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日本海セトロジー研究 (NihonkaiCetology) (13) : 25 32 (2003)
Some Histological Observations on a Harbor Porpoise, Phocoena phocoenaラ
Stranded on Nishiyama Beachラ NiigataPrefecture, Sea of Japan
Yoshiharu Honma'>ぺ TatsuoUshiki'>, Jiro Hitomi'>, Masaei Takeda'> and Junji Shindo'>
1) Division of Microscopic Anatomy and Bio-imαging, Department of Cellular Function, NiigtαUniversity Graduαte School
of Medical αnd Dentαi Sciences, Asahimachi dori-1, Niigαta, 951-8510 Japan
2)Niigata City Aquarium, Nishザunαmicho5932-445, Niigata 951-8101, J.αrpan
匂-mail: [email protected]α-uβc.jp
Key words : visceral organ histology, stranding, female exhumed the specimen and removed the visceral organs
harbor porpoise, Phocoena phocoena, Nishiyama-machi (preserved in 10% formol) for further examination. The
organs were forwarded to the senior author, a histological
examination of the urino-genital organs having already been
reported (Honma, et al., 2002) .
The remaining organs were also examined histologically,
the former still appearing fresh despite the animal having
been buried for on巴 day.Because histological criteria for
several organs of harbor po叩oise have only been
documented for a s巴nilemale individual (Honma et., 1992) ,
the study of a female will be a valuable addition to our
Abstract Histological observations to determine physical
condition were performed on some organs of a young female
harbor porpoise, Phocoena phocoena, stranded on the beach
at Nishiyama-machi, Niigata Prefecture, Sea of Japan. Most
of the hepatic cells appeared normalョalthoughsome areas
of fatty liver, heavy hemorrhaging and necrotic tissue were
detected. The exocrine pancreas consisted of acini
comprising granular ( = zymogen) acinar cells and a
centroacinar cell. On the other hand, the endocrine pancreas
(islets of Langerhans) wer巴 composed of 3 types of
endocrine cells, A-( glucagon producing) , B-( insulin
producing) and a few D (somatostatin producing) cells.
The cortical region of the spleen appeared normal, with
healthy lymphocytes, while the medullarγregion contained
numerous macrophages. Considerable pigment ( lipofuscins)
were apparent in the macrophages, but no plasma cells w巴re
encounter巴d.No kidney abnormalities W巴reobserved in the
distal and collecting tubule cells, and most of th巳 glomeruliラ
although a few of the latter had collapsed. Noticeably,
sev巴ralepithelial po口ionsof the urinarγbladder were in an
early papillomatous phas巴 Allof the lung alveolar cells had
collapsed due to stranding, although the peripheral region
(cartilagenous rings supporting the bronchi) was unchanged.
A longitudinal section of anastomosed cardiac muscle fibers
revealed intercalated discs, while in a cross (transverse)
section Cohnh巴imfields were det巴cted.
Introduction
As reported previously, a young female harbor porpoise,
Phocoe刀a phocoena, was stranded ashor巴 at
Nishiyama-machi, west ofNiigata City on 26 February, 2001
(Honma et al., 2002) . Because of a heavy visible injurγ,the
finders hurried the individual in the sandy beach.
Soon after this action, several aquarists and a V巴terinarian
present knowledge data base.
Materials and Methods
A number of organs (preserved in 10% formalin),
including the liver, pancreas, spleen, kidney, urinary bladderラ
lung and heart were used in this study. Blocks removed from
each organ were fixed secondarily in Bouin’s solution,
dehydrated in an alcohol series, embedded in paraffin, cut at
5 ,um thickness, stained chiefly with hematoxylin-eosin
(HE) double stain and Masson-Goldner (MG) associated
with aldehyde fuchsin (AF) tetrachrome stain, and observed
under a light microscope ( Orthoplan, Leitz) .
Results of Observations
Liver : Although a lobular pattern was indistinct, the liver
was composed of lobules of epithelial ( parenchymal hepatic)
cells arranged radially in a central vein, associated in parallel
with sinusoids (Fig. I). The polyhedral hepatic cells were
coarsely granular, each with an ovoid and/or round nucleus.
