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EMBRYOLOGY, ANATOMY, AND SURGICAL APPLICATIONS OF THE PREPERITONEAL SPACE
SURGICAL ANATOMY AND EMBRYOLOGY
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EMBRYOLOGY, ANATOMY, AND SURGICAL APPLICATIONS OF THE PREPERITONEAL SPACE Andrew N. Kingsnorth, BSc, MS, FRCS, Panagiotis N. Skandalakis, MD, Gene L. Colborn, PhD, Thomas A. Weidman, PhD, Lee J. Skandalakis, MD, and John E. Skandalakis, MD, PhD
By definition, the preperitoneal (also called extraperitoneal or properitoneal) space lies in the abdominal cavity between the peritoneum internally and the transversalis fascia externally. Although the authors use the term preperitoneal throughout this article, in keeping with the popular choice of nomenclature, the more inclusive term, extraperitoneal, is probably preferable because it more clearly includes all of the potential space just external to the peritoneum, including the retroperitoneal area, whereas preperitoneal implies the ventral portion of the extraperitoneal space. Another name for the space is parietoperitoneal,22 which the authors believe to be a good term, although somewhat unwieldy. Within the preperitoneal space is a variable quantity of adipose tissue, loose connective tissue, and membranous tissue. Membranous tissue lies just internal to the transversalis fascia. Perhaps the classic definition of the preperitoneal space is correct, but if one accepts the bilaminar formation of the transversalis fascia into the anterior and posterior laminae, two spaces are formed: (1) one between the peritoneum (i.e., the innermost layer of the abdominal wall) and the posterior lamina of the transversalis fascia and (2) one between the two laminae of the transversalis fascia (Fig. 1).In some cases, the posterior lamina is
From the. Centers for Surgical Anatomy and Technique (PNS, GLC, LJS, JES) and Department of Surgery (LJS, JES), Emory University School of Medicine, Atlanta; Piedmont Hospital, Atlanta (JES); Center for Clinical Anatomy (GLC) and Department of Surgery (GLC, JES), The Medical College of Georgia, Augusta; and Mercer University School of Medicine, Macon, Georgia (JES); the Department of Surgery, Medical School, University of Athens, Athens, Greece (PNS); University of Plymouth, Plymouth, United Kingdom (ANK); and the Department of Anatomical Sciences, Ross University School of Medicine, Roseau, Commonwealth of Dominica, West Indies (TAW)
SURGICAL CLINICS OF NORTH AMERICA VOLUME 80 NUMBER 1 FEBRUARY 2000
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KINGSNORTH et a1 Post. Lamina T.F. Peritoneum
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Fruchauds orifice + the 4 ing. fern herniae 3 Fossae
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New concept of space of Bogros
Original space of Bogros
Figure 1. Laparoscopic anatomy of inguinal area demonstrating layers, fossae, and spaces. TF = transversalis fascia; Tr Abd Apon = transversus abdominis aponeurosis; Ing fern = inguinofemoral. (From Colborn GL, Skandalakis JE: Laparoscopic cadaveric anatomy of the inguinal area. Problems in General Surgery 12:13, 1995; with permission.)
not well developed and the space is limited by the peritoneum internally and the anterior lamina of the transversalis fascia externally (previously referred to as the transversalis fascia). Both laminae of the transversalis fascia insert inferiorly on the ligament of Cooper. Superiorly, they are perhaps united somewhere at the anterior abdominal wall and then continue upward as the transversalis fascia. The extensions of the [new] and [old] spaces, laterally and posteriorly, have not yet been clearly defined because they extend into the at-large preperitoneal spaces, including the posterior retroperitoneal space and the highly complex preperitoneal spaces of the pelvis. The preperitoneal space of the abdomen is filled with a variable amount of connective tissue and other anatomic entities, such as arteries; veins; nerves; and various organs, such as the kidneys and ureters. EMBRYOLOGY
The genesis of the preperitoneal space belongs to the in toto genesis of the abdominal wall. Perhaps all of the preperitoneal space and its subdivisions or extensions between the inguinal ligament below and the respiratory diaphragm above are formed "by necessity" to permit the downward and upward transmission of anatomic structures, such as arteries, veins, lymphatics, nerves, spermatic cord, and McArdleI6 discussed the evolutionary problems of gravitational stress secondary to erect posture, such as the carriage of the intra-abdominal organs and a lack of a strong posterior rectus sheath and transversalis fascia.
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Perhaps extending or illustrating his thoughts are three developments related to the embryologic formation of the preperitoneal spaces: Inguinal canal (the space above the inguinal ligament)-The testicular pathway from the retroperitoneal space to the scrotum Spaces below the inguinal ligament-Permit the exodus of muscles, nerves, and vessels destined to provide for the lower extremity Closure of the obturator foramen and the formation of the obturator canal-Comprise a third necessary pathway An understanding of the embryogenesis of the preperitoneal space is dependent on study of the embryogenesis of the anterior abdominal wall, more specifically, the part of the abdominal wall below the umbilicus. The anterior abdominal wall is formed by the ectoderm and parietal mesoderm, which form the somatopleure. At this stage, no muscles, vessels, or nerves are present. During the sixth week of gestation, the mesoderm from myotomes lying on either side of the vertebral column invades the somatopleure. The right and left rectus abdominis muscles are formed first; then the mesodermal sheets of muscle split into three layers. By the middle of the seventh week of gestation, the three paired, flat abdominal muscles and the rectus abdominis can be recognized. Between approximately the 9th and 10th weeks of gestation, the ossification of the pelvis begins, and at 13 weeks of gestation, the hip bones are evident. In the infraumbilical region, the invasion of the somatopleure by the somatic mesoderm is preceded by a layer of mesoderm that arises from the primitive streak just behind the cloaca. This "secondary mesoderm" surrounds the margin of the cloaca and invades the abdominal wall caudal to the body stalk, separating the layers of ectoderm and endoderm of the cranial end of the cloaca1 plate.3I The second mesoderm provides primary closure of the body wall between the external genitalia and the body stalk and forms part of the musculature of the bladder8 The secondary mesoderm is in position by the 7th week of gestation; it is followed by the somatic mesoderm, which fuses with it externally by the 12th week of gestation. Approximation of the two recti proceeds from the cranial and caudal ends, so that the abdomen becomes essentially closed by the 12th week of gestation, except for the umbilical ring. At the ring, the body wall, with its developing muscles, gives way to undifferentiated somatopleure over the surface of the umbilical cord. Although true skin may grow a short distance beyond the body, the structure of the cord remains embryonic. KlippeP3 suggested a new theory about the development of the anterior abdominal wall. Considering the embryo as a vector field and using vector analysis, he reported that the development of the embryo progresses not only by lateral infolding of the embryologic entities closing at the future umbilicus but also by an outward process from a fixed midpoint, perhaps from the middle to the periphery. This concept is interesting but sufficiently revolutionary to demand further practical and theoretic investigation. According to Lytle,I5 a diaphragm formed by the inguinal and lacunar ligaments and transversalis and pectineal fasciae bears the responsibility for closing the abdominal cavity off from the thigh. The embryology of the inguinal canal is peculiar. In a highly synergistic way, the skin, parietal peritoneum, and connective tissues and the muscles between them produce the future pathway for the testes. The skin forms the scrotum (scrota1 folds) in boys and the labia (labial folds) in girls. The parietal peritoneum produces the processus vaginalis, and the muscles and their fasciae contribute to the formation of the coverings of the spermatic cord. Although
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present in both genders, the peritoneal diverticulum is more important to male fetuses because it permits the descent of the testicles. The embryologic entities between the skin and peritoneum permit the processus vaginalis to penetrate them and form the inguinal canal, so the downward journey of the testicles to the scrotum is allowed. In girls, the ovary descends into the developing pelvis, accompanying the primordia of urogenital organs. The processus vaginalis finally closes to obstruct ovarian exodus but leaves the formation of the inguinal canal in situ. OgilvieZ0correctly stated that the descent of the testicles into the scrotum makes a mess of the three-layered abdominal wall. Lateral to the pubic tubercle are two openings in the anterior abdominal wall that permit the exodus of the processus vaginalis and testicle (or the round ligament of the uterus) from the abdomen. One is just superolateral to the pubic tubercle, provided by an opening in the aponeurosis of the external oblique and its fascia (i.e., the superficial, or external, inguinal ring). The other penetrates the underlying transversus abdominis and the transversalis fascia in an oblique way (i.e., the deep, or internal, inguinal ring) approximately 4 cm further laterally in adults. The passageway between the two openings is the inguinal canal. SURGICAL ANATOMY The clinically significant parts of the preperitoneal space include the space associated with the structural elements related to the myopectineal orifice of Fruchaud, the prevesical space of Retzius, the space of Bogros, and the retroperitoneal periurinary space. Myopectineal Orifice of Fruchaud Condon5 reported that, in groin hernia repair surgery, the preperitoneal space is developed medially and superiorly for a distance on the deep aspect of the musculoaponeurotic abdominal wall. The surgical anatomy of the preperitoneal space at the inguinofemoral area may be studied by dissecting from the skin to the peritoneum and from the peritoneum to the skin. Figure 2 is the basis of orientation to study the preperitoneal spaces as understood in the classic and newer views, respectively. The authors present these as viewed in dissection, starting from the skin to the myopectineal orifice of Fruchaud and from the peritoneum to the myopectineal orifice of Fruchaud. The myopectineal orifice beneath the arching lower border of the transversus abdominis and internal oblique muscles is bounded laterally by the iliopsoas muscle, medially by the lateral edge of the rectus abdominis, and inferiorly by the pubic pecten. It is divided by the iliopubic tract and the inguinal ligament, which separate the ”inguinal outlet” (allowing for the escape of the spermatic cord elements) above from the ”femoral outlet” below (permitting the exit of the femoral artery, vein, and nerve into the thigh). In the thinking of Fruchaud, the myopectineal orifice represents the potentially weak area in the abdominal wall that permits inguinal and femoral Umbilical Ligaments and Retzius’ Space In the peritoneum below the umbilicus, especially at the inguinofemoral area, several peritoneal folds produced by underlying anatomic entities (Fig. 3)
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Figure 2. Innominate fascia (1). External oblique aponeurosis (2). Internal oblique muscle (3).Transversus abdominis muscle (4). Transversalis fascia anterior (5). External spermatic fascia (6).Cooper’s ligament (7). Pubic bone (8). Pectineus muscle (9).Transversalis fascia (1 0). Transversalis fascia posterior lamina (11). Vessels (1 2). Peritoneum (1 3). Bogros’ space, home (space) of prosthesis (14). Preperitoneal fat (1 5). Transversus abdominis, aponeurosis,and anterior lamina of transversalis fascia (16). Femoral artery (17).Femoral vein (18). (From Skandalakis JE, Colborn GL, Androulakis JA, et al: Embryologic and anatomic basis of inguinal herniorrhaphy. Surg Clin North Am 73:799, 1993.)
are readily observed. The obliterated (or patent in varying degrees) urachus, with its overlying peritoneum, forms the median umbilical ligament, a midline peritoneal fold from the dome of the urinary bladder to the umbilicus. The left and right obliterated umbilical arteries and peritoneum form the medial umbilical ligaments, which travel upward toward the umbilicus. The left and right deep inferior epigastric arteries and veins, with their peritoneal coverings, form the lateral umbilical ligaments. These three peritoneal folds delineate three peritoneal fossae that can be observed within the peritoneal cavity. These fossae are sometimes shallow or deep. The fossa between the median and medial umbilical ligaments is the supravesical fossa. The fossa between the medial and lateral inguinal ligaments
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E !t'
..
