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Distribution of the internal pudendal artery in male and female llama (Lama glama)
ARTICLE IN PRESS Ann Anat 189 (2007) 295—298
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Distribution of the internal pudendal artery in male and female llama (Lama glama) Guillermo Horacio Graziotti, Jose ´ Manuel Rodrı´guez Mene ´ndez, Clara Marı´a Rı´os, Carlos Lisandro Victorica Area of Anatomy, Faculty of Veterinary Sciences, Buenos Aires University (UBA), Chorroarı´n 280, Capital Federal CWO 1427, Argentina Received 17 February 2006; accepted 31 October 2006
KEYWORDS Arterial system; Llama; Pelvic cavity; Pudendal internal artery; Comparative anatomy
Summary The aim of this research has been to describe the internal pudendal artery distribution in male and female llama and to compare it with that of other domestic animals including the one-humped camel (Camelus dromedarius). The arterial system was perfused with a solution of 14% coloured plaster and preserved in a solution of a 10% formalin, 3% carbolic acid and 3% glycerine. The systematic dissection was made using traditional working techniques and standard instruments. The internal pudendal artery is the ventral terminal branch of the internal iliac artery at the level of the third sacral vertebra. The main supply of the pelvic organs comes from the prostatic or vaginal arteries; notwithstanding these arteries arise from the internal pudendal artery, showing an important difference between ruminants and pig (long iliac type). Similarities between the distribution of the internal pudendal artery of the llama and those obtained in the camel provide strong evidence of a common phylogenetic origin. & 2006 Elsevier GmbH. All rights reserved.
Introduction In the last years, we carried out research on the arterial and venous system of the Lama glama and this work is a continuation of this subject (Graziotti et al., 1997, 1998, 1999, 2000, 2003). Corresponding author. Tel.: +54 11 4524 8460;
fax: +54 11 4524 8480. E-mail address: [email protected] (G.H. Graziotti).
We have previously determined that the internal iliac artery in the llama belongs to an intermediate long iliac type of Dellbru ¨gge, cited by Nitschke and Preuss (1971), in which the parietal branches arise from the internal iliac artery and the visceral branches from the internal pudendal artery. The arterial distribution of the internal pudendal artery is described and compared with other domestic animals including the one-humped camel (Camelus dromedarius).
0940-9602/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2006.10.004
ARTICLE IN PRESS 296
G.H. Graziotti et al.
We believe that this study is a contribution revealing new aspects for consideration in teaching and research in comparative anatomy. It refers to a species that is growing in importance as a pet and farm animal.
Materials and methods This research was conducted on 13 post-mortem specimens, five males and eight females, 2.5–3-year-old llamas (Lama glama) from Trenque La ´uquen, Buenos Aires, Argentina, which were destined as source of food. They were perfused via an arterial path using the No. 18 Levine type catheter, from the abdominal aorta with a 14% coloured plaster solution; then they were preserved by immersion into a pool of a 10% formalin, 3% carbolic acid and 3% glycerine solution. The systematic dissection was made using traditional working techniques and standard instruments.
Results The internal pudendal artery was the ventral terminal branch of the internal iliac artery at the level of the third sacral vertebra. It ran caudoventrally on the internal surface of the broad sacrotuberous ligament, ending as the ventral perineal artery and the artery of the penis or the artery of the clitoris at the level of the caudal edge of the obturator foramen (Figs. 1–3). The internal pudendal artery gave off the prostatic or vaginal artery near its origin. The prostatic artery (Fig. 2) ran towards the prostatic gland and postprostatic urethra. Along its course the prostatic artery gave off two collateral branches: the first one, the ductus deferens artery ran cranioventrally supplying it and in turn gave off the caudal vesical artery and the ureteral branch; the second collateral branch was the urethral artery which terminated on the preprostatic urethra. The vaginal artery (Fig. 1A) was included in the broad ligament ending in several branches to the vagina and the urethra. Its first collateral branch was the uterine artery, which ran along the lateral edge of the neck, body and horn of the uterus; it sent out the caudal vesical artery that had a distribution similar to the male. Finally, the internal pudendal artery gave off the urethral artery near its end. Once, a slender middle rectal artery arising from the internal pudendal artery was found in a female (Fig. 1B and C).
Figure 1. General distribution of the internal pudendal artery in female llama (A); more detailed dissection (B) and (C) showed the terminal branches. Lateral aspect.
