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The Surgical Physiology of the Colon
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The Surgical Physiology of the Colon HAROLD LAUFlVIA;,\, PH.D., :M.D., F.A.C.S.*
THIS discussion will review the surgical significance of four fundamental functions of the colon-motility, digestion, absorption and excretion. MOTILITY
Motility of the human colon has been described in terms of four types of waves, designated types I, II, III and IV.! Type I waves are probably very small contractions of the muscularis mucosae the function of "'hich is unknown. They may represent normal tonus. Type II waves are of greater duration and amplitude than type I ''laves, lasting 20 to 30 seconds in the sigmoid colon. Their pressure is less in the distal colon than in the proximal colon. In normal persons type II waves generally constitute more than 90 per cent of the recorded activity.2 These waves probably account for the haustral contractions, and their function appears to be that of mixing rather than propelling. Type III waves are complex, long-lasting (about one minute) and seldom-occurring. They probably aid absorption by increasing intraluminal pressure. Type IV waves are simple, large waves, without the secondary small movements seen superimposed on type III waves. Type IV waves are definitely propulsive, but do not possess the progressive quality of peristaltic movements, tending to occur simultaneously in the proximal and distal colons. 3 These waves are regular, occurring every three to four minutes and diminishing in rate when the bowel is emptied. In ulcerative colitis, over-all activity is reduced. Balloon studies 2 indicate that these patients actually do not have "too much motility," but rather the motility is decreased. However, roentgenologically, spasm of the sigmoid is encountered in most of the functional disorders of the colon, such as chronic constipation, chronic spastic colitis, and mucous colitis. It is also present in the inflammatory lesions, such as diverticulitis and ulcerative colitis. 4 Garry 5 and Y oumans 6 have reviewed the known data on the neural regulation of motor patterns of the bowel. Stimulation of the parasympathetic nerves or the administration of acetylcholine or related drugs generally leads to an increase in propulsive activity of the colon and a
* Associate
Professor of Surgery, Northwestern University Medical School, Chicago.
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decrease in mlxmg activity, as well as a decrease in the tone of the ileocecal and internal anal sphincters. Sympathetic and parasympathetic denervation theoretically produce the opposite effects from those of stimulation of the same outflows. Koelle 7 has suggested, however, that the state of activity of the bowel at the time when nerves are stimulated or cut determines, to a great extent, the type of response both qualitatively and quantitatively. Despite these effects, a "considerable degree of normal function is retained or regained following partial or complete extrinsic denervation."7 These conclusions, derived experimentally, have been borne out clinically in several instances, such as in the failure of sympathectoniy to yield lasting results in congenital megacolon; the lack of permanent results following vagotomy for ulcerative colitis; the impermanence of sacral parasympathectomy in the treatment of ulcerative colitis. Certain humoral agents, recently reviewed by Koelle,7 appear to have specific functions in the nerve-muscle mechanism relating to motility. Acetylcholine, a mediator of either excitatory or inhibitory responses, is synthesized by ganglionic cells of the intrinsic plexuses of the bowel wall, as well as by the interstitial cells. 8, 9 Cholinesterase is an enzyme present in the membranes of most of the ganglion cells and nerve fibers of the myenteric and submucosal plexuses. Its primary function is presumably the hydrolysis of acetylcholine. lo Epinephrine and norepinephrine exert predominantly inhibitory action on the gastrointestinal tract, with the exception of the sphincters. These mediators or transmitting agents are inactivated at significant rates by certain mammalian enzymes, such as monoamine oxidase. l l Substance P is probably a mediator in the muscularis mucosae.1 2 In animals, the highest concentrations of the substance occur in the duodenum, jejunum, colon and rectum. 13 ,14 Histamine is present throughout the gastrointestinal tract, particularly in the muscularis mucosae. Despite the emphasis given this substance in the past, it probably has no neurohumeral function. 7 Enteramine is concentrated mainly in the glandular mucosa. IS Its function has not been elucidated. One of the most intriguing defects in motility encountered by the surgeon is that seen in congenital megacolon, It is characterized by spasm of the sigmoid or rectosigmoid colon and marked dilation and hypertrophy of the segment proximal to the spastic area. In 1901, TitteP6 first noted the complete absence of ganglion cells from the myenteric plexus of the spastic portion. In the same region there are numerous thick, closely packed bundles of nonmyelinated nerve fibers. In 1946, Ehrenpreis I7 suggested that the lack of propulsive peristalsis in the spastic segment was due to the agenesis of the ganglion cells, and that the dilatation of the proximal segment was secondarily compensatory. In 1949 Swenson, Rheinlander and Diamond I8 reported that resection of the spastic segment is frequently followed by normal appearance and
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function of the previously dilated colon. Kamijo, Hiatt and Koelle 19 recently studied the cholinesterase content of excised surgical specimens from cases of congenital megacolon. They formulated the hypothesis that the basic defect in the spastic segment is an absence of adrenergic neurons rather than an absence of cholinergic neurons. Diminutions in normal motility may be protective in nature, and follow peritoneal irritation of any type. The "silent belly" of peritonitis is well known in diagnosis. The "splinting" of the area immediately adjacent to an anastomosis is a similar phenomenon more locally confined. Although a low degree of motility may occur above and below the spastic, splinted area, the ability of the colon to participate in so-called "mass contractions" is recovered only after the local tissue reaction and localized peritonitis become lessened. A greatly distended bowel usually has diminished or absent motility. Noxious stimuli such as trauma (including external blunt trauma), electrical stimulation, and extremes of heat or cold may inhibit colonic motility if severe, but may increase motility if milder. Distention of the colon with water, saline or soapsuds first inhibits, then augments motility. Mechanical irritation or electrical stimulation of the anal sphincter area increases local tone and motility, but depresses the activity and tone of the proximal colon. 20 Stress reactions, including exposure to cold, pain, hypoglycemia or worry tend to augment colonic tone. 21 Following bowel resection, early oral feeding is tolerated poorly. Postsurgical "splinting" of the bowel and the resultant retarded evacuation of the colon results in delayed gastric emptying which can occur in the absence of pylorospasm. 22 Furthermore, jejunal peristalsis may be inhibited by colonic irritation. 23 Ivy and associates 24 observed that constipation, irritation of the colon, or stimulation of the nerves from the colon inhibits the flow of bile in the dog. Alterations in colon motility are usually accompanied by alterations in mucus secretion of the colon mucosa. Under normal circumstances mucus protects the mucosa against mechanical injury by reducing friction, and by diluting or buffering the chemical substances which may pass through the colon. Postoperative gastric suction is usually desirable after colon surgery. The prevention of distention will tend to reduce the incidence of postoperative obstructions due to adhesions,25 and will permit earlier resumption of peristalsis. DIGESTION
The colon is not ordinarily considered a digestive organ; yet it is the only portion of the digestive tract in which cellulose and connective tissue of the diet are digested. According to Quigley,20 no enzyme is produced by the digestive tract which acts on cellulose and connective tissue, even in such forms of life as the termite, whose diet consists largely of cellulose.