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Figure 3. Sites of groin hernia and their relationship to bladder and ligaments of lower abdominal wall. Umbilicus (A). Urachus (B). Lateral umbilical ligament (obliterated hypogastric artery) (C). Deep epigastric artery (D). Internal inguinal ring (E). Falciform ligament (F). Lateral fossa (indirect inguinal hernia) (1). Medial fossa (direct inguinal hernia) (2). Supravesical fossa (paravesical hernia) (3). Femoral ring (femoral hernia) (4). (From Rowe JS Jr, Skandalakis JE, Gray SW: Multiple bilateral inguinal hernias. Am Surg 39:269, 1973; with permission.)
is the medial inguinal fossa, and the shallow fossa lateral to the lateral umbilical ligament is the lateral inguinal fossa. Each fossa represents the potential home of an inguinal hernia. From medial to lateral, the hernias are the external supravesical, direct, and indirect. The preperitoneal space that lies deep to the supravesical fossa and the medial inguinal fossa is the prevesical space of Retzius. Extending between the left and right inferior epigastric vessels is a variably thick mantle of preperitoneal connective tissue that incorporates the umbilical vessels and the midline urachus, referred to as the vesicournbilical fascia. It is a roughly triangular plane of tissue that extends upward to the umbilicus. Between the vesicoumbilical fascia and the posterior lamina of the rectus sheath is the space of Retzius. From the arcuate line of the posterior lamina of the rectus sheath above to the pubic bones below, the posterior lamina becomes increasingly thin, consisting of a translucent or nearly transparent lamina of aponeurotic
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fibers of the transversus abdominis and underlying transversalis fascia. Retzius believed that the weakened area of the rectus sheath facilitated the filling of the urinary bladder, which, in fetal development, is an abdominal, not a pelvic, organ. The space is “a continuous bursa-like cleft in the areolar tissue at the sides and front of the bladder which allows the bladder to fill and empty without hindran~e.”~ In the minds of many, the space of Retzius is thought of only as the potential space between the bladder posteriorly and the pubic bones anteriorly, but as originally described, the space of Retzius extends from the muscular floor of the pelvis to the level of the umbilicus. Anteriorly, it is bounded by the bodies of the pubic bones; medial portions of the pubic rami; and posterior lamina of the rectus sheath, at least to the level of the arcuate lines of Douglas. In the pelvis, the space of Retzius is bounded posteriorly by the prevesical fascia and the lateral pillars of the urinary bladder and the covering of pelvic peritoneum. More superiorly, the vesicoumbilical fascia and peritoneum provide a posterior wall for the space. The ductus deferens and the round ligament of the uterus traverse the umbilicovesical fascia en route to the deep inguinal ring. The space of Retzius is closed laterally along the line of fusion provided by the inferior epigastric vessels and the tissue that encloses them (whether that be the posterior lamina of transversalis fascia, extraperitoneal connective tissue, or a fascia1 fusion between transversalis and extraperitoneal membranous fascia). This lateral limit to the space is well illustrated on CT scans of the pelvis in cases in which the prevesical space is distended with fluid (Fig. 4). The space of Retzius contains loose connective tissue and fat. More importantly, vascular elements present there can be of importance in trauma and surgical procedures, especially urologic, urogynecologic, and orthopedic procedures. The aberrant obturator artery and vein can be of major significance in perioperative and postoperative bleeding. In the event that a patient has a normal obturator artery arising from the internal iliac and an aberrant obturator arising from the inferior epigastric or external iliac, with anastomoses between the two obturator vessels, bleeding of such volume can occur that the anatomic vascular pattern has been referred to as the ”circle of death.” Aberrant obturator arteries occur in 25% to 40% of individuals in the United States, but the prevalence in other countries has been reported to be as high as 80%. When present, they typically cross medial to, lateral to, or directly across the femoral ring and then the pectineal ligament of Cooper en route to the obturator canal in the pelvis. They can be readily injured in orthopedic, urologic, urogynecologic, or general surgical procedures that involve the pectineal ligament. To make matters worse, and the possibility of vascular injury even more possible for unwary physicians, such vessels are commonly well hidden by overlying lymphatic tissue confluent with that of the femoral canal. Aberrant obturator veins occur far more commonly than do aberrant obturator arteries. When torn under laparoscopic conditions, bleeding can be scant or absent until the pressure of insufflation stops, with potentially severe postoperative bleeding occurring thereafter. Vessels that can be found in the retropubic space also include atypical arteries and veins for the urinary bladder arising from aberrant obturator, inferior epigastric, or external iliac sources. Retropubic branches of obturator and aberrant obturator sources are common. In approximately 10% of cases, accessory pudendal vessels may pass through the prevesical space, traveling from internal iliac sources and under the pubic bones to reach the dorsum of the penis or clitoris. Laterally in the space are the obturator nerve, obturator artery, and vein in the terminal parts of their course to reach and enter the obturator canal.
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Urnbilicovesicel fasda
Preveslcal space Perivesical space
A Prevesical space fluid
B Figure 4. Fluid in the prevesical Retzius' space. A, Sagittal cross-section of lower abdomen and pelvis. Umbilicovesical fascia, prevesical space, and the expanded prevesical space. B, Axial cross-section. Large collection of fluid distends prevesical space with a characteristic form like a molar tooth. R = rectum; U = uterus; B = bladder; C = cecum; S = sigmoid. Peritoneum (Dotted line). (From Korobkin M, Silverman PM, Quint LE, et al: CT of the extraperitoneal space: Normal anatomy and fluid connections. AJR 159:940, 1992; with permission.)
Read2' stated: The presence of this space allows for the properitoneal placement of large prostheses with minimal fixation as pioneered by Stoppa et a1J8 . . . It also makes laparoscopic herniorrhaphy possible since there are no major structures which pass through it. However, there are important nerves and blood vessels in the wall which have to be protected during cleavage. This space allows for prosthetic plugs to be placed with minimal dissection from the classical groin incision, there being room enough for them to expand and protect the femoral and inguinal orifices, obviating recurrent herniation.
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Bogros' Space
Although any anatomic description of the posterior preperitoneal space, as well as the lateral pathways and extensions of this space, is open to question, some boundaries are presented from a surgicoanatomic standpoint. In his thesis presented in Paris in 1823, Bogros4 described a triangular space between the abdominal wall and the peritoneum that could be entered by means of an incision through the roof and floor of the inguinal canal. In this way, aneurysms of the iliac or inferior epigastric vessels could be secured and treated without the considerable surgical risk of entering the peritoneal cavity. Nyhus entered this space in similar, but unidentical, fashion in his exemplary series of studies on the posterior preperitoneal approach for hernia repair (see the excellent but succinct discussion by Read).22 Although Bogros described the space at the termination of the external iliac artery as being only approximately 13 mm to 15 mm wide and 4 mm to 6 mm deep, modern interpretation seems to be extending this space upward into the retroperitoneal area, and some workers state that it is continuous medially with the space of Retzi~s,*~ but the authors believe that communication between the two spaces is an artifact of dissection or a result of disease processes; they are normally separated from one another by the plane of fusion between extraperitoneal connective tissue and transversalis fascia that occurs along the path of the inferior epigastric vessels. This conclusion is supported by clinical studies, such as those by Korobkin et al.14 Retroperitoneal Space
The " o l d preperitoneal or extraperitoneal space (i.e., the space between the peritoneum and anterior lamina of transversalis fascia) is a pathway for vessels and nerves to and from the lower extremity. It is partially the home of several anatomic entities. It includes the perirenal and pararenal spaces (Fig. 5). Stoppa (personal communication, 1992) wisely stated that the cleavable interparietoperitoneal space of Bogros is considered to be the lower prolongation of the great posterior paraurinary space. After radiologic and anatomic studies of this area, Hureau et al'Ql1 considered the composition of the posterior paraurinary area to be the following: anteriorly, Gerota's fat contained within the fascia; and posteriorly, a cellular space that most likely incorporates the space of Bogros in the internal iliac fossa. When Stoppa (personal communication, 1992) and Hureau et all0,l1 talk about the paraurinary space and area, they are probably referring to the same area as the pararenal space of US literature. To best understand the posterior pararenal space, the anatomy of the retroperitoneal area must be considered. The posterior parietal peritoneum and the transversalis fascia provide the anterior and posterior boundaries of the retroperitoneal space, respectively. This space extends from the pelvic brim inferiorly to the diaphragm superiorly. Among the major structures it encompasses are the adrenal glands, kidneys, ureters, pancreas, inferior vena cava, aorta, portal vein, ascending and descending colon, and parts of the duodenum. In a horizontal cross-section, it is somewhat C-shaped because of the curvature of the lumbar spine. As a result, some retroperitoneal structures (i.e., the pancreas and duodenal loop) lie anterior to others (i.e., the spleen, kidneys, and posterior aspect of the liver). These relationships are illustrated in Figure 6 and in the excellent work of Hureau et a1.I0,l1 Meyers17 divided the extraperitoneal region into three compartments ac-
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Figure 5. Normal anatomy of inguinal region viewed from internal (preperitoneal) aspect.
(FromCondon RE: Prosthetic repair of abdominal hernia. In Nyhus LM, Condon RE (eds): Hernia, ed 3. Philadelphia, Lippincott, 1989, p 559; with permission.)
cording to their demarcation by well-defined fascial planes. The anterior and posterior layers of Gerota’s fascia are central to the division of the extraperitoneal region. The kidney and the perirenal fat are enveloped by this dense sheath. The fusion of its two layers behind the ascending or descending colon forms a single lateroconal fascia. This continues around the flank to blend with the peritoneal reflection and form the paracolic gutter. Meyers named these three compartments (Figs. 7-9) the (1)anterior pararenal space, which extends from the posterior parietal peritoneum to the anterior renal fascia and is confined laterally by the lateroconal fascia; (2) perirenal space, in which the kidney and perirenal fat reside within the confines of Gerota’s fascia; and (3) posterior pararenal space, whch extends from the posterior renal fascia to the transversalis fascia. A thin layer of fat lateral to the lateroconal fascia, also known as the preperitoneal fat, is present in varying amounts. The extraperitoneal portions of the alimentary tract, ascending and descending colon, duodenal loop, and pancreas are included within the anterior pararenal space. This space is continuous across the midline. Some investigators believe that the perirenal spaces have no continuity across the midline because of the fusion of the posterior fascial layers with the psoas or quadratus lumborum fascia medially, and to the fusion of the renal fascia with the dense mass of connective tissue surrounding the great vessels in the root of the mesentery and behind the pancreas and duodenum anteriorly. Others have reported continuity of the spaces at the level of the lower poles of the kidneys, especially in some patients with extravasation of blood or other fluids from one side to the other. In cadaveric dissections by the authors, they have observed many cases in which spatial continuity could be easily demonstrated without artifactual separation of tissues. Text continued on page 15
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B Figure 6. Major retroperitoneal compartments. A, Axial cross-section at level of kidneys. 6,Sagittal cross-section in plane of right kidney. Anterior pararenal space (Hatched). Cross-hatchedareas = perirenal space; Stippled areas = posterior pararenal space; L = liver; P = pancreas; LS = lesser sac; S = spleen; V = vena cava; A = aorta; K = kidney; RK = right kidney; LK= left kidney; C =colon; D =duodenum. (From Korobkin M, Silverman PM, Quint LE, et al: CT of the extraperitoneal space: Normal anatomy and fluid connections. AJR 159:934, 1992; with permission.)
