Topographic Anatomy

The cecum and colon of dogs and cats are clearly recognizable within the abdomen. Although frequently described as the first part of the large intestine, the cecum in dogs⁶⁶ and cats⁶¹ is a true diverticulum that connects to the proximal colon. Whereas the cecum is relatively long and spiraled in dogs, it is short and comma shaped in cats⁶¹ (Figure 93-1). It usually lies in a caudoventral direction or may be positioned transversely. The cecocolic orifice is approximately 1 cm distal to the ileocolic orifice in the dog, and it is adjacent to the ileocolic orifice in cats. The cecum is attached to the antimesenteric border of the ileum in dogs with the antimesenteric ileal vessels arising from the single or double ileocecal fold.

The colon is usually paler in color than the rest of the intestines and is readily identified by its position relative to the cecum and rectum and the fact that it is usually of greater diameter and is seen to be feces filled. Grossly, there are three distinct parts to the colon: ascending, transverse, and descending. The length and position of the ascending colon vary greatly; in general, however, the ascending colon lies on the right side and extends approximately 5 cm cranially from the ileocolic orifice to the right colic flexure, where it becomes the transverse colon. Ventrally, the ascending colon is covered by the small intestine. It is bounded by the descending duodenum on the right and lies ventral to the right limb of the pancreas, mesoduodenum, and right kidney. The ascending colon is relatively fixed in its position by its attachments to mesoduodenum and mesocolon. The mesocolon is very short at its point of origin (ileocecolic junction), lengthening to 2 to 3 cm at the level of the right colic flexure.

The transverse colon lies cranial to the cranial mesenteric artery and root of the mesentery and passes from right to left, from the right colic flexure of the ascending to the descending colon at the left colic flexure. It lies caudodorsal to the stomach and caudoventral to the left limb of the pancreas and is tethered by the mesocolon, which is about 3 cm in length in dogs.

The longest part of the colon is the descending colon, which extends from the left colic flexure to the pelvic inlet; it is contiguous with the rectum and anatomically indistinguishable. Cranially, the descending colon is in contact with the left kidney. The left ureter lies dorsal to the medial border of the colon; however, caudally, the ureter traverses obliquely and dorsally over the colon and then lies lateral to it as the ureter enters the bladder. The caudal aspect of the descending colon lies dorsal to and in contact with the uterus or prostate. The duodenocolic ligament, which is very short, joins the descending colon to the ascending duodenum. Identifying the descending colon and its associated mesentery greatly facilitates exploratory celiotomy because the long descending mesocolon is the most dorsally located. Grasping the descending colon (colonic maneuver) allows the intestines to be retracted to the right to expose the left sublumbar fossa.

Vasculature, Lymphatics, and Nerves

The bulk of the colon receives its blood supply initially via the cranial mesenteric artery. This branches as the common colic artery, which further subdivides to supply the cecum (ileocolic artery), ascending colon (ileocolic artery proximally and right colic artery distally), transverse colon (right colic artery proximally and middle colic artery), and proximal half of the descending colon (middle colic artery). The distal half of the descending colon is supplied by the left colic branch of the caudal mesenteric artery, with the most distal portion supplied by the cranial rectal artery as it courses along the mesenteric border to the rectum (Figure 93-2).

The arteries connect to the colon via the vasa recti, which are short, irregular branches that bifurcate upon entering the intestine and penetrate the muscular layer in the antimesenteric portion. There are large numbers of anastomoses along the colon’s mesenteric border. The colon contains two arterial networks: subserous and mural. The latter is formed by direct and plexiform anastomoses and lies predominantly within the submucosa.

Venous drainage of the cecum and colon eventually enters the portal vein. Caudally, the left colic vein courses from the distal descending colon to the caudal mesenteric vein, acquiring its tributaries, including the middle colic vein, along the way before inserting on the portal vein. The ileocolic vein arises from the cecal vein and right colic vein and is joined by the middle colic vein about 1 cm before it enters the portal vein.

Serous membranes have a very rich network of lymphatic capillaries (lacteals) that play an important role in reabsorption of serous fluid from the body cavities. Subserous and submucosal lymphatic plexuses are present in the digestive tract, although their arrangement is different in various segments of the digestive tract.91,194 Colonic afferent lacteals drain into the right, middle, and left colic lymph nodes (Figure 93-3).

Autonomic innervation to the colon is from the cranial and caudal mesenteric plexuses, which travel with the mesenteric vasculature to the intestine (Table 93-1).