However, in some pa口s, the cell mass included a
considerable amount of adipose components, the congestive
portions being surrounded by deeply-stained hepatic cells
(Fig. 2). Nodules containing such cells wer巴 alsostained
deeply.
Each hepatic cell characteristically had a clearcut round
nucleus, including distinct nucleoli. However, necrotic
に-uつ臼
Yoshiharu Honma, Tatsuo Ushiki, Jiro Hitomi, Masae』Takedaand Junji Shindo
po口ionswere encountered in the nodules. The bile duct,
consisting of columnar cells, in addition to Kupper and
dicaryonate cells, was observed only with difficulty.
Exocrine pancreas : The organ includ巴dnumerous acini in
th巴 lobules, vascular components and interlobular ducts.
Each acinus comprised s巴veral(or mor巴) pyramidal cells
a汀angedaround a centroacinal cell. Two types of acinal
cells were found : a larger cell containing coarse granules
(=zymogen granules) and a smaller pale cell that lacked
granules (i. e., granule exhousted) . No anomalies were
detected in the exocrine pancreas (Fig. 3)
Endocrine pancreas : Numerous small masses of islets of
Langerhans were scattered throughout the exocrin巴 pancreas.
MG-AF stain disclosed three types of endocrine cells in the
islets, the former being included within or in contact with
tubuloacinal tissues.
The abundant polyhedral cells showed a strong affinity for
AF, being categorized as insulin-producing B cells, whereas
the smaller acidophile (phloxinophil) cells with peripherally-
shifted nucl巴iwere considered to be glucagon-producing A
cells. Cells stained with light green wer巴 located
sporadically, being identified as somatostatin producing D
cells (Fig. 4)
Spleen : The spleen consisted of a collagenous frame work,
a well-developed trabeculae, and roughly divided cortical
and medullary portions. The organ was covered with a
comparatively thick, loose connective tissue containing
a口eries and veins. Separation of the white (mass of
lymphocytes) and red (circulating blood cells) pulps was
incomplete (Fig. 5).
The cortical region appeared normal, with healthy
lymphocytes, whereas a considerable number of
macrophages much yellow brownian pigment (probably
lipofuscin) both within and around the latter were d巴tected
in the medullarγregion. The texture of the medulla was
rough and lacuna!. However, no areas of highly active
phagocytosis were encountered (Fig. 6) .
Kidney ・ Although only one reniculus was examined, no
notably aberrant and/or pathological conditions were found
in the renal tissues, except for minor changes in a few renal
coゅuscles.Just beneath and at the entrance of the capillary
glomerulus (the vascular pole), juxtaglomerular cells with
granules and the macula densa consisting of low columnar
cells were clearly defined (Fig. 7) .
Glomerular necrosis was very seldom巴ncountered.The
proximal and collecting tubules were distinguishable adjacent
to or near the renal coゅuscle.The apices of th巴formercells
were each equipped with a brush border, while the
cytoplasm of th巴 lattercells was light. The juxtaglomerular
and Goormaghtigh cells, corresponding to smooth muscular
cells, contained rich cytoplasm (Fig. 8) .
Urinary bladder : The bladder was constructed from① a
serous membrane of loose connective tissue,② an outer
layer of longitudinal smooth muscle,③ a middle layer of
circular smooth muscle,④ an inner layer of longitudinal
smooth muscle,⑤ a lamina propria of collagenous
connective tissue and ⑤ transitional epithelium. It is
notable that slight swellings in the epithelium, diagnosed as
benign papillomatous growths, were encounter巴d. The
comparatively large, polyhedral cells, each cpontaining a
round or ovoid nucleus, were very weakly positive with AF.
The cell membrane was equipped with intercellular bridges
(Fig. 9), and the epithelial margin showed keratinization.
However, no mitotic figures and I or pyknotic features were
detected (Fig. 10).
