Contribution to the Surgical Anatomy of the Ligaments of the Rectum M. Nano, M.D.,* H. M. Dal Corso, M.D.,* G. Lanfranco, M.D.,* M. Ferronato, M.D.,* J. P. Hornung, M.D.t From the *Department of Clinical Pathophysiology, Section of General and Geriatric Surgery, Motinette Hospital, University of Turin, 2brino, Italy, and the ~Institute of Cellular Biology, and Morphology, University of Lausanne, Lausanne, Switzerland PURPOSE: Many authors have discussed the presence and
the importance of the lateral ligaments of the rectum. Our contribution aims at clarifying some aspects of surgical anatomy that help in the preservation of the urogenital functions and may influence the sttrgical practice. METHODS: From 1994 to 1998 we examined 27 fresh cadavers and five embalmed pelves. We performed all dissections with a technique similar to that used for the surgical mobilization of the rectum. RESULTS:The lateral ligaments of the rectum are trapezoid structures originating from mesorectum and are anchored to the endopelvic fascia; as lateral extensions of the mesorectttm, they must be included in the surgical specimen. According to our results, three main structures can be recognized laterally to the rectum: 1) the lateral ligament, which does not contain important structures; 2) the inferior hypogastric plexus and the urogenital bundle; and 3) the lateral neurovascular pedicle of the rectum that comprises the nervi recti and the middle rectal artery, both running under the lateral ligament, although at different angles. CONCLUSION: At the point of insertion into the endopelvic fascia, the lateral ligaments nm close to the urogenital bundle. Nevertheless, the dissection at its attachment is safe ff the urogenital bundle is kept under visual control. [Key words: Rectmn; Surgical anatomy of the rectum; Lateral ligaments; Urogenital bundle; Middle rectal artery] Nano M, Dal Corso HM, Lanfranco G, Ferronato M, Hornung JP. Contribution to the surgical anatomy of the ligaments of the rectum. Dis Colon Rectum 2000;43:1592-1598. urgical treatment of rectal cancer has changed during the last several years, Because the cure of rectal cancer is almost exclusively surgical, all technical aspects have been studied and reviewed extensively in the attempt to reduce local recurrences and to decrease the incidence of urinary and sexual morbidity. The problem of lateral spread of rectal cancer was first raised by Sauer and Bacon 1 in 1951, but this fact was not considered of prognostic relevance until the early 1980s, w h e n Heald et aL 2 demonstrated that a correctly performed, total mesorectal excision (TME) alone could lead to an amazingly low rate of recurrence of rectal cancer in the pelvis and a high disease-
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Address reprints requests to Prof. Nano: Via Boston 22/5, 10137 Torino, Italy.
free survival rate. >5 Pelvic recurrence after conventional resection is a c o m m o n complication, with a worldwide incidence of approximately 30 percent for tumors that have penetrated the rectal wall, irrespective of nodal status. 6-~ As clarified by Quirke et al. 9 and Enker, 10 pelvic recurrence of rectal cancer that persists along positive lateral margins is directly related to inadequate surgery that failed to render the pelvis free of disease. In 1942, Jones 11 addressed the importance of postoperative impotence as a serious consequence of rectal cancer surgery caused by injury to nervi erigentes (as EckhardO 2 named them in 1863). In the following years, a certain number of anatomic studies confirmed this observation. 13-15 According to Hojo et aL, 6 postoperative urinary bladder complications ranged between 48 and 80 percent of patients, and complete impotence ranged between 38 and 76 percent, depending on the type of operation (conventional vs. extended excision). In the last decade, the surgical approach to the treatment of rectal cancer has been greatly refined, and from a gross, blunt, and blind dissection with flush clamping of lateral expansions, it became a more accurate procedui'e. ~6-17 All of these improvements are related to a better understanding and a wider knowledge of the anatomy of the pelvis. 18-2° We reviewed studies on the lateral structures of the rectum and, in particular, on the lateral ligaments, published from the end of the 1940s to the present. Although some erroneous concepts of classical anatomy have been corrected, many interpretations still exist on this area, and studies published during the same period may present different, and sometimes opposite, descriptions. In 1949, Goligher, 21 although considering lateral ligaments as important structures, postulated the poor relevance of the middle rectal artery. Michels et al. 22 in 1963, confirmed these concepts from an anatomic point of view, and Patricio et aL 23 in 1988, confirmed
