary arteries (Truex, Nolan and Truex, 1961) ; arteriosclerosis (Roberts et al., 1963); and multiple instances of fibromatous “husks” (Cockrill, 1960).
We thus feel it is desirable to record and describe lesions discovered during the examination of over 2,000 carcasesby one of us (P.B.B.) as part of a biological investigation into whales landed at Saldanha Whaling Station, Saldanha Bay (33”S., 18”E.). These details are summarised in Table 1. MATERIALS
AND
METHODS
Formol-fixed and paraffin-embedded tissues were sectioned and stained with haematoxylin and eosin in all cases. In addition, where indicated, further sections were stained with van Gieson’s method for collagen, Wilder’s method for reticulin, the periodic acid Schiff method (P.A.S.) and Perl’s method for haemosiderin. Lipids were demonstrated in frozen sections by Sudan III. In calculating the age of individual whales two methods have been used. For female sei and Bryde whales the annual accumulation of ovarian corpora has been assumed to be comparable to that of the fin whale (0.5 per year) and the age at sexual maturity taken as 10 years. In the interpretation of the laminations in male baleen whale ear plugs and sperm whale teeth a production rate of 1 per year has
PATHOLOGY
408
been assumed. These calculations individual ages.
OF WHALE
LESIONS
are thus only very approximate
estimates of
RESULTS
Neoplastic Lesions Only 2 neoplasms, both benign, were found comprising multiple fibromyomata in 1 whale and a melanotic tumour of the lip in another. Fibromyomata of uterus. These were from a 35 ft. (10.7 m.) female sperm whale (Physetcr catodon), approximately 19 years old, and presented as a mass weighing 1,121 g. and measuring 13 x 12 x 8.5 cm. in the wall of the right uterine cornu, and as a smaller, but similar growth, in the left uterine cornu. When sectioned they were firm and fibrous in consistency and their cut surfaces had the typical whorled appearance of a fibromyoma (Fig. 1). No degenerative changes were noted. Histologically, these masses were composed of wellTABLE LESIONS
OBSERVED
Nature of hion Multiple fibromyomata Benign melanotic tumour
IN
2,000
WHALES
1 FLENSED
AT SALDANM
Site Uterus Upper lip
BAY,
S.A.
species Sperm Sei
“vo.of w?K?L?s :
Non-neoplastic Focal muscle and fat necrosis with replacement fibrosis Necrotic renal mass Necrotic endometrial mass Caseous necrosis associated with a tuberculoid inflammatory reaction Ductal obstruction with ectasia Moderate siderosis + fatty change Anal tonsil
Muscle back and jaw; adipose tissue around lungs and viscera Inside kidney Left uterine comu Right testis and epididymis
Sei (11) and W-de (1) Bryde Sei Blue
Right mammary gland Liver Peri-anal skin
Sei Sei Sperm
12 2 : t 1
differentiated smooth muscle and connective tissue fibres arranged in fasciculated bundles (Fig. 2). These diagnostic appearances very closely simulated those of the human fibromyoma. Benign melanotic tumour. The lesion appeared as a rounded dark nodule, 1.5 cm. in diameter, on the lip of a female sei whale (Bdaenoptera borealis) 51 ft. (15.5 m.) in length and approximately 48 years old. The cut surface had a jetblack featureless appearance (Fig. 3). Histologically, the nodule was composed of sheets of cells heavily packed with melanin granules which obscured all cytological detail (Fig. 4). Another feature was the number of well-formed arteries and arterioles in the stroma of the nodule. After bleaching the melanin with hydrogen peroxide, the cells were noted to have the vesicular nuclei and prominent nucleoli of melanocytes, but on the whole more cytoplasm. While the surface epithelium covering the nodule contained abundant melanin, no junctional activity could be demonstrated at the epidermal-dermal junction. The overall
C. J. UYS
AND
P. B. BEST
appearances of this growth suggested a hamartomatous proliferation melanocytes and arterial-type blood vessels. Tissue Necrosis with Formation
of Tumour-like
409 involving
Masses
Focal tissue necrosis, occurring at a variety of sites and presenting as a tumourlike mass showing various degrees of fibrous replacement, was the commonest non-neoplastic lesion. Taking into consideration the appearances and location of these massesthey are described under the following headings. Necrosis of muscle or fat with replacement fibrosis. These masses, found in 13 whales (12 sei and 1 Bryde, Balaenoptera edenzJ one of which was less than 10 years and the other about 14 years old, usually occurred in the back muscles grouped together in fibrous-walled pockets measuring 30 to 60 cm. in length by 7 to 10 cm. in width, each pocket containing up to 6 separate masses.However, in 1 whale the masses occurred in muscle near the articular surface of the mandible. Another whale, as well as having the muscular masses,showed similar ones on the pleural and peritoneal surfaces of the viscera, and in another, approximately 20 years old, a mass was found in the mammary gland. In 2 others, one a Bryde whale about 13 and the other a sei whale about 17 years old, the