Is the testis intraperitoneal?

Pediatr Surg Int (2005) 21: 231–239 DOI 10.1007/s00383-005-1364-2 R EV IE W A RT I C L E Su B. T. Pham Æ Matthew K.-H. Hong Julie A. Teague Æ John M. Hutson Is the testis intraperitoneal? Accepted: 12 October 2004 / Published online: 9 March 2005 Ó Springer-Verlag 2005 Abstract The relationship of the testis to the peritoneal cavity, and hence its position as an intraperitoneal or extraperitoneal organ, remains controversial. Adult anatomy texts favour an extraperitoneal position during and after testicular descent, whereas journal articles favour an intraperitoneal position. Interestingly, there is no similar debate around the position of the ovary despite the common origin of each as indifferent gonads. Through direct observation and the literature review, we aimed to determine whether the testis should be considered an intraperitoneal or an extraperitoneal organ. The anatomical and embryological literature relevant to human and animal models was reviewed. Direct dissections were made in rats (n=8) during foetal development, postnatally, and in mature animals, allowing comparison of foetus with adult and male with female. The position of the human testis was also recorded in various pathological states. Direct dissection in rats reveals an intraperitoneal testis on a mesorchium during both foetal and postnatal life. Intraperitoneal testes are demonstrated in humans in cases of gastroschisis (where the testis may protrude through the periumbilical defect with the bowel), testicular torsion (where the testis is mobile within the peritoneum), and bell clapper testis (where the testes are identifiable as intraperitoneal). We conclude that the foetal testis is an intraperitoneal organ. In the adult rat the testis remains intraperitoneal. The postnatal human testis is intraperitoneal. The adult human testis is intraperitoneal but may appear extraperitoneal. The apparent discrepancy between the adult S. B. T. Pham Æ M. K.-H. Hong Æ J. A. Teague Æ J. M. Hutson (&) F. Douglas Stephens Surgical Research Laboratory, Murdoch Children’s Research Institute, Department of Paediatrics, University of Melbourne, Melbourne, Australia J. M. Hutson General Surgery, Royal Children’s Hospital, Parkville, Australia E-mail: [email protected] Tel.: +61-3-93455805 Fax: +61-3-93457997 testis being intraperitoneal or extraperitoneal is likely to result from differences in the relative size of the tunica vaginalis between infant boys and elderly men. Keywords Testis Æ Peritoneum Æ Anatomy Æ Intraperitoneal Æ Extraperitoneal Introduction We hoped to correctly identify the position of the testis in relation to the peritoneum. Hence, is the testis intraperitoneal or extraperitoneal? Literature review both assists in determining the position of the testis and explaining in part why a discrepancy exists. Direct dissection in rats and observation in humans were used to clarify and conclude our aim to determine the location of the testes related to the peritoneum. There is a consensus as to the definition of extraperitoneal or retroperitoneal: being external or posterior to the parietal peritoneum and partially covered by it. However, the exact definition of intraperitoneal is not so clear. Two authors may agree on the nature of the testis being intraperitoneal, but their meanings may not be concordant. Authors of the same or distant disciplines may not agree on the definition of the term, and thus the adjective ‘‘intraperitoneal’’ must be clarified in order to appropriately define the position of the testis. Despite many publications on the mechanisms of testicular descent, testicular maldescent, and inguinal hernias, controversy still surrounds the exact nature of the gonadal position—that is, whether the testis is an intraperitoneal or extraperitoneal organ during its embryonic descent. A survey of the literature demonstrates a variety of opinions. The term ‘‘intraperitoneal’’ is often used to describe organs that are completely covered by visceral peritoneum, except for the sites of attachment of their associated mesenteries [1, 2]. However, Last [3] and Hart [4] use the term to denote the property of being within the 232 peritoneal cavity itself, the peritoneal cavity being the potential space enclosed by the parietal and visceral peritoneum. ‘‘Intraperitoneal’’ in the former sense would be