VETERINARSKI ARHIV 69 (6), 309-318, 1999

ISSN 1331-8055 Published in Croatia




Histological studies on the arterial walls of main arteries supplying the mammary glands of black Bengal goats (Capra hircus) in Bangladesh

Mohammad Abdul Awal1*, Mohammad Abdul Aziz Prodan1, Mohammad Asaduzzaman1, and Masamichi Kurohmaru2

1Department of Anatomy and Histology, Faculty of Veterinary Sciences, Bangladesh Agricultural University, Mymensingh, Bangladesh

2Department of Veterinary Anatomy, Faculty of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo, Japan




* Contact address:
Prof. Dr. Mohammad Abdul Awal,
Department of Veterinary Anatomy, Faculty of Agricultural and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan,
Phone: 81 3 5841 5384; Fax: 81 3 5841 8181; E-mail: amaawal@mail.ecc.u-tokyo.ac.jp


AWAL, M. A., M. A. A. PRODAN, M. ASADUZZAMAN, M. KUROHMARU: Histological studies on the arterial walls of main arteries supplying the mammary glands of black Bengal goats (Capra hircus) in Bangladesh. Vet. arhiv 69, 309-318, 1999.

ABSTRACT

Histological studies on the arterial walls from the ascending aorta to the mammary glands of indigenous goats (Capra hircus) in Bangladesh were investigated using a light microscope. Based on the histological characteristics and organization of connective tissue fibres and smooth muscle cells in the tunica media, the arterial segments were clearly classified into elastic, transitional and muscular types. The ascending aorta, aortic arch, brachiocephalic trunk, subclavian artery and thoracic aorta were elastic type. The maximum number of elastic lamellae in the tunica media of elastic arteries was recorded in the ascending aorta as 85-90. The abdominal aorta, proximal and distal part of the external iliac, and the distal part of femoral artery, were identified as transitional type. The proximal and distal part of the deep femoral, pudendoepigastric trunk, external pudendal, mammary, the cranial, caudal, and middle mammary, and the caudal superficial epigastric arteries were muscular types. The reproductive stages did not affect the general histological characteristics of the arterial walls. It may be assumed that every artery belonging to the three types had different morphological structures at different levels. The artery distant from the heart gradually decreases its elastic lamellae in the tunica media as well as its elasticity, and at the periphery of the arterial tree the elastic lamellae were replaced by the smooth muscle cells. The existence of well-defined elastic lamellae in the wall of the arteries nearest to the heart is due to resistance of comparatively high arterial pressure compared to that of the muscular arteries. The type of arteries does not depend on the size or diameter of the arteries but on relative distances from the heart.

Key words: histology, arterial wall, mammary gland, black Bengal goat, Capra hircus



Introduction

Histological studies of the arterial walls of dog (BUNCE, 1974), miniature swine (TANIGAWA et al., 1985) and Wistar rats (AWAL et al., 1995) are available. Effects of different reproductive stages on the arterial walls of Wistar rats, Japanese swine and dog have been reported (AWAL et al., 1995, 1997, 1998). A review of available literature reveals no information regarding the histology and type of the arterial walls of main arteries supplying the mammary glands of indigenous black Bengal goats (Capra hircus) in Bangladesh.

Therefore, the present study was undertaken to investigate the general histology of arterial walls in order to clarify whether or not the various reproductive stages affect the histology of the arterial walls of large domesticated animals.

Materials and methods

A total of 16 adult female apparently healthy indigenous black Bengal goats (Capra hircus) were used during the study. All animals were of local Mymensingh breed (Fig. 1). The animals were maintained in the laboratory animal house of the Department of Anatomy and Histology, Bangladesh Agricultural University, and supplied feed and water regularly. The animals were routinely checked for any parasitic or other infectious diseases. They were grouped into 4 stages, each group consisting of 4 animals (4 at 180-day-old virgin, 4 at 90-100 days of pregnancy, 4 at 60 days of lactation and 4 at 30 days post-weaning). The pregnancy was made to allow the counterpart male at the peak of the oestrus and was confirmed by external behaviour and symptoms and from rectal palpation. The animals were anaesthetized with Nembutal (R) (sodium pentobarbital 50 µg/kg body mass) by intramuscular injection and subsequently sacrificed by making an incision on the left common carotid artery. The pectoral and abdominal cavity was opened and eighteen arterial segments (Fig. 2) were carefully dissected soon after the death of the animals and were immediately preserved in 10% buffered neutral formalin. Aseptic measures were taken during sampling in order to avoid inadvertent contamination. All the tissues were dehydrated with a series of graded alcohols, routinely embedded in paraffin wax and sectioned in 5µm thickness. Four stains were used during the study: Mayer's haematoxylin and eosin for general histological study, Weigert's elastica Van Gieson for elastic fibres, Weigert's resorcin fuchsin for smooth muscle cells, and Azan stain for collagen fibres (GRIDLEY, 1960; AWAL et al., 1995). All the tissues were observed with a light microscope (Olympus, Japan). Elastic lamellae were counted (30 slides for each arterial segment) by using higher magnification and from the enlarged microphotographs (AWAL et al., 1995). The diagram and photographs were produced to illustrate the results.