masseswere confined to the fat bodies on the surface of the lungs, while 3 whales also had similar massesin the peritoneal fat of the inguinal region. Individually these masses were flattened and oval, had smooth glistening external surfaces and measured up to 6 cm. in diameter (Figs. 5 and 6). When sectioned they were composed of rubbery, yellowish translucent tissue in which were obvious gritty foci of calcification with a putty-like appearance on the cut surface. Histologically the appearances were those of muscle and fat necrosis of varying duration and associated replacement fibrosis. Striated muscle was observed in the earliest lesions, in which not only the fibres but all stromal elements including vessels showed complete necrosis as in infarction. The necrotic fibres retained their outlines, but had lost their normal nuclear and cytoplasmic staining. Signs of an accompanying reactive acute inflammatory response were minimal (Fig. 7). In the older lesions the necrotic muscle fibres were barely recognisable and prrsented as distorted shrunken cells or as eosinophilic granular debris showing hasophilic foci of calcification. The necrotic tissue was encapsulated and replaced to varying degrees by dense, relatively acellular collagen in which scanty aggregates of pigment and lipid-laden macrophages occurred. Some of the pigment proved to be haemosiderin, but most of it resembled lipofuscin and except for being Schiff-positive gave negative staining reactions. In the smaller lesions, particularly those around the lungs, and in those of longest duration, fibrous replacement was complete (Fig. 8). As expected where the necrosis involved adipose tissue, larger numbers of lipid-filled phagocytes were demonstrated (Fig. 9). No parasitic remnants or any other causative factors could be demonstrated in any of these lesions. 1\‘ecrotic renal and endometrial masses. In 2 Bryde whales, approximately 8 and 14 years old, solitary pale masseswere seen inside the kidney. Histologically both lesions were similar and consisted of very autolysed, completely necrotic tissue, in which moderate numbers of disintegrating polymorphonuclears were
410
PATHOLOGY
OF
WHALE
LESIONS
recognisable. The tissue could not be identified, but at the edge of one mass a little viable tissue remained which was composed predominantly of smooth muscle. If this tissue is a reflection of the structure of the entire mass, then it may well be a necrotic leiomyoma. Neither mass showed evidence of replacement fibrosis. Remnants of parasites were carefully sought for, but not demonstrated. In 1 sei whale, approximately 40 years old, a structure (1 x 1.5 cm. in size) found lying free in the left uterine comu proved to be necrotic endometrium surrounded by a fibrous capsule. Gaseous Necrosis of Epididymis
and Testis
In a blue whale (Balaenoptera musculus), length 66 ft. (20.1 m.), the right testis was enlarged (42,620 g.) and fi rm, and when sectioned had a fibrous consistency. The epididymis appeared prominent and showed ducts containing solid yellow material. The contralateral testis was normal in size (8,440 g.) and appearance. Histologically, no normal epididymis was recognisable. The tissue was replaced by foci of caseous necrosis which were surrounded by epithelioid cells, lymphocytes, plasma cells and occasional eosinophiles. In the body of the testis similar changes were noted except that caseation was more extensive and acute in appearance (Fig. lo), the overall picture being that of a tuberculoid lesion which in many ways resembled that of human tuberculosis. No acid-fast bacilli were demonstrated by Ziehl-Neelsen stain and no other organisms noted. Duct Obstruction
of Right
Mammary
Gland
The right mammary gland of a 51 ft. (15.5 m.), pregnant sei whale approximately 36 years old, showed very wide and ectatic ducts. The corresponding nipple was deformed and no external opening could be demonstrated. Microscopically the gland showed the lobular proliferation of a prelactating breast. A notable feature was the degree of ductular and ductal dilatation throughout the gland tissue with retention of an amorphous eosinophilic substance in the lumina. The acinar lining cells showed some atrophy. These changes conform with those of duct obstruction of some duration, and their diffuse distribution suggests obstruction of the major ducts as would occur in a lesion of the nipple. Siderosis and Fatty Change of the Liver The liver of a 50 ft. (15.2 m.) pregnant sei whale, approximately 16 years old, showed brown patches. Microscopically these areas revealed diffuse siderosis with haemosiderin appearing in the cytoplasm of the liver cells and in enlarged Kupffer cells. The cells in the periportal zones of the lobule contained more haemosiderin than those in the central areas. In addition, there were sharplyoutlined foci, cornposed of several lobules at a time, of diffuse fatty change of the liver cells (Fig. 11). Anal ccTonsilS)
Six sperm whales showed numerous lumps externally around the anal opening.
C.
J.
UYS
AND
P.
B.