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them from a surgical point of view. In 1959, Kimmel and McCrea 24 in their study on the development and distribution of splanchnic nerves, confirmed that two groups of fibers can be recognized within the plexus, each distributing to specific "target organs." In 1974, Crapp e t al., 25 in a comment on Waldeyer's work, based on the results of Uhlenhuth e t aL, 26 described the lateral ligaments as an expansion of the endopelvic fascia. In 1982, Heald e t al. 2 in their article on rectal surgery for cancer, described the technique of TME and did not mention the lateral ligaments; neither did they do so in a subsequent work published in 1986.17 In the same year, two other important contributions to the study of the lateral ligaments were published; according to H o j o 27 the lateral ligaments were rectal structures that should have been removed completely, whereas for Pearl e t al. 28 they were pararectal reflections of the endopelvic fascia. In 1987, Church e t al. 29 gave the first m o d e r n interpretation of the anatomy of the lateral ligaments describing the relationship between lateral ligament and middle rectal artery. These observations were based on the works published earlier by Goligher, 3° Gabriel, 31 Boxall e t al., 32 Wilson, 33 and a y o u b . 34 In 1989, Northover, 35 in a detailed article of surgical technique, gave an interpretation similar to Heald et al. 2 and Church e t aL 29 In the same year, Moriya e t al. 36 attached more importance to the lateral ligaments, and in 1991, Sato and Sato 2° published an extremely detailed work from which emerges the term "lateral ligaments," by which the authors meant all of the lateral structures of the rectum. In 1992, Enker 1° reviewed the importance of the lateral ligaments. In 1993, Block and Michelassi 37 described the relationship of the lateral ligaments, the middle rectal artery, and the nervi erigentes. In the same textbook, Moriya, 3* having very accurately described the ligaments, suggested they be cut at the level of the endopelvic fascia. While Lazorthes e t al. 39 agreed with Moriya, Campbell e t al. 4° suggested an opposite dissection of the rectum. In 1994, the same controversy took ptac e between Harnsberger, 41 w h o proposed sectioning the lateral ligaments, and Moreira e t aI., 42 w h o suggested a complete resection of the lateral ligaments. In 1995, Moriya e t al. 43 made a brief mention of the lateral ligaments. In 1996, Reynolds e t al., 7 in a description of mesorectal dissection did not even refer to the lateral ligaments, and in the same year Havenga e t al. 44 suggested that sectioning the lateral ligaments was an adequate maneuver. In 1997, RutegS.rd e t al. 45 emphasized that the lateral ligaments
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contain important nerves. Finally-, in 1998 Curti e t al. 46 gave an accurate description of the surgical anatomy of the lateral ligaments based on the conclusions of Church e t al. 29 We believe that some confusion still exists on the lateral ligaments of the rectum. For this reason, w e examined a series of cadavers to contribute to a better understanding of the relationship of the lateral aspects of the rectum and, particularly, of the lateral ligaments. MATERIALS A N D M E T H O D S From April 1994 to April 1998 w e examined 27 cadavers (15 males) within 24 hours after death, and five embalmed pelves obtained by sectioning the cadaver at the level of the L-4 vertebra and at the upper one-third of the thigh. The dissection was performed through a median laparotomic incision, removing the small bowel and the colon (from the right up to the sigmoid); from that point on, the dissection of the rectum was performed as in ordinary rectal surgery. Having recognized and freed both ureters, the peritoneum was removed to show" tSe aortic plexus. The pelvic splanchnic nerves were individually identified and traced from their origin to termination. When present, the middle rectal artery was carefully identified; the rectum, the mesorectum, and the lateral ligaments were isolated with particular attention to the anatomic relationship between the middle rectal vessels and the splanchnic nerves (urogenital bundle). Denonvilliers' aponeurosis was identified and dissected anteriorly to the point where it fuses with the denser retroperitoneal connective tissue and laterally to the seminal vesicles. RESULTS All information relevant to mesorectum, middle rectal artery, Denonvilliers' aponeurosis, and superior and inferior hypogastric plexuses are described elsewhere 47 and represent the first part of this study. In this article, we only describe the anatomy of the lateral ligaments of the rectum and their relationship to surrounding structures. The lateral ligaments can be clearly recognized in the embalmed trunk as approximately trapezoid structures, with their apex toward the rectum. They originate from the lateral aspect of mesorectum at the middle third of the rectum (3 o'clock and 9 o'clock positions, respectively). At its origin, each ligament is