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Figure 7. Sagittal section through abdomen. Striped area = anterior pararenal space; Stippled area = perirenal space; Cross-hatched area = posterior pararenal space. (From Meyers MA: Dynamic Radiology of the Abdomen, ed 4. New York, Springer-Verlag, 1994, p 223; with permission.)
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Figure 8. Three extraperitoneal spaces. Anterior pararenal space (1). Perirenal space (2). Posterior pararenal space (3). C = colon; K = kidney; PM = psoas muscle; QL= quadratus lumborum muscle. (From Meyers MA: Dynamic Radiology of the Abdomen, ed 4. New York, Springer-Verlag, 1994, p 222; with permission.)
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B
/
Figure 9. Relations and structures of the three extraperitoneal spaces. A, Horizontal cross-section. B, Left parasagittal view. Striped area = Anterior pararenal space; Stippled area = perirenal space; Cross-hatched area = posterior pararenal space; C = colon; K = kidney; L = liver; P = pancreas. (from Meyers MA: Acute extraperitoneal infection. Semin Roentgenol 8:445,1973; with permission.)
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Questions remain. On its downward journey, does the fascia of Gerota form an open pathway or a closed space? The authors believe that it is open anatomically and radiologically. In the 1950s, an injection of air into the presacral space, which travelled upward into the perirenal space, was used to study the renal silhouette. Another question, perhaps of considerable significance to some investigators, is, What is the origin of the perirenal fascia? Determining the answer to this question is likely an important key to the question concerning the possible bilaminar nature of the transversalis fascia. If the perirenal fascia is a specialized, normal regional condensation of extraperitoneal connective tissue, is it not reasonable to think that such a condensation is present also in the inguinal region (there, called the posterior lamina of transversalis fascia), enclosing the inferior epigastric vessels, reinforcing the iliopubic tract, and continuing medially in the form of vesicoumbilical fascia? Is the perirenal fascia derived from the transversalis fascia? The authors have seen no significant evidence to support this conclusion. Davies6suggested that the inner linings of the peritoneal cavity are comparable with the outer coverings of the abdominal wall but reversed in orientation, so the skin (i.e., peritoneum) lies on an adipose layer of Camper (i.e., extraperitoneal fat), which is succeeded by the membranous layer of the fascia of Scarpa (i.e., the membranous layer of extraperitoneal fascia), and this by the muscle fascia of Gallaudet (i.e., transversalis fascia), beneath which is external oblique musculature (i.e., transversus abdominis). This is probably a terrible oversimplification of a highly complex structure, but the authors still find it interesting.
CONTENTS OF THE PREPERITONEAL SPACE OF THE INGUINOFEMORAL REGION
The contents of the preperitoneal space can be characterized as vascular (i.e., arteries, veins, lymphatics), nerves, and adipose tissue (thick or thin). These include: Vascular Arteries External iliac artery with its branches Deep circumflex iliac artery Inferior epigastric artery with its branches Suprapubic and retropubic arteries, accessory obturator artery Cremasteric artery Veins External iliac vein Inferior epigastric veins Suprapubic and retropubic tributaries Rectusial tributaries from rectus abdominis Accessory obturator veins Deep circumflex iliac vein The Bendavid circle Nerves Ilioinguinal Iliohypogastric Spermatic plexus (sympathetic and sensory)
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L1, L2, L3 ventral rami Genitofemoral Genital branch Femoral branch Femoral Lateral femoral cutaneous Vessels of the Preperitoneal Space
The external iliac artery and vein are located at the medial area of the psoas muscle. They snake above the fascia of the muscle and travel under the iliopubic tract and inguinal ligament. Here they change names and become femoral vessels. In most cases, the inferior epigastric vessels are branches from the external iliac artery and vein. From their origins, they initially descend for a short distance, then, curving upward, they travel superomedially in the direction of the umbilicus and are located between the posterior lamina of the transversalis fascia and the peritoneum. During their upward journey, they pierce the posterior lamina of the transversalis fascia and enter the posterior area of the rectus sheath. In the inguinal area, the inferior epigastric artery typically provides origin for the cremasteric artery and the pubic branch. The pathway of each branch is different from the other. The cremasteric artery may be found at the medial area of the deep inguinal ring. It proceeds to be an element associated with the spermatic cord. In female patients, the cremasteric artery provides origin for the artery of the round ligament, one of the sources of origin of Sampson’s artery. The pubic or accessory obturator artery anastomoses with the obturator artery. The obturator artery springs from the inferior epigastric artery or directly from the external iliac artery. Other vessels that take origin from the external iliac artery are the deep circumflex artery and vein. These vessels pass slightly distally from origin and then laterally, deep to the iliopubic tract, and are “sandwiched“ between the internal oblique and transversus abdominis. Near the anterior superior iliac spine, they give origin to a large, ascending branch that is significant in vascular supply to the anterior abdominal wall. Staples placed laterally here during laparoscopic herniorrhaphy may result in significant hematoma. The deep circumflex iliac vessels anastomose with the iliolumbar vessels. In male patients, 10 to 12 veins that segregate into anterior and posterior groups form the pampiniform plexus. The two groups are drained by three or four veins joined to form two veins proximal to the internal inguinal ring. The two veins pass on either side of the testicular artery through the extraperitoneal space. The right testicular vein opens into the inferior vena cava. The left testicular vein enters the left renal vein. The cremasteric vein flows to the inferior epigastric veins. The deferential vein drains into the pampiniform plexus and the vesical plexus. The vesical plexus is drained by the prostatic venous plexus to the internal iliac vein. Ergun et a17further classified the veins of the pampiniform plexus as follows. Group I-Tight plexus of venovenous anastomoses around the testicular artery Group 11-Similar construct to group I, but found in fatty tissue Group 111-Similar formation, located between groups I and I1 Group IV-Arteriovenous anastomoses with the testicular artery
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Wishahi30 reported the following. [Tlhe venous drainage of the testis cannot be looked upon as it is in the standard anatomy; on the contrary, it deviates from the description in the text. We demonstrated that the venous drainage of the testis is via the pampiniform plexus, which is primarily drained by the testicular and external pudendal veins. The testicular vein-midway between the internal inguinal ring and the lower pole of the kidney-divides into the medial and lateral branch to form a delta. The medial branch communicates with the ureteral and contralateral veins; there, it terminates in the left renal vein or inferior vena cava on the right side. The lateral branch communicates with colonic and renal capsular veins and terminates in the perinephric space. There is no cross-communication between the left and right testicular venous system in the scrotal, retropubic or pelvic areas. The only cross-communication is in the abdomen, and is seen in only 50% of men. The testicular vein has no valves. Sofikitis et alZ6advised that the possible existence of more than one left testicular vein, especially at the lumbar level, was a reason for attentive identification of all testicular veins during varicocelectomy. The authors question the validity of the assertion of Hahn-Pedersen et a19 that the distention of veins of the pampiniform plexus may prevent the formation of inguinal hernia. Although their suggestion has some merit, much research remains to be done before this idea is accepted. The venous circle of Bendavid is located at the subinguinal space of Bogros. It is a network composed of the deep inferior epigastric, iliopubic, rectusial, suprapubic, and retropubic veins (Figs. 10 and 11). These veins may produce hematomas because they collapse during laparoscopic surgery and during the placement of prosthetic material. In dissections performed by the authors, they have seen suprapubic veins as large as 1 cm in external diameter passing along the superior pubic ramus to the external iliac vein. Such vessels may receive tributaries from the bladder and also the aberrant obturator vein. Aberrant obturator veins occur in at least 70% of individuals. In many cases, an aggregation of lymph nodes and lymphatic vessels crosses the pectineal ligament of Cooper from the femoral canal to the obturator canal, providing communication between the node of Cloquet (Rosenmuller) and pelvic lymph nodes. This lymphatic tissue often obscures aberrant obturator vessels crossing the pectineal ligament, causing them to be more vulnerable to injury from dissectors, refractors, and staplers. Nerves of the Preperitoneal Space
Within the preperitoneal inguinofemoral region are several nerves that may be subject to injury in laparoscopic herniorrhaphy, including the genitofemoral, ilioinguinal, lateral femoral cutaneous, and femoral nerves. The genitofemoral nerve typically divides into a femoral (lumboinguinal) branch and a genital (external spermatic) branch. The genital branch was commonly combined with the ilioinguinal nerve (7.7% of cases) in a study in the authors’ l a b o r a t ~ r y .In ~ ~most cases, the genital branch of the genitofemoral nerve descends on the external iliac artery after leaving the ventral surface of the psoas muscle. Just proximal to the origin of the inferior epigastric artery, the
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lateral margin of rectus abdominis /
i
\/ rectusio-epigastric communicating v. rectusial v.
