Seminars in Pediatric Surgery 23 (2014) 326–330
Contents lists available at ScienceDirect
Seminars in Pediatric Surgery journal homepage: www.elsevier.com/locate/sempedsurg
Anatomy and physiology of the peritoneum Simon C. Blackburn, MBBS, BSc (Hons), MEd, FRCS (Paed Surg), Michael P. Stanton, MBBS, MD, FRCS (Paed Surg)n Department of Paediatric Surgery, University Hospital Southampton NHS Foundation Trust, Tremona Rd, Southampton SO16 6YD, UK
a r t i c l e in f o
Keywords: Peritoneum Anatomy Physiology Embryology Peritoneal dialysis
abstract The peritoneum is commonly encountered in abdominal surgery. The development and rotation of the primitive gut tube lead to the normal adult arrangement of the peritoneal cavity, which forms bloodless planes allowing the retroperitoneal portions of the bowel to be safely mobilised. The arrangement of the peritoneum also forms spaces in which infected fluid or pus can collect. The microcirculation of peritoneal fluid is now well understood, and the large absorptive surface of the peritoneum can be exploited in peritoneal dialysis. The absorption of gas by the peritoneum following abdominal surgery is faster in neonates than in older children, and understanding this process contributes to the interpretation of post-operative radiographs. & 2014 Elsevier Inc. All rights reserved.
Introduction An understanding of the normal anatomy and function of the peritoneum is essential to the understanding of abdominal and groyne surgery in children. This article addresses the embryology, anatomy and physiology of the peritoneum as a prelude to the articles that follow in this issue and provides an aid in understanding this important layer of tissue.
The anatomy of the peritoneum Embryology The peritoneum is derived from the mesoderm lining the body cavity of the primitive embryo. Within this body cavity, the primitive gut tube is formed. It is described to have a parietal layer, lining the body wall, and a visceral layer, which lies over the abdominal organs. The primitive foregut separates the upper part of the body cavity into left and right cavities by the virtue of its dorsal and ventral mesenteries. The primitive midgut and hindgut are supported by a dorsal mesentery but have no ventral mesentery. Foregut rotation The cavities formed within the abdominal cavity by the peritoneum are best understood by considering the rotation of n
Corresponding author. E-mail address: [email protected] (M.P. Stanton).
http://dx.doi.org/10.1053/j.sempedsurg.2014.06.002 1055-8586/& 2014 Elsevier Inc. All rights reserved.
the foregut separately from the midgut and hindgut (Figure 1). The foregut gives rise to the liver, within the ventral mesentery, and the spleen, within the dorsal mesentery. Rotation of the foregut then occurs 901 to the right, such that the ventral mesentery comes to lie to the right of the stomach, and the dorsal mesentery to the left. The differential growth of the contained structures then somewhat distorts this arrangement, such that the liver comes to occupy the entire right upper quadrant and the stomach takes on a curve to the right. The ventral mesentery persists as the lesser omentum, containing the common bile duct, hepatic artery and portal vein within its lower free border. The lower edge of the lesser omentum forms the anterior border of the epiploic foramen (of Winslow), which allows communication from the space in front of the stomach and its associated primitive mesenteries, the greater sac and the space behind, the lesser sac. The epiploic foramen is bordered posteriorly by the inferior vena cava, superiorly by the caudate lobe and inferiorly by the duodenum, meaning that none of its borders can be safely divided.1 The dorsal mesentery persists as the gastro-splenic ligament, and then ensheathes the spleen, attaching to the posterior abdominal wall over the left kidney—the lieno-renal ligament (Figure 2). Midgut rotation The rotation of the midgut is perhaps more familiar to paediatric surgeons. The midgut is suspended by a dorsal mesentery and outgrows the body cavity, herniating through the umbilicus before returning at 8–10 weeks gestation. As it does so, it rotates through a total of 2701 anticlockwise, such that the DJ flexure comes to lie on the left of the midline and the caecum in the right iliac fossa.
S.C. Blackburn, M.P. Stanton / Seminars in Pediatric Surgery 23 (2014) 326–330
Fig. 1. Lateral view of the primitive gut tube at the point of herniation of the primitive gut tube through the umbilicus. Note the presence of a ventral mesentery to the foregut only, but a dorsal mesentery to all parts of the bowel. (Reproduced with permission from Faiz et al.25)
The process of fixation of parts of the bowel to the posterior abdominal wall renders them “retroperitoneal,” although it should be remembered that they are not retroperitoneal in the developmental sense, but intra-abdominal. This process fuses the duodenum, ascending colon and descending colon to the posterior abdominal wall. These places of fusion (sometimes referred to as planes of Zygosis) can, of course, be divided surgically in a relatively bloodless fashion, allowing the right and left hemicolons to be mobilised without compromising their blood supply, and the duodenum to be Kocherized medially without damaging the biliary structures entering its medial side.