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approximately 30 to 32 mm wide, whereas at its distal end, each ligament is 35 to 37 mm wide; the ligament is directed caudally and dorsally. Approact~ng the endopelvic fascia, the ligament becomes progressic-ely thicker and detaches from the mesorectum, forming an acute angle, with the apex of the ligament directed cranially. The superior aspect of the ligament is covered wRh a thin layer that represents the continuation of the same layer that envelops the mesorectum. Near the distal end of the ligament, this layer becomes gradually thinner until it disappears. The distal end of the ligament is made of dense connective tissue that fixes it to the endopelvic fascia, anteriorly to the inferior hypogastric plexus, and just under the urogenital bundle. The anterior and the posterior margins of the lateral ligament are well evidenced in the embalmed pelvis; in the fresh cadaver they can be viewed after an accurate dissection (Fig. 1). After cutting the ligament at its distal end, it becomes evident h o w this thin layer runs also on its inferior aspect, where it can be traced as far as the middle portion of the ligament. The ligament contains fat tissue in direct continuity with that of the mesorectum. Inside the fat of the lateral ligament, we have not found any macroscopic vascular structure. The relationships of the lateral ligament, the middle rectal artery, and the urogenital bundle are of extreme importance. The middle rectal artery crosses almost perpendicularly the inferior aspect of the ligament at it distal end, before entering the anterolateral aspect of the rectal wall. According to our study, the middle rectal artery was present bilaterally in 25 cases, and on one side in 4 cases (in 3 cases on the left). When the artery has not been isolated as a single structure, it was probably made of an arborization of small vessels. We have not noticed any difference in the diam-
Dis Colon Rectum, November 2000
eter of the superior rectal artery w h e n the middle rectal artery was absent (3 cadavers) or present. The inferior rectal artery has not been studied. We did not observe collateral ascending branches of the middle rectal artery in any of the cadavers. A various number of secondary branches pierced Denonvilliers' aponeurosis, probably heading toward the prostate and the seminal vesicles (or the vagina). In all male cadavers, one to three of these branches of bigger caliber were directed to the prostate gland. In the female cadavers, we did not observe collateral vessels of different diameters. The biggest branches (in the males) were extending off before the main trunk crossed the lateral ligament. The urogenital bundle runs just above the lateral ligament at the level of its insertion on the endopelvic fascia; in front of the anterior margin of the lateral ligament (outside the ligament) it crosses the middle rectal artery, dividing it into medial and lateral portions. From the inferior hypogastric plexus originate the nerve fibers (nervi recti) that course transversely under the lateral ligament to the rectal wall (Fig. 2). From the observation reported above we can distinguish basically three main anatomic structures: 1)
k
Pubis
Sacrum
B
Figure 1. Fresh cadaver showing the lateral ligament (a) and mesorectum (b).
Figure 2. A. Diagram of the lateral ligament (a), middle rectal artery passing under the lateral ligament (b), and urogenital bundle crossing the middle rectal artery in front of the lateral ligament (c). B. Embalmed cadaver showing the structures presented in the diagram.
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the lateral ligament, which does not contain important vessels; 2) the inferior hypogastric plexus and the urogenital bundle; and 3) the lateral neurovascular pedicle of the rectum that comprises the nervi recti and the middle rectal artery, both running under the lateral ligament, although at different angles. It is worth noting that when present, the middle rectal artery runs anterolaterally and not laterally, respective to the lateral ligament (Fig. 3).