The ventral perineal artery in the male (Figs. 2 and 3) coursed on the medial aspect of the bulbourethral gland, which was irrigated by a proper branch. After that the ventral perineal artery passed between the bulb of the penis and the anus, sending branches to the ischiocavernosus muscle and the bulb of the penis, and giving rise to the caudal rectal artery to supply the most caudal portion of the rectum. The ventral perineal artery ended in several branches that ramified on the ventral part of the perineum. In the female, the ventral perineal artery gave off the vestibular branch and the caudal rectal artery and continued as the dorsal labial artery (Fig. 1B and C).
ARTICLE IN PRESS Distribution of the internal pudendal artery in male and female llama
Figure 2. Lateral view of the general distribution of the internal pudendal artery in male llama (A) and general scheme (B).
The artery of the penis (Fig. 3) obliquely crossed the lateral surface of the pelvic urethra giving off the artery of the bulb of the penis and passing under the ischiatic arch. Afterwards, it ran cranioventrally sending the deep artery of the penis and the dorsal artery of the penis, which coursed on the dorsal aspect of this organ. The artery of the clitoris (Fig. 1B and C) coursed on the lateral aspect of the constrictor vestibular muscle giving off the artery of the vestibular bulb; more peripheral, the artery of the clitoris gave rise to the deep artery of the clitoris in relation to the body of the clitoris, and finally continued as the dorsal artery of the clitoris.
Discussion According to Grasse´ (1971), Nickel et al. (1984) and Barone (1996) in the long iliac type (ruminant and pigs) the internal iliac artery gives off the visceral intrapelvic and parietal branches; the internal pudendal artery only supplies the perineum and the external genital organs. Notwithstanding the intrapelvic visceral branches in the llama arise from the internal pudendal artery as it occurs in horses and carnivores (short iliac type). This is an important difference in relation to the distribution in characteristics of long iliac type in
297
Figure 3. Detailed dissection showed the terminal branches of the penis artery in llama. Caudolateral aspect. 1, Internal iliac artery; 2, caudal gluteal artery; 3, internal pudendal artery; 4, vaginal/prostatic artery; 5, uterine artery/artery of the deferens duct; 6, caudal vesical artery; 7, ureteral branch; 8, urethral branch; 9, middle rectal artery; 10, urethral artery; 11, ventral perineal artery; 12, caudal rectal artery; 13, dorsal labial branch; 14, vestibular branch; 15, artery of the clitoris/ penis; 16, artery of the vestibular bulb/artery of the bulb of the penis; 17, deep artery of clitoris/penis; 18, dorsal artery of the penis/clitoris (displaced partially); 19, branch for the bulbourethral gland; a, ampulla of the rectum; b, deferens duct; c, bladder; d, ureter (cut and removed partially); e, prostate; f, urethra; g, bulbourethral gland; h, bulb of the penis; i, crus of penis; j, body of penis; k, testicle/ovary; l, uterine horn; m, vagina; n, vestibular bulb; p, vestibule of the vagina; A, ischiatic table; B, ischiatic tuberosity; C, ischiatic arch; D, tail; E, symphysis pelvis.
ruminants and pigs and in the artiodactyla type of Nitschke and Preuss (1971). The origin of the vaginal or prostatic arteries from the internal pudendal artery in llama is in accordance with a long intermediate type of the internal iliac artery in this species, as reviewed by Graziotti et al. (2003). The main supply of the uterus comes from the vaginal artery via the uterine artery as is the case in the carnivore and dromedary camel (Kadhim et al., 2001). There are no branches to the uterus from
ARTICLE IN PRESS 298 the external iliac or umbilical arteries as found in the mare, cow and sow. As would be expected, in the male the umbilical artery does not supply the deferent duct because the main blood supply of this organ comes from the prostatic artery. The caudal part of the urethra is nourished by a branch of the prostatic artery, which occurs in the horse and rabbit (Baron, 1996). The middle rectal artery is absent in llama or it is rarely developed. The territory nourished by this vessel in other species is supplied by the cranial rectal artery in llama, which is very distinct. When the middle rectal artery is present, it arises from the internal pudendal artery as occurrs in the ox, ram (Nickel et al., 1984) and dromedary camel (Kadhim et al., 2001). We have found the middle rectal artery in one female llama only. The bulbourethral gland is irrigated by an innominate proper branch (Schaller, 1996) originating from the ventral perineal artery. A well-developed vestibular branch is present in llama as also found in the mare and cow; however it arises from the ventral perineal artery (at the same level as the proper branch for the bulbourethral gland), while it takes origin from the internal pudendal artery in these species (Barone, 1996; Nickel et al., 1984). As is the case in horses, human (Barone, 1996) and one-humped camel (Kadhim et al., 2001) the dorsal perineal artery is absent in llama. Similarities between the distribution of the internal pudendal artery and internal iliac artery in llama (Graziotti et al., 2003) and those obtained in dromedary camel by Kadhim et al. (2001) are strong evidence of a common phylogenetic origin (Nuevo Freire, 1994).