Fig. 1.

Fig. 1. Indigenous black Bengal goat (Capra hircus) in Bangladesh



Fig. 2.

Fig. 2. Location of the arterial segments removed from the black Bengal goat and type of artery. Elastic type: 1=ascending aorta, 2=aortic arch, 3=brachiocephalic trunk, 4=subclavian artery, 5=thoracic aorta; Transitional type: 6=abdominal aorta, 7=external iliac artery (proximal part), 8=external iliac artery (distal part), 9=femoral artery; Muscular type: 10=deep femoral artery (proximal part), 11=deep femoral artery (distal part), 12=pudendo-epigastric trunk, 13=external pudendal artery, 14=mammary artery, 15=caudal mammary artery, 16=cranial mammary artery, 17=middle mammary artery, 18=caudal superficial epigastric artery.



Results and discussion

The arterial segments of the black Bengal goats (Capra hircus) were classified into elastic, transitional and muscular types. Classification was based on the histological characteristics and organization of connective tissue fibres and smooth muscle cells in the three distinct tunics: tunica intima, tunica media, and tunica externa as reported by ARTHUR (1969), ADAM et al. (1970), BUNCE (1974), BLOOM and FAWCETT (1975), BROWN (1976), TANIGAWA et al. (1985), and AWAL et al. (1995).

The ascending aorta, aortic arch, brachiocephalic trunk, subclavian artery, and the thoracic aorta were elastic type (Fig. 2). The tunica intima consisted of a single layer of flattened endothelial cells resting on the internal elastic membrane. The subendothelial layer was observed in large calibre arteries, particularly in the ascending aorta, aortic arch, brachiocephalic trunk, and the thoracic aorta, and was composed of predominantly branched elastic fibres, collagen fibres and reticular fibres. The arterial segments from the ascending aorta to the thoracic aorta were elastic type in miniature swine (TANIGAWA et al., 1985) and was in complete accord with our present study. AWAL et al. (1995) in Wistar rats reported that the arterial segments from the ascending aorta to the abdominal aorta were elastic type. The tunica media of the elastic arteries was the thickest of the three tunics and consisted of predominantly concentric layers of well-defined elastic lamellae (Figs. 3, 4). The number of elastic lamellae in the tunica media was 85-90 in the ascending aorta, 70-75 in the aortic arch, 40-45 in the brachiocephalic trunk, 12-15 in the subclavian artery, and 25-30 in the thoracic aorta. The number of elastic lamellae in the tunica media depends on the size and relative distance of the arteries from the heart (AWAL et al., 1995) and also varies among domestic and laboratory animals (AWAL et al., 1997, 1998). The spaces between the elastic lamellae were occupied with connective tissue fibres and smooth muscle cells arranged circumferentially. The tunica externa was comparatively thin and composed of connective tissue fibres, vasa vasorum, smaller blood vessels and nerves (Fig. 3). Similar histological characters were also observed in miniature swine (TANIGAWA et al., 1985), and Japanese dog (AWAL et al., 1998).

Fig. 3.

Fig. 3. Ascending aorta. Elastic type. The tunica intima (TI) is thin. Subendothelial layer (TI arrow heads) is scanty. The tunica media (TM) is thick and consists of well-defined elastic lamellae. The tunica externa (TE) is thin and consists of connective tissue fibres and vasa vasorum (arrow heads). Van Gieson stain; ×87; scale bar=100 mm.



Fig. 4.

Fig. 4. Thoracic aorta. Elastic type. Subendothelial space is present (arrow heads). Well-defined elastic lamellae (El) in the tunica media. The tunica externa (TE) is thin. Van Gieson stain; ×87; scale bar=100 mm.

The abdominal aorta, proximal and distal part of the external iliac, and the distal part of the femoral artery, were muscular type (Fig. 2). The transitional type was between elastic and muscular types and possessed a mixture of characteristic features common to both of them. Among the transitional arteries, the subendothelial layer was poorly defined in the abdominal aorta, but in other cases this layer was either indistinct or absent. The subendothelial layer gradually becomes thinner and eventually disappears with decreasing vessel size (BUCH, 1979). This was confirmed in the present study. The internal elastic lamina was present but the external elastic lamina was indistinct. The tunica media was comparatively thicker than the tunica externa. The tunica media consisted of thin elastic lamellae. The number of elastic lamellae in the tunica media was 15-20 in the abdominal aorta, 6-7 in the external iliac, and 3-4 in the distal part of the femoral artery. The elastic lamellae in the media were thin and irregular. The inter-laminal spaces were broad and occupied by bundles of smooth muscle cells (Fig. 5). The islands of smooth muscle fibres in the inter-laminal spaces interrupted the continuity of the normal coarseness of the elastic lamellae in the tunica media.