Peritoneal attachments Having discussed the embryology of some of the peritoneal attachments, the course of the entire peritoneum may be considered. This can be conveniently started on the anterior abdominal wall just above the umbilicus. The parietal peritoneum inferiorly covers the anterior abdominal wall, being raised in a series of folds: the median, medial, and lateral umbilical folds. These folds overly the obliterated urachus, obliterated umbilical arteries and inferior epigastric vessels, correspondingly. The peritoneum continues down and is reflected over the dome of the bladder. In males, the peritoneum sweeps down to the back of the bladder and then onto the anterior surface of the rectum, whereas in females, it first covers the uterus before dipping down to form the recto-uterine pouch (of Douglas). The peritoneum then passes up the posterior abdominal wall before being reflected over the root of the mesentery and the small bowel. The root of the mesentery runs from the DJ flexure to the ileocecal junction. Laterally at this level, the peritoneum overlies the retroperitoneal portions of the
Fig. 2. Transverse section through the abdomen viewed from below and demonstrating the relationship of the lesser sac to the stomach, lieno-renal and gastrosplenic ligaments. (Reproduced with permission from Faiz et al.25)
327
descending and ascending colon and is reflected over the mobile sigmoid colon and caecum. Superior to the mesenteric root, the peritoneum again gains the posterior abdominal wall and is reflected onto the inferior surface of the transverse mesocolon, before contributing to the greater omentum. At the distal limit of the greater omentum, this layer then passes over the anterior surface of the stomach and forms the anterior layer of the lesser omentum, before passing over the liver and then onto the anterior abdominal wall. The peritoneum is reflected at this level around the obliterated umbilical vein (ligamentum teres) forming the falciform ligament, which represents the most anterior remnant of the embryonic ventral mesentery. The peritoneal lining of the lesser sac contributes to the lienorenal and gastro-splenic ligaments before passing over the posterior wall of the stomach, where it folds into the greater omentum before passing posteriorly, covering the posterior portion of the transverse colon and gaining the posterior abdominal wall. Thus, the lesser sac can be entered surgically by creating a window in either the transverse mesocolon or the greater omentum. Peritoneal spaces The reflections of the peritoneum over the various viscera form a number of potential spaces, notable because they may be the site of abdominal collections. Pelvic collections can occupy the pouch of Douglas in a female. The right and left paracolic gutters may also contain fluid as may the subhepatic spaces. The right subhepatic space (Morrison's pouch) lies between the inferior portion of the liver superiorly and is related to the hepatic flexure of the colon, duodenum and right kidney posteriorly. The left subhepatic space is the lesser sac. The right subphrenic space lies above the liver and is limited by the right coronary ligament. The left is in free communication with the greater sac via the space around the anterior surface of the spleen. Peritoneal reflections on and over the liver The attachments of the peritoneum to the liver need to be divided if mobilisation of the liver is to be safely accomplished. The peritoneum forming the falciform ligament divides into two parts once it abuts the liver surface, thus dividing the left and right subphrenic spaces, and defining a part of the liver surface free of a peritoneal covering, the bare area (Figure 1). The right leaflet
Fig. 3. Sagittal section through the abdomen demonstrating the reflection of the peritoneum over the small bowel, transverse colon, stomach and liver. (Reproduced with permission from Faiz et al.25)
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Fig. 4. The liver viewed anteriorly (A) and inferiorly (B) demonstrating the reflections of the peritoneum on its surface. (Reproduced with permission from Faiz et al.25)
passes backwards and then turns abruptly to the left before reaching the porta hepatis (Figure 4). This sharp turn is referred to as the right triangular ligament. The left leaflet passes backwards to the porta hepatis more directly, with a triangular deviation in its course to the left, referred to as the left triangular ligament. Processus vaginalis The processus vaginalis is an outpouching of the peritoneal cavity associated with testicular descent, although it is present in both sexes. In normal development, it obliterates, leaving a sealed peritoneal layer covering the deep inguinal ring.2 The distal part ensheathes the testis as the double-layered tunica vaginalis. The persistence of the processus vaginalis is associated with the development of congenital hernias and hydroceles. Nerve supply The nerve supply of the parietal and visceral peritoneum is different. The parietal peritoneum is innervated by the segmental spinal nerves supplying the overlying muscle. This is derived from T7 to L1. It is useful to remember that the umbilicus is supplied by T10 and the groyne by L1, allowing the segmental supply to be approximately mapped.1 The peritoneum overlying the diaphragm derives its nerve supply from C4,3 by efferent fibres carried in the phrenic nerve, explaining the shoulder tip pain experienced when this area of peritoneum is stretched or inflamed, for example, after laparoscopy. The visceral peritoneum is innervated by the vagus nerves and sympathetic fibres and is insensate to pain, but sensitive to stretch. The innervation of the peritoneum overlying the mesentery is also autonomic.4 The difference in nerve supply of the peritoneum explains the change in character of pain related to appendicitis. Early in the disease, the patient experiences a dull ache related to the umbilicus, related to stretching of the visceral peritoneum over the appendix. Once the somatically innervated parietal peritoneum is involved, however, a more precisely located and sharp pain is reported. Greater omentum—Anatomy and function As noted above, the greater omentum is formed from four layers of peritoneum, those investing the stomach anteriorly and those investing the transverse colon posteriorly. Whilst this description is anatomically “neat,” in reality these layers are fused
together such that the lesser sac is completed well proximal to the distal limit of the omentum (Figure 3). The role of the omentum as the abdominal “policeman” is familiar to surgeons, as first famously espoused by Rutherford Morison in the early 20th century. Understanding beyond the initial observation that the omentum was often found near to, if not adherent to, inflamed abdominal viscera has advanced considerably. The omentum has an important role in the immunoprotection and the absorptive capacity of the peritoneal cavity. The omental milky spots (of Ranvier) act as areas of macrophage and leucocyte aggregation and migration and are thought by some even to act as secondary lymphoid organs.