Microscopic Structure

As with the small intestine, colonic muscle and mucosal layers are relatively thick and identifiable by ultrasonography.¹⁵⁹ Colonic layers, from inside to out, include mucosa, submucosa, muscularis, and serosal layers. Colonic mucosa is composed of columnar and cuboidal epithelial cells arranged in parallel crypts and interspersed with numerous goblet cells. A third morphologically distinct cell type, enterochromaffin cells, accounts for approximately 5% of the cellular population. Colonic mucosa differs significantly from small intestinal mucosa in that there are no villi or aggregated lymph nodules. Instead, relatively large, elevated solitary lymphoglandular complexes, through which the colonic glands discharge, are found within the mucosa. These are approximately 3 mm in diameter; in cats, they are only found within the cecum.

Within the lamina propria is a double layer of lymphatic channels—one near the mucosal surface and the second just above the muscularis mucosae. Some lymphatics penetrate into the submucosa; these have prominent valves and form collecting lymphatic trunks that arise parallel to blood vessels.⁹²

The submucosa is the supporting layer of the colon (Figure 93-4). In addition to its connective tissue, the submucosa has a rich supply of nerve vessels and lymphatics running through it. The muscularis is a double layer composed of an inner circular layer and outer longitudinal layer of smooth muscle. The serosa is connective tissue covered by a mesothelial layer, the visceral peritoneum, which is a continuation and reflection of the parietal peritoneum.

Electrolyte Transport

Colonic mucosal epithelium is a typical electrolyte-transporting epithelium, being able to move large quantities of water and sodium and chloride ions from the luminal side to the vascular side and vice versa (Figure 93-5). Electrical gradients are used as driving forces for this salt and solute transport mechanism across cells, and the gradients are established by the basolateral sodium pump (Na⁺, K⁺, ATP-ase) and apical brush border K⁺ selective ion channels, which hyperpolarize the plasma membrane, allowing electrically driven transport to occur.

To maintain physiologic excretion of sodium chloride into the feces, under physiologic conditions, the colon absorbs up to 1.5 L/d of fluid. The mechanism of ion transport in the colon has been recognized for decades,48,88,118 but it is only more recently that the responsible transport proteins have been identified. Within either the apical (luminal) or basolateral cell membrane, colonic epithelial cells have a number of ion channels, carriers, and pumps that allow the transport system to work efficiently. Colonic absorption of solutes may occur by either electroneutral or electrogenic pathways. The proportion of each appears to be species specific, and further research is required to identify the ratio in the dog and cat. The ratio would also seem to vary with hormonal influence on the epithelium; for instance, aldosterone increases the activity of amiloride-sensitive Na⁺ channels. The result of this regulatory ion transport mechanism is the net absorption of electrolytes under normal physiologic conditions. However, colonocytes are able to switch from absorption to secretion when stimulated by secretagogues. Disruption of this balance of ion transport by disease can either lead to net secretion and diarrhea or excessive absorption and constipation.

As mentioned above, solute absorption is either electrogenic via sodium channels or electroneutral via Na/H and Cl/HCO₃⁻ exchange. The majority of salt absorption is via the electroneutral pathway. The colon has three types of Na/H exchangers within the cell membranes: Na/H exchanger-1 in the basolateral membrane and Na/H exchanger-2 and Na/H exchanger-3 in the apical membrane. The function of the Na/H exchangers appears to be tightly linked to Cl/HCO₃⁻ exchange; additionally, some recent evidence suggests that cystic fibrosis transmembrane regulator and Na/H exchanger regulatory factor may influence the exchange process. Three anion exchangers have also been identified (two in the apical membrane and one in the basolateral) and are influenced by cystic fibrosis transmembrane regulator.

Enhanced Na⁺ uptake is via the electrogenic route, with electrogenic via sodium channels protein channels localized in the apical membrane of colonocytes. The driving force for Na⁺ uptake via electrogenic via sodium channels results from the electrochemical Na⁺ gradient combined with negative membrane voltage. Na⁺ uptake is mirrored by Cl⁻ absorption through the apical Cl⁻ channels and via paracellular transport. Na⁺ is then passed out of the cell by the Na⁺, K⁺, and ATP-ase in the basolateral membrane. This net Na⁺ absorption is matched by Cl⁻ passing through the basolateral membrane, either via Cl⁻ channels or Cl/HCO₃^– exchange. Creating such an NaCl gradient leads to parallel water absorption; as noted above, the exact mechanism has yet to be elucidated, although the majority may occur via paracellular shunts rather than transcellularly via aquaporins. Electrogenic via sodium channels activity is enhanced by aldosterone and can be modulated by interaction with the cystic fibrosis transmembrane regulator ion channel.