Figure 10. Deep inguinal vasculature in Bogros’ space. int = internal. (From Bendavid R: The space of Bogros and the deep inguinal venous circulation. Surgery, Gynecology, and Obstetrics 174:356, 1992; with permission.)
genital branch ascends to the inferomedial angle of the deep inguinal ring to enter the canal. Then it accompanies the cremasteric branches of the inferior epigastric vessels. Lying deep to the cremaster, it supplies that muscle and some of the skin of the scrotum. Within the deep inguinal ring, the genital branch is deep medially, with the cremasteric vessels, that is, medial in such a way that the suturing of the crura of the internal ring is above and superficial to the position of the nerve. Entrapment of the genital branch of the genitofemoral nerve at the deep ring should occur rarely-perhaps just in those unusual cases in which the genital branch and the ilioinguinal nerves are combined and located more superficially. Leaving the deep inguinal ring, the genital branch is located at the lower margin of the iliopubic tract, together with the cremasteric vessels. Entrapment and injury of the nerve can occur only with deep suturing of the iliopubic tract (Fig. 12). The femoral branch of the genitofemoral continues inferiorly into the anterior lamina of the femoral sheath. It supplies sensory fibers to the skin in the vicinity of the femoral triangle of Scarpa. The femoral nerve emerges from the protection of the psoas muscle approximately 6 cm above the inguinal ligament, entering the preperitoneal space. It then passes deep to the iliopubic tract and inguinal ligament to enter the thigh. Staples pressed deeply, just lateral to the deep inguinal ring, may injure the femoral nerve. At the lateral border of the psoas, an early rising anterior femoral
THE PREPERITONEAL SPACE
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Figure 11. A-D, Variations in the vasculature of the deep inguinal venous system. (From Bendavid R: The space of Bogros and the deep inguinal venous circulation. Surgery, Gynecology, and Obstetrics 174:356,1992; with permission.)
cutaneous branch of the femoral nerve can also be inadvertently encountered and injured. The authors have observed that the femoral branch of the genitofemoral may communicate with, or be replaced by, an intermediate femoral cutaneous nerve arising from the femoral nerve in the iliac fossa. As the femoral nerve courses through the preperitoneal space, it is subject to compression or injury from diverse sources, including iliacus hematoma,I9 iliopectineal ligament compression,'8 and laparoscopic inguinal herniorrhaphy.'2 Compression of the femoral nerve or more traumatic insult with staples or sutures results in debilitating pain and weakness or paralysis of the quadriceps extensor musculature of the thigh. According to most anatomy texts (e.g., Gray's Anatomyz9),the ilioinguinal nerve passes within the abdominal wall, above the iliac crest, deep to the internal oblique to a point just medial to the anterosuperior iliac spine, at which point it becomes visible between the external and internal obliques and then passes into the inguinal canal. In the authors' inve~tigation:~the ilioinguinal nerve crossed the iliac fossa in 25.5% of cases. There, it was often combined in whole or in part with the lateral femoral cutaneous nerve. The lateral femoral cutaneous nerve usually exits the preperitoneal space within 1 cm from the anterosuperior iliac spine, there passing under or through the lateral extremity of the inguinal ligament. It may lie as many as 4 cm medial to the anterosuperior spine. The ilioinguinal nerve or the lateral femoral
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'
iliac spine
Deep inguinal ring
Inferior epigastric a. Genital branch ol genttofemoral nerve
Shelving edge of inguinal ligament and iliopubic tract
A
Posterior inguinal wall (vansversalis fascia and transversus abdominis aponeurosk)
At& of internal oblique muscle
\
Transversalis lascia
.,:
Aponeurosis of external oblioue
The surgical beginnin of iliopubic tract (prox
B /
Inguinal ligamenl with shelving edge elevated and relraded
Cremasler vessels and genital btanch ofgenitolemoral nerve
Figure 12. Genital branch of the genitofemoral nerve. A, Pathway of genital branch of genitofemoral nerve from deep inguinal ring to medial side of spermatic cord. FA=femoral artery; FV=femoral vein. 6,lliopubic tract and its relations to genital branch of genitofemoral nerve. (From Colborn GL, Skandalakis JE: Importance of the iliopubic, Cooper's, and Gimbernat's ligaments. Problems in General Surgery 12:37, 1995; with permission.)
THE PREPERITONEAL SPACE
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cutaneous nerve can be penetrated by staples or sutures that pierce the iliopubic tract lateral to the deep inguinal ring. In the preperitoneal region, one should carefully avoid the contents of the "triangle of and the "triangle of pain."', The triangle of doom is bounded medially by the ductus deferens and laterally by the gonadal vessels and contains principally the external iliac artery and vein. The triangle of pain is bordered by the gonadal vessels medially and the iliopubic tract laterally. It regularly contains, from lateral to medial, the lateral femoral cutaneous nerve, femoral branch of the genitofemoral nerve, and the femoral nerve. In many cases, it contains the atypical ilioinguinal nerve; the early rising anterior femoral cutaneous nerve; and, often, small nerves, the identity and function of which are unclear. Preperitoneal Landmarks
Within the preperitoneal space, some landmarks can usually be found with little effort, visually or by palpation. Typically, one can quickly find the inferior epigastric vessels, medial umbilical ligament, gonadal vessels, and ductus deferens, although each one of these may be somewhat hidden, in varying degree, by adipose tissue and adhesions. Medially, the somewhat flattened pectineal ligament can be palpated with a dissection instrument and then clarified with a little dissection. Likewise, the pubic tubercle can be palpated externally with the fingers and internally with instruments. Laterally, the iliopubic tract provides a bright band extending from the anterosuperior iliac spine laterally to the medial border of the femoral ring medially. The iliopubic band is composed mostly of aponeurotic fibers of origin of the transversus abdominis. It receives contributions from the transversalis fascia and membranous preperitoneal connective tissue and often a stout contribution from the psoas fascia. APPROACHES TO THE PREPERITONEAL SPACE
The preperitoneal space can be entered by open or closed (laparoscopic) approaches. The open approach includes various modifications of the classic open operation for herniorrhaphy, except that all layers of the anterior abdominal wall are divided to allow for access to the preperitoneal space. After the transversalis fascia is divided, the peritoneum is displaced to allow entrance into, and expansion of, the preperitoneal space, followed by herniorrhaphy or placement of prosthetic mesh to cover any or all of the points of egress of hernias through the myopectineal orifice of Fruchaud. The midline infraumbilical procedures, such as the Cheatle-Henry and Stoppa procedures, and the suprainguinal approach of Nyhus (Fig. 13) are well-known examples of this means of entering the preperitoneal space. Laparoscopic entry to the preperitoneal space can be performed by the transabdominal preperitoneal approach, in which the peritoneal cavity is typically insufflated and then entered with the laparoscope and dissecting instruments. Following a transverse incision of the peritoneum above the level of the deep inguinal ring, it is reflected bluntly, thereby allowing entry into the preperitoneal space. The posterior preperitoneal approach has been adapted for laparoscopic hernia repair, especially for the treatment of recurrent and bilateral hernias.
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Transversalis fascia --:
Figure 13.Operative approach to preperitoneal space. It is seldom necessary to ligate and sever the inferior epigastric artery and vein. (From Nyhus LM: The preperitoneal approach and iliopubic tract repair of inguinal hernia. In Nyhus LM, Condon RE: Hernia, ed 4. Philadelphia, Lippincott, 1995, p 153; with permission.)
Infraumbilical placement of the entry site for the laparoscope is followed by expansion of the preperitoneal space by insufflation with carbon dioxide to enhance visibility. Prosthetic mesh can be placed readily and fixed. Laparoscopic hernia repair has been performed intraperitoneally with an onlay graft, in which the prosthetic material is placed within the peritoneal cavity, such as in the procedure of Toy and Smoot, who found, in some cases, the need for converting to open herniorrhaphy when large, direct, sliding hernias occurred, with the urinary bladder making up the medial wall of the hernial sac. The procedure has the additional disadvantage of leaving prosthetic material within the peritoneal cavity.
Anterior Approach
The rectus anterior sheath may be incised through a transverse lower abdominal incision. After the muscle is retracted medially, the three flat muscles are incised carefully. The incision is extended laterally and down to the aponeurosis of the transversus abdominis, which is fused with the anterior lamina of the transversalis fascia. The preperitoneal space is exposed by careful incision of the aponeurosis and anterior lamina of the transversalis fascia without opening the peritoneum. Posterior Approach
The authors mention four open and three laparoscopic pathways for approaching the space of Bogros through the peritoneum. These pathways may be used at the space of Bogros for the repair of inguinofemoral hernia with or without prosthesis.
THE PREPERITONEAL SPACE
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Open Approaches
Open approaches include: Cheatle-Henry approach-Through an infraumbilical midline incision; the peritoneum is not opened Nyhus approach-Through a transverse incision above the inguinal ligament down to the transversalis fascia; the peritoneum is not opened (Fig. 13) Anterior inguinal approach-By an oblique incision just above the inguinal ligament down to the posterior inguinal wall; the peritoneum is not opened Transabdominal approach-The peritoneum is opened Laparoscopic Approaches
Laparoscopic approaches include: Transabdominal preperitoneal-Pneumoperitoneum; formation of peritoneal flap; anatomic view of the myopectineal orifice; fixation of prosthetic material; closure of peritoneal flap Intraperitoneal only mesh-Pneumoperitoneum; intraperitoneal onlay mesh fixed on the peritoneal surface Total extraperitoneal-Preparation of preperitoneal space by finger or balloon insufflation for maintenance of surgical space; prosthetic material is fixed SUMMARY
The preperitoneal space is presented from an embryologic, anatomic, and surgical standpoint in detail. Because this space is one of the most used areas for the repair of groin hernias, knowledge of its embryology and anatomy is essential.