Physiology of the peritoneum The physiological properties of the peritoneum are of interest to paediatric surgeons for a variety of reasons. Normal peritoneal fluid secretion, circulation and absorption (gaseous and liquid) are of relevance with respect to gas insufflation for laparoscopy, gas reabsorption after laparoscopy or laparotomy and peritoneal dialysis. The pressure and flow characteristics of the peritoneal cavity, as well as its anatomical spaces discussed earlier, contribute to the typical sites that intra-abdominal fluid collections may occur. Histological structure and circulation The peritoneum is a single layer of flat, simple, stratified squamous epithelial cells, which sits on a basal laminar. Deeper than this lies a thicker layer of connective tissue, which varies in its density, being thinner in areas that can undergo expansion (e.g., lower abdominal wall), and thicker in more fixed areas (e.g., pelvic fascia). The mesothelial cells are linked by intercellular junctions and have surface microvilli. The peritoneum covers a large surface area, on average covering 4 100 m2 in adults, with the largest parietal area being that in the supra-colic compartment over the diaphragm.5,6 The parietal and visceral layers of the peritoneum are separated by a small volume of fluid, typically 50–100 ml in total in adults. Indeed, the finding of small pockets of anechoic fluid in both asymptomatic adults and children on abdominal sonography can be considered a normal finding.7,8 This volume increases slightly at the midpoint of the menstrual cycle in females.9 Turnover of peritoneal fluid occurs at a rate of approximately 5 ml/24 h. This fluid lubricates the peritoneal surfaces allowing, for example, loops of bowel to freely slide over one another during peristalsis. If this normal property is lost by obliteration, adherence of bowel surfaces occurs.
S.C. Blackburn, M.P. Stanton / Seminars in Pediatric Surgery 23 (2014) 326–330
Peritoneal fluid contains water, electrolytes, solutes, proteins and cells. Peritoneal fluid passes via the mesothelial layer to the surrounding interstitium and into the lymphatics. The lymphatic channels (“stomata”) were first described by Von Recklinghausen in the 19th century, later disputed as histological artefact, and subsequently confirmed by electron microscopy. They were thought to be principally located in the subdiaphragmatic spaces; however, it is likely that there is a relatively even distribution of lymphatic channels from where the lymph passes on into the anterior mediastinum and then to the right lymphatic duct. An additional pathway of lymph drainage is via the omental lymphatics into the thoracic duct.5 This process of transport occurs by ultrafiltration down a hydrostatic pressure gradient and is governed by Starling's forces. The more recent “three-pore model” describes capillary–peritoneal flow in more detail. The three pores are the frequent “small pores,” which allow passage of water and small solutes; very infrequent “large pores,” which are permeable to protein and “ultra-small pores” (also called aquaporin-1), which are permeable to water only. Under normal physiological conditions, there is a small net filtration (0.1 ml/min in adults) from the capillary blood (18 mmHg) to the peritoneal space (17 mmHg), and then on into the lymphatics.10–12 Morphologically, there are clefts between endothelial cells, resulting in permeable spaces. At the cellular level, the fluid contains mesothelial cells, macrophages, mast cells and fibroblasts. Intra-peritoneal particles undergo phagocytosis by macrophages and are transported away via the lymph.10–13 Normal peritoneal fluid has a specific gravity between 1.010 and 1.020. Traditionally, accumulated peritoneal fluid (ascites) would be classified as transudate (o1.010) or exudate (41.020). Transudate, with low protein content, accumulates in excess because of secondary changes in Starling's forces. Portal hypertension or cardiac failure, for example, leads to increased portal pressure and higher peritoneal capillary pressures. Inflammation of the peritoneum, by contrast, results in exudate with a higher protein content. More recent recommendations adapting techniques for pleural fluid analysis (Light's criteria)14 have been applied to peritoneal fluid and involve fluid/serum protein ratios and fluid/ serum lactate dehydrogenase calculations to aid in differentiating transudates and exudates.15 Chylous ascites results from the presence of lipid in the peritoneal fluid secondary to impaired lymphatic drainage of any cause. The pressure and flow characteristics of gas and liquid within the peritoneal cavity have been studied for many decades and have relevance to sites of abdominal collections and the diagnosis of abdominal compartment syndrome. For example, subdiaphragmatic pressure was previously thought to be negative (less than atmospheric) and to be a possible explanation for subphrenic abscesses occurring after pathological processes distant from this site.16 The subdiaphragmatic pressure, however, is likely to vary during the respiratory cycle. Peritoneal pressure elsewhere is slightly above atmospheric. The specific gravity of peritoneal fluid is such that gas-filled bowel loops float upwards in the presence of ascites. When gas (e.g., at laparoscopy) is introduced under pressure, gas-filled bowel is displaced downwards. The directional flow of peritoneal fluid has been studied by injecting radio-opaque contrast at surgery and undertaking sequential radiographs.17 Flow occurred up and down the right paracolic gutter between the caecal pole and the right subdiaphragmatic space. From the pelvis, fluid can flow upwards to the left paracolic gutter, but not as far as the left subdiaphragmatic space (due to the phreno-colic ligament). Fluid does not usually accumulate centrally as the small bowel is mobile. Peritoneal dialysis The pH of peritoneal fluid is 7.5–8.0 and the fluid has buffering capacity.18 The filtration properties of the peritoneal membrane