Water Transport

Net movement of water across the colon is osmotically driven by active absorption and secretion and occurs via paracellular and transepithelial transport routes.¹⁸⁸ The proportion of water transport that occurs via the paracellular route, and how much is transported via epithelial cells is uncertain.¹⁸⁸ Water channel proteins aquaporins have recently been identified; it is postulated that the presence of the isoform aquaporin-4 in the basolateral membrane of colonocytes may play an important role in fluid absorption.^88,118,130 It is, however, uncertain if the aquaporin water channels are essential for colonic water absorption. It has also been suggested that the cystic fibrosis transmembrane regulator Cl⁻ selective channel has an impact on water transport; this role is currently controversial and remains to be convincingly demonstrated. Although it has been unclear how water is absorbed against the high osmotic gradient produced by high effective osmolality of feces, the recent recognition that active fluid absorption can occur in the crypts makes it easier to reconcile this fact.

Secretion

Absorption is closely balanced by secretion of electrolytes, ensuring maintenance of homeostasis. Secretion of electrolytes has also been postulated to aid in transport of mucus and maintain its hydration status. Mucus is a key macromolecule that creates a local microclimate, ensuring protection of epithelial cells from abrasion and bacterial invasion. Goblet and columnar epithelial cells secrete mucus of differing composition. The cystic fibrosis transmembrane regulator ion channel plays a key role in regulating mucus secretion. Maintaining secretion requires ion uptake by the basolateral membrane to be at such a rate that matches any increase in apical exit to ensure that the internal cellular milieu is kept constant. This essential homeostatic step is maintained by the Na⁺ 2Cl K cotransporter type 1 protein in the basolateral membrane. This ion channel has its enhanced activity triggered by lowered intracellular Cl⁻ concentration as a result of secretion of Cl⁻ ions at the apical border. It would appear that the majority of apical border Cl⁻ efflux is via the cystic fibrosis transmembrane regulator channel, and messengers such as cyclic adenosine monophosphate, protein kinase A, protein kinase C, calcium/calmodulin-dependent kinase, and a cyclic guanosine monophosphate-dependent kinase increase its activity. Cystic fibrosis transmembrane regulator Cl⁻ efflux is also enhanced by increased intracellular Cl⁻ after Na⁺ 2Cl K cotransporter type 1 channel activation.

Potassium ions are secreted via two types of channel in the apical membrane; channel activity is known to be increased by aldosterone and glucocorticoids. Intracellular potassium levels are maintained by the presence of two potassium channels in the basolateral membrane that are triggered by increases in intracellular Ca²⁺ or cyclic adenosine monophosphate.74,89,171

Absorption and secretion by colonocytes is regulated by a complex interaction of endocrine autocrine, paracrine, and neuronal stimuli. The interaction and interrelationship of the numerous secretagogues involved is complex and outside the scope of this chapter. Any alteration to this essential homeostatic mechanism will lead to either serious excessive secretions, with resultant diarrhea, or excessive absorption and constipation.74,89,118,174

Short-Chain Fatty Acids

Short-chain fatty acids are products of colonic bacterial fermentation of dietary fiber. Short-chain fatty acids are absorbed by colonic epithelium in parallel with NaCl. Short-chain fatty acid are metabolized by colonocytes and have a marked trophic effect on epithelium. The short-chain fatty acids butyrate, acetate, and propionate are absorbed by paracellular paths and by nonionic diffusion. As well as being cellular nutrients, short-chain fatty acids stimulate Na⁺ absorption by a combination of acidification (because of their cationic nature) and activation of apical membrane Na/H. They also stimulate increased HCO₃⁻ production and hence increased Cl⁻ absorption. The increase in secreted HCO₃⁻ is important in the regulation of colonic luminal pH. Short-chain fatty acids are also important in preventing colonic irritation by reducing ionization of bile acids and long-chain fatty acids. Feeding of a nonfermentable fiber source leads to production of less short-chain fatty acids and, because the feces have increased dry matter content, tends to lead to constipation.74,164,169,174