described as a practical definition, such as may be used by surgeons to imply the appearance of being within the peritoneal cavity, whereas the latter is a literal definition. Hall-Craggs [1] agrees with our assessment that the adjective ‘‘intraperitoneal’’ is misleading, as no part of the small bowel, which is considered ‘‘intraperitoneal,’’ is inside the peritoneal cavity and therefore should be extraperitoneal. Moore and Dalley [2] take this literal definition further and contend that the peritoneal cavity contains no organs. According to Hart [4], the testis is not actually covered by peritoneum, which stops at the beginning of the tunica albuginea, but by a layer of germ epithelium, like the ovary, and therefore is defined as being within the peritoneal cavity. In either case, an intraperitoneal testis, apparent or literal, would still be readily discernible from a retroperitoneal one. Many authors favour the theory that the testis develops as a retroperitoneal organ and either descends behind the processus vaginalis to the scrotum (and eventually invaginates the remnant processus, which has atrophied superiorly to become the tunica vaginalis of the testis) [1, 2, 5–9] or descends and drags the processus with it [10, 11]. The evidence suggests that this is not so, for we would then have to ask how the ovaries were to mature within the peritoneal cavity if their male counterparts had indeed started life outside the peritoneal cavity. If the testis were retroperitoneal, it would be firmly attached to the continuous extraperitoneal connective tissue that lies between the parietal peritoneum and the walls of the abdominal and pelvic cavities [3]. Stewart et al. [12] and Johansen [13] observe that the testes are freely mobile within the peritoneal cavity of the processus vaginalis. Lemeh [14] suggests the testis Table 1 Textbook and journal references regarding position of testis begins retroperitoneally but later becomes intraperitoneal and possesses a mesorchium because of its growth and the degeneration of the mesonephros. This study aimed to determine whether the testis should be regarded as intraperitoneal or extraperitoneal. The reasons for this apparent discrepancy are also addressed. Materials and methods A general literature review was completed utilising several computer databases, including Medline. Various journal articles and relevant chapters in current textbooks in the disciplines of anatomy, embryology, and surgery were collated. Excerpts were taken and tabulated according to the nature of their respective authors’ opinions of the site and descent of the testis. Dissections were performed on male and female rats (n=8) at various ages: gestational day 17, postnatal day 30, and adulthood. The location of the testis at that time and, in adult male rats, the ability to move the testis via traction were tested and recorded. Histological examination was performed on a male rat embryo at 15 days of gestation. Photographic evidence was collected to show the position of the testis in the human embryo and neonate. Results At approximately 7–8 months’ gestation, the testis descends from the abdominopelvic cavity to the scrotum. A review of the literature demonstrated various beliefs of the position of the testis during its descent from the abdominopelvic cavity to the scrotum (Table 1). A predominance of opinions favouring the testis being Extraperitoneal Intraperitoneal Anatomy (texts) Hall-Craggs [1], April [6], Moore and Dalley [2], Seeley [51], Snell [7] Embryology (texts) Larsen [17], Moore and Persaud [37, 38], Carlson [5], O’Rahilly and Muller [18] Surgery (texts) Rescorla [9], Lobe [52], Johnstone [8], Schwartz [11], Donnellan [53], Rowe et al. [10], Filston [54], O’Neill et al. [55], Ashcroft et al. [56] Journals Lewis [57], Whitehorn [22], Scorer [23, 58] Anatomy (texts) Last [3], Williams et al. [16] Embryology (texts) McLachlan [19] Surgery (texts) Beasley, Hutson, Auldist [20], Hutson [21] Journals Backhouse [46], Gier and Marion [29], Hadziselimovic and Herzog [27], Hadziselimovic and Kruslin [45], Hart [4], Heyns and Hutson [47], Hutson [31], Johansen [13], Lemeh [14], Lockwood [59], Martin [49], Martin et al. [50], Stewart et al. [12], Wensing [25, 60], Williams and Hutson [30], Zaw Tun [28] 233 extraperitoneal was found in textbooks in the disciplines of anatomy, embryology