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are utilised during peritoneal dialysis for patients with renal failure. Dialysate fluid is infused and exchanged, allowing normalisation of the overall fluid volume and purification of the blood solutes. Overall function is determined by various factors such as available peritoneal surface area, composition of dialysate (in particular dextrose concentration), patient tolerance and dwell times. The surface area that contributes to dialysis is usually only less than half of the anatomical surface area of the peritoneum. The contact area is influenced by factors such as patient position and the volume of fluid used, as well as pathological processes such as adhesions. Long-term morbidity such as dialysisassociated peritonitis and ultrafiltration failure may limit the duration of treatment.19 Clinical applications of the rapid absorption of solute by the peritoneum include the diagnosis of intraperitoneal bladder rupture, where elevated serum urea, as well as creatinine and potassium may be seen.20 Gas absorption from the peritoneum It has been evident since at least the 1940s that there can be considerable delay in the disappearance of a post-operative pneumo-peritoneum on plain radiography after abdominal surgery. Differing rates were later correlated to different procedures.21 This is of relevance when considering whether free air visible radiologically after surgery is part of this re-absorptive process or represents bowel perforation or leak. Body habits affects this process; absorption is slower in obese patients than in thin patients. Air is detectable for longer on CT scanning compared to plain radiography.22 Only one series of children has been reported where the duration of post-operative pneumoperitoneum after abdominal surgery was measured specifically. In 1985, Ein et al.23 described 88 neonates and children in whom daily plain radiographs were performed, starting on the second post-operative day. Radiographs were repeated until free air had resolved. Of the 25 neonates (o5.4 kg) studied, no free air was visible in any patient by day 2 post-operatively. A further subset of infants/older children was analysed. These had all undergone appendicectomy through a McBurney incision and 13% had free air by day 3, which resolved in all by day 8. Otherwise the persistence of free air tended to correlate with increasing age, weight (quicker in smaller patients), length of incision and longer operative time. Other than for neonates, no firm conclusions could be drawn for specific times for physiological resolution of free air. The range of 3–9 days was similar to that reported in the 1960s following abdominal surgery in adults.21 Recent attention has focussed on gas re-absorption following laparoscopy where iatrogenic bowel perforation may occur away from the site of surgery and go unnoticed. Carbon dioxide is routinely used to insufflate for laparoscopy and is absorbed more rapidly than oxygen. Schauer et al.24 reported that the pneumoperitoneum on plain radiography resolves more quickly following laparoscopic cholecystectomy than after open cholecystectomy. They concluded that free air 424 h after laparoscopic cholecystectomy was likely to be pathological. The authors suggest that this may be due to the more rapid absorption of insufflated CO2 and the smaller incisions allowing less atmospheric air into the peritoneal cavity.
Conclusion The anatomy and physiology of the peritoneum are of relevance to the paediatric surgeon in day-to-day practice, whether mobilising bowel during abdominal surgery, managing a patient with abdominal collections following appendicectomy or evaluating the aetiology of intra-abdominal air on an abdominal x-ray, this basic science is of great relevance.
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References 1. Ellis H. Clinical Anatomy. 9th ed., London: Blackwell Science Ltd; 1997. 2. Pham SBT, Hong MK-H, Teague JA, et al. Is the testis intraperitoneal? Pediatr Surg Int. 2005;21(4):231–239. 3. Sinnatamby CS. Last's Anatomy. 10th ed., London: Elsevier Science Ltd, Philadelphia; 2003. 4. Sheehan D. The afferent nerve supply of the mesentery and its significance in the causation of abdominal pain. J Anat. 1933;67(Pt 2):233–249. 5. Borley N. Peritoneum and peritoneal cavity. In: Standring S, editor. Grays Anatomy. 40th ed., Philadelphia: Churchill Livingstone Elsevier; 2008. p. 1099–1111. 6. Albanese AM, Albanese EF, Miño JH, et al. Peritoneal surface area: measurements of 40 structures covered by peritoneum: correlation between total peritoneal surface area and the surface calculated by formulas. Surg Radiol Anat. 2009;31(5):369–377. 7. Jéquier S, Jéquier J-C, Hanquinet S. Intraperitoneal fluid in children: normal ultrasound findings depend on which scan head you use. Pediatr Radiol. 2003;33(2):86–91. 8. Brown SE, Dubbins PA. Detection of free intraperitoneal fluid in healthy young men. J Ultrasound Med. 2012;31(10):1527–1530. 9. Hann LE, Hall DA, Black EB, et al. Mittelschmerz. Sonographic demonstration. J Am Med Assoc. 1979;241(25):2731–2732. 10. Flessner MF. Peritoneal transport physiology: insights from basic research. J Am Soc Nephrol. 1991;2(2):122–135. 11. Rippe B, Davies S. Permeability of peritoneal and glomerular capillaries: what are the differences according to pore theory? Perit Dial Int. 2011;31(3):249–258. 12. Rippe B, Venturoli D, Simonsen O, et al. Fluid and electrolyte transport across the peritoneal membrane during CAPD according to the three-pore model. Perit Dial Int. 2004;24(1):10–27.