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Cellulose is digested by the bacteria in the ileum, cecum and proximal colon where bacteria are in abundance and where they digest the cellulose and liberate food substances. It is from the action of bacteria on cellulose that the body derives a wide variety of vitamin substances, such as vitamin K, vitamin B I2, biotin, niacin, thiamine and riboflavin. In addition, indole, skatol and various gases are produced by this bacterial action. Cooper in 191426 was apparently the first to suggest actual synthesis of vitamins by intestinal flora. It is probable that most animals, particularly human beings, rarely eat a completely balanced diet, and therefore must depend upon intestinal organisms for synthesis of the missing; vitamin factors. The importance of intestinal flora in nutrition is unquestioned. "Certainly the quantitative requirement of many of the vitamins, some of the amino acids and perhaps some of the fatty acids is directly dependent upon the intestinal bacteria, and indirectly the microflora is probably related to the requirement of practically all nutrients."27 It appears that the vitamin-producing efficiency of intestinal bacteria is somewhat inversely related to the adequacy of vitamin intake. Thus, when certain vitamin components are absent from the diet, they are produced in the bowel. Conversely, when the diet is adequate in vitamins, they are less likely to be synthesized. 28 This mechanism is, of course, subject to the nature of the ingested nutrients. For example, certain carbohydrates are more favorable to vitamin synthesis than are others. High fat rations are known to decrease the production of riboflavin. 27 The effect of the poorly absorbed sulfa drugs and of antibiotics upon bacterial growth in the bowel has formed the basis for one of the greatest advances in bowel surgery. Sterilization of the bowel has made it possible to perform primary anastomosis anywhere in the colon. Yet we must not lose sight of the collateral effects of such bowel preparation. Actually, some of the best evidence for intestinal synthesis of vitamins was obtained 29 when succinylsulfathiazole or phthalylsulfathiazole was added to the diet of rats, resulting in the development of folic acid and biotin deficiencies. The precise role of the antibiotics on interference with vitamin formation remains to be assessed. 30 Most of the other complications following antibiotic use are now generally appreciated by surgeons. In the days of the five to seven day preoperative preparation of the bowel with sulfonamides, there often resulted a sufficient decrease in vitamin K production to cause an increased bleeding tendency. This was usually corrected by the co-administration of synthetic vitamin K. Now that shortacting antibiotics have replaced sulfonamides almost exclusively for preoperative bowel preparation, other complications have been noted. The most serious complication is micrococcic enteritis, due either to the overgrowth of antibiotic-resistant micrococci or that of yeast or
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yeastlike organisms. 30 Fairlie and Kenda1l 3! believe the phenomenon is more than merely an overgrowth, and that a direct stimulation of the staphylococcus by antibiotics must be considered. The severely debilitating effects of postantibiotic diarrhea, particularly when it occurs in the postoperative patient, are often fatal. Recently, van Prohaska32 has reported encouraging results in some of these patients from the use of ACTH. Anal pruritus is a common complication following oral wide-spectrum antibiotics. It may be very mild and self-limited, or it may be severe enough to require such measures as ACTH or cortisone. Some instances are intractable to all forms of treatment.30 ABSORPTION
The proximal, or absorbing colon, absorbs significant amounts of water and salts, while the distal, or storage colon, absorbs very little. It has been estimated 20 that of the 620 cc. of water discharged daily from ileum to colon, 500 cc. is absorbed, leaving 120 cc. in the feces. In the absence of this absorbing mechanism, as for example when an ileostomy is present, the entire water content of the ileal fecal stream is lost to the outside, leading to dehydration, until the ileum adjusts to a greater water-absorbing role. The solid residue of the feces is composed of approximately one-third bacteria, the remainder consisting of bile pigment, mucin and cellular debris. Two to 3 per cent is nitrogenous, 10 to 20 per cent is fat, and 10 to 20 per cent inorganic material. Most of the bacteria are discharged dead. The fat consists of split and unsplit fat, the split portion coming from the unabsorbed fatty acids of the diet. The neutral fat is derived from bacteria and epithelial cell debris. Many factors affect absorption from the intestine. These include pH, motility, condition of the mucosa, the presence and action of bacteria, hormones and vitamins, and certain disease conditions, as well as variations imposed by surgery.33 Whereas normal man absorbs at least 90 per cent of his daily fat intake, steatorrhea results when 85 per cent or less of the dietary fat is absorbed. 33 It behooves the surgeon to keep in mind some of the postsurgical lesions which may lead to this condition. Following pancreatectomy the absence of the normal discharge of pancreatic enzymes into the intestine results in undigested and unabsorbed foodstuffs reaching the expelled stool. Severe steatorrhea may follow any of a wide variety of surgical procedures affecting continuity and motility of the gastrointestinal tract. It may follow total or subtotal gastrectomy in which a jejunal anastomosis has been made; sidetracking operations, such as ileotransverse colostomy or long-step enteroenterostomy; massive resection of proximal colon or small intestine with resultant decrease in absorptive surface, and as a temporary complication of ileostomy.