References 1. Annibali R Surgical anatomy of the inguinal region and lower abdominal wall from the laparoscopic perspective. In Nyhus LM, Condon RE (eds): Hernia, ed 4. Philadelphia, JB Lippincott, 1995, p 64 2. Annibali R, Quinn T, Fitzgibbons RJ Jr: Anatomy of the inguinal region from the laparoscopic perspective: Critical areas for laparoscopic hernia repair. In Hernia 93: Advances or controversies. Meeting Abstracts, Society of American Gastrointestinal Endoscopic Surgeons. Indianapolis, May 23-27, 1993 3. Basmajian JV, Slonecker CE: Grant's Method of Anatomy, ed 11. Baltimore, Williams & Wilkins, 1989, p 209 4. Bogros AJ: Essai sur L'Anatomie Chirurgicale de la Region !liacque et Description d'un Nouveau Procede pour faire la Ligature des Arteres Epigastrique et Iliaque Externe. ThGse de Medecine, Paris, 29 aout 283. Didot le Jeune, Imprimeur, Paris, 1823 5. Condon RE: Prosthetic repair of abdominal hernia. In Nyhus LM, Condon RE (eds). Hernia, ed 3. Philadelphia, JB Lippincott, 1989, p 571 6 . Davies J W Abdominal and pelvic fascias with surgical applications. Surg Gynecol Obstet 54:495, 1932 7. Ergun S, Bruns T, Soyka A, et al: Angioarchitecture of the human spermatic cord. Cell Tissue Res 288:391, 1997 '
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7a. Fruchaud H: Anatomie Chirurgical des Hemies de l'Aine. Paris, G. Doin, 1956 8. Glenister TW A correlation of the normal and abnormal development of the penile urethra and of the infraumbilical abdominal wall. Br J Urol 30:117, 1958 9. Hahn-Pedersen J, Lund L, Hojhus JH, et al: Evaluation of direct and indirect inguinal hernia by computed tomography. Br J Surg 81:569, 1994 10. Hureau J, Pradel J, Agossou-Voyeme AK, et al: Les espaces interparieto-peritoneaux posterieures ou espaces retroperitoneaux: Anatomie tomodensitometrique pathologique. J Radiol 72:205, 1991 11. Hureau J, Agossou-Voyeme AK, Germain M, et al: Les espaces interparieto-peritoneaux posterieures ou espaces retroperitoneaux: Anatomie topographique normale. J Radiol 72:101, 1991 12. Keating JE,' Morgan A: Femoral nerve palsy following laparoscopic inguinal herniorrhaphy. J Laparoendosc Surg 3:557, 1993 13. Klippel CH Jr: The embryo considered as a vector field. In El Shafie M, Klippel CH Jr (eds): Associated Congenital Anomalies. Baltimore, Williams & Wilkins, 1981, p 157 14. Korobkin M, Silverman PM, Quint LE, et al: CT of the extraperitoneal space: Normal anatomy and fluid connections. AJR Am J Roentgenol 159:933, 1992 15. Lytle WJ: Inguinal anatomy. J Anat 128:581, 1979 16. McArdle G: Is inguinal hernia a defect in human evolution and would this insight improve concepts for methods of surgical repair? Clin Anat 10:47, 1997 17. Meyers MA: Acute extraperitoneal infection. Semin Roentgenol 8445, 1973 18. Natelson SE: Surgical correction of proximal femoral nerve entrapment. Surg Neurol 48:326, 1997 19. Nobel W, Marks SC, Kubik S : The anatomical basis for femoral nerve palsy following iliacus hematoma. J Neurosurg 52:533, 1980 20. Ogilvie H: Hernia. London, Edward Arnold, 1959 21. Read RC: Surgical comments on the Bogros thesis. Postgrad Gen Surg 6:15, 1995 22. Read RC: Anatomy of abdominal herniation: The parietoperitoneal spaces. In Nyhus LM, Baker RJ, Fischer JE (eds): Mastery of Surgery, ed 3. Boston, Little, Brown, 1997, p 1795 23. Retzius AA: Some remarks on the proper design of the semilunar lines of Douglas. Edinburgh Med J 3:865, 1858 24. Skandalakis JE, Colborn GL, Skandalakis LJ: The embryology of the inguinofemoral area: An overview. Hernia 1:45, 1997 25. Skandalakis JE, Skandalakis LJ, Colbom GL: Testicular atrophy and neuropathy in herniorrhaphy. Am Surg 62:775, 1996 26. Sofikitis N, Dritsas, Miyagawa I, et al: Anatomical characteristics of the left testicular venous system in man. Arch Androl30:79, 1993 27. Spaw AT, Ennis BW, Spaw LP: Laparoscopic hernia repair: The anatomic basis. J Laparoendosc Surg 1:269, 1991 28. Stoppa RE, Warlaumont CR: The preperitoneal approach and prosthetic repair of groin hernia. In Nyhus LM, Condon RE (eds): Hernia, ed 3. Philadelphia, JB Lippincott, 1985, p 199 29. Williams PL (ed): Gray's Anatomy, ed 38. New York, Churchill Livingstone, 1995, p 1278 30. Wishahi MM: Anatomy of the venous drainage of the human testis: Testicular vein cast, microdissection and radiographic demonstration. A new anatomical concept. Eur Urol 20:154, 1991 31. Wyburn GM: The development of the infra-umbilical portion of the abdominal wall with remarks on the aetiology of ectopia vesicae. J Anat 71:201, 1937
Address reprint requests to John E. Skandalakis, MD, PhD Centers for Surgical Anatomy and Technique Emory University School of Medicine 1462 Clifton Road, NE Suite 303 Atlanta, GA 30322
0039-6109/00 $8.00
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EMBRYOLOGY, ANATOMY, AND SURGICAL APPLICATIONS OF THE PREPERITONEAL SPACE Andrew N. Kingsnorth, BSc, MS, FRCS, Panagiotis N. Skandalakis, MD, Gene L. Colborn, PhD, Thomas A. Weidman, PhD, Lee J. Skandalakis, MD, and John E. Skandalakis, MD, PhD
By definition, the preperitoneal (also called extraperitoneal or properitoneal) space lies in the abdominal cavity between the peritoneum internally and the transversalis fascia externally. Although the authors use the term preperitoneal throughout this article, in keeping with the popular choice of nomenclature, the more inclusive term, extraperitoneal, is probably preferable because it more clearly includes all of the potential space just external to the peritoneum, including the retroperitoneal area, whereas preperitoneal implies the ventral portion of the extraperitoneal space. Another name for the space is parietoperitoneal,22 which the authors believe to be a good term, although somewhat unwieldy. Within the preperitoneal space is a variable quantity of adipose tissue, loose connective tissue, and membranous tissue. Membranous tissue lies just internal to the transversalis fascia. Perhaps the classic definition of the preperitoneal space is correct, but if one accepts the bilaminar formation of the transversalis fascia into the anterior and posterior laminae, two spaces are formed: (1) one between the peritoneum (i.e., the innermost layer of the abdominal wall) and the posterior lamina of the transversalis fascia and (2) one between the two laminae of the transversalis fascia (Fig. 1).In some cases, the posterior lamina is
From the. Centers for Surgical Anatomy and Technique (PNS, GLC, LJS, JES) and Department of Surgery (LJS, JES), Emory University School of Medicine, Atlanta; Piedmont Hospital, Atlanta (JES); Center for Clinical Anatomy (GLC) and Department of Surgery (GLC, JES), The Medical College of Georgia, Augusta; and Mercer University School of Medicine, Macon, Georgia (JES); the Department of Surgery, Medical School, University of Athens, Athens, Greece (PNS); University of Plymouth, Plymouth, United Kingdom (ANK); and the Department of Anatomical Sciences, Ross University School of Medicine, Roseau, Commonwealth of Dominica, West Indies (TAW)
SURGICAL CLINICS OF NORTH AMERICA VOLUME 80 NUMBER 1 FEBRUARY 2000
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KINGSNORTH et a1 Post. Lamina T.F. Peritoneum
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Apon.
Fruchauds orifice + the 4 ing. fern herniae 3 Fossae
+
3 Herniae
w
New concept of space of Bogros
Original space of Bogros
Figure 1. Laparoscopic anatomy of inguinal area demonstrating layers, fossae, and spaces. TF = transversalis fascia; Tr Abd Apon = transversus abdominis aponeurosis; Ing fern = inguinofemoral. (From Colborn GL, Skandalakis JE: Laparoscopic cadaveric anatomy of the inguinal area. Problems in General Surgery 12:13, 1995; with permission.)
not well developed and the space is limited by the peritoneum internally and the anterior lamina of the transversalis fascia externally (previously referred to as the transversalis fascia). Both laminae of the transversalis fascia insert inferiorly on the ligament of Cooper. Superiorly, they are perhaps united somewhere at the anterior abdominal wall and then continue upward as the transversalis fascia. The extensions of the [new] and [old] spaces, laterally and posteriorly, have not yet been clearly defined because they extend into the at-large preperitoneal spaces, including the posterior retroperitoneal space and the highly complex preperitoneal spaces of the pelvis. The preperitoneal space of the abdomen is filled with a variable amount of connective tissue and other anatomic entities, such as arteries; veins; nerves; and various organs, such as the kidneys and ureters. EMBRYOLOGY
The genesis of the preperitoneal space belongs to the in toto genesis of the abdominal wall. Perhaps all of the preperitoneal space and its subdivisions or extensions between the inguinal ligament below and the respiratory diaphragm above are formed "by necessity" to permit the downward and upward transmission of anatomic structures, such as arteries, veins, lymphatics, nerves, spermatic cord, and McArdleI6 discussed the evolutionary problems of gravitational stress secondary to erect posture, such as the carriage of the intra-abdominal organs and a lack of a strong posterior rectus sheath and transversalis fascia.
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Perhaps extending or illustrating his thoughts are three developments related to the embryologic formation of the preperitoneal spaces: Inguinal canal (the space above the inguinal ligament)-The testicular pathway from the retroperitoneal space to the scrotum Spaces below the inguinal ligament-Permit the exodus of muscles, nerves, and vessels destined to provide for the lower extremity Closure of the obturator foramen and the formation of the obturator canal-Comprise a third necessary pathway An understanding of the embryogenesis of the preperitoneal space is dependent on study of the embryogenesis of the anterior abdominal wall, more specifically, the part of the abdominal wall below the umbilicus. The anterior abdominal wall is formed by the ectoderm and parietal mesoderm, which form the somatopleure. At this stage, no muscles, vessels, or nerves are present. During the sixth week of gestation, the mesoderm from myotomes lying on either side of the vertebral column invades the somatopleure. The right and left rectus abdominis muscles are formed first; then the mesodermal sheets of muscle split into three layers. By the middle of the seventh week of gestation, the three paired, flat abdominal muscles and the rectus abdominis can be recognized. Between approximately the 9th and 10th weeks of gestation, the ossification of the pelvis begins, and at 13 weeks of gestation, the hip bones are evident. In the infraumbilical region, the invasion of the somatopleure by the somatic mesoderm is preceded by a layer of mesoderm that arises from the primitive streak just behind the cloaca. This "secondary mesoderm" surrounds the margin of the cloaca and invades the abdominal wall caudal to the body stalk, separating the layers of ectoderm and endoderm of the cranial end of the cloaca1 plate.3I The second mesoderm provides primary closure of the body wall between the external genitalia and the body stalk and forms part of the musculature of the bladder8 The secondary mesoderm is in position by the 7th week of gestation; it is followed by the somatic mesoderm, which fuses with it externally by the 12th week of gestation. Approximation of the two recti proceeds from the cranial and caudal ends, so that the abdomen becomes essentially closed by the 12th week of gestation, except for the umbilical ring. At the ring, the body wall, with its developing muscles, gives way to undifferentiated somatopleure over the surface of the umbilical cord. Although true skin may grow a short distance beyond the body, the structure of the cord remains embryonic. KlippeP3 suggested a new theory about the development of the anterior abdominal wall. Considering the embryo as a vector field and using vector analysis, he reported that the development of the embryo progresses not only by lateral infolding of the embryologic entities closing at the future umbilicus but also by an outward process from a fixed midpoint, perhaps from the middle to the periphery. This concept is interesting but sufficiently revolutionary to demand further practical and theoretic investigation. According to Lytle,I5 a diaphragm formed by the inguinal and lacunar ligaments and transversalis and pectineal fasciae bears the responsibility for closing the abdominal cavity off from the thigh. The embryology of the inguinal canal is peculiar. In a highly synergistic way, the skin, parietal peritoneum, and connective tissues and the muscles between them produce the future pathway for the testes. The skin forms the scrotum (scrota1 folds) in boys and the labia (labial folds) in girls. The parietal peritoneum produces the processus vaginalis, and the muscles and their fasciae contribute to the formation of the coverings of the spermatic cord. Although
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present in both genders, the peritoneal diverticulum is more important to male fetuses because it permits the descent of the testicles. The embryologic entities between the skin and peritoneum permit the processus vaginalis to penetrate them and form the inguinal canal, so the downward journey of the testicles to the scrotum is allowed. In girls, the ovary descends into the developing pelvis, accompanying the primordia of urogenital organs. The processus vaginalis finally closes to obstruct ovarian exodus but leaves the formation of the inguinal canal in situ. OgilvieZ0correctly stated that the descent of the testicles into the scrotum makes a mess of the three-layered abdominal wall. Lateral to the pubic tubercle are two openings in the anterior abdominal wall that permit the exodus of the processus vaginalis and testicle (or the round ligament of the uterus) from the abdomen. One is just superolateral to the pubic tubercle, provided by an opening in the aponeurosis of the external oblique and its fascia (i.e., the superficial, or external, inguinal ring). The other penetrates the underlying transversus abdominis and the transversalis fascia in an oblique way (i.e., the deep, or internal, inguinal ring) approximately 4 cm further laterally in adults. The passageway between the two openings is the inguinal canal. SURGICAL ANATOMY The clinically significant parts of the preperitoneal space include the space associated with the structural elements related to the myopectineal orifice of Fruchaud, the prevesical space of Retzius, the space of Bogros, and the retroperitoneal periurinary space. Myopectineal Orifice of Fruchaud Condon5 reported that, in groin hernia repair surgery, the preperitoneal space is developed medially and superiorly for a distance on the deep aspect of the musculoaponeurotic abdominal wall. The surgical anatomy of the preperitoneal space at the inguinofemoral area may be studied by dissecting from the skin to the peritoneum and from the peritoneum to the skin. Figure 2 is the basis of orientation to study the preperitoneal spaces as understood in the classic and newer views, respectively. The authors present these as viewed in dissection, starting from the skin to the myopectineal orifice of Fruchaud and from the peritoneum to the myopectineal orifice of Fruchaud. The myopectineal orifice beneath the arching lower border of the transversus abdominis and internal oblique muscles is bounded laterally by the iliopsoas muscle, medially by the lateral edge of the rectus abdominis, and inferiorly by the pubic pecten. It is divided by the iliopubic tract and the inguinal ligament, which separate the ”inguinal outlet” (allowing for the escape of the spermatic cord elements) above from the ”femoral outlet” below (permitting the exit of the femoral artery, vein, and nerve into the thigh). In the thinking of Fruchaud, the myopectineal orifice represents the potentially weak area in the abdominal wall that permits inguinal and femoral Umbilical Ligaments and Retzius’ Space In the peritoneum below the umbilicus, especially at the inguinofemoral area, several peritoneal folds produced by underlying anatomic entities (Fig. 3)
THE PREPERITONEAL SPACE I
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11 12 17 -18
Figure 2. Innominate fascia (1). External oblique aponeurosis (2). Internal oblique muscle (3).Transversus abdominis muscle (4). Transversalis fascia anterior (5). External spermatic fascia (6).Cooper’s ligament (7). Pubic bone (8). Pectineus muscle (9).Transversalis fascia (1 0). Transversalis fascia posterior lamina (11). Vessels (1 2). Peritoneum (1 3). Bogros’ space, home (space) of prosthesis (14). Preperitoneal fat (1 5). Transversus abdominis, aponeurosis,and anterior lamina of transversalis fascia (16). Femoral artery (17).Femoral vein (18). (From Skandalakis JE, Colborn GL, Androulakis JA, et al: Embryologic and anatomic basis of inguinal herniorrhaphy. Surg Clin North Am 73:799, 1993.)