DISCUSSION Goethe wrote, "Was man weiss, sieth man." Walsh and Schlege115 translated this as, "You only see what y o u look for, and you only look for what you know'." In our opinion, the dissection on cadavers represents an indispensable exercise to learn the correct surgical technique and to recognize during the operation the correct planes of cleavage to avoid unnecessary injuries to important nerves. To support this view and the importance for the surgeon of having a good ana-
A Pubis
Sacrum
Figure 3. A. Diagram of the middle rectal artery (a), urogenital bundle (b), and rectum (c). Rectal nerves have been sectioned. The middle rectal artery passing among the fibers of the urogenital bundle is evident. B. Intraoperative photograph showing the structures presented in the diagram.
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tomic knowledge, w e report some statements made by four leading, pioneer, American surgeons: "The surgeon's method of dealing with the blood vessels is a criterion of his proficiency in his art." (W. S. Halsted). 4a "A man can no more do good surgery without anatomical knowledge, than a pilot can safely guide his boat without knowing the channel." (J. Chalmers da Costa). 49 "You cut only what you see; as corollary, do not cut until you do see." (J. B. Deaver). 5° "One cannot operate with implicit faith equipped only with a textbook picture. Many and sometimes tragic are the lessons learned fi'om experience." (W. Mayo). 5~ Modern surgery of the rectum basically lies within two philosophies. The first originates from Heald's article 2 published in 1982 and considers a correct TME the key to surgical success. The second, supported by J a p a n e s e surgeons, 6-36-42 associates a variously extended lymphadenectomy with TME. In both approaches, the preservation of pelvic splanchnic nerves and the reduction of pelvic recurrences represents the most important part of modern rectal surgery. For these reasons, a sound knowledge of the surgical anatomy of the lateral aspects of the rectum, with their complex relationships, is imperative. The first observation that can be drawn from our work is that lateral ligaments do not originate from the endopelvic fascia, but they are an extension of the mesorectum, anchoring it to the endopelvic fascia. To obtain a complete excision of mesorectum, the lateral ligaments should, necessarily, be included in the specimen. The second observation is that being part of the mesorectum, the lateral ligament is in contact with the lateral neurovascular pedicle of the rectum, which comprises nervi recti to the rectum and the middle rectal artery,. The term "lateral neurovascular pedicle" has been used here probably for the first time, because, in our opinion, this definition allows a better understanding of the complex relationships of the lateral aspect of the rectum. During mobilization of the rectum, all of these structures necessaNy must be resected. The third and most important observation is relevant to the relationship between the lateral ligament and the urogenital bundle. The point of insertion of the lateral ligament to the endopelvic fascia is dangerously close to the urogenital bundle (it runs above the ligament). Nevertheless, the dissection of the lateral ligament at its attachment to the endopelvic fascia can be completed safely if the urogenital bundle is kept in view throughout the procedure.
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NANO ETAL CONCLUSIONS
From our experience with anatomic dissection applied to surgery, s o m e considerations can be drawn: • Lateral ligaments are extensions of the mesorecturn and must be cut at their attachment at the endopelvic fascia for TME to take place. • Lateral ligaments contain fatty tissue in c o m m u nication with the mesorectal fat and possibly s o m e vessels and nerve filaments that are of little importance. • Insertion o f lateral ligaments at the endopelvic fascia is placed u n d e r the urogenital bundle. • The middle rectal artery courses anteriorly a n d inferiorly in respect to the lateral ligament. • Lateral ligaments can b e cut at their insertion o n the endopelvic fascia w i t h o u t injuring the urogenital n e r v o u s bundle, which, however, should be kept in v i e w during this procedure, b e c a u s e it crosses the middle rectal artery and fans out b e h i n d the seminal vesicles. • The lateral aspect of the rectum receives the lateral pedicle, w h i c h consists of the nervi recti and the middle rectal artery.