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Steatorrhea may complicate gastrocolic fistulas, where it may be due to contamination of the high small intestine by colon bacteria. Absorption may also be interfered with as a result of hyperperistalsis or paralytic obstruction. Either extreme in motility prevents absorption, the former because of diminished contact time between contents and absorbing surface; the latter because of increased secretion of intestinal fluid, encouraged by the reversed osmotic relationship between contents and mucosal cells. The diarrhea of partial obstruction is the result of seepage of this overflow through the narrowed lumen. Enteric infection and inflammation inevitably interfere with absorption. The degree is dependent upon the extent and severity of the infection. The resultant diarrhea and impairment of absorption is akin to that following administration of antibiotics. Diarrhea or steatorrhea and impaired absorption lead to multiple vitamin deficiencies. Fat-soluble vitamin deficiency occurs with steatorrhea, but water-soluble vitamin deficiency does not occur unless the diarrhea leads to great water loss. Electrolyte disturbances and weight loss are proportional to the severity and frequency of the watery stools. Potassium and sodium loss in the stools may be great. When dietary or endogenous calcium is excessively excreted with unabsorbed fecal fat, tetany may result. It is not uncommon to find a relatively normal blood calcium level shortly after a tetanic seizure; however, adequate intravenous replacement will usually prevent recurrence of this symptom. Protein depletion may be seen, particularly if the diarrhea extends over several days during which intake has been impaired. Following massive resection of the large and small bowel, physiologic compensation may not be complete for 18 months. 33 The compensatory mechanism is accomplished by villous hypertrophy and delayed motility. In the interim, therapy should consist of intensive efforts to provide all nutrients, utilizing strained and emulsified foods, replacement of lost electrolytes and the administration of anticholinergic drugs to diminish hypermotility. Once oral feedings are permitted, potassium, sodium and calcium usually can be provided by the oral route. Vitamins are best administered by the intramuscular route when deficient absorption is present. EXCRETION
In higher animals and in man excretion is the most important function of the colon. It is a composite mechanism actually involving all other activities of the colon. Integral parts of this function include secretion, motility and a highly developed set of receptor and motor nerve reflexes. The degree to which the intricate coordination of widely disseminated body efforts participate in the act of defecation is exemplified by the characteristic attitude assumed by the dog during defecation. The act represents a progressive,
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combined set of voluntary and involuntary actions, so coordinated and precise in their execution that variations from normalcy can understandably arise from anyone of a large number of possible alterations in the chain of physiologic events. To discuss excretion, therefore, in terms of continence of the sphincteric mechanism only, would be to overlook other equally important contributions. Under conditions of normal stool consistency and normal anal continence, and provided proprioceptive and other reflex mechanisms are normal, the act of defecation is initiated by closure of the glottis. Intrathoracic pressure is increased, causing the diaphragm to descend. The diaphragmatic depression forces the bowel downward and causes the right colon to become globular in shape. Propulsive contractions occur in the cecum and ascending colon, pushing contents into the transverse colon. At the same time mass contractions empty the rectum, pelvic colon and descending colon. The entire colon thus participates in the act of defecation. Material from the more proximal portion takes the place of that expelled from the more distal portion. The urge to defecate is initiated by a wide variety of impulses ranging from psychologic to organic. In addition, a spurious desire to move the bowels may be the result of pressure from external sources on the walls of the rectum, such as from a prostatic tumor, a large bladder calculus, fetal head in the pelvis, rectal tumor, external hemorrhoids, and local inflammatory disease. 34 Restraint of defecation depends upon the combined effects of voluntary and involuntary muscles about the perineum, the levator ani and the coordinated actions of internal and external sphincters. The functions of the rectal valves are said to be prevention of feces from crowding down on the anus, equalization of pressure of the feces that accumulates in the rectum, and to give a spiral motion to movement of the contents. 35 The physiology of anal continence has been the subject of a great deal of controversy for many years. Milligan and Morgan 36 in their classical contributions named three portions of the external sphincter: the subcutaneous external sphincter, superficial external sphincter, and deep external sphincter. In the ensuing paragraphs, the term "external sphincter" applies mainly to the subcutaneous external sphincter, since it is the prime mover of the three components. . Recently, Gaston 37 made a valuable contribution to the understanding of the phenomenon. He considered two types of fecal continence: (1) reservoir continence (previously termed colonic continence), and (2) sphincteric continence. Reservoir continence does not depend upon sphincteric action. The left colon, like other smooth muscle reservoirs, adapts itself to the bulk of its contents up to a given point. Beyond this point the bowel is stimulated to eject the fecal mass. This type of continence is seen in the
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usual sigmoid colostomy, where proper attention to diet and irrigation creates a "habit" type of excretion. Sigmoid colostomies in the perineum may exhibit some degree of continence on this basis. It is probable that in a number of reported series of perineal colostomies, reservoir continence has been erroneously attributed to retained sphincters. Sphincteric continence depends upon the active participation of the anal sphincters in resisting the propulsive force of colonic contractions. To be effective, the sphincteric contractions must exceed the propulsive force of the colon until the mass has reached the sphincteric level. This consideration is important in explaining the relative ineffectiveness of otherwise normal sphincters after anastomosing the ileum (normally not a reservoir organ) to the lower rectum following colectomy.37 Gaston's observations and those of other investigators indicate that nervous reflexes exist between the rectum and internal sphincter, and between the rectum and external sphincter. Denny-Brown and Robertson 38 have shown that voluntary contractions of the anal sphincter have no direct effect on colonic contractions above the rectum. Under normal circumstances, the descent of a fecal mass stimulates receptor units in the lower rectum, causing relaxation of the internal sphincter. Stretching of the internal sphincter stimulates the external sphincter to contract. 