G.H. Graziotti et al.
References Barone, R., 1996. Anatomie Compare´e des Mammife `res Domestiques. Angiologie. Vigot, Paris, pp. 357–385. Grasse´, P., 1971. Traite´ de Zoologie, tome XVI, fasc. IV. Masson et Cie, Paris, pp. 782–789. Graziotti, G.H., Rı´os, C.M., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., 1997. La irrigacio ´n arterial del muslo de la llama (Lama glama). Rev. Chil. Anat. 15, 35–40. Graziotti, G.H., Rı´os, C.M., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., 1998. Irrigacio ´n de la rodilla y pierna de la llama (Lama glama). Rev. Chil. Anat. 16, 89–94. Graziotti, G.H., Rı´os, C.M., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., 1999. Non satellite veins in the pelvic limb of the llama. Anat. Rec. 256, 99–103. Graziotti, G.H., Rı´os, C.M., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., 2000. Arteries of the hindfoot of the llama (Lama glama). Anat. Histol. Embryol. 29, 273–276. Graziotti, G.H., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., Fux, G.F., Rı´os, C.M., 2003. Systematic study of the internal iliac artery in llama (Lama glama). Ann. Anat. 185, 461–463. Kadhim, K.K., Khamas, W.A., Al-Shaikhly, A.K., 2001. Arterial supply to the genital system of dromedary camel. J. Camel Pract. Res. 8, 137–141. Nickel, R., Schummer, A., Seiferle, E., 1984. The Anatomy of the Domestic Animals, vol. 3. Verlag Paul Parey, Berlin–Hamburg, pp. 162–166, 183–190. Nitschke, T., Preuss, F., 1971. Main branches of the internal iliac artery in man and domestic mammals in a comparative anatomical study. Anat. Anz. 128, 439–453. Nuevo Freire, C.M., 1994. Sinopsis de historia natural de los came ´lidos sudamericanos. Excerta Anat. Camelidae 1, 4–8. Schaller, O., 1996. Nomenclatura Anato ´mica Veterinaria Ilustrada. Acribia, Zaragoza, pp. 312–319.
www.elsevier.de/aanat
Distribution of the internal pudendal artery in male and female llama (Lama glama) Guillermo Horacio Graziotti, Jose ´ Manuel Rodrı´guez Mene ´ndez, Clara Marı´a Rı´os, Carlos Lisandro Victorica Area of Anatomy, Faculty of Veterinary Sciences, Buenos Aires University (UBA), Chorroarı´n 280, Capital Federal CWO 1427, Argentina Received 17 February 2006; accepted 31 October 2006
KEYWORDS Arterial system; Llama; Pelvic cavity; Pudendal internal artery; Comparative anatomy
Summary The aim of this research has been to describe the internal pudendal artery distribution in male and female llama and to compare it with that of other domestic animals including the one-humped camel (Camelus dromedarius). The arterial system was perfused with a solution of 14% coloured plaster and preserved in a solution of a 10% formalin, 3% carbolic acid and 3% glycerine. The systematic dissection was made using traditional working techniques and standard instruments. The internal pudendal artery is the ventral terminal branch of the internal iliac artery at the level of the third sacral vertebra. The main supply of the pelvic organs comes from the prostatic or vaginal arteries; notwithstanding these arteries arise from the internal pudendal artery, showing an important difference between ruminants and pig (long iliac type). Similarities between the distribution of the internal pudendal artery of the llama and those obtained in the camel provide strong evidence of a common phylogenetic origin. & 2006 Elsevier GmbH. All rights reserved.
Introduction In the last years, we carried out research on the arterial and venous system of the Lama glama and this work is a continuation of this subject (Graziotti et al., 1997, 1998, 1999, 2000, 2003). Corresponding author. Tel.: +54 11 4524 8460;
fax: +54 11 4524 8480. E-mail address: [email protected] (G.H. Graziotti).
We have previously determined that the internal iliac artery in the llama belongs to an intermediate long iliac type of Dellbru ¨gge, cited by Nitschke and Preuss (1971), in which the parietal branches arise from the internal iliac artery and the visceral branches from the internal pudendal artery. The arterial distribution of the internal pudendal artery is described and compared with other domestic animals including the one-humped camel (Camelus dromedarius).
0940-9602/$ - see front matter & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2006.10.004
ARTICLE IN PRESS 296
G.H. Graziotti et al.