Lung ・ Unfortunately, most of the alveolar cells, with long
ovoid nuclei, were congested and I or collapsed. However,
interlobular loose connective tissues existed in the alveolar
ducts, bronchioles and arteries, and alveolar septa were
apparent.
Rings of hyaline cartilage, constituting part of the
myoelastic sphincter accompanying muscule fiber bundles
and epithelial cells were apparent at the bottom of alveolar
duct (Fig. 11). The surface of the cartilage ring fragments
was covered with a mucosal epithelium of cuboidal cells and
lined with smooth muscle fiber bundles, as mentioned
above. The cuboidal cells each had a deeply-stained nucleus.
Between the sphincters and veins masses of circular mucous
glands consisting of tall cells, were seen, the mucus showing
an affinity to AF (Fig. 12) .
Cardiac muscle : This involuntary striated muscle
consisted of th巴musclecells joined end to end at junctional
zones, the so-called intercalated discs (Fig. 13). A single
cardiac muscle cell comprised an elongated nucleus and
sarcoplasm. However, branching muscle fibers were
anastomosed. In cross section, so-called Cohnheim fields
were seen (Fig. 14), the nuclei and pale portions without
myofibrils being located in the central portions of fibers,
each fiber b巴ingassociated with myofibrils. Between the
muscle fiber strands, flat, spindle-shap巴d cells were
recognized.
Discussion
All organ specimens used in this study were removed
円。円ノL】
Some Histological Observations on a Harbor Porpoise, Phocoena phocoena, stranded on Nishiyama Beach, Niigata Preたcture,Sea of Japan
from a young female harbor porpoise, together with the
genital apparatus examined reported previously (Honma, et
al., 2002).
Kikkawa ( 1943~1944), who reported histological
characteristics of several visceral organs of cetaceans, briefly
mentioned that the liver of sei and blue whales contained a
comparatively small amount of connective tissue, had a
disrupted radial arrangement of hepatic cords toward the
peripheral region, and lacked a defined gall bladder. Similar
characteristics wer巴 reported for a senile male harbor
porpoise (Honma et al., 1992) and were evident in the
pn巴sentexamination.
Cockrill ( 1960) noted fat storage of fats in the livers of
pregnant cetaceans, as did Honma et al. ( 1992) . However,
in th巴 presentyoung specimen, the amount of fat deposited
was small.
Kikkawa ( 1944), Saito ( 1969), Simpson and Gardner
( 1972) and Honma et al. ( 1992) dscribed the exocrine and
endocrine pancreas of cetceans, and emphasized that th巴y
contained a smaller amount of stromatous connective tissues
than found in teηestrial tetrapod animals. Excepting
Kikkawa ( 1944), they also pointed out the relativ巴lylarge
number (but smaller size) of islet tissues comprising A, B
and D cells. The present examination confirmed these
findings.
Lymphoid organs, including the spleen of marine
mammals, were described and r巴vi巴wed by Kikkawa
( 1943), Simpson and Gardner ( 1972), Schmacher and
Welsch ( 1987), Honma et al. (1992), Nakamine et al.
(1992) and Cowan and Smith (1999). Cowan (1966),
Schumacher et al. ( 1990) and Honma et al. (2001) also
noted resp巴ctivepathological conditions of marine mammal
spleens. Among others, Nakamine et al. ( 1992) documented
a type of primitive mammalian spleen in an odontocetous
whale. Cowan and Smith ( 1999), who dissect巴d 50
beach-stranded bottlenose dolphins noted many small巴r
accessory spleens, some even embedded in the pancreas.
Such a condition was not apparent in the pres巴ntspecim巴n.
It is well documented that the kidney of marine mammals
is compos巴d of many reniculi ; such Oobate) structures
(Lappenbildung) having been often described ( e. g.,
Beauregard et Boulart, 1882 . Ping, 1926 ; Kamiya, 1958 ;
Slijper, 1962 ; Honma, et al., 1992) . How巴ver, no
histologically-different architecture of kidney elements has
been detected when compared with terrestrial mammals,
including man.