are readily observed. The obliterated (or patent in varying degrees) urachus, with its overlying peritoneum, forms the median umbilical ligament, a midline peritoneal fold from the dome of the urinary bladder to the umbilicus. The left and right obliterated umbilical arteries and peritoneum form the medial umbilical ligaments, which travel upward toward the umbilicus. The left and right deep inferior epigastric arteries and veins, with their peritoneal coverings, form the lateral umbilical ligaments. These three peritoneal folds delineate three peritoneal fossae that can be observed within the peritoneal cavity. These fossae are sometimes shallow or deep. The fossa between the median and medial umbilical ligaments is the supravesical fossa. The fossa between the medial and lateral inguinal ligaments
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E !t'
..
\
Y!, /
Figure 3. Sites of groin hernia and their relationship to bladder and ligaments of lower abdominal wall. Umbilicus (A). Urachus (B). Lateral umbilical ligament (obliterated hypogastric artery) (C). Deep epigastric artery (D). Internal inguinal ring (E). Falciform ligament (F). Lateral fossa (indirect inguinal hernia) (1). Medial fossa (direct inguinal hernia) (2). Supravesical fossa (paravesical hernia) (3). Femoral ring (femoral hernia) (4). (From Rowe JS Jr, Skandalakis JE, Gray SW: Multiple bilateral inguinal hernias. Am Surg 39:269, 1973; with permission.)
is the medial inguinal fossa, and the shallow fossa lateral to the lateral umbilical ligament is the lateral inguinal fossa. Each fossa represents the potential home of an inguinal hernia. From medial to lateral, the hernias are the external supravesical, direct, and indirect. The preperitoneal space that lies deep to the supravesical fossa and the medial inguinal fossa is the prevesical space of Retzius. Extending between the left and right inferior epigastric vessels is a variably thick mantle of preperitoneal connective tissue that incorporates the umbilical vessels and the midline urachus, referred to as the vesicournbilical fascia. It is a roughly triangular plane of tissue that extends upward to the umbilicus. Between the vesicoumbilical fascia and the posterior lamina of the rectus sheath is the space of Retzius. From the arcuate line of the posterior lamina of the rectus sheath above to the pubic bones below, the posterior lamina becomes increasingly thin, consisting of a translucent or nearly transparent lamina of aponeurotic
THE PREPERITONEAL SPACE
7
fibers of the transversus abdominis and underlying transversalis fascia. Retzius believed that the weakened area of the rectus sheath facilitated the filling of the urinary bladder, which, in fetal development, is an abdominal, not a pelvic, organ. The space is “a continuous bursa-like cleft in the areolar tissue at the sides and front of the bladder which allows the bladder to fill and empty without hindran~e.”~ In the minds of many, the space of Retzius is thought of only as the potential space between the bladder posteriorly and the pubic bones anteriorly, but as originally described, the space of Retzius extends from the muscular floor of the pelvis to the level of the umbilicus. Anteriorly, it is bounded by the bodies of the pubic bones; medial portions of the pubic rami; and posterior lamina of the rectus sheath, at least to the level of the arcuate lines of Douglas. In the pelvis, the space of Retzius is bounded posteriorly by the prevesical fascia and the lateral pillars of the urinary bladder and the covering of pelvic peritoneum. More superiorly, the vesicoumbilical fascia and peritoneum provide a posterior wall for the space. The ductus deferens and the round ligament of the uterus traverse the umbilicovesical fascia en route to the deep inguinal ring. The space of Retzius is closed laterally along the line of fusion provided by the inferior epigastric vessels and the tissue that encloses them (whether that be the posterior lamina of transversalis fascia, extraperitoneal connective tissue, or a fascia1 fusion between transversalis and extraperitoneal membranous fascia). This lateral limit to the space is well illustrated on CT scans of the pelvis in cases in which the prevesical space is distended with fluid (Fig. 4). The space of Retzius contains loose connective tissue and fat. More importantly, vascular elements present there can be of importance in trauma and surgical procedures, especially urologic, urogynecologic, and orthopedic procedures. The aberrant obturator artery and vein can be of major significance in perioperative and postoperative bleeding. In the event that a patient has a normal obturator artery arising from the internal iliac and an aberrant obturator arising from the inferior epigastric or external iliac, with anastomoses between the two obturator vessels, bleeding of such volume can occur that the anatomic vascular pattern has been referred to as the ”circle of death.” Aberrant obturator arteries occur in 25% to 40% of individuals in the United States, but the prevalence in other countries has been reported to be as high as 80%. When present, they typically cross medial to, lateral to, or directly across the femoral ring and then the pectineal ligament of Cooper en route to the obturator canal in the pelvis. They can be readily injured in orthopedic, urologic, urogynecologic, or general surgical procedures that involve the pectineal ligament. To make matters worse, and the possibility of vascular injury even more possible for unwary physicians, such vessels are commonly well hidden by overlying lymphatic tissue confluent with that of the femoral canal. Aberrant obturator veins occur far more commonly than do aberrant obturator arteries. When torn under laparoscopic conditions, bleeding can be scant or absent until the pressure of insufflation stops, with potentially severe postoperative bleeding occurring thereafter. Vessels that can be found in the retropubic space also include atypical arteries and veins for the urinary bladder arising from aberrant obturator, inferior epigastric, or external iliac sources. Retropubic branches of obturator and aberrant obturator sources are common. In approximately 10% of cases, accessory pudendal vessels may pass through the prevesical space, traveling from internal iliac sources and under the pubic bones to reach the dorsum of the penis or clitoris. Laterally in the space are the obturator nerve, obturator artery, and vein in the terminal parts of their course to reach and enter the obturator canal.
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Urnbilicovesicel fasda
Preveslcal space Perivesical space
A Prevesical space fluid
B Figure 4. Fluid in the prevesical Retzius' space. A, Sagittal cross-section of lower abdomen and pelvis. Umbilicovesical fascia, prevesical space, and the expanded prevesical space. B, Axial cross-section. Large collection of fluid distends prevesical space with a characteristic form like a molar tooth. R = rectum; U = uterus; B = bladder; C = cecum; S = sigmoid. Peritoneum (Dotted line). (From Korobkin M, Silverman PM, Quint LE, et al: CT of the extraperitoneal space: Normal anatomy and fluid connections. AJR 159:940, 1992; with permission.)
Read2' stated: The presence of this space allows for the properitoneal placement of large prostheses with minimal fixation as pioneered by Stoppa et a1J8 . . . It also makes laparoscopic herniorrhaphy possible since there are no major structures which pass through it. However, there are important nerves and blood vessels in the wall which have to be protected during cleavage. This space allows for prosthetic plugs to be placed with minimal dissection from the classical groin incision, there being room enough for them to expand and protect the femoral and inguinal orifices, obviating recurrent herniation.
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Bogros' Space
Although any anatomic description of the posterior preperitoneal space, as well as the lateral pathways and extensions of this space, is open to question, some boundaries are presented from a surgicoanatomic standpoint. In his thesis presented in Paris in 1823, Bogros4 described a triangular space between the abdominal wall and the peritoneum that could be entered by means of an incision through the roof and floor of the inguinal canal. In this way, aneurysms of the iliac or inferior epigastric vessels could be secured and treated without the considerable surgical risk of entering the peritoneal cavity. Nyhus entered this space in similar, but unidentical, fashion in his exemplary series of studies on the posterior preperitoneal approach for hernia repair (see the excellent but succinct discussion by Read).22 Although Bogros described the space at the termination of the external iliac artery as being only approximately 13 mm to 15 mm wide and 4 mm to 6 mm deep, modern interpretation seems to be extending this space upward into the retroperitoneal area, and some workers state that it is continuous medially with the space of Retzi~s,*~ but the authors believe that communication between the two spaces is an artifact of dissection or a result of disease processes; they are normally separated from one another by the plane of fusion between extraperitoneal connective tissue and transversalis fascia that occurs along the path of the inferior epigastric vessels. This conclusion is supported by clinical studies, such as those by Korobkin et al.14 Retroperitoneal Space
The " o l d preperitoneal or extraperitoneal space (i.e., the space between the peritoneum and anterior lamina of transversalis fascia) is a pathway for vessels and nerves to and from the lower extremity. It is partially the home of several anatomic entities. It includes the perirenal and pararenal spaces (Fig. 5). Stoppa (personal communication, 1992) wisely stated that the cleavable interparietoperitoneal space of Bogros is considered to be the lower prolongation of the great posterior paraurinary space. After radiologic and anatomic studies of this area, Hureau et al'Ql1 considered the composition of the posterior paraurinary area to be the following: anteriorly, Gerota's fat contained within the fascia; and posteriorly, a cellular space that most likely incorporates the space of Bogros in the internal iliac fossa. When Stoppa (personal communication, 1992) and Hureau et all0,l1 talk about the paraurinary space and area, they are probably referring to the same area as the pararenal space of US literature. To best understand the posterior pararenal space, the anatomy of the retroperitoneal area must be considered. The posterior parietal peritoneum and the transversalis fascia provide the anterior and posterior boundaries of the retroperitoneal space, respectively. This space extends from the pelvic brim inferiorly to the diaphragm superiorly. Among the major structures it encompasses are the adrenal glands, kidneys, ureters, pancreas, inferior vena cava, aorta, portal vein, ascending and descending colon, and parts of the duodenum. In a horizontal cross-section, it is somewhat C-shaped because of the curvature of the lumbar spine. As a result, some retroperitoneal structures (i.e., the pancreas and duodenal loop) lie anterior to others (i.e., the spleen, kidneys, and posterior aspect of the liver). These relationships are illustrated in Figure 6 and in the excellent work of Hureau et a1.I0,l1 Meyers17 divided the extraperitoneal region into three compartments ac-
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Figure 5. Normal anatomy of inguinal region viewed from internal (preperitoneal) aspect.