13. Krediet RT. Fluid absorption in the peritoneum—it is less simple than you thought. Nephrol Dial Transplant. 1994;9(4):341–343. 14. Light RW, Macgregor MI, Luchsinger PC, et al. Pleural effusions: the diagnostic separation of transudates and exudates. Ann Intern Med. 1972; 77(4):507–513. 15. Paramothayan NS, Barron J. New criteria for the differentiation between transudates and exudates. J Clin Pathol. 2002;55(1):69–71. 16. Overholt R. Intraperitoneal pressure. Arch Surg. 1931;22(5):691–703. 17. Mitchell GAG. The spread of acute intraperitoneal effusions. Br J Surg. 1940; 28(110):291–313. 18. Howard JM, Singh LM. Peritoneal fluid pH after perforation of peptic ulcers: the myth of “acid-peritonitis”. Arch Surg. 1963;87(3):483–484. 19. Chadha V, Schaefer FS, Warady BA. Dialysis-associated peritonitis in children. Pediatr Nephrol. 2010;25(3):425–440. 20. Ciftci AO, Tanyel FC, Senocak ME, et al. Biochemical predictors for differentiating intraperitoneal and extraperitoneal bladder perforation. J Pediatr Surg. 1999;34(2):367–369. 21. Bevan PG. Incidence of post-operative pneumoperitoneum and its significance. Br Med J. 1961;2(5252):605–609. 22. Gayer G, Hertz M, Zissin R. Postoperative pneumoperitoneum: prevalence, duration, and possible significance. Semin Ultrasound CT MR. 2004;25(3): 286–289. 23. Ein SH, Stephens CA, Reilly BJ. The disappearance of free air after pediatric laparotomy. J Pediatr Surg. 1985;20(4):422–424. 24. Schauer PR, Page CP, Ghiatas AA, et al. Incidence and significance of subdiaphragmatic air following laparoscopic cholecystectomy. Am Surg. 1997; 63(2):132–136. 25. Faiz O, Blackburn SC, Moffat D. Anatomy at a Glance. 3rd ed., Oxford: WileyBlackwell; 2011.
Contents lists available at ScienceDirect
Seminars in Pediatric Surgery journal homepage: www.elsevier.com/locate/sempedsurg
Anatomy and physiology of the peritoneum Simon C. Blackburn, MBBS, BSc (Hons), MEd, FRCS (Paed Surg), Michael P. Stanton, MBBS, MD, FRCS (Paed Surg)n Department of Paediatric Surgery, University Hospital Southampton NHS Foundation Trust, Tremona Rd, Southampton SO16 6YD, UK
a r t i c l e in f o
Keywords: Peritoneum Anatomy Physiology Embryology Peritoneal dialysis
abstract The peritoneum is commonly encountered in abdominal surgery. The development and rotation of the primitive gut tube lead to the normal adult arrangement of the peritoneal cavity, which forms bloodless planes allowing the retroperitoneal portions of the bowel to be safely mobilised. The arrangement of the peritoneum also forms spaces in which infected fluid or pus can collect. The microcirculation of peritoneal fluid is now well understood, and the large absorptive surface of the peritoneum can be exploited in peritoneal dialysis. The absorption of gas by the peritoneum following abdominal surgery is faster in neonates than in older children, and understanding this process contributes to the interpretation of post-operative radiographs. & 2014 Elsevier Inc. All rights reserved.
Introduction An understanding of the normal anatomy and function of the peritoneum is essential to the understanding of abdominal and groyne surgery in children. This article addresses the embryology, anatomy and physiology of the peritoneum as a prelude to the articles that follow in this issue and provides an aid in understanding this important layer of tissue.
The anatomy of the peritoneum Embryology The peritoneum is derived from the mesoderm lining the body cavity of the primitive embryo. Within this body cavity, the primitive gut tube is formed. It is described to have a parietal layer, lining the body wall, and a visceral layer, which lies over the abdominal organs. The primitive foregut separates the upper part of the body cavity into left and right cavities by the virtue of its dorsal and ventral mesenteries. The primitive midgut and hindgut are supported by a dorsal mesentery but have no ventral mesentery. Foregut rotation The cavities formed within the abdominal cavity by the peritoneum are best understood by considering the rotation of n
Corresponding author. E-mail address: [email protected] (M.P. Stanton).
http://dx.doi.org/10.1053/j.sempedsurg.2014.06.002 1055-8586/& 2014 Elsevier Inc. All rights reserved.
the foregut separately from the midgut and hindgut (Figure 1). The foregut gives rise to the liver, within the ventral mesentery, and the spleen, within the dorsal mesentery. Rotation of the foregut then occurs 901 to the right, such that the ventral mesentery comes to lie to the right of the stomach, and the dorsal mesentery to the left. The differential growth of the contained structures then somewhat distorts this arrangement, such that the liver comes to occupy the entire right upper quadrant and the stomach takes on a curve to the right. The ventral mesentery persists as the lesser omentum, containing the common bile duct, hepatic artery and portal vein within its lower free border. The lower edge of the lesser omentum forms the anterior border of the epiploic foramen (of Winslow), which allows communication from the space in front of the stomach and its associated primitive mesenteries, the greater sac and the space behind, the lesser sac. The epiploic foramen is bordered posteriorly by the inferior vena cava, superiorly by the caudate lobe and inferiorly by the duodenum, meaning that none of its borders can be safely divided.1 The dorsal mesentery persists as the gastro-splenic ligament, and then ensheathes the spleen, attaching to the posterior abdominal wall over the left kidney—the lieno-renal ligament (Figure 2). Midgut rotation The rotation of the midgut is perhaps more familiar to paediatric surgeons. The midgut is suspended by a dorsal mesentery and outgrows the body cavity, herniating through the umbilicus before returning at 8–10 weeks gestation. As it does so, it rotates through a total of 2701 anticlockwise, such that the DJ flexure comes to lie on the left of the midline and the caecum in the right iliac fossa.