Examining the Atlantic bottlenosed dolphin, Simpson and
Gardner ( 1972) illustrated a section of urinary bladder
consisting of a transitional epithelium, loose connective
tissue and concentric smooth muscle layers. They further
mentioned one instance of acute necrotizing cystitis in this
species, in which the epithelial lining was denuded, beeing
the site of an acute inflammatory reaction. However, there
appear to b巴noliterature accounts of papillomatous growths
of urinary bladder epithelium, as found in the present
specimen. Although the grade of growth was slight in this
case, a remarkable epithelial swelling with numerous
intercellular bridges constructed合omprominent d巴smosomes
has recently been described in an aquarium-reared Acipe刀ser
(Honma et al., 1999).
Barbosa ( 1914)日rstdescribed bronchiole sphincters,
peculiar to dolphins. Subsequently, Fiebiger ( 1916), Nayr巴S
and Laurie ( 1937), Belanger ( 1940), Wislocki ( 1942),
Kikkawa (1944), Murata (1951), Engel (1966), Ito et al.
(1967), Simpson and Gardner ( 1972) and Honma et al.
( 1992) r巴po目ed microscopic observations on cetacean
lungs.
Among others, Wislocki ( 1942) and Honma et al.
( 1992) described a specialized system of myoelastic
sphincters constituting“valvular segments” such involving
even the smallest bronchiolar passages in the lungs. They
noted also that such a characteristic was not pr巴sentin larger
cetaceans. As indicated in the results, in small odontocetous
whales, which have a relatively short diving time, the
myoelastic sphincters connecting the cartilage 合agments,
which surround and support the tubular wall of the
bronchiole, are well develop巴dand extended down to the
respiratory bronchiole, at the beginning of the alveolar duct.
On the other hand. Lacoste and Baudrimont ( 1938),
Goudappel and Slりper( 1958) and Harrison and Tomlinson
( 1963) pointed out that bronchiolar sphincters were absent
in larger whales, which are characterized by deep and
prolonged diving, and relatively small lung capacity.
Although Simpson and Gardner ( 1972) described the
cardiovascular system of marine mammals, the present study
could examine only a small block of cardiac muscle and
detailed comparisons cannot be made at this time.
As described above, the histological examination gave no
insight into the factors leading up to the death of the present
harbor porpoise. More fresh material of marine mammals
stranded on the coast of Niigata District, Sea of Japan, are
necessaiγfor elucidating the cause of death during the
winter season and for the accumulation of knowledge on the
comparative histology of marine mammals.
ヴ
inノ白
Yoshiharu Honma, Tatsuo Ushiki, Jiro Hitomi, Masaei Takeda and Junji Shindo
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口。つ,“
Some Histological Obse刊atio日son a Harbor Porpoise, Phocoeno phocoena, stranded on Nishiyama Beach, Niigata Prefecture, Sea of Japan
Fig. I. Section of liver from a harbor porpoise, Phocoena
phocoena, showing polyhedral hepatic cell cords running
parallel with sinusoidal cords (s) Note granular cytoplasm
and distinct nucleolus (arrow) in hepatic cell. Masson
Goldner associat巳dwith AF (MG-AF) stain.×400
Fig. 2. S巴ctionof liver showing consid巴rablefat components (f) .
Note round nucleus (arrow) in granular hepatic cells.
MG-AF.×400
Fig. 3. Section of pancreas consisting of granular
(zymogen) cells (z) and granule-exhausted light cells (I).