(FromCondon RE: Prosthetic repair of abdominal hernia. In Nyhus LM, Condon RE (eds): Hernia, ed 3. Philadelphia, Lippincott, 1989, p 559; with permission.)
cording to their demarcation by well-defined fascial planes. The anterior and posterior layers of Gerota’s fascia are central to the division of the extraperitoneal region. The kidney and the perirenal fat are enveloped by this dense sheath. The fusion of its two layers behind the ascending or descending colon forms a single lateroconal fascia. This continues around the flank to blend with the peritoneal reflection and form the paracolic gutter. Meyers named these three compartments (Figs. 7-9) the (1)anterior pararenal space, which extends from the posterior parietal peritoneum to the anterior renal fascia and is confined laterally by the lateroconal fascia; (2) perirenal space, in which the kidney and perirenal fat reside within the confines of Gerota’s fascia; and (3) posterior pararenal space, whch extends from the posterior renal fascia to the transversalis fascia. A thin layer of fat lateral to the lateroconal fascia, also known as the preperitoneal fat, is present in varying amounts. The extraperitoneal portions of the alimentary tract, ascending and descending colon, duodenal loop, and pancreas are included within the anterior pararenal space. This space is continuous across the midline. Some investigators believe that the perirenal spaces have no continuity across the midline because of the fusion of the posterior fascial layers with the psoas or quadratus lumborum fascia medially, and to the fusion of the renal fascia with the dense mass of connective tissue surrounding the great vessels in the root of the mesentery and behind the pancreas and duodenum anteriorly. Others have reported continuity of the spaces at the level of the lower poles of the kidneys, especially in some patients with extravasation of blood or other fluids from one side to the other. In cadaveric dissections by the authors, they have observed many cases in which spatial continuity could be easily demonstrated without artifactual separation of tissues. Text continued on page 15
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B Figure 6. Major retroperitoneal compartments. A, Axial cross-section at level of kidneys. 6,Sagittal cross-section in plane of right kidney. Anterior pararenal space (Hatched). Cross-hatchedareas = perirenal space; Stippled areas = posterior pararenal space; L = liver; P = pancreas; LS = lesser sac; S = spleen; V = vena cava; A = aorta; K = kidney; RK = right kidney; LK= left kidney; C =colon; D =duodenum. (From Korobkin M, Silverman PM, Quint LE, et al: CT of the extraperitoneal space: Normal anatomy and fluid connections. AJR 159:934, 1992; with permission.)
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Figure 7. Sagittal section through abdomen. Striped area = anterior pararenal space; Stippled area = perirenal space; Cross-hatched area = posterior pararenal space. (From Meyers MA: Dynamic Radiology of the Abdomen, ed 4. New York, Springer-Verlag, 1994, p 223; with permission.)
THE PREFERITONEAL SPACE
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Figure 8. Three extraperitoneal spaces. Anterior pararenal space (1). Perirenal space (2). Posterior pararenal space (3). C = colon; K = kidney; PM = psoas muscle; QL= quadratus lumborum muscle. (From Meyers MA: Dynamic Radiology of the Abdomen, ed 4. New York, Springer-Verlag, 1994, p 222; with permission.)
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B
/
Figure 9. Relations and structures of the three extraperitoneal spaces. A, Horizontal cross-section. B, Left parasagittal view. Striped area = Anterior pararenal space; Stippled area = perirenal space; Cross-hatched area = posterior pararenal space; C = colon; K = kidney; L = liver; P = pancreas. (from Meyers MA: Acute extraperitoneal infection. Semin Roentgenol 8:445,1973; with permission.)
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Questions remain. On its downward journey, does the fascia of Gerota form an open pathway or a closed space? The authors believe that it is open anatomically and radiologically. In the 1950s, an injection of air into the presacral space, which travelled upward into the perirenal space, was used to study the renal silhouette. Another question, perhaps of considerable significance to some investigators, is, What is the origin of the perirenal fascia? Determining the answer to this question is likely an important key to the question concerning the possible bilaminar nature of the transversalis fascia. If the perirenal fascia is a specialized, normal regional condensation of extraperitoneal connective tissue, is it not reasonable to think that such a condensation is present also in the inguinal region (there, called the posterior lamina of transversalis fascia), enclosing the inferior epigastric vessels, reinforcing the iliopubic tract, and continuing medially in the form of vesicoumbilical fascia? Is the perirenal fascia derived from the transversalis fascia? The authors have seen no significant evidence to support this conclusion. Davies6suggested that the inner linings of the peritoneal cavity are comparable with the outer coverings of the abdominal wall but reversed in orientation, so the skin (i.e., peritoneum) lies on an adipose layer of Camper (i.e., extraperitoneal fat), which is succeeded by the membranous layer of the fascia of Scarpa (i.e., the membranous layer of extraperitoneal fascia), and this by the muscle fascia of Gallaudet (i.e., transversalis fascia), beneath which is external oblique musculature (i.e., transversus abdominis). This is probably a terrible oversimplification of a highly complex structure, but the authors still find it interesting.
CONTENTS OF THE PREPERITONEAL SPACE OF THE INGUINOFEMORAL REGION
The contents of the preperitoneal space can be characterized as vascular (i.e., arteries, veins, lymphatics), nerves, and adipose tissue (thick or thin). These include: Vascular Arteries External iliac artery with its branches Deep circumflex iliac artery Inferior epigastric artery with its branches Suprapubic and retropubic arteries, accessory obturator artery Cremasteric artery Veins External iliac vein Inferior epigastric veins Suprapubic and retropubic tributaries Rectusial tributaries from rectus abdominis Accessory obturator veins Deep circumflex iliac vein The Bendavid circle Nerves Ilioinguinal Iliohypogastric Spermatic plexus (sympathetic and sensory)
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L1, L2, L3 ventral rami Genitofemoral Genital branch Femoral branch Femoral Lateral femoral cutaneous Vessels of the Preperitoneal Space
The external iliac artery and vein are located at the medial area of the psoas muscle. They snake above the fascia of the muscle and travel under the iliopubic tract and inguinal ligament. Here they change names and become femoral vessels. In most cases, the inferior epigastric vessels are branches from the external iliac artery and vein. From their origins, they initially descend for a short distance, then, curving upward, they travel superomedially in the direction of the umbilicus and are located between the posterior lamina of the transversalis fascia and the peritoneum. During their upward journey, they pierce the posterior lamina of the transversalis fascia and enter the posterior area of the rectus sheath. In the inguinal area, the inferior epigastric artery typically provides origin for the cremasteric artery and the pubic branch. The pathway of each branch is different from the other. The cremasteric artery may be found at the medial area of the deep inguinal ring. It proceeds to be an element associated with the spermatic cord. In female patients, the cremasteric artery provides origin for the artery of the round ligament, one of the sources of origin of Sampson’s artery. The pubic or accessory obturator artery anastomoses with the obturator artery. The obturator artery springs from the inferior epigastric artery or directly from the external iliac artery. Other vessels that take origin from the external iliac artery are the deep circumflex artery and vein. These vessels pass slightly distally from origin and then laterally, deep to the iliopubic tract, and are “sandwiched“ between the internal oblique and transversus abdominis. Near the anterior superior iliac spine, they give origin to a large, ascending branch that is significant in vascular supply to the anterior abdominal wall. Staples placed laterally here during laparoscopic herniorrhaphy may result in significant hematoma. The deep circumflex iliac vessels anastomose with the iliolumbar vessels. In male patients, 10 to 12 veins that segregate into anterior and posterior groups form the pampiniform plexus. The two groups are drained by three or four veins joined to form two veins proximal to the internal inguinal ring. The two veins pass on either side of the testicular artery through the extraperitoneal space. The right testicular vein opens into the inferior vena cava. The left testicular vein enters the left renal vein. The cremasteric vein flows to the inferior epigastric veins. The deferential vein drains into the pampiniform plexus and the vesical plexus. The vesical plexus is drained by the prostatic venous plexus to the internal iliac vein. Ergun et a17further classified the veins of the pampiniform plexus as follows. Group I-Tight plexus of venovenous anastomoses around the testicular artery Group 11-Similar construct to group I, but found in fatty tissue Group 111-Similar formation, located between groups I and I1 Group IV-Arteriovenous anastomoses with the testicular artery
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Wishahi30 reported the following. [Tlhe venous drainage of the testis cannot be looked upon as it is in the standard anatomy; on the contrary, it deviates from the description in the text. We demonstrated that the venous drainage of the testis is via the pampiniform plexus, which is primarily drained by the testicular and external pudendal veins. The testicular vein-midway between the internal inguinal ring and the lower pole of the kidney-divides into the medial and lateral branch to form a delta. The medial branch communicates with the ureteral and contralateral veins; there, it terminates in the left renal vein or inferior vena cava on the right side. The lateral branch communicates with colonic and renal capsular veins and terminates in the perinephric space. There is no cross-communication between the left and right testicular venous system in the scrotal, retropubic or pelvic areas. The only cross-communication is in the abdomen, and is seen in only 50% of men. The testicular vein has no valves. Sofikitis et alZ6advised that the possible existence of more than one left testicular vein, especially at the lumbar level, was a reason for attentive identification of all testicular veins during varicocelectomy. The authors question the validity of the assertion of Hahn-Pedersen et a19 that the distention of veins of the pampiniform plexus may prevent the formation of inguinal hernia. Although their suggestion has some merit, much research remains to be done before this idea is accepted. The venous circle of Bendavid is located at the subinguinal space of Bogros. It is a network composed of the deep inferior epigastric, iliopubic, rectusial, suprapubic, and retropubic veins (Figs. 10 and 11). These veins may produce hematomas because they collapse during laparoscopic surgery and during the placement of prosthetic material. In dissections performed by the authors, they have seen suprapubic veins as large as 1 cm in external diameter passing along the superior pubic ramus to the external iliac vein. Such vessels may receive tributaries from the bladder and also the aberrant obturator vein. Aberrant obturator veins occur in at least 70% of individuals. In many cases, an aggregation of lymph nodes and lymphatic vessels crosses the pectineal ligament of Cooper from the femoral canal to the obturator canal, providing communication between the node of Cloquet (Rosenmuller) and pelvic lymph nodes. This lymphatic tissue often obscures aberrant obturator vessels crossing the pectineal ligament, causing them to be more vulnerable to injury from dissectors, refractors, and staplers. Nerves of the Preperitoneal Space
Within the preperitoneal inguinofemoral region are several nerves that may be subject to injury in laparoscopic herniorrhaphy, including the genitofemoral, ilioinguinal, lateral femoral cutaneous, and femoral nerves. The genitofemoral nerve typically divides into a femoral (lumboinguinal) branch and a genital (external spermatic) branch. The genital branch was commonly combined with the ilioinguinal nerve (7.7% of cases) in a study in the authors’ l a b o r a t ~ r y .In ~ ~most cases, the genital branch of the genitofemoral nerve descends on the external iliac artery after leaving the ventral surface of the psoas muscle. Just proximal to the origin of the inferior epigastric artery, the
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lateral margin of rectus abdominis /
i
\/ rectusio-epigastric communicating v. rectusial v.