Fecal Storage

The distal colon is the main site for fecal storage in dogs and cats, and its ability to carry out this function has an important role in maintaining fecal continence. Colonic transit is slow to ensure that fecal contents are mixed.90,185 This is achieved by a combination of segmentation and propulsive movement,³¹ and in the proximal colon of cats, by retrograde peristalsis.¹¹⁵ Segmentation is the result of coordinated circular contractions that may move either orally or aborally and is the major movement seen in the midcolon in both the dog and the cat. In the distal colon, motor activity is a combination of segmentation and propulsive aboral peristalsis.^90,185

The major control of motility depends on the colonic wall intrinsic plexuses, which are located between the longitudinal and circular muscle layers (myenteric or Auerbach’) or in the colonic submucosa (submucous or Meissner’ plexus). Whereas parasympathetic innervation via preganglionic vagal and pelvic fibers stimulates colonic motility, sympathetic stimulation via the superior mesenteric plexus, inferior mesenteric plexus, and hypogastric plexus inhibits it.

Immune System

The cecum and colon are well supplied with gut-associated lymphoid tissue. This includes mononuclear cells distributed throughout the large intestinal lamina propria and mononuclear cell aggregates that have follicular and parafollicular zones. Cecal gut-associated lymphoid tissue aggregates in the cecal apex in the cat and at the ileocecal orifice of the dog.⁴⁹

As with the remainder of the gastrointestinal tract, the immune system of the colon has been described as having innate and adaptive components, although immunologists have recently suggested that this is an oversimplification of the immune response, with cells not fitting neatly into such a bimodal model.¹⁶ The defense mechanism of the colon must be able to respond to potentially pathogenic antigens; at the same time, however, it needs to be able to discriminate and not react to the abundance of food and commensal bacterial antigens to which it is exposed. Antigenic stimulus provided by some commensal bacteria is important in modulating the immune response.⁹⁷

As part of the innate system, a major contribution to immunity is the barrier created by colonocytes that prevents interaction between luminal material and cells lining the gut. The epithelium provides impermeability; it rapidly renews, is constantly moving (segmentation and propulsion), and is protected by mucus and a multitude of molecules with antimicrobial activity, such as cryptdins (α-defensins), lysozyme, phospholipases, and chemokines.56,218 This antimicrobial layer aids in reducing bacterial numbers and prevents colonization and mucosal invasion. The barrier’s static response is enhanced by external signals, which induce the increased expression of antimicrobial molecules and mobilization of phagocytic cells.

The adaptive component of the colonic immune system gives a more specific and longer term response in that it has memory, allowing rapid elimination of any pathogen that is re-encountered. Mucosal immunity is compartmentalized,16,17,56 with the mucosa having distinct inductive and effector sites. Key to an effective adaptive response is presentation of the antigen to lymphoid follicles and to specialized sampling cells—microfold cells (M-cells) and dendritic cells (D-cells). Priming of these sampling cells leads to maturation of B- and T-cells that will migrate to the lamina propria, where they function as part of the defense system. Microfold cells of the colon differ from their neighboring colonocytes in that they lack microvilli and membrane-associated hydrolytic enzymes and produce proinflammatory chemokines and cytokines. M-cells move proteins, viruses, bacteria, and noninfectious particles transepithelially to the subepithelial lymphoid cells. The distinctive feature of M-cells is an invagination at the basolateral membrane, forming an intraepithelial pocket where memory T-cells interact with naïve and memory B-cells and D-cells interact with M-cells. After they are activated, D-cells migrate to the mesenteric lymph nodes, where they prime T-helper-1 (Th-1) cells and induce IgG and IgA production by B-cells,^105,152,165 leading to colonic inflammation. D-cells may also penetrate epithelium and directly sample luminal antigens.

A further cell type that is important in the colonic immune system is the intraepithelial lymphocyte. These are lymphocytes that have migrated to above the basement membrane and are found between colonocytes.92,218 They are predominantly effector memory cells with γ and δ T-cell receptor chains, although αβ T-cell receptor cells and those that lack co-receptor expression are also recognized. The unique feature of intraepithelial lymphocyte cells is their ability to express CD8αα, a characteristic of intestinal mucosal T-cells. Intraepithelial lymphocytes are thought to play an important role in epithelial homeostasis, cancer surveillance, and defense against pathogens. Paneth cells that produce antibacterial factors, such as α-defensins, in the epithelial crypts of the small intestine are not found in the colon.^92,218

Stages of Wound Healing

Healing in the colon has been studied extensively and follows the classic phases that have been described for skin, but with some important differences. As noted above, it is important to remember the limitations of many of the studies. The three phases—lag, proliferative, and maturation—are discussed in isolation for simplification; however, there is overlap between each phase to ensure the process occurs efficiently.