37 The internal sphincter reflex is retained following transection of the cord, while the external reflex is destroyed. Therefore, cerebral connections appear necessary for completion of the external sphincter reflex, but not that of the internal sphincter reflex. A tonic external sphincter is retained in 40 to 80 per cent of patients with spinal cord injuries. Incontinence occurs when the stool is soft, but when it is hard, actual obstipation may result. 39 The interdependence between internal and external sphincters has been misunderstood for many years. The closing and opening of the external sphincter must be looked upon as a relative phenomenon. Anal dilation during defecation is not a true relaxation of the sphincter in the sense of losing tone. A toneless external sphincter is incontinent. Rather, the anal dilatation occurring during defecation is a stretching of highly toned muscle fibers by the expulsive force from above, aided by the reflex between internal and external sphincter mechanisms. Defecation, then, can be said to take place against the resistance of a contracted external sphincter. The distal fourth of the rectum must be preserved to retain true continence. This appears to be necessary because of the need for proprioceptive receptors in that area to set up the internal-external sphincter reflex. Surgeons who have not followed this principle in the performance of low resections have had to contend with an incontinent patient until reservoir continence supervened. Preservation of the external sphincter and its motor nerve supply is
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no guarantee of continence. If less than the distal fourth of the rectum (approximately 3 cm.) is preserved the bowel content escapes before there is any warning that escape is imminent; there is no reflex impulse transmitted under these circumstances to the external sphincter to increase its tone. Furthermore, injury to or interference with the nerve supply of the external sphincter can result in temporary incontinence in spite of an intact internal sphincter. Such accidents can occur in certain perineal and rectal operations since the inferior hemorrhoidal nerves are closely applied to the inferior surfaces of the levator ani muscle. Temporary incontinence (lasting four months) has been known to follow undercutting operations for pruritus ani. Here the mechanism is probably associated with loss of proprioception. Only if the subcutaneous external sphincter is divided in the posterior midline (posterior sphincterotomy) can continence be preserved; cutting the external sphincter in any other area of its circumference will lead to temporary incontinence. This is due to the support afforded the cut fibers by the posterior median raphe, whereas the remainder of the circumference is relatively unsupported. SUMMARY
Four fundamental functions of the colon are discussed from the standpoint of surgical physiology. These are: motility, digestion, absorption and excretion. It is hoped that a review of this type may lessen the distance between the experimental laboratory and operating room. REFERENCES 1. Adler, H. F., Atkinson, A. J. and Ivy, A. C.: Am. J. Dig. Dis. 8: 197,1941. 2. Code, C. F., Hightower, N. C. Jr. and Morlock, C. G.: Am. J. Med.13: 328,1952. 3. Spriggs, E. A., Code, C. F., Bargen, J. A., Curtiss, R. K and Hightower, N. C. Jr.: Gastroenterology 19: 480, 1951. 4. Weintraub, S.: Ann. New York Acad. Sc. 58: 345,1954. 5. Garry, R. C.: Physiol. Rev. 14: 103, 1934. 6. Youmans, W. B.: Am. J. Med. 13: 209,1952. 7. Koelle, G. B.: Ann. New York Acad. Sc. 58: 307, 1954. 8. Feldberg, W. and Lin, R. C. Y.: J. Physiol. 109: 475, 1949. 9. Koelle, G. B.: J. Pharmacol. & Exper. Ther. 103: 153, 1951. 10. Burn, J. H., Kordik, P. and Prole, R. H.: Brit. J. Pharmacol. 7: 58, 1952. 11. Blaschko, H., Richter, D. and Schlossman, H.: Biochem. J. 31: 2187,1937. 12. von Euler, U. S. and Gaddum, J. H.: J. Physiol. 72: 74, 1931. 13. Douglas, W. W., Feldberg, W., Paton, W. D. M. and Schachter, M.: J. Physiol. 115: 163, 1951. 14. Pernow, B.: Acta physiol. Scandinav. 24: 97, 1951. 15. Feldberg, W. and Toh, C. C.: J. Physiol. 119: 352,1953. 16. Tittel, K: Wien. klin. Wchschr. 14: 903, 1901. Quoted by Koelle. 7 17. Ehrenpreis, T.: Acta clin. Scandinav. 94 (Suppl. 112): 1, 1946. 18. Swenson, A., Rheinlander, H. F. and Diamond, 1.: New England J. Med. 241: 551, 1949. 19. Kamijo, K, Hiatt, R. B. and Koelle, G. B.: Gastroenterology 24: 173, 1953. 20. Quigley, J. P.: Ann. New York Acad. Sc. 58: 297,1954. 21. Almy, T. P., Kern, F. and Tulin, M.: Gastroenterology 12: 425, 1949.
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22. Quigley, J. P., Bavor, H., Read, M. R. and Brofman, B.: J. Clin. Investigation 22: 839, 1943. 23. Steinhaus, A. H.: Proc. Soc. Exper. BioI. & Med. 25: 599,1928. 24. Ivy, A. C. and Goldman, L.: J.A.M.A. 113: 2413,1939. 25. Paine, J. R.: Surgery 36: 850, 1954. 26. Cooper, E. A.: J. Hygiene 14: 12, 1914. 27. Elvehjem, C. A.: Fed. Proc. 7: 410,1948. 28. Hutchings, 1. J.: Nutritional Observatory 10: 45, 1949. 29. Schweigert, quoted by Elvehjem,21 30. Turell, R. and Maynard, A. deL.: J.A.M.A. 156: 217, 1954. 31. Fairlie, C. W. and Kendall, R. E.: J.A.M.A. 153: 90, 1953. 32. Prohaska, J. v., Govostis, M. C. and Taubenhaus, M. T.: J.A.M.A.154: 320-323, 1954. 33. Turner, D. A.: Internat. Forum 2: 224, 1954. 34. Rankin, F. W., Bargen, J. A. and Buie, L. A.: The Colon, Rectum and Anus. Philadelphia, W. B. Saunders Co., 1932. 35. Pennington, J. R.: A Treatise on Diseases and Injuries of the Rectum, Anus and Pelvic Colon. Philadelphia, P. Blakiston's Son & Co., 1923. 36. Milligan, E. T. C. and Morgan, C. N.: Lancet 2: 1150 and 1213,1934. 37. Gaston, E. A.: Surg., Gynec. & Obst. 87: 280-290 and 669-678, 1948. 38. Quoted by Rankin, et al. 34 39. Davis, L.: A.M.A. Arch. Surg. 69: 488-495, 1954. 720 N. Michigan Avenue Chicago 11, Illinois
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The Surgical Physiology of the Colon HAROLD LAUFlVIA;,\, PH.D., :M.D., F.A.C.S.*
THIS discussion will review the surgical significance of four fundamental functions of the colon-motility, digestion, absorption and excretion. MOTILITY