and surgery. On the other hand, journal articles were dominated by fervent arguments favouring an intraperitoneally descending testis, and few articles discuss the testis as extraperitoneal. Anatomy texts Snell [7] and other anatomists believe the testis develops retroperitoneally from the urogenital ridge and descends posterior to the peritoneum and processus vaginalis, following the gubernaculum. Moore and Dalley [2] assert that the testis does not pass through the processus vaginalis. Moore and Dalley [2] and Hall-Craggs [1] define the adjective ‘‘intraperitoneal’’ as meaning almost completely surrounded by visceral peritoneum, and both agree that the (human) testis is only partly covered by peritoneum. Contrary to an extraperitoneal mechanism of testicular descent, Woodburne and Burkel [15] hold the view that the testis develops in the extraperitoneal connective tissue but maintain the opinion, first suggested by Lemeh [14], that the testis does not descend retroperitoneally. Instead, the testis becomes intraperitoneal with a mesorchium at about 7 weeks of development because of its growing bulk and close association with the mesonephros. However, Last [3] contests this intermediate position and states that in the foetus, the testis develops in the peritoneum of the posterior abdominal wall and projects through the peritoneum into the coelomic cavity during its descent. The anterior surface of the testis is not covered by peritoneum but by germinal epithelium, Fig. 1 Schematic diagrams illustrating descent of the testis in man. The testis is presented as a retroperitoneal organ that descends posterior to the processus vaginalis. (Langman [61], by permission) which may be continuous with it, and the ‘‘tunica vaginalis has, strictly, only a parietal and no visceral layer’’ [3]. Last’s [3] use of the term ‘‘intraperitoneal’’ implies the nature of an organ being within the peritoneal cavity, or coelom, itself. Gray’s Anatomy [16] is not definite as to its position on the subject but states that the testis is necessarily accompanied by its peritoneal covering and is drawn into the processus vaginalis. Embryology texts Many embryologists also describe the testis as extraperitoneal (Fig. 1). Larsen [17] states that the testes ‘‘remain within the plane of the subserous fascia associated with the posterior wall of the processus vaginalis’’ through which they descend towards the scrotum. In contrast, O’Rahilly and Müller [18] suggest that the testis ‘‘slides down’’ the processus and invaginates it. McLachlan [19], who supports an intraperitoneally descending testis as do Woodburne and Burkel [15], believes the testis enters the wall of the processus vaginalis through the deep inguinal ring from an external position and that the testis remains under the surface of the mesoderm during this movement and does not enter the coelom. Surgical texts The view that the testis migrates retroperitoneally is supported by many surgical texts. Adams [11] and Rowe et al. [10] assert that the ‘‘processus vaginalis is formed and pulled along with the migrating testicle’’ and that 234 the testis is not preceded by the processus vaginalis. Beasley et al. [20] and Hutson [21] disagree and state that rather than the testis being partially covered by peritoneum, it is instead inside an ‘‘extension of the peritoneum’’—that is, the processus vaginalis. Journal articles Few journal articles discuss the testis as extraperitoneal. Whitehorn [22] observed a testis that was found ‘‘within Gerota’s fascia in the right renal fossa’’ and states that ventral and inferior surfaces were ‘‘closely adherent to the peritoneum.’’ Scorer [23] states that the testis and epididymis are normally retroperitoneal but occasionally the testis is found on a mesorchium, which makes the testis prone to torsion. Some ignore the issue or do not specifically address it: Walker and Mills’s [24] statement that the testis is ‘‘partially covered by a reflected fold of mesothelium from the processus vaginalis which becomes the visceral tunica vaginalis testis’’ is ambiguous on the issue. However, journal articles are the most supportive of the foetal testis being an intraperitoneal organ (Fig. 2). The exact meaning of the term differs among authors, though, and some of the details are not concordant. Wensing [25, 26] states that the testis migrates within the peritoneal fold that carries the gubernaculum proper, which is consistent with the statement by Hadziselimovic and Herzog [27] that the testis is almost entirely covered by peritoneum with the exception of the dorsal Fig. 2 Testicular descent is intraperitoneal (a1–b1) rather than extraperitoneal (a–b), as believed in the 19th century. (Williams and Hutson [30], by permission, from Hart 1910) side and caudal pole. Hadziselimovic and Herzog [27] state that the ‘‘innermost layer (eporchium) of the testicular sheath is a continuation of the peritoneum.’’ Zaw Tun [28] agrees that the testis becomes completely intraperitoneal. Gier and Marion [29] state that the testis lies within the processus vaginalis, not retroperitoneally as commonly drawn, and is encased by the original tunica albuginea with its coelomic epithelium. Stewart et al. [12] and Johansen [13] support this view with the observation that the testis is freely mobile within an open processus vaginalis. This is consistent with Lemeh’s [14] contention that the testis becomes an intraperitoneal organ with the degeneration of the mesonephros and the suspension of the testis from the dorsal abdominal wall. The testis is then suspended by a mesorchium within the peritoneal cavity. Hart [4] maintains the distinction that the ‘‘testis is covered by germ epithelium like the ovary and is not extraperitoneal.’’ He states that in contrast to the squamous endothelium that comprises the parietal peritoneum, the foetal testis is covered by low columnar epithelium. According to Hart [4], the testis is literally within the peritoneal cavity, a view that is supported by Williams and Hutson [30] and Hutson [31]. Direct observations In our observations of rat dissections, the testis, like the ovary, was found freely mobile within the abdominal cavity at the various stages during testicular descent, giving credence to the view that the testis is an intraperitoneal organ during its descent. By 30 days of age, the testes have already completed their descent into the scrotum. However, the processus vaginalis is still patent, and the testis is easily and freely relocated out of the scrotum by applying traction to the fat pad superior to the testis (Fig. 3). Histological examination of the 15- Fig. 3 Photograph of testis and its mesorchium during dissection of adult rat. The testis was pulled back into the abdomen and held up on its mesentery 235 sistent with its intraperitoneal location. The bell-clapper anomaly predisposing to testicular torsion is caused by excessive length of the mesorchium [35, 36] (Fig. 6). Comparison with the human ovary Fig. 4 Histological examination of male rat embryo at 15 days of gestation. Surface epithelium over the testis shows stratified cuboidal cells day-old embryo showed the testis to be enveloped in an irregularly arranged stratified, rather than simple, cuboidal or low columnar epithelium, with little evidence of a basement membrane over the protruding portion of the testis (Fig. 4). The controversy that surrounds the position of the testis is not as fierce where the ovary is concerned. Researchers, including advocates for an extraperitoneal testis, generally agree that the ovaries are intraperitoneal, suspended on a double fold of peritoneum called the mesovarium of the broad ligament [1–3, 7, 37, 38]. If the ovaries are intraperitoneal, and the testis is characterised by a mesorchium early in its development, there has been no satisfactory description as to how the testis becomes extraperitoneal during its descent. Various authors [2, 3, 7, 39] agree that the ovaries are covered by a layer of cuboidal or low columnar surface epithelium rather than the mesothelium of the adjacent peritoneum. It was thought that the layer gave rise to the female gametes, and thus was mistakenly termed Human pathological states We investigated several diseases in humans in which there is evidence for an intraperitoneal testis. In infants with gastroschisis, the bowel protrudes from a periumbilical defect at birth. In a small percentage of cases, the testis may also be protruding with the bowel, consistent with its intraabdominal origin (Fig. 5) [32]. Another rare malformation in humans is splenogonadal fusion. In this condition, the spleen is connected to the left undescended testis across the peritoneal cavity [33, 34]. In boys with