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9. Quirke P, Dixon MF, Durdey P, Williams NS. Local recurrence of rectal cancer due to inadequate surgical resection. Lancet 1986;2:996-9. 10. Enker WE. Potency, cure, and local control in the operative treatment of rectal cancer. Arch Surg 1992;127: 1396-402. 11. Jones TE. Complications of one-stage abdominoperineal resection of rectum. JAMA 1942;120:104-7. 12. Eckhardt C. Untersuchungen uber die erektion des penis beim unde. Beitr Anat Physiol 1863;3:123. Cited by: Walsh PC, Donker pJ. Impotence following radical prostatectomy: insight into etiology and prevention. J Urol 1982;128:492-7. 13. Ashley FL, Anson BJ. The pelvic autonomic nerves in the male. Surg Gynecol Obstet 1946;82:598408. 14. Lee JF, Maurer "v2vl, Block GE. Anatomic relations of pelvic autonomic nerves to pelvic operations. Arch Surg 1973;107:324-8. 15. Walsh PC, Schlegel PN. Radical pelvic surgery with preservation of sexual function. Ann Surg 1988;208: 391-400. 16. Prete F. L'approccio neuroanatomico alia chirurgia oncologica del retto: esigenza o moda? Chimrgia (Bucur) 1996;9:543-5. 17. Heald RJ, Ryall RDH. Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1986;1: 1479-82. 18. Heald RJ. Discussion. In: Walsh PC, Schlegel PN. Radical pelvic surgery with preservation of sexual function. Ann Surg 1988;208:391-400. 19. Heald RJ. Breaching the mesorectum. Lancet 1990;335: 1067-8. 20. Sato K, Sato T. The vascular and neuronal composition of the lateral ligament of the rectum and the rectosacral fascia. Surg Radiol Anat 1991;13:17-22. 21. Goligher JC. The blood supply to the sigmoid colon and rectum with reference to the technique of rectal resection with restoration of continuity. Br J Surg 1949;37: 157-62. 22. Michels NA, Siddharth P, Kornblith PL, Parke WW. The variant blood supply to the small and large intestines: its import in regional resections. J Int Coll Surg 1963;39: 127-70. 23. Patricio J, Bemades A, Nuno D, Falcao F, Silveira L. Surgical anatomy of the arterial blood supply of the human rectum. Surg Radiol Anat 1988;10:71-5. 24. Kimmel DL, McCrea LE. The development of the pelvic plexuses and the distribution of the pelvic splanchnic nerves in the human embryo and fetus. J Comp Neurol 1959;10:271-91. 25. Crapp AR, Cuthbertson MS. William Waldeyer and the rectosacrat fascia. Surg Gynecol Obstet 1974;138:252-6. 26. Uhlenhuth E, Day EC, Smith RD, Middteton EB. The visceral endopelvic fascia and the hypogastric sheath. Surg Gynecol Obstet 1948;86:9-28.
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27. Hojo K. Anastomotic recurrence after sphincter-saving resection for rectal cancer. Dis Colon Rectum 1986;29: 11-14. 28. Pearl RK, Monsen H, Abcarian H. Surgical anatomy of the pelvic autonomic nerves: a practical approach. Ann Surg 1986;52:236-7. 29. Church JM, Raudkivi PJ, Hill GL. The surgical anatomy of the rectum--a review with particular relevance to the hazards of rectal mobilisation. IntJ Colorectal Dis 1987; 2:158-66. 30. Goligher JC. Surgery of anus, rectum and colon. London: Bailliere Tindall, 1980. 31. Gabriel WB. The principles and practice of rectal surgery. London: H. K. Lewis, 1963:1-33. 32. Boxall TA, Smart PJG, Griffiths JD. The blood supply of the distal segment of the rectum in anterior resection. Br J Surg 1962;50:399-404. 33. Wilson PM. Anchoring mechanisms of the anorectal region. S Afr MedJ 1967;141:1138-43. 34. Ayoub SF. Arterial supply to the human rectum. Acta Anat (Basel) 1978;100:317-27. 35. Northover JMA. The dissection in anterior resection for rectal cancer. Int J Colorectal Dis 1989;4:134-8. 36. Moriya Y, Hojo K, Sawada T, Koyama Y. Sig~ficance of lateral node dissection for advanced rectal carcinoma at or below the peritoneal reflection. Dis Colon Rectum 1989;32:307-15. 37. Block GE, Michelassi F. Pelvic lymphadenectomy with resection of the rectum. In: Wanebo HJ, ed. Colorectal cancer. Boston: Mosby, 1993:263-73. 