Motility of the human colon has been described in terms of four types of waves, designated types I, II, III and IV.! Type I waves are probably very small contractions of the muscularis mucosae the function of "'hich is unknown. They may represent normal tonus. Type II waves are of greater duration and amplitude than type I ''laves, lasting 20 to 30 seconds in the sigmoid colon. Their pressure is less in the distal colon than in the proximal colon. In normal persons type II waves generally constitute more than 90 per cent of the recorded activity.2 These waves probably account for the haustral contractions, and their function appears to be that of mixing rather than propelling. Type III waves are complex, long-lasting (about one minute) and seldom-occurring. They probably aid absorption by increasing intraluminal pressure. Type IV waves are simple, large waves, without the secondary small movements seen superimposed on type III waves. Type IV waves are definitely propulsive, but do not possess the progressive quality of peristaltic movements, tending to occur simultaneously in the proximal and distal colons. 3 These waves are regular, occurring every three to four minutes and diminishing in rate when the bowel is emptied. In ulcerative colitis, over-all activity is reduced. Balloon studies 2 indicate that these patients actually do not have "too much motility," but rather the motility is decreased. However, roentgenologically, spasm of the sigmoid is encountered in most of the functional disorders of the colon, such as chronic constipation, chronic spastic colitis, and mucous colitis. It is also present in the inflammatory lesions, such as diverticulitis and ulcerative colitis. 4 Garry 5 and Y oumans 6 have reviewed the known data on the neural regulation of motor patterns of the bowel. Stimulation of the parasympathetic nerves or the administration of acetylcholine or related drugs generally leads to an increase in propulsive activity of the colon and a
* Associate
Professor of Surgery, Northwestern University Medical School, Chicago.
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decrease in mlxmg activity, as well as a decrease in the tone of the ileocecal and internal anal sphincters. Sympathetic and parasympathetic denervation theoretically produce the opposite effects from those of stimulation of the same outflows. Koelle 7 has suggested, however, that the state of activity of the bowel at the time when nerves are stimulated or cut determines, to a great extent, the type of response both qualitatively and quantitatively. Despite these effects, a "considerable degree of normal function is retained or regained following partial or complete extrinsic denervation."7 These conclusions, derived experimentally, have been borne out clinically in several instances, such as in the failure of sympathectoniy to yield lasting results in congenital megacolon; the lack of permanent results following vagotomy for ulcerative colitis; the impermanence of sacral parasympathectomy in the treatment of ulcerative colitis. Certain humoral agents, recently reviewed by Koelle,7 appear to have specific functions in the nerve-muscle mechanism relating to motility. Acetylcholine, a mediator of either excitatory or inhibitory responses, is synthesized by ganglionic cells of the intrinsic plexuses of the bowel wall, as well as by the interstitial cells. 8, 9 Cholinesterase is an enzyme present in the membranes of most of the ganglion cells and nerve fibers of the myenteric and submucosal plexuses. Its primary function is presumably the hydrolysis of acetylcholine. lo Epinephrine and norepinephrine exert predominantly inhibitory action on the gastrointestinal tract, with the exception of the sphincters. These mediators or transmitting agents are inactivated at significant rates by certain mammalian enzymes, such as monoamine oxidase. l l Substance P is probably a mediator in the muscularis mucosae.1 2 In animals, the highest concentrations of the substance occur in the duodenum, jejunum, colon and rectum. 13 ,14 Histamine is present throughout the gastrointestinal tract, particularly in the muscularis mucosae. Despite the emphasis given this substance in the past, it probably has no neurohumeral function. 7 Enteramine is concentrated mainly in the glandular mucosa. IS Its function has not been elucidated. One of the most intriguing defects in motility encountered by the surgeon is that seen in congenital megacolon, It is characterized by spasm of the sigmoid or rectosigmoid colon and marked dilation and hypertrophy of the segment proximal to the spastic area. In 1901, TitteP6 first noted the complete absence of ganglion cells from the myenteric plexus of the spastic portion. In the same region there are numerous thick, closely packed bundles of nonmyelinated nerve fibers. In 1946, Ehrenpreis I7 suggested that the lack of propulsive peristalsis in the spastic segment was due to the agenesis of the ganglion cells, and that the dilatation of the proximal segment was secondarily compensatory. In 1949 Swenson, Rheinlander and Diamond I8 reported that resection of the spastic segment is frequently followed by normal appearance and
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function of the previously dilated colon. Kamijo, Hiatt and Koelle 19 recently studied the cholinesterase content of excised surgical specimens from cases of congenital megacolon. They formulated the hypothesis that the basic defect in the spastic segment is an absence of adrenergic neurons rather than an absence of cholinergic neurons. Diminutions in normal motility may be protective in nature, and follow peritoneal irritation of any type. The "silent belly" of peritonitis is well known in diagnosis. The "splinting" of the area immediately adjacent to an anastomosis is a similar phenomenon more locally confined. Although a low degree of motility may occur above and below the spastic, splinted area, the ability of the colon to participate in so-called "mass contractions" is recovered only after the local tissue reaction and localized peritonitis become lessened. A greatly distended bowel usually has diminished or absent motility. Noxious stimuli such as trauma (including external blunt trauma), electrical stimulation, and extremes of heat or cold may inhibit colonic motility if severe, but may increase motility if milder. Distention of the colon with water, saline or soapsuds first inhibits, then augments motility. Mechanical irritation or electrical stimulation of the anal sphincter area increases local tone and motility, but depresses the activity and tone of the proximal colon. 20 Stress reactions, including exposure to cold, pain, hypoglycemia or worry tend to augment colonic tone. 21 Following bowel resection, early oral feeding is tolerated poorly. Postsurgical "splinting" of the bowel and the resultant retarded evacuation of the colon results in delayed gastric emptying which can occur in the absence of pylorospasm. 22 Furthermore, jejunal peristalsis may be inhibited by colonic irritation. 23 Ivy and associates 24 observed that constipation, irritation of the colon, or stimulation of the nerves from the colon inhibits the flow of bile in the dog. Alterations in colon motility are usually accompanied by alterations in mucus secretion of the colon mucosa. Under normal circumstances mucus protects the mucosa against mechanical injury by reducing friction, and by diluting or buffering the chemical substances which may pass through the colon. Postoperative gastric suction is usually desirable after colon surgery. The prevention of distention will tend to reduce the incidence of postoperative obstructions due to adhesions,25 and will permit earlier resumption of peristalsis. DIGESTION
The colon is not ordinarily considered a digestive organ; yet it is the only portion of the digestive tract in which cellulose and connective tissue of the diet are digested. According to Quigley,20 no enzyme is produced by the digestive tract which acts on cellulose and connective tissue, even in such forms of life as the termite, whose diet consists largely of cellulose.