intratunical or intravaginal torsion, the testis is freely mobile within the tunica vaginalis, con- Fig. 5 An infant with gastroschisis. The testis is seen herniating along with the small bowel through the anterior abdominal wall Fig. 6 Peritoneal relations of the testis showing the anatomy of torsion. a The normal undescended testis. b The testis projecting into a mesentery before descent. c After descent, the mesentery lengthens and the testis lies horizontally. (The interrupted line represents the peritoneum.) (Scorer 1981, reprinted with permission) 236 ‘‘germinal epithelium’’ [2, 3, 7]. Some have claimed that, likewise, the testis is not actually covered by peritoneum but by a cuboidal ‘‘germinal’’ epithelium [3, 4]. Thus, it could even be argued that the testis and ovary literally are the only true intraperitoneal organs in the body. Our examination of the histology of the rat testis supports the idea that the testis is indeed covered by a layer of modified cuboidal surface epithelium that lacks a basement membrane. However, it is unlikely, as in the ovaries, to be germinal epithelium as Hart proposed (Fig. 3). Discussion Views are divided on the issue of whether the testis is an intraperitoneal organ during its embryonic descent. Whereas textbooks generally favour the (human) testis as extraperitoneal, with a partial peritoneal covering, journal articles are often in favour of an intraperitoneally descending (rodent) testis. The major theory of testicular descent put forth by textbooks purports that the testis descends Fig. 8 Schematic diagram of the pig showing the gubernaculum and surrounding structures shortly before descent (Backhouse and Butler [62], reprinted with permission from Blackwell Publishing) Fig. 7 Histological examination of male human embryo showing the testis (T) suspended in a narrow mesorchium (arrow) retroperitoneally or extraperitoneally behind the processus vaginalis from the urogenital ridge. It follows the route of the gubernaculum into the scrotum and then protrudes into the processus vaginalis to obtain a covering of peritoneum [1, 2, 5–9, 40]. Some have suggested that instead of following the processus vaginalis, the testis actually pulls the peritoneal outpouching into the scrotum [10, 11]. 237 The alternative view is that the testis descends inside a fold of peritoneum, its mesentery or mesorchium, which it retains as it ‘‘glides’’ down the processus vaginalis. Another view contends that the bare testis projects within the peritoneal cavity and is lined not by squamous mesothelial cells of the peritoneum but by germinal epithelium with which the peritoneum is continuous [3, 4]. By definition, an extraperitoneal testis should lack a mesenteric fold. It has been well documented that the testis is characterised by a mesenteric attachment, the mesorchium, just as the ovaries are attached to a mesovarium. The testis develops retroperitoneally from the gonadal ridge on the ventromedial surface of the mesonephros on the posterior abdominal wall [39, 41]. Grooves appear on the medial and lateral aspects of the testis and deepen as the testis grows, so that by the end of the 7th week it is suspended on a narrow mesorchium [14, 37, 38, 41, 42]. This mesorchium attaches the testis to the mesonephric fold and is the route by which the testicular arteries and nerves reach it (Fig. 7); it is prolonged superiorly from the testis as the cranial suspensory ligament and caudally as the plica gubernaculi [43]. Lemeh [14] states that with the further degeneration of the mesonephros, the mesorchium is ‘‘regarded as having been lengthened by the thinning mesonephric fold’’ so that it eventually contains the differentiation of the mesonephros: epididymis, vas deferens, paradidymis, the appendix of the epididymis, and dense strands of connective tissue [14, 29, 44]. At 6 months of gestation the entire foetal testis is covered by peritoneum, with the exception of the dorsal side and caudal pole [27, 45]. Contrary to this view, Backhouse [46] suggests that the processus vaginalis is actually an invagination of the peritoneal cavity into the extraperitoneal gubernacular mesenchyme (Fig. 8). This was later supported by Wensing [25] and Heyns and Hutson [47]. As described by Wensing [25, 26], the gubernaculum exists in three parts: the plica gubernaculi (gubernaculum proper), the pars