BEST
411
One measured 4.5 cm. in diameter, and consisted of a rounded pale maSS covered by skin which had multiple pits on the external surface (Fig. 12); the tissue was soft and the cut surface had a greyish appearance. Histologically the mass consisted of well-differentiated lymphoid tissue covered by squamous epithelium. Epithelial-lined crypts extended from the surface into the lymphoid tissue as in mammalian faucial tonsils. A degree of follicular hyperplasia was apparent, and the crypts contained an acute inflammatory cellular infiltrate of polymorphonuclears, which also extended into the lining epithelium. Plasma cells were abundant in lymphoid tissue. Similar lumps were found at the base of the tongue in 2 sperm whales. DISCUSSION
To the list of known neoplasms recorded in Cetacea these findings add a further instance of multiple uterine fibromyomata and of a benign melanotic tumour of the lip, a neoplasm previously not recorded. The appearances of both tumours closely simulate those of related lesions found in other mammalian species. Other lesions, hitherto undescribed in whales and of interest, are siderosis and fatty change of the liver and caseous necrosis of the testis, the latter being histologically similar to tuberculosis of the testis. Although no acid-fast bacilli were demonstrated the possibility that a species of Mycobucterium was responsible for the lesion cannot be excluded. As the nature of the lesion was not suspected initially no unfixed tissues were available for further investigation. Besides these new records, which are not surprising considering the small amount of material so far examined by pathologists, the present report represents the first collection of lesions from sei and Bryde whales. It is significant that as with other reports on the lesions of baleen whale species, tumour-like masses, particularly of dorsal muscles and of adipose tissue around the viscera, constitute the most frequent finding. These masses are referred to colloquially among whalermen, as “husks”, and their occurrence is well-known, though their aetiology remains unexplained. Cockrill (1960) considers they may be parasitic in origin. Our findings indicate that these lesions are essentially focal areas of infarct-like tissue necrosis. In late lesions the necrotic tissues undergo fibrous encapsulation and may be completely or partially replaced by fibrous tissue. The aetiology of the necrosis is not obvious, but there is no evidence of parasitic infestation. The mild inflammatory signs observed are not to be interpreted as an indication of underlying infection and constitute a reaction to tissue necrosis. While trauma cannot be completely excluded as a mechanism of the necrosis, the location of some lesions is against this explanation. Whereas the lesions of the jaw and back muscles are at sites which may be more prone to trauma in a whale, this hardly can be said of pleural and peritoneal fat which are the sites involved next in frequency. Finally, gaseous emboli are known to produce ischaemia and tissue necrosis, and one wonders whether a similar mechanism may be responsible for the initial tissue necrosis in the whale whose marine environment and mode of existence must subject it to decompression stresses. NO doubt under normal conditions physiological adaptations enable this mammal to compensate for the phenomenon, but this doa not rule out the possibility that under abnormal conditions air embolism ma)r sometimes occur.
F
412
PATHOLOGY
OF
WHALE
LESIONS
CONCLUSIONS
The lesions observed in 2,000 whales flensed at Saldanha Whaling
Station in
South Africa are described. Significant amongst these were two benign neoplasms, consisting of multiple uterine fibromyomata, a benign melanotic tumour of the lip in a sperm and sei whale respectively, multiple fibromatous masses (husks) of skeletal muscle and adipose tissue in sei and Bryde whales. The last appear to be the result of spontaneous tissue necrosis with subsequent fibrous replacement or encapsulation of the necrotic tissue. The mechanism of necrosis is not obvious, but possible causes are discussed. REFERENCES
Clarke, R. (1956). Discovery Rep., 28, 237. Cocknll, W. Ross (1960). Bit. vet. I., 116, 113, 175. Rewell, R. E., and Willis, R. A. (1949). J. Path. Bact., 61, 454; (1950). Ibid., 62,450. Roberts, J. C. (Jnr.), Brown, D. H., and Brice, R. C. (1963). Circulufion, 2%, 670. Stolk, A. (1950). Amsterdam Naturalist, 1, 1; (1952). Proc. Kon. Ned. Akud., v. Wetensch., SC, 275; (1953a). Ibid., SC, 364; (195313).Ibid., 369; (1953c). Ibid., 375; (1954). Ibid., 57C, 258; (1962). Ibid., 65C, 250. Truex, R. C., Nolan, F. G., and Truex, R. C. (Jnr.) (1961). Anut. Rec., 141, 325. [Received
for
publication,
LEGENDS
TO
December
8th, 19651
ILLUSTRATIONS
Fig. 1. Slices of uterine fibromyoma of sperm whale showing the typically whorled cut surface Scale in cm. Fig. 2. Fibromyoma showing bundles of spindle-celled smooth muscle fibres with little connective tissue interspersed. H. & E. x 72. Fig. 3. Benign melanotic tumour of sei whale. Scale in cm. Fig. 4. Benign subepidermal melanoma showing closely-packed masses of melanin-packed cells. The profusion of vascular channels is also obvious. H. & E. x 72. Figs. 5 and 6. Masses of necrotic muscle which have been encapsulated and partially replaced by fibrous tissue. Fig. 7. Recent necrosis of voluntary muscle. The nuclear staining of sarcolemmal sheaths has been almost lost. H.&E. x 72. Fig. 8. Long-standing necrosis of muscle. Necrotic muscle fibres have disintegrated and are replaced eripherally by collagenous fibrous tissue. H. & E. x 72. Fig. 9. % ng-standing fat necrosis. Necrotic fat cells are replaced by lipid-laden macrophages and fibrous tissue. x 72. Fig. 10. An area of caseous necrosis of the testis demarcated by proliferating epithelioid cells and fibroblasts. H. & E. x 72. Fig. 11. Fatty change of liver cells. H. & E. x 36. Fig. 12. Anal “tonsils”. The openings of the crypts can be seen on the external surface (left). Scale in cm.
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