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Cellulose is digested by the bacteria in the ileum, cecum and proximal colon where bacteria are in abundance and where they digest the cellulose and liberate food substances. It is from the action of bacteria on cellulose that the body derives a wide variety of vitamin substances, such as vitamin K, vitamin B I2, biotin, niacin, thiamine and riboflavin. In addition, indole, skatol and various gases are produced by this bacterial action. Cooper in 191426 was apparently the first to suggest actual synthesis of vitamins by intestinal flora. It is probable that most animals, particularly human beings, rarely eat a completely balanced diet, and therefore must depend upon intestinal organisms for synthesis of the missing; vitamin factors. The importance of intestinal flora in nutrition is unquestioned. "Certainly the quantitative requirement of many of the vitamins, some of the amino acids and perhaps some of the fatty acids is directly dependent upon the intestinal bacteria, and indirectly the microflora is probably related to the requirement of practically all nutrients."27 It appears that the vitamin-producing efficiency of intestinal bacteria is somewhat inversely related to the adequacy of vitamin intake. Thus, when certain vitamin components are absent from the diet, they are produced in the bowel. Conversely, when the diet is adequate in vitamins, they are less likely to be synthesized. 28 This mechanism is, of course, subject to the nature of the ingested nutrients. For example, certain carbohydrates are more favorable to vitamin synthesis than are others. High fat rations are known to decrease the production of riboflavin. 27 The effect of the poorly absorbed sulfa drugs and of antibiotics upon bacterial growth in the bowel has formed the basis for one of the greatest advances in bowel surgery. Sterilization of the bowel has made it possible to perform primary anastomosis anywhere in the colon. Yet we must not lose sight of the collateral effects of such bowel preparation. Actually, some of the best evidence for intestinal synthesis of vitamins was obtained 29 when succinylsulfathiazole or phthalylsulfathiazole was added to the diet of rats, resulting in the development of folic acid and biotin deficiencies. The precise role of the antibiotics on interference with vitamin formation remains to be assessed. 30 Most of the other complications following antibiotic use are now generally appreciated by surgeons. In the days of the five to seven day preoperative preparation of the bowel with sulfonamides, there often resulted a sufficient decrease in vitamin K production to cause an increased bleeding tendency. This was usually corrected by the co-administration of synthetic vitamin K. Now that shortacting antibiotics have replaced sulfonamides almost exclusively for preoperative bowel preparation, other complications have been noted. The most serious complication is micrococcic enteritis, due either to the overgrowth of antibiotic-resistant micrococci or that of yeast or
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yeastlike organisms. 30 Fairlie and Kenda1l 3! believe the phenomenon is more than merely an overgrowth, and that a direct stimulation of the staphylococcus by antibiotics must be considered. The severely debilitating effects of postantibiotic diarrhea, particularly when it occurs in the postoperative patient, are often fatal. Recently, van Prohaska32 has reported encouraging results in some of these patients from the use of ACTH. Anal pruritus is a common complication following oral wide-spectrum antibiotics. It may be very mild and self-limited, or it may be severe enough to require such measures as ACTH or cortisone. Some instances are intractable to all forms of treatment.30 ABSORPTION
The proximal, or absorbing colon, absorbs significant amounts of water and salts, while the distal, or storage colon, absorbs very little. It has been estimated 20 that of the 620 cc. of water discharged daily from ileum to colon, 500 cc. is absorbed, leaving 120 cc. in the feces. In the absence of this absorbing mechanism, as for example when an ileostomy is present, the entire water content of the ileal fecal stream is lost to the outside, leading to dehydration, until the ileum adjusts to a greater water-absorbing role. The solid residue of the feces is composed of approximately one-third bacteria, the remainder consisting of bile pigment, mucin and cellular debris. Two to 3 per cent is nitrogenous, 10 to 20 per cent is fat, and 10 to 20 per cent inorganic material. Most of the bacteria are discharged dead. The fat consists of split and unsplit fat, the split portion coming from the unabsorbed fatty acids of the diet. The neutral fat is derived from bacteria and epithelial cell debris. Many factors affect absorption from the intestine. These include pH, motility, condition of the mucosa, the presence and action of bacteria, hormones and vitamins, and certain disease conditions, as well as variations imposed by surgery.33 Whereas normal man absorbs at least 90 per cent of his daily fat intake, steatorrhea results when 85 per cent or less of the dietary fat is absorbed. 33 It behooves the surgeon to keep in mind some of the postsurgical lesions which may lead to this condition. Following pancreatectomy the absence of the normal discharge of pancreatic enzymes into the intestine results in undigested and unabsorbed foodstuffs reaching the expelled stool. Severe steatorrhea may follow any of a wide variety of surgical procedures affecting continuity and motility of the gastrointestinal tract. It may follow total or subtotal gastrectomy in which a jejunal anastomosis has been made; sidetracking operations, such as ileotransverse colostomy or long-step enteroenterostomy; massive resection of proximal colon or small intestine with resultant decrease in absorptive surface, and as a temporary complication of ileostomy.