infravaginalis gubernaculi (infravaginal part of the gubernaculum), and the pars vaginalis gubernaculi (vaginal part of the gubernaculum; Figs. 9, 10). While the latter two are extraperitoneal, the gubernaculum proper, which has a direct attachment to the caudal pole of the testis [48] and the cauda epididymis, is invested with peritoneum. It has a mesentery, which pertains to the plica genitoinguinalis or gonadal fold, a system of serosal folds [49]. Also inconsistent with an extraperitoneal theory of the testicular position is the observation of an intraperitoneal testis during its descent in the rat. While the rat is morphologically different from humans in that the processus vaginalis is still patent in the adult and thus allows free communication with the peritoneal cavity [47], making it an unsuitable model for human testicular descent, our observation concurs with those observed in larger mammals such as the pig [26, 46], dog [29], sheep [49, 50], and horse [44], in which there is a greater resemblance to humans [46, 47]. While it is not expected Fig. 9 Schematic drawing illustrating the three parts of the gubernaculum. a Plica gubernaculi (proper gubernaculum). b Pars vaginalis gubernaculi (vaginal part). c Pars infravaginalis gubernaculi (infravaginal part); (1) testis, (2) epididymis, (3) mesorchium, (4) parietal peritoneum, (5) vaginal process, (6) gubernaculum, (7) external spermatic fascia, (8) scrotum (Baumans et al. [63], reprinted with permission, used by Wensing [26]) that the process of testicular descent is the same across different species, which Backhouse [46] states as mainly in the timing of particular processes and the complexity of the cremaster muscle in the pig, it seems odd that the human testis should not conform to this interspecies pattern of intraperitoneal descent. Furthermore, other pathological examples support an intraperitoneal testis. Splenogonadal fusion is the abnormal fusion of splenic tissue to the gonad, most often the testis, or the differentiated mesonephros [33]. It has been postulated that adhesion of the splenic and gonadal anlage across coelomic epithelium may play a role. In another example, in cases of gastroschisis the testis is often observed to herniate along with the bowel through the anterior abdominal wall, freely mobile and attached to a fold of peritoneum (Fig. 5) [32]. The weight of the evidence suggests an intraperitoneally descending testis after retroperitoneal development of the gonads from the genital ridge. It seems that the testis is intraperitoneal in the neonate, yet appears ‘‘retroperitoneal’’ in elderly men and cadavers. The reduction of mass and involution of the testis and 238 ciated with age, with the position of the testis relative to the tunica vaginalis. References Fig. 10 Schematic drawing of testis and gubernaculum (epididymis and deferent duct have been omitted). The left-hand side of the gubernaculum is sectioned longitudinally: (1) testis, (2) gubernaculum, (2a) plica gubernaculi, (2b) pars infravaginalis gubernaculi, (2c) pars vaginalis gubernaculi, (3) cavity of the vaginal process, (4) testicular artery, (5) vaginal ring, (6) internal inguinal ring, (7) external inguinal ring (Wensing et al. 1980, reprinted with permission, used by Wensing [26]) epididymis in the elderly [16] may possibly account for this. Another possibility could be a gradual recession of the tunica vaginalis from the surface of the testes with age, due to factors associated with the prenatal obliteration of the processus vaginalis. In either event, the discrepancy between an intraperitoneal or extraperitoneal testes may have arisen from differences in the timing of observations of testicular development. Moreover, extrapolation of observations in older men or cadavers, and the assumption that the gubernaculum is entirely extraperitoneal, may have resulted in the theory that the testis descends extraperitoneally. This study suggests that the human testis is intraperitoneal during descent and in the neonate but in later life is less obviously intraperitoneal and may appear extraperitoneal, except in males with a bell-clapper testis. The apparent discrepancy possibly appears as a result of differences in timing of observation and is reconciled by the possibility of a gradual change, asso- 1. 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