We believe that this study is a contribution revealing new aspects for consideration in teaching and research in comparative anatomy. It refers to a species that is growing in importance as a pet and farm animal.
Materials and methods This research was conducted on 13 post-mortem specimens, five males and eight females, 2.5–3-year-old llamas (Lama glama) from Trenque La ´uquen, Buenos Aires, Argentina, which were destined as source of food. They were perfused via an arterial path using the No. 18 Levine type catheter, from the abdominal aorta with a 14% coloured plaster solution; then they were preserved by immersion into a pool of a 10% formalin, 3% carbolic acid and 3% glycerine solution. The systematic dissection was made using traditional working techniques and standard instruments.
Results The internal pudendal artery was the ventral terminal branch of the internal iliac artery at the level of the third sacral vertebra. It ran caudoventrally on the internal surface of the broad sacrotuberous ligament, ending as the ventral perineal artery and the artery of the penis or the artery of the clitoris at the level of the caudal edge of the obturator foramen (Figs. 1–3). The internal pudendal artery gave off the prostatic or vaginal artery near its origin. The prostatic artery (Fig. 2) ran towards the prostatic gland and postprostatic urethra. Along its course the prostatic artery gave off two collateral branches: the first one, the ductus deferens artery ran cranioventrally supplying it and in turn gave off the caudal vesical artery and the ureteral branch; the second collateral branch was the urethral artery which terminated on the preprostatic urethra. The vaginal artery (Fig. 1A) was included in the broad ligament ending in several branches to the vagina and the urethra. Its first collateral branch was the uterine artery, which ran along the lateral edge of the neck, body and horn of the uterus; it sent out the caudal vesical artery that had a distribution similar to the male. Finally, the internal pudendal artery gave off the urethral artery near its end. Once, a slender middle rectal artery arising from the internal pudendal artery was found in a female (Fig. 1B and C).
Figure 1. General distribution of the internal pudendal artery in female llama (A); more detailed dissection (B) and (C) showed the terminal branches. Lateral aspect.
The ventral perineal artery in the male (Figs. 2 and 3) coursed on the medial aspect of the bulbourethral gland, which was irrigated by a proper branch. After that the ventral perineal artery passed between the bulb of the penis and the anus, sending branches to the ischiocavernosus muscle and the bulb of the penis, and giving rise to the caudal rectal artery to supply the most caudal portion of the rectum. The ventral perineal artery ended in several branches that ramified on the ventral part of the perineum. In the female, the ventral perineal artery gave off the vestibular branch and the caudal rectal artery and continued as the dorsal labial artery (Fig. 1B and C).
ARTICLE IN PRESS Distribution of the internal pudendal artery in male and female llama
Figure 2. Lateral view of the general distribution of the internal pudendal artery in male llama (A) and general scheme (B).
The artery of the penis (Fig. 3) obliquely crossed the lateral surface of the pelvic urethra giving off the artery of the bulb of the penis and passing under the ischiatic arch. Afterwards, it ran cranioventrally sending the deep artery of the penis and the dorsal artery of the penis, which coursed on the dorsal aspect of this organ. The artery of the clitoris (Fig. 1B and C) coursed on the lateral aspect of the constrictor vestibular muscle giving off the artery of the vestibular bulb; more peripheral, the artery of the clitoris gave rise to the deep artery of the clitoris in relation to the body of the clitoris, and finally continued as the dorsal artery of the clitoris.
Discussion According to Grasse´ (1971), Nickel et al. (1984) and Barone (1996) in the long iliac type (ruminant and pigs) the internal iliac artery gives off the visceral intrapelvic and parietal branches; the internal pudendal artery only supplies the perineum and the external genital organs. Notwithstanding the intrapelvic visceral branches in the llama arise from the internal pudendal artery as it occurs in horses and carnivores (short iliac type). This is an important difference in relation to the distribution in characteristics of long iliac type in
297
Figure 3. Detailed dissection showed the terminal branches of the penis artery in llama. Caudolateral aspect. 1, Internal iliac artery; 2, caudal gluteal artery; 3, internal pudendal artery; 4, vaginal/prostatic artery; 5, uterine artery/artery of the deferens duct; 6, caudal vesical artery; 7, ureteral branch; 8, urethral branch; 9, middle rectal artery; 10, urethral artery; 11, ventral perineal artery; 12, caudal rectal artery; 13, dorsal labial branch; 14, vestibular branch; 15, artery of the clitoris/ penis; 16, artery of the vestibular bulb/artery of the bulb of the penis; 17, deep artery of clitoris/penis; 18, dorsal artery of the penis/clitoris (displaced partially); 19, branch for the bulbourethral gland; a, ampulla of the rectum; b, deferens duct; c, bladder; d, ureter (cut and removed partially); e, prostate; f, urethra; g, bulbourethral gland; h, bulb of the penis; i, crus of penis; j, body of penis; k, testicle/ovary; l, uterine horn; m, vagina; n, vestibular bulb; p, vestibule of the vagina; A, ischiatic table; B, ischiatic tuberosity; C, ischiatic arch; D, tail; E, symphysis pelvis.