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Steatorrhea may complicate gastrocolic fistulas, where it may be due to contamination of the high small intestine by colon bacteria. Absorption may also be interfered with as a result of hyperperistalsis or paralytic obstruction. Either extreme in motility prevents absorption, the former because of diminished contact time between contents and absorbing surface; the latter because of increased secretion of intestinal fluid, encouraged by the reversed osmotic relationship between contents and mucosal cells. The diarrhea of partial obstruction is the result of seepage of this overflow through the narrowed lumen. Enteric infection and inflammation inevitably interfere with absorption. The degree is dependent upon the extent and severity of the infection. The resultant diarrhea and impairment of absorption is akin to that following administration of antibiotics. Diarrhea or steatorrhea and impaired absorption lead to multiple vitamin deficiencies. Fat-soluble vitamin deficiency occurs with steatorrhea, but water-soluble vitamin deficiency does not occur unless the diarrhea leads to great water loss. Electrolyte disturbances and weight loss are proportional to the severity and frequency of the watery stools. Potassium and sodium loss in the stools may be great. When dietary or endogenous calcium is excessively excreted with unabsorbed fecal fat, tetany may result. It is not uncommon to find a relatively normal blood calcium level shortly after a tetanic seizure; however, adequate intravenous replacement will usually prevent recurrence of this symptom. Protein depletion may be seen, particularly if the diarrhea extends over several days during which intake has been impaired. Following massive resection of the large and small bowel, physiologic compensation may not be complete for 18 months. 33 The compensatory mechanism is accomplished by villous hypertrophy and delayed motility. In the interim, therapy should consist of intensive efforts to provide all nutrients, utilizing strained and emulsified foods, replacement of lost electrolytes and the administration of anticholinergic drugs to diminish hypermotility. Once oral feedings are permitted, potassium, sodium and calcium usually can be provided by the oral route. Vitamins are best administered by the intramuscular route when deficient absorption is present. EXCRETION
In higher animals and in man excretion is the most important function of the colon. It is a composite mechanism actually involving all other activities of the colon. Integral parts of this function include secretion, motility and a highly developed set of receptor and motor nerve reflexes. The degree to which the intricate coordination of widely disseminated body efforts participate in the act of defecation is exemplified by the characteristic attitude assumed by the dog during defecation. The act represents a progressive,
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combined set of voluntary and involuntary actions, so coordinated and precise in their execution that variations from normalcy can understandably arise from anyone of a large number of possible alterations in the chain of physiologic events. To discuss excretion, therefore, in terms of continence of the sphincteric mechanism only, would be to overlook other equally important contributions. Under conditions of normal stool consistency and normal anal continence, and provided proprioceptive and other reflex mechanisms are normal, the act of defecation is initiated by closure of the glottis. Intrathoracic pressure is increased, causing the diaphragm to descend. The diaphragmatic depression forces the bowel downward and causes the right colon to become globular in shape. Propulsive contractions occur in the cecum and ascending colon, pushing contents into the transverse colon. At the same time mass contractions empty the rectum, pelvic colon and descending colon. The entire colon thus participates in the act of defecation. Material from the more proximal portion takes the place of that expelled from the more distal portion. The urge to defecate is initiated by a wide variety of impulses ranging from psychologic to organic. In addition, a spurious desire to move the bowels may be the result of pressure from external sources on the walls of the rectum, such as from a prostatic tumor, a large bladder calculus, fetal head in the pelvis, rectal tumor, external hemorrhoids, and local inflammatory disease. 34 Restraint of defecation depends upon the combined effects of voluntary and involuntary muscles about the perineum, the levator ani and the coordinated actions of internal and external sphincters. The functions of the rectal valves are said to be prevention of feces from crowding down on the anus, equalization of pressure of the feces that accumulates in the rectum, and to give a spiral motion to movement of the contents. 35 The physiology of anal continence has been the subject of a great deal of controversy for many years. Milligan and Morgan 36 in their classical contributions named three portions of the external sphincter: the subcutaneous external sphincter, superficial external sphincter, and deep external sphincter. In the ensuing paragraphs, the term "external sphincter" applies mainly to the subcutaneous external sphincter, since it is the prime mover of the three components. . Recently, Gaston 37 made a valuable contribution to the understanding of the phenomenon. He considered two types of fecal continence: (1) reservoir continence (previously termed colonic continence), and (2) sphincteric continence. Reservoir continence does not depend upon sphincteric action. The left colon, like other smooth muscle reservoirs, adapts itself to the bulk of its contents up to a given point. Beyond this point the bowel is stimulated to eject the fecal mass. This type of continence is seen in the