Fig. 5.

Fig. 5. Abdominal aorta. Transitional type. High magnification shows tunica media (TM) of abdominal aorta. Scanty subendothelial space is seen (big arrow). The inter-laminal spaces (Isp) are wide. Bundles of collagen fibres are seen in the inter-laminal spaces (small arrows). Van Gieson stain; ×347; scale bar=300 mm.

The tunica externa was well developed and comparatively thicker than the elastic arteries and was composed of abundant collagen fibres, together with some elastic and smooth muscle fibres. Cross-section of blood vessels and nerves was also observed. Coarse elastic fibres in the tunica externa form a circular arrangement around the tunica media in dog (BUNCE, 1974) and Japanese swine (AWAL et al., 1997), but this histological characteristic was not observed in the present study.

The proximal and distal part of the deep femoral, pudendo-epigastric trunk, external pudendal, mammary, cranial, caudal and middle mammary, and the caudal superficial epigastric arteries were muscular type (Fig. 2). The tunica intima consisted of a single layer of flattened endothelium resting on the internal elastic membrane. The tunica media, completely devoid of elastic lamellae, consisted mainly of smooth muscle cells with a mixture of a few elastic fibres (Fig. 6). The subendothelial layer was absent. Usually, the smaller arteries, the peripheral branches of the arterial tree, were identified as muscular type and the media was composed of circularly arranged smooth muscle cells with a few fine elastic fibres (GROSS et al., 1933; TANIGAWA et al., 1985; AWAL et al., 1995; AWAL et al., 1997, respectively). Similar histological features were observed in the present study and accord well with their descriptions (GROSS et al., 1933; TANIGAWA et al., 1985; AWAL et al., 1995, 1998). Similar histological features were also observed in the present study and accord well with their description (GROSS et al., 1993; TANIGAWA et al., 1985; AWAL et al., 1995, 1998). The internal elastic membrane was present and well developed, but the external elastic lamina was either indistinct or absent. Both internal and external elastic lamina were present in the muscular arteries of Wistar rats (AWAL et al., 1995). The tunica externa was well developed and consisted of predominantly collagen fibres with coarse elastic fibres and smooth muscle cells. Cross-sections of small blood vessels and nerve bundle were also observed. A similar histological feature was reported in dog (BUNCE, 1974) and in Japanese swine (AWAL et al., 1997). In the present study, the tunica media of the muscular arteries was the thickest of the three tunics, whereas the tunica media of the muscular arteries of miniature swine and Wistar rats were thinner than that of the tunica externa (TANIGAWA et al., 1985; AWAL et al., 1995).

Fig. 6.

Fig. 6. External pudendal artery. Muscular type. Internal elastic membrane (Iem) is present. The tunica media consists of smooth muscle cells (Sm). The tunica externa (TE) contains a high number of coarse elastic tissues. The elastic tissues in the tunica externa form a circular arrangement around the tunica media (arrow heads). Weigert's resorcin fuchsin stain; ×87; scale bar=100 mm.

The reproductive stages did not affect the histological characteristics of the arterial wall.

Conclusion

The histological classification of the arterial walls of indigenous goats (Capra hircus) was similar to that of large domestic and laboratory animals. It is possible to suggest here that every artery belonging to the three types possessed different histological structures at different levels. The type of arterial wall does not depend on the sizes or diameters of the arteries, but is related to relative distance from the heart. Given the presence of elastic lamellae in the elastic arteries, it is assumed that the vessel nearest to the heart might resist the comparatively high arterial pressure, which might not be case with peripheral muscular arteries. Therefore, the media of the arteries nearest to the heart consisted of a comparatively higher number of elastic lamellae. Similarly, the media of muscular arteries are composed of smooth muscle cells for efficient response to the functional physiological demands of the body.


Acknowledgment
This study was conducted at the Department of Veterinary Anatomy and Histology, Bangladesh Agricultural University. We are grateful to the late Prof. Dr. M. Nazrul Islam, former Head of that Department for his valuable suggestions during this research. Our thanks also go to Prof. M. A. Bari Khan for his critical reading of this manuscript. This work was partly supported by a Grant in Aid from the Bangladesh Agricultural University Research, Education Science. The laboratory facilities provided by the Department of Veterinary Anatomy, Faculty of Agricultural and Life Sciences, University of Tokyo, for some special histological staining and photography are also acknowledged. We offer our sincere thanks to Mr. laikot Hossain for his expert care for the experimental animals.