38. Moriya Y. Pelvic node dissection with autonomic neIve sparing for invasive lower rectal cancer: Japanese experience. In: Wanebo HJ, ed. Colorectal cancer. Boston: Mosby, 1993:274-89. 39. Lazorthes F, Materre JP, Istvan G. Anatomie des nerfs pelviens et anastomose ildo-anale. Ann Chit 1993;47: 996-9. 40. Campbell SC, Church JM, Fazio VW, Klein EA, Pontes JE. Combined radical retropubic prostatectomy and proctosigmoidectomy for e n bloc removal of locally invasive carcinoma of the rectum. Surg Gynecol Obstet 1993;176:605-8. 41. Hamsbe,'ger JR, Vernava III AM, Longo WE. Radical abdominopelvic lymphadenectomy: historic perspective and current role in the surgical management of rectal cancer. Dis Colon Rectum 1994;37:73-87. 42. Moreira LF, Hizuta A, Iwagaki H, Tanaka N, Orita K. Lateral lymph node dissection for rectal carcinoma below the peritoneal reflection. Br J Surg 1994;81:293-6. 43. Moriya Y, Sugihara K, Akasu T, Fujita S. Pattems of recurrence after nerve-sparing surgery for rectal adenocarcinoma with special reference to loco-regional recurrence. Dis Colon Rectum 1995;38:1162-8. 44. Havenga K, Enker \VE, McDermott K, Cohen AM, Minsky BD, Guitlem J. Male and female sexual and urinary
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function after total mesorectal excision with autonomic nerve preservation for carcinoma of the rectum. J Am Coil Surg 1996;182:495-502. RutegSrd J, Sandzdn B, Stenling R, Wiig J, Heald RJ. Lateral rectal ligaments contain important nerves. Br J Surg 1997;84:1544-5. Curti G, Maurer CA, Buchler MW. Colorectal carcinoma: is lymphadenectomy useful? Dig Surg 1998;15:193-208. Nano M, Levi AC, Borghi F, et al. Observations on surgical anatomy for rectal cancer. Hepatogastroenterology 1998;21:716-26. Halsted WS cited by. Michels NA, Siddharth P, Komblith PL, Parke WW. The variant blood supply to the small and large intestines: its import in regional resections. J Int Coil Surg 1963;39:127-70. Chalmers da Costa J cited by. Michels NA, Siddharth P, Kombtith PL, Parke WW. The variant blood supply to the small and large intestines: its import in regional resections. J Int Coll Surg 1963;39:127-70. Deaver JB cited by. Michels NA, Siddharth P, Kornblith PL, Parke WW. The variant blood supply to the small and large intestines: its import in regional resections. J Int Colt Surg 1963;39:127-70. Mayo W cited by. Michels NA, Siddharth P, Kornblith PL, Parke WW. The variant blood supply to the small and large intestines: its import in regional resections. J Int Coil Surg 1963;39:127-70.
Invited Editorial To the E d i t o r - - T h e lateral ligaments o f the rectum are almost mythical structures that s u r g e o n s performing p r o c t e c t o m y k n o w must b e present but w h i c h are often ill-defined. The reality of rectal dissection in a deep, n a r r o w pelvis filled with a mass of fatty mesentery is far r e m o v e d from m o r e precise anatomic studies in often thin cadavers. In the f o r m e r situation, s u r g e o n s cling to fascial planes established at the pelvic brim, following t h e m d o w n into the n a r r o w pelvic depths. In the latter, the v i e w is better, the stakes are less, and dissection is academic rather than clinical. Anatomic studies are important, h o w e v e r , and this current study b y N a n o and colleagues serves not only to remind us of the importance of the lateral ligaments o f the rectum, but goes s o m e w a y t o w a r d d e m y t h o l o g i z i n g them. Rectal surgeons e n c o u n t e r w h a t t h e y s u p p o s e to be the lateral ligaments during dissection of the lower one-half of the rectum. The rectosacral fascia has b e e n incised and the m e s o r e c t u m has b e e n lifted out of the h o l l o w o f the sacrum. Fingers p a s s e d into the h o l l o w o f the sacrum a n d s w e p t anteriorly o n either side o f the m e s o r e c t u m b u m p into a c o n d e n s a t i o n o f