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usual sigmoid colostomy, where proper attention to diet and irrigation creates a "habit" type of excretion. Sigmoid colostomies in the perineum may exhibit some degree of continence on this basis. It is probable that in a number of reported series of perineal colostomies, reservoir continence has been erroneously attributed to retained sphincters. Sphincteric continence depends upon the active participation of the anal sphincters in resisting the propulsive force of colonic contractions. To be effective, the sphincteric contractions must exceed the propulsive force of the colon until the mass has reached the sphincteric level. This consideration is important in explaining the relative ineffectiveness of otherwise normal sphincters after anastomosing the ileum (normally not a reservoir organ) to the lower rectum following colectomy.37 Gaston's observations and those of other investigators indicate that nervous reflexes exist between the rectum and internal sphincter, and between the rectum and external sphincter. Denny-Brown and Robertson 38 have shown that voluntary contractions of the anal sphincter have no direct effect on colonic contractions above the rectum. Under normal circumstances, the descent of a fecal mass stimulates receptor units in the lower rectum, causing relaxation of the internal sphincter. Stretching of the internal sphincter stimulates the external sphincter to contract. 37 The internal sphincter reflex is retained following transection of the cord, while the external reflex is destroyed. Therefore, cerebral connections appear necessary for completion of the external sphincter reflex, but not that of the internal sphincter reflex. A tonic external sphincter is retained in 40 to 80 per cent of patients with spinal cord injuries. Incontinence occurs when the stool is soft, but when it is hard, actual obstipation may result. 39 The interdependence between internal and external sphincters has been misunderstood for many years. The closing and opening of the external sphincter must be looked upon as a relative phenomenon. Anal dilation during defecation is not a true relaxation of the sphincter in the sense of losing tone. A toneless external sphincter is incontinent. Rather, the anal dilatation occurring during defecation is a stretching of highly toned muscle fibers by the expulsive force from above, aided by the reflex between internal and external sphincter mechanisms. Defecation, then, can be said to take place against the resistance of a contracted external sphincter. The distal fourth of the rectum must be preserved to retain true continence. This appears to be necessary because of the need for proprioceptive receptors in that area to set up the internal-external sphincter reflex. Surgeons who have not followed this principle in the performance of low resections have had to contend with an incontinent patient until reservoir continence supervened. Preservation of the external sphincter and its motor nerve supply is
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no guarantee of continence. If less than the distal fourth of the rectum (approximately 3 cm.) is preserved the bowel content escapes before there is any warning that escape is imminent; there is no reflex impulse transmitted under these circumstances to the external sphincter to increase its tone. Furthermore, injury to or interference with the nerve supply of the external sphincter can result in temporary incontinence in spite of an intact internal sphincter. Such accidents can occur in certain perineal and rectal operations since the inferior hemorrhoidal nerves are closely applied to the inferior surfaces of the levator ani muscle. Temporary incontinence (lasting four months) has been known to follow undercutting operations for pruritus ani. Here the mechanism is probably associated with loss of proprioception. Only if the subcutaneous external sphincter is divided in the posterior midline (posterior sphincterotomy) can continence be preserved; cutting the external sphincter in any other area of its circumference will lead to temporary incontinence. This is due to the support afforded the cut fibers by the posterior median raphe, whereas the remainder of the circumference is relatively unsupported. SUMMARY
Four fundamental functions of the colon are discussed from the standpoint of surgical physiology. These are: motility, digestion, absorption and excretion. It is hoped that a review of this type may lessen the distance between the experimental laboratory and operating room. REFERENCES 1. Adler, H. F., Atkinson, A. J. and Ivy, A. C.: Am. J. Dig. Dis. 8: 197,1941. 2. Code, C. F., Hightower, N. C. Jr. and Morlock, C. G.: Am. J. Med.13: 328,1952. 3. Spriggs, E. A., Code, C. F., Bargen, J. A., Curtiss, R. K and Hightower, N. C. Jr.: Gastroenterology 19: 480, 1951. 4. Weintraub, S.: Ann. New York Acad. Sc. 58: 345,1954. 5. Garry, R. C.: Physiol. Rev. 14: 103, 1934. 6. Youmans, W. B.: Am. J. Med. 13: 209,1952. 7. Koelle, G. B.: Ann. New York Acad. Sc. 58: 307, 1954. 8. Feldberg, W. and Lin, R. C. Y.: J. Physiol. 109: 475, 1949. 9. Koelle, G. B.: J. Pharmacol. & Exper. Ther. 103: 153, 1951. 10. Burn, J. H., Kordik, P. and Prole, R. H.: Brit. J. Pharmacol. 7: 58, 1952. 11. Blaschko, H., Richter, D. and Schlossman, H.: Biochem. J. 31: 2187,1937. 12. von Euler, U. S. and Gaddum, J. H.: J. Physiol. 72: 74, 1931. 13. Douglas, W. W., Feldberg, W., Paton, W. D. M. and Schachter, M.: J. Physiol. 115: 163, 1951. 14. Pernow, B.: Acta physiol. Scandinav. 24: 97, 1951. 15. Feldberg, W. and Toh, C. C.: J. Physiol. 119: 352,1953. 16. Tittel, K: Wien. klin. Wchschr. 14: 903, 1901. Quoted by Koelle. 7 17. Ehrenpreis, T.: Acta clin. Scandinav. 94 (Suppl. 112): 1, 1946. 18. Swenson, A., Rheinlander, H. F. and Diamond, 1.: New England J. Med. 241: 551, 1949. 19. Kamijo, K, Hiatt, R. B. and Koelle, G. B.: Gastroenterology 24: 173, 1953. 20. Quigley, J. P.: Ann. New York Acad. Sc. 58: 297,1954. 21. Almy, T. P., Kern, F. and Tulin, M.: Gastroenterology 12: 425, 1949.
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22. Quigley, J. P., Bavor, H., Read, M. R. and Brofman, B.: J. Clin. Investigation 22: 839, 1943. 23. Steinhaus, A. H.: Proc. Soc. Exper. BioI. & Med. 25: 599,1928. 24. Ivy, A. C. and Goldman, L.: J.A.M.A. 113: 2413,1939. 25. Paine, J. R.: Surgery 36: 850, 1954. 26. Cooper, E. A.: J. Hygiene 14: 12, 1914. 27. Elvehjem, C. A.: Fed. Proc. 7: 410,1948. 28. Hutchings, 1. J.: Nutritional Observatory 10: 45, 1949. 29. Schweigert, quoted by Elvehjem,21 30. Turell, R. and Maynard, A. deL.: J.A.M.A. 156: 217, 1954. 31. Fairlie, C. W. and Kendall, R. E.: J.A.M.A. 153: 90, 1953. 32. Prohaska, J. v., Govostis, M. C. and Taubenhaus, M. T.: J.A.M.A.154: 320-323, 1954. 33. Turner, D. A.: Internat. Forum 2: 224, 1954. 34. Rankin, F. W., Bargen, J. A. and Buie, L. A.: The Colon, Rectum and Anus. Philadelphia, W. B. Saunders Co., 1932. 35. Pennington, J. R.: A Treatise on Diseases and Injuries of the Rectum, Anus and Pelvic Colon. Philadelphia, P. Blakiston's Son & Co., 1923. 36. Milligan, E. T. C. and Morgan, C. N.: Lancet 2: 1150 and 1213,1934. 37. Gaston, E. A.: Surg., Gynec. & Obst. 87: 280-290 and 669-678, 1948. 38. Quoted by Rankin, et al. 34 39. Davis, L.: A.M.A. Arch. Surg. 69: 488-495, 1954. 720 N. Michigan Avenue Chicago 11, Illinois