Figure 10. Deep inguinal vasculature in Bogros’ space. int = internal. (From Bendavid R: The space of Bogros and the deep inguinal venous circulation. Surgery, Gynecology, and Obstetrics 174:356, 1992; with permission.)
genital branch ascends to the inferomedial angle of the deep inguinal ring to enter the canal. Then it accompanies the cremasteric branches of the inferior epigastric vessels. Lying deep to the cremaster, it supplies that muscle and some of the skin of the scrotum. Within the deep inguinal ring, the genital branch is deep medially, with the cremasteric vessels, that is, medial in such a way that the suturing of the crura of the internal ring is above and superficial to the position of the nerve. Entrapment of the genital branch of the genitofemoral nerve at the deep ring should occur rarely-perhaps just in those unusual cases in which the genital branch and the ilioinguinal nerves are combined and located more superficially. Leaving the deep inguinal ring, the genital branch is located at the lower margin of the iliopubic tract, together with the cremasteric vessels. Entrapment and injury of the nerve can occur only with deep suturing of the iliopubic tract (Fig. 12). The femoral branch of the genitofemoral continues inferiorly into the anterior lamina of the femoral sheath. It supplies sensory fibers to the skin in the vicinity of the femoral triangle of Scarpa. The femoral nerve emerges from the protection of the psoas muscle approximately 6 cm above the inguinal ligament, entering the preperitoneal space. It then passes deep to the iliopubic tract and inguinal ligament to enter the thigh. Staples pressed deeply, just lateral to the deep inguinal ring, may injure the femoral nerve. At the lateral border of the psoas, an early rising anterior femoral
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Figure 11. A-D, Variations in the vasculature of the deep inguinal venous system. (From Bendavid R: The space of Bogros and the deep inguinal venous circulation. Surgery, Gynecology, and Obstetrics 174:356,1992; with permission.)
cutaneous branch of the femoral nerve can also be inadvertently encountered and injured. The authors have observed that the femoral branch of the genitofemoral may communicate with, or be replaced by, an intermediate femoral cutaneous nerve arising from the femoral nerve in the iliac fossa. As the femoral nerve courses through the preperitoneal space, it is subject to compression or injury from diverse sources, including iliacus hematoma,I9 iliopectineal ligament compression,'8 and laparoscopic inguinal herniorrhaphy.'2 Compression of the femoral nerve or more traumatic insult with staples or sutures results in debilitating pain and weakness or paralysis of the quadriceps extensor musculature of the thigh. According to most anatomy texts (e.g., Gray's Anatomyz9),the ilioinguinal nerve passes within the abdominal wall, above the iliac crest, deep to the internal oblique to a point just medial to the anterosuperior iliac spine, at which point it becomes visible between the external and internal obliques and then passes into the inguinal canal. In the authors' inve~tigation:~the ilioinguinal nerve crossed the iliac fossa in 25.5% of cases. There, it was often combined in whole or in part with the lateral femoral cutaneous nerve. The lateral femoral cutaneous nerve usually exits the preperitoneal space within 1 cm from the anterosuperior iliac spine, there passing under or through the lateral extremity of the inguinal ligament. It may lie as many as 4 cm medial to the anterosuperior spine. The ilioinguinal nerve or the lateral femoral
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'
iliac spine
Deep inguinal ring
Inferior epigastric a. Genital branch ol genttofemoral nerve
Shelving edge of inguinal ligament and iliopubic tract
A
Posterior inguinal wall (vansversalis fascia and transversus abdominis aponeurosk)
At& of internal oblique muscle
\
Transversalis lascia
.,:
Aponeurosis of external oblioue
The surgical beginnin of iliopubic tract (prox
B /
Inguinal ligamenl with shelving edge elevated and relraded
Cremasler vessels and genital btanch ofgenitolemoral nerve
Figure 12. Genital branch of the genitofemoral nerve. A, Pathway of genital branch of genitofemoral nerve from deep inguinal ring to medial side of spermatic cord. FA=femoral artery; FV=femoral vein. 6,lliopubic tract and its relations to genital branch of genitofemoral nerve. (From Colborn GL, Skandalakis JE: Importance of the iliopubic, Cooper's, and Gimbernat's ligaments. Problems in General Surgery 12:37, 1995; with permission.)
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cutaneous nerve can be penetrated by staples or sutures that pierce the iliopubic tract lateral to the deep inguinal ring. In the preperitoneal region, one should carefully avoid the contents of the "triangle of and the "triangle of pain."', The triangle of doom is bounded medially by the ductus deferens and laterally by the gonadal vessels and contains principally the external iliac artery and vein. The triangle of pain is bordered by the gonadal vessels medially and the iliopubic tract laterally. It regularly contains, from lateral to medial, the lateral femoral cutaneous nerve, femoral branch of the genitofemoral nerve, and the femoral nerve. In many cases, it contains the atypical ilioinguinal nerve; the early rising anterior femoral cutaneous nerve; and, often, small nerves, the identity and function of which are unclear. Preperitoneal Landmarks
Within the preperitoneal space, some landmarks can usually be found with little effort, visually or by palpation. Typically, one can quickly find the inferior epigastric vessels, medial umbilical ligament, gonadal vessels, and ductus deferens, although each one of these may be somewhat hidden, in varying degree, by adipose tissue and adhesions. Medially, the somewhat flattened pectineal ligament can be palpated with a dissection instrument and then clarified with a little dissection. Likewise, the pubic tubercle can be palpated externally with the fingers and internally with instruments. Laterally, the iliopubic tract provides a bright band extending from the anterosuperior iliac spine laterally to the medial border of the femoral ring medially. The iliopubic band is composed mostly of aponeurotic fibers of origin of the transversus abdominis. It receives contributions from the transversalis fascia and membranous preperitoneal connective tissue and often a stout contribution from the psoas fascia. APPROACHES TO THE PREPERITONEAL SPACE
The preperitoneal space can be entered by open or closed (laparoscopic) approaches. The open approach includes various modifications of the classic open operation for herniorrhaphy, except that all layers of the anterior abdominal wall are divided to allow for access to the preperitoneal space. After the transversalis fascia is divided, the peritoneum is displaced to allow entrance into, and expansion of, the preperitoneal space, followed by herniorrhaphy or placement of prosthetic mesh to cover any or all of the points of egress of hernias through the myopectineal orifice of Fruchaud. The midline infraumbilical procedures, such as the Cheatle-Henry and Stoppa procedures, and the suprainguinal approach of Nyhus (Fig. 13) are well-known examples of this means of entering the preperitoneal space. Laparoscopic entry to the preperitoneal space can be performed by the transabdominal preperitoneal approach, in which the peritoneal cavity is typically insufflated and then entered with the laparoscope and dissecting instruments. Following a transverse incision of the peritoneum above the level of the deep inguinal ring, it is reflected bluntly, thereby allowing entry into the preperitoneal space. The posterior preperitoneal approach has been adapted for laparoscopic hernia repair, especially for the treatment of recurrent and bilateral hernias.
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Transversalis fascia --:
Figure 13.Operative approach to preperitoneal space. It is seldom necessary to ligate and sever the inferior epigastric artery and vein. (From Nyhus LM: The preperitoneal approach and iliopubic tract repair of inguinal hernia. In Nyhus LM, Condon RE: Hernia, ed 4. Philadelphia, Lippincott, 1995, p 153; with permission.)
Infraumbilical placement of the entry site for the laparoscope is followed by expansion of the preperitoneal space by insufflation with carbon dioxide to enhance visibility. Prosthetic mesh can be placed readily and fixed. Laparoscopic hernia repair has been performed intraperitoneally with an onlay graft, in which the prosthetic material is placed within the peritoneal cavity, such as in the procedure of Toy and Smoot, who found, in some cases, the need for converting to open herniorrhaphy when large, direct, sliding hernias occurred, with the urinary bladder making up the medial wall of the hernial sac. The procedure has the additional disadvantage of leaving prosthetic material within the peritoneal cavity.
Anterior Approach
The rectus anterior sheath may be incised through a transverse lower abdominal incision. After the muscle is retracted medially, the three flat muscles are incised carefully. The incision is extended laterally and down to the aponeurosis of the transversus abdominis, which is fused with the anterior lamina of the transversalis fascia. The preperitoneal space is exposed by careful incision of the aponeurosis and anterior lamina of the transversalis fascia without opening the peritoneum. Posterior Approach
The authors mention four open and three laparoscopic pathways for approaching the space of Bogros through the peritoneum. These pathways may be used at the space of Bogros for the repair of inguinofemoral hernia with or without prosthesis.
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Open Approaches
Open approaches include: Cheatle-Henry approach-Through an infraumbilical midline incision; the peritoneum is not opened Nyhus approach-Through a transverse incision above the inguinal ligament down to the transversalis fascia; the peritoneum is not opened (Fig. 13) Anterior inguinal approach-By an oblique incision just above the inguinal ligament down to the posterior inguinal wall; the peritoneum is not opened Transabdominal approach-The peritoneum is opened Laparoscopic Approaches
Laparoscopic approaches include: Transabdominal preperitoneal-Pneumoperitoneum; formation of peritoneal flap; anatomic view of the myopectineal orifice; fixation of prosthetic material; closure of peritoneal flap Intraperitoneal only mesh-Pneumoperitoneum; intraperitoneal onlay mesh fixed on the peritoneal surface Total extraperitoneal-Preparation of preperitoneal space by finger or balloon insufflation for maintenance of surgical space; prosthetic material is fixed SUMMARY
The preperitoneal space is presented from an embryologic, anatomic, and surgical standpoint in detail. Because this space is one of the most used areas for the repair of groin hernias, knowledge of its embryology and anatomy is essential.
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