References

ADAM, W. S., M. L. CALHOUM, E. M. SMITH, A. W. SISSION (1970): Microscopic Anatomy of the Dod. Charles Thomas Pub. Springfield, Illinois.

ARTHUR, W. H. (1969): Histology. Igaku Shoin Ltd. Tokyo, Japan.

AWAL, M. A., M. MATSUMOTO, H. NISHINAKAGAWA (1995): Morphometrical changes of the arterial walls of main arteries from heart to the abdomino-inguinal mammary glands of Wistar rat from virgin through pregnancy, lactation and post-weaning. J. Vet. Med. Sci. 57, 251-256.

AWAL, M. A., H. NISHINAKAGAWA, M. MATSUMOTO (1997): Histological studies on e arterial walls of main arteries supplying to the mammary glands of Japanese swine (Berkshire). Progress. Agric. 8, 73-76.

AWAL, M. A., M. MATSUMOTO, H. NISHINAKAGAWA (1998): Histology on the main arteries of mammary glands of Japanese dog. Bang. J. Anim. Sci. 27, 49-55.

BLOOM, W., W. D. FAWCETT (1975): A Textbook of Histology. W. B. Saunders Co. Philadelphia and London.

BROWN, E. M. (1976): Textbook of Veterinary Histology. Lea & Febiger Inc. Philadelphia and London.

BUCH, R. C. (1979): The longitudinal orientation of structures in subendothelial space of rat aorta. Am. J. Anat. 156, 1-14.

BUNCE, D. F. M. (1974): Atlas of Arterial Histology. Warren H. Green Inc. Mizouri.

GRIDLEY, M. F. (1960): Manual of Histologic and Special Techniques. McGraw Hill book Co. Inc. New York.

GROSS, M. D., Z. E. EPSTEIN, M. A. KUGEL (1933): Histology of the coronary arteries in human heart. Am. J. Pathol. 10, 253-273.

TANIGAWA, M., J. ADACHI, K. MOCHIZUKI (1985): Histological study on the arterial wall of Gottingen miniature swine. Exp. Anim. 35, 35-45.

Received: 5 July 1999
Accepted: 15 December 1999



AWAL, M. A., M. A. A. PRODAN, M. ASADUZZAMAN, M. KUROHMARU: Histoloska istrazivanja stijenki glavnih arterija koje opskrbljuju krvlju vime crne bengalske koze (Capra hircus) iz Bangladesa. Vet. arhiv 69, 309-318, 1999.

SAZETAK

Svjetlosnim mikroskopom istrazene su stijenke arterija od uzlazne aorte pa sve do vimena domacih koza (Capra hircus) iz Bangladesa. Na osnovi histoloskih osobitosti i raspodjele vezivnotkivnih vlakana i glatkih misicnih stanica u tuniki mediji tih arterija, one su jasno podijeljene u elasticni, prijelazni i misicni tip arterija. Aorta ascendens, arcus aortae, truncus brachiocephalicus, arteria subclavia i aorta thoracica elasticnog su tipa. Najveci broj elasticnih lamela (85-90), tunike medije ovih arterija, utvrden je u uzlaznoj aorti. Kao prijelazni tip arterija utvrdene su: trbusna aorta, pocetni i zavrsni djelovi vanjske ilijacne arterije, kao i zavrsni dio bedrene arterije. Misicnom tipu arterija pripadaju: pocetni i krajnji dio duboke bedrene arterije, truncus pudendoepigastricus, vanjska stidna arterija, arteria mammaria, arteriae mammariae cranialis, caudalis et media te arteria epigastrica caudalis superficialis. Opce histoloske osobitosti arterijskih stijenki nisu ovisne o stanju razmnozavanja u kojem se koza nalazi. Moze se pretpostaviti da svaka od arterija koja pripada svima trima tipovima ima razlicitu gradu na razlicitim svojim odsjeccima. S udaljavanjem od srca arterije postupno gubi svoje elasticne lamele u tuniki mediji kao i svoju elasticnost, te konacno glatke misicne stanice zamjenjuju elasticne lamele. Postojanje dobro izrazenih elasticnih lamela u stijenci arterija najblizih srcu posljedica je toga sto je u ovim arterije visi arterijski krvni tlak, nego sto je taj tlak u arterijama misicnog tipa. Tip arterije ne ovisi o velicini ili promjeru arterije nego o njezinoj relativnoj udaljenosti od srca.

Kljucne rijeci: histoloska grada, arterijska stijenka, vime, crna bengalska koza, Capra hircus


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