S.C. Blackburn, M.P. Stanton / Seminars in Pediatric Surgery 23 (2014) 326–330
Fig. 1. Lateral view of the primitive gut tube at the point of herniation of the primitive gut tube through the umbilicus. Note the presence of a ventral mesentery to the foregut only, but a dorsal mesentery to all parts of the bowel. (Reproduced with permission from Faiz et al.25)
The process of fixation of parts of the bowel to the posterior abdominal wall renders them “retroperitoneal,” although it should be remembered that they are not retroperitoneal in the developmental sense, but intra-abdominal. This process fuses the duodenum, ascending colon and descending colon to the posterior abdominal wall. These places of fusion (sometimes referred to as planes of Zygosis) can, of course, be divided surgically in a relatively bloodless fashion, allowing the right and left hemicolons to be mobilised without compromising their blood supply, and the duodenum to be Kocherized medially without damaging the biliary structures entering its medial side.
Peritoneal attachments Having discussed the embryology of some of the peritoneal attachments, the course of the entire peritoneum may be considered. This can be conveniently started on the anterior abdominal wall just above the umbilicus. The parietal peritoneum inferiorly covers the anterior abdominal wall, being raised in a series of folds: the median, medial, and lateral umbilical folds. These folds overly the obliterated urachus, obliterated umbilical arteries and inferior epigastric vessels, correspondingly. The peritoneum continues down and is reflected over the dome of the bladder. In males, the peritoneum sweeps down to the back of the bladder and then onto the anterior surface of the rectum, whereas in females, it first covers the uterus before dipping down to form the recto-uterine pouch (of Douglas). The peritoneum then passes up the posterior abdominal wall before being reflected over the root of the mesentery and the small bowel. The root of the mesentery runs from the DJ flexure to the ileocecal junction. Laterally at this level, the peritoneum overlies the retroperitoneal portions of the
Fig. 2. Transverse section through the abdomen viewed from below and demonstrating the relationship of the lesser sac to the stomach, lieno-renal and gastrosplenic ligaments. (Reproduced with permission from Faiz et al.25)
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descending and ascending colon and is reflected over the mobile sigmoid colon and caecum. Superior to the mesenteric root, the peritoneum again gains the posterior abdominal wall and is reflected onto the inferior surface of the transverse mesocolon, before contributing to the greater omentum. At the distal limit of the greater omentum, this layer then passes over the anterior surface of the stomach and forms the anterior layer of the lesser omentum, before passing over the liver and then onto the anterior abdominal wall. The peritoneum is reflected at this level around the obliterated umbilical vein (ligamentum teres) forming the falciform ligament, which represents the most anterior remnant of the embryonic ventral mesentery. The peritoneal lining of the lesser sac contributes to the lienorenal and gastro-splenic ligaments before passing over the posterior wall of the stomach, where it folds into the greater omentum before passing posteriorly, covering the posterior portion of the transverse colon and gaining the posterior abdominal wall. Thus, the lesser sac can be entered surgically by creating a window in either the transverse mesocolon or the greater omentum. Peritoneal spaces The reflections of the peritoneum over the various viscera form a number of potential spaces, notable because they may be the site of abdominal collections. Pelvic collections can occupy the pouch of Douglas in a female. The right and left paracolic gutters may also contain fluid as may the subhepatic spaces. The right subhepatic space (Morrison's pouch) lies between the inferior portion of the liver superiorly and is related to the hepatic flexure of the colon, duodenum and right kidney posteriorly. The left subhepatic space is the lesser sac. The right subphrenic space lies above the liver and is limited by the right coronary ligament. The left is in free communication with the greater sac via the space around the anterior surface of the spleen. Peritoneal reflections on and over the liver The attachments of the peritoneum to the liver need to be divided if mobilisation of the liver is to be safely accomplished. The peritoneum forming the falciform ligament divides into two parts once it abuts the liver surface, thus dividing the left and right subphrenic spaces, and defining a part of the liver surface free of a peritoneal covering, the bare area (Figure 1). The right leaflet
Fig. 3. Sagittal section through the abdomen demonstrating the reflection of the peritoneum over the small bowel, transverse colon, stomach and liver. (Reproduced with permission from Faiz et al.25)