a : Note several masses of islets of Langerhans (aπow
head). Lower magnification. MA-AF.×1 00, b . Higher
magnification. MA-AF.×400
Fig. 4. Part of islet of Langerhans in exocrine pancreatic
tissue exhibiting three types of endocrine cells ・ AF
strongly positive B (B) cells, phroxine stained A (A) cells
and light green faintly stained D ( D) cells. Note two types
of acinar cells (z, I). MG-AF.×400
Qd
つ山
Yoshiharu Honma, Tatsuo Ushiki, Jiro Hitomi, Masaei Takeda and Junji Shindo
Fig. 5. Part of spleen showing small lymphocytes ( 1), red
blood c巴lls(r) and macrophages (m) Hematoxylin-eosin
(HE) stain.×400
Fig. 6. Medullarγportion of loose lacunal spleen, showing
slightly active macrophages ( m), some of which were
contaminated with lipofuscin (aπow) MG・AF.×400
Fig. 7. Part of glomerular capillaries ( G) and macula densa
(md). HE.×400
Fig. 8. Glomerulus (G), proximal (p) and collecting (c)
convoluted tubules in the renal cortex. Apices of proximal
tubule cells equipped with cilial brush border. Note
juxtaglomerular apparatus copmprising Goormaghtigh cells
(arrow head) and juxtaglomerular cells (arrow). HE.×
400
-30一
Some Histological Observations on a Harbor Porpoise, Phocoeno phocoeno, stranded on Nishiyama Beach, Niigata Prefecture, Sea of Japan
Fig. 9. Part of th巴 transitionalepithelium of urinarγbladder,
showing papillarγ 巴levation.Note polyhedral cell with a
distinct nucleus (↑) and cell membrane equipped with an
intercelular bridge (arrow h巴ad).MG-AF.×400
Fig. I 0. Papillomatous growth of transitional epithelium.
Note mitotic figures absent from nuclei. HE.× 400
Fig. 11. Endothelial cells of alveolus (a), a cartilage
fragment (c) and pa口ofth巴myoelasticsphincter. ( v巴ins,
v) HE.×400
Fig. 12. Circular mucous glands between the myoelastic
sphincter and vein. HE.×400
Fig. 13. Part of cardiac muscl巴 showinganastomosis of
branching muscle fibers. Note intercalated discs (a汀ow)
MG-AF.×400
Fig. 14. Cross-section of cardiac muscle fibers showing
so-called Cohnheim fields. Note nuclei ( n) and pale
po口ions without myofibrils (arrow) located in central
portion of fib巴rs.HE.×400
11ム
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Yoshiharu Honma. Tatsuo Ushiki, Jiro Hitomi, Masaei Takeda and Junji Shindo
新潟県西山海岸へ漂着したネズミイルカ諸器官の組織学的観察
本間義治1)・牛木辰男]).人見次郎け・武田政衛1).進藤順治2)
1)新潟大学大学院医歯学総合研究科顕微解剖学分野 干95卜8510 新潟市旭町1-757
2)新潟市水族館 干95ト8101 新潟市西船見町5932-445
2001年2月初日に、新潟県西山海岸へ漂着した若い♀ネズミイルカ(Honma et al. 2002)の諸器官を組織学的に
観察し、漂着理由の一端を解明することを試みた。肝小葉は不明瞭で、多角状の肝細胞は、ほとんどが正常で、一部
に脂肪蓄積や出血ならびに壊死が認められた。勝臓外分泌部は、酵素原頼粒を含有するものと、放出したと思われる
腺房細胞との両者および腺房中心細胞から成る。内分泌部(ランゲルハンス小島)は外分泌組織中に多数散在し、 A
F陽性のB (インシュリン産生)、フロキシン陽性のA (グルカゴン産生)、およびライトグリーン淡染のD (ソマト
スタチン産生)細胞が識別できた。牌住が発達した牌皮質部の白牌髄と赤牌髄の区別はあまり明瞭でなかったが、髄
質部には大食細胞やリポフスチンが目だ‘った。腎臓は腎分体の集合より成るが、ごく少数の腎小体が壊死を起こして
いた以外に、尿細管には異常が認められなかった。腸脱の移行上皮には、軽度の乳頭腫が発生していた。肺胞の筋弾
性活約結束は、大半を軟骨片が取り巻き、イルカ類の特徴を備えていた。心筋は、不随意横紋筋繊維が吻合し合い、
繊維境界を成す介在板が観察された。一方、横断面では筋原繊維束がコーンハイム野として現れた。しかし、死因と
なるような像はみられなかった。
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