ruminants and pigs and in the artiodactyla type of Nitschke and Preuss (1971). The origin of the vaginal or prostatic arteries from the internal pudendal artery in llama is in accordance with a long intermediate type of the internal iliac artery in this species, as reviewed by Graziotti et al. (2003). The main supply of the uterus comes from the vaginal artery via the uterine artery as is the case in the carnivore and dromedary camel (Kadhim et al., 2001). There are no branches to the uterus from
ARTICLE IN PRESS 298 the external iliac or umbilical arteries as found in the mare, cow and sow. As would be expected, in the male the umbilical artery does not supply the deferent duct because the main blood supply of this organ comes from the prostatic artery. The caudal part of the urethra is nourished by a branch of the prostatic artery, which occurs in the horse and rabbit (Baron, 1996). The middle rectal artery is absent in llama or it is rarely developed. The territory nourished by this vessel in other species is supplied by the cranial rectal artery in llama, which is very distinct. When the middle rectal artery is present, it arises from the internal pudendal artery as occurrs in the ox, ram (Nickel et al., 1984) and dromedary camel (Kadhim et al., 2001). We have found the middle rectal artery in one female llama only. The bulbourethral gland is irrigated by an innominate proper branch (Schaller, 1996) originating from the ventral perineal artery. A well-developed vestibular branch is present in llama as also found in the mare and cow; however it arises from the ventral perineal artery (at the same level as the proper branch for the bulbourethral gland), while it takes origin from the internal pudendal artery in these species (Barone, 1996; Nickel et al., 1984). As is the case in horses, human (Barone, 1996) and one-humped camel (Kadhim et al., 2001) the dorsal perineal artery is absent in llama. Similarities between the distribution of the internal pudendal artery and internal iliac artery in llama (Graziotti et al., 2003) and those obtained in dromedary camel by Kadhim et al. (2001) are strong evidence of a common phylogenetic origin (Nuevo Freire, 1994).
G.H. Graziotti et al.
References Barone, R., 1996. Anatomie Compare´e des Mammife `res Domestiques. Angiologie. Vigot, Paris, pp. 357–385. Grasse´, P., 1971. Traite´ de Zoologie, tome XVI, fasc. IV. Masson et Cie, Paris, pp. 782–789. Graziotti, G.H., Rı´os, C.M., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., 1997. La irrigacio ´n arterial del muslo de la llama (Lama glama). Rev. Chil. Anat. 15, 35–40. Graziotti, G.H., Rı´os, C.M., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., 1998. Irrigacio ´n de la rodilla y pierna de la llama (Lama glama). Rev. Chil. Anat. 16, 89–94. Graziotti, G.H., Rı´os, C.M., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., 1999. Non satellite veins in the pelvic limb of the llama. Anat. Rec. 256, 99–103. Graziotti, G.H., Rı´os, C.M., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., 2000. Arteries of the hindfoot of the llama (Lama glama). Anat. Histol. Embryol. 29, 273–276. Graziotti, G.H., Rodrı´guez Mene´ndez, J.M., Victorica, C.L., Fux, G.F., Rı´os, C.M., 2003. Systematic study of the internal iliac artery in llama (Lama glama). Ann. Anat. 185, 461–463. Kadhim, K.K., Khamas, W.A., Al-Shaikhly, A.K., 2001. Arterial supply to the genital system of dromedary camel. J. Camel Pract. Res. 8, 137–141. Nickel, R., Schummer, A., Seiferle, E., 1984. The Anatomy of the Domestic Animals, vol. 3. Verlag Paul Parey, Berlin–Hamburg, pp. 162–166, 183–190. Nitschke, T., Preuss, F., 1971. Main branches of the internal iliac artery in man and domestic mammals in a comparative anatomical study. Anat. Anz. 128, 439–453. Nuevo Freire, C.M., 1994. Sinopsis de historia natural de los came ´lidos sudamericanos. Excerta Anat. Camelidae 1, 4–8. Schaller, O., 1996. Nomenclatura Anato ´mica Veterinaria Ilustrada. Acribia, Zaragoza, pp. 312–319.