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Fig. 4. The liver viewed anteriorly (A) and inferiorly (B) demonstrating the reflections of the peritoneum on its surface. (Reproduced with permission from Faiz et al.25)
passes backwards and then turns abruptly to the left before reaching the porta hepatis (Figure 4). This sharp turn is referred to as the right triangular ligament. The left leaflet passes backwards to the porta hepatis more directly, with a triangular deviation in its course to the left, referred to as the left triangular ligament. Processus vaginalis The processus vaginalis is an outpouching of the peritoneal cavity associated with testicular descent, although it is present in both sexes. In normal development, it obliterates, leaving a sealed peritoneal layer covering the deep inguinal ring.2 The distal part ensheathes the testis as the double-layered tunica vaginalis. The persistence of the processus vaginalis is associated with the development of congenital hernias and hydroceles. Nerve supply The nerve supply of the parietal and visceral peritoneum is different. The parietal peritoneum is innervated by the segmental spinal nerves supplying the overlying muscle. This is derived from T7 to L1. It is useful to remember that the umbilicus is supplied by T10 and the groyne by L1, allowing the segmental supply to be approximately mapped.1 The peritoneum overlying the diaphragm derives its nerve supply from C4,3 by efferent fibres carried in the phrenic nerve, explaining the shoulder tip pain experienced when this area of peritoneum is stretched or inflamed, for example, after laparoscopy. The visceral peritoneum is innervated by the vagus nerves and sympathetic fibres and is insensate to pain, but sensitive to stretch. The innervation of the peritoneum overlying the mesentery is also autonomic.4 The difference in nerve supply of the peritoneum explains the change in character of pain related to appendicitis. Early in the disease, the patient experiences a dull ache related to the umbilicus, related to stretching of the visceral peritoneum over the appendix. Once the somatically innervated parietal peritoneum is involved, however, a more precisely located and sharp pain is reported. Greater omentum—Anatomy and function As noted above, the greater omentum is formed from four layers of peritoneum, those investing the stomach anteriorly and those investing the transverse colon posteriorly. Whilst this description is anatomically “neat,” in reality these layers are fused
together such that the lesser sac is completed well proximal to the distal limit of the omentum (Figure 3). The role of the omentum as the abdominal “policeman” is familiar to surgeons, as first famously espoused by Rutherford Morison in the early 20th century. Understanding beyond the initial observation that the omentum was often found near to, if not adherent to, inflamed abdominal viscera has advanced considerably. The omentum has an important role in the immunoprotection and the absorptive capacity of the peritoneal cavity. The omental milky spots (of Ranvier) act as areas of macrophage and leucocyte aggregation and migration and are thought by some even to act as secondary lymphoid organs.
Physiology of the peritoneum The physiological properties of the peritoneum are of interest to paediatric surgeons for a variety of reasons. Normal peritoneal fluid secretion, circulation and absorption (gaseous and liquid) are of relevance with respect to gas insufflation for laparoscopy, gas reabsorption after laparoscopy or laparotomy and peritoneal dialysis. The pressure and flow characteristics of the peritoneal cavity, as well as its anatomical spaces discussed earlier, contribute to the typical sites that intra-abdominal fluid collections may occur. Histological structure and circulation The peritoneum is a single layer of flat, simple, stratified squamous epithelial cells, which sits on a basal laminar. Deeper than this lies a thicker layer of connective tissue, which varies in its density, being thinner in areas that can undergo expansion (e.g., lower abdominal wall), and thicker in more fixed areas (e.g., pelvic fascia). The mesothelial cells are linked by intercellular junctions and have surface microvilli. The peritoneum covers a large surface area, on average covering 4 100 m2 in adults, with the largest parietal area being that in the supra-colic compartment over the diaphragm.5,6 The parietal and visceral layers of the peritoneum are separated by a small volume of fluid, typically 50–100 ml in total in adults. Indeed, the finding of small pockets of anechoic fluid in both asymptomatic adults and children on abdominal sonography can be considered a normal finding.7,8 This volume increases slightly at the midpoint of the menstrual cycle in females.9 Turnover of peritoneal fluid occurs at a rate of approximately 5 ml/24 h. This fluid lubricates the peritoneal surfaces allowing, for example, loops of bowel to freely slide over one another during peristalsis. If this normal property is lost by obliteration, adherence of bowel surfaces occurs.
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Peritoneal fluid contains water, electrolytes, solutes, proteins and cells. Peritoneal fluid passes via the mesothelial layer to the surrounding interstitium and into the lymphatics. The lymphatic channels (“stomata”) were first described by Von Recklinghausen in the 19th century, later disputed as histological artefact, and subsequently confirmed by electron microscopy. They were thought to be principally located in the subdiaphragmatic spaces; however, it is likely that there is a relatively even distribution of lymphatic channels from where the lymph passes on into the anterior mediastinum and then to the right lymphatic duct. An additional pathway of lymph drainage is via the omental lymphatics into the thoracic duct.5 This process of transport occurs by ultrafiltration down a hydrostatic pressure gradient and is governed by Starling's forces. The more recent “three-pore model” describes capillary–peritoneal flow in more detail. The three pores are the frequent “small pores,” which allow passage of water and small solutes; very infrequent “large pores,” which are permeable to protein and “ultra-small pores” (also called aquaporin-1), which are permeable to water only. Under normal physiological conditions, there is a small net filtration (0.1 ml/min in adults) from the capillary blood (18 mmHg) to the peritoneal space (17 mmHg), and then on into the lymphatics.10–12 Morphologically, there are clefts between endothelial cells, resulting in permeable spaces. At the cellular level, the fluid contains mesothelial cells, macrophages, mast cells and fibroblasts. Intra-peritoneal particles undergo phagocytosis by macrophages and are transported away via the lymph.10–13 Normal peritoneal fluid has a specific gravity between 1.010 and 1.020. Traditionally, accumulated peritoneal fluid (ascites) would be classified as transudate (o1.010) or exudate (41.020). Transudate, with low protein content, accumulates in excess because of secondary changes in Starling's forces. Portal hypertension or cardiac failure, for example, leads to increased portal pressure and higher peritoneal capillary pressures. Inflammation of the peritoneum, by contrast, results in exudate with a higher protein content. More recent recommendations adapting techniques for pleural fluid analysis (Light's criteria)14 have been applied to peritoneal fluid and involve fluid/serum protein ratios and fluid/ serum lactate dehydrogenase calculations to aid in differentiating transudates and exudates.15 Chylous ascites results from the presence of lipid in the peritoneal fluid secondary to impaired lymphatic drainage of any cause. The pressure and flow characteristics of gas and liquid within the peritoneal cavity have been studied for many decades and have relevance to sites of abdominal collections and the diagnosis of abdominal compartment syndrome. For example, subdiaphragmatic pressure was previously thought to be negative (less than atmospheric) and to be a possible explanation for subphrenic abscesses occurring after pathological processes distant from this site.16 The subdiaphragmatic pressure, however, is likely to vary during the respiratory cycle. Peritoneal pressure elsewhere is slightly above atmospheric. The specific gravity of peritoneal fluid is such that gas-filled bowel loops float upwards in the presence of ascites. When gas (e.g., at laparoscopy) is introduced under pressure, gas-filled bowel is displaced downwards. The directional flow of peritoneal fluid has been studied by injecting radio-opaque contrast at surgery and undertaking sequential radiographs.17 Flow occurred up and down the right paracolic gutter between the caecal pole and the right subdiaphragmatic space. From the pelvis, fluid can flow upwards to the left paracolic gutter, but not as far as the left subdiaphragmatic space (due to the phreno-colic ligament). Fluid does not usually accumulate centrally as the small bowel is mobile. Peritoneal dialysis The pH of peritoneal fluid is 7.5–8.0 and the fluid has buffering capacity.18 The filtration properties of the peritoneal membrane
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are utilised during peritoneal dialysis for patients with renal failure. Dialysate fluid is infused and exchanged, allowing normalisation of the overall fluid volume and purification of the blood solutes. Overall function is determined by various factors such as available peritoneal surface area, composition of dialysate (in particular dextrose concentration), patient tolerance and dwell times. The surface area that contributes to dialysis is usually only less than half of the anatomical surface area of the peritoneum. The contact area is influenced by factors such as patient position and the volume of fluid used, as well as pathological processes such as adhesions. Long-term morbidity such as dialysisassociated peritonitis and ultrafiltration failure may limit the duration of treatment.19 Clinical applications of the rapid absorption of solute by the peritoneum include the diagnosis of intraperitoneal bladder rupture, where elevated serum urea, as well as creatinine and potassium may be seen.20 Gas absorption from the peritoneum It has been evident since at least the 1940s that there can be considerable delay in the disappearance of a post-operative pneumo-peritoneum on plain radiography after abdominal surgery. Differing rates were later correlated to different procedures.21 This is of relevance when considering whether free air visible radiologically after surgery is part of this re-absorptive process or represents bowel perforation or leak. Body habits affects this process; absorption is slower in obese patients than in thin patients. Air is detectable for longer on CT scanning compared to plain radiography.22 Only one series of children has been reported where the duration of post-operative pneumoperitoneum after abdominal surgery was measured specifically. In 1985, Ein et al.23 described 88 neonates and children in whom daily plain radiographs were performed, starting on the second post-operative day. Radiographs were repeated until free air had resolved. Of the 25 neonates (o5.4 kg) studied, no free air was visible in any patient by day 2 post-operatively. A further subset of infants/older children was analysed. These had all undergone appendicectomy through a McBurney incision and 13% had free air by day 3, which resolved in all by day 8. Otherwise the persistence of free air tended to correlate with increasing age, weight (quicker in smaller patients), length of incision and longer operative time. Other than for neonates, no firm conclusions could be drawn for specific times for physiological resolution of free air. The range of 3–9 days was similar to that reported in the 1960s following abdominal surgery in adults.21 Recent attention has focussed on gas re-absorption following laparoscopy where iatrogenic bowel perforation may occur away from the site of surgery and go unnoticed. Carbon dioxide is routinely used to insufflate for laparoscopy and is absorbed more rapidly than oxygen. Schauer et al.24 reported that the pneumoperitoneum on plain radiography resolves more quickly following laparoscopic cholecystectomy than after open cholecystectomy. They concluded that free air 424 h after laparoscopic cholecystectomy was likely to be pathological. The authors suggest that this may be due to the more rapid absorption of insufflated CO2 and the smaller incisions allowing less atmospheric air into the peritoneal cavity.
Conclusion The anatomy and physiology of the peritoneum are of relevance to the paediatric surgeon in day-to-day practice, whether mobilising bowel during abdominal surgery, managing a patient with abdominal collections following appendicectomy or evaluating the aetiology of intra-abdominal air on an abdominal x-ray, this basic science is of great relevance.
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