Factors That Negatively Affect Wound Healing

Factors that have been shown clinically and experimentally to have a detrimental effect on colonic wound healing are divided into local and systemic categories (Table 93-2). Local factors include hypoperfusion, poor wound apposition, wound tension, infection, and distal obstruction. Systemic influences that negatively affect healing are hypovolemia; recent blood transfusion; icterus; use of chemotherapeutic agents, such as cisplatin; immunodeficiency; and poorly controlled diabetes mellitus. Experimentally, deficiencies in zinc and iron (both co-factors required for protein synthesis) result in reduced fibroblast activity and poor collagen production. Infection leads to prolongation of the lag phase of healing and increased local levels of proteases, which delay reepithelialization and collagen formation. Disease processes, such as diabetes mellitus, hyperadrenocorticism, and hypothyroidism, are known to have profound effects on healing pathways at a cellular level, but their influence on clinical colonic healing is unproven. In a recent human review of anastomosis failure, hyperadrenocorticism and hypothyroidism were found to be nonsignificant variables.⁶⁰

Methods for Improving Colonic Wound Healing

Colonic wound healing may be improved or supported with the use of vascularized tissue wraps, reinforcement with synthetic or biologic materials, or administration of cytokines.

Suture Closure

Staplers

Stapling devices can be used either to form an anastomosis or to close a bowel wound.37,116,205 Options include use of gastrointestinal anastomosis (GIA), thoracoabdominal (TA), end-to-end anastomosis (EEA), or skin staplers. The biggest disincentives to routine use of stapling devices in small animal surgery are cost, lack of experience, and size limitations of the instrument or staples.

GIA staplers create a functional, rather than a true, end-to-end anastomosis with a GIA stapler also requires closure of cut ends of the bowel by hand suturing or use of a suitably sized TA stapler.²⁰⁵ TA staplers have also been used for closure of cecal resection sites in dogs³⁷ and for end-to-end anastomosis of intestines. With the latter technique, an everting anastomosis is performed by firing a TA stapler across one third of the apposed end segments. The process is repeated two more times, with staple lines overlapping at each end to ensure complete apposition. End-to-end anastomosis with a TA stapler is difficult to perform on small-diameter intestine and is therefore rarely used in dogs and cats.

Of greater potential benefit in colonic surgery is the tubular-shaped EEA device, which creates a true inverting anastomosis by placement of a circumferential staggered double row of surgical stainless steel staples. The EEA device can be placed transcecally, through an enterotomy, or transrectally.6,116 Stapled anastomosis with the EEA device is described later in this chapter (see Colectomy).

Experimentally, use of skin staples for small intestinal anastomosis achieved good apposition of intestinal anastomosis.⁴² Anastomosis of large or small intestine with skin staplers has not been described clinically.

Biofragmentable Anastomosis Ring

The biofragmentable anastomosis ring (Valtrac, Covidien Autosuture, Norwalk, CT) is composed of polyglycolic acid and barium sulfate. The technique for colonic anastomosis with a biofragmentable anastomosis ring device is described later in this chapter (see Colectomy). Biofragmentable anastomosis ring anastomosis produces an inverted wound that has a high initial bursting strength that is maintained over a 28-day period.³⁰ Its successful use has been described in normal experimental cats¹⁰³ and clinically for the management of feline idiopathic megacolon.¹⁷³ Serosal tearing appears to be a common occurrence because of the large size of the ring (available sizes are limited) but is readily rectified. The authors also reported that short-term minor complications, such as anemia and anorexia, were more common with biofragmentable anastomosis ring anastomosis than sutured colocolostomy.

Sutureless Closure

Diagnostic Techniques for Large Intestinal Disease

Large intestinal disease presents with clinical signs that include diarrhea, dyschezia, tenesmus, hematochezia, and constipation. The veterinarian should always obtain a complete history and carry out a through clinical examination, including hydration status, mucous membrane color, abdominal palpation, examination of the anal and perineal areas, and digital rectal examination. Basic blood work and urinalysis should be evaluated for signs of systemic disease. Based on initial examination and laboratory findings, further information may be obtained by using radiography, ultrasonography, advanced imaging (computed tomography [CT] or magnetic resonance imaging [MRI]), and flexible (colonoscopy), or rigid endoscopy (proctoscopy) of the lower gastrointestinal tract.

Preoperative Preparation of the Colon

Preparation of the colon in dogs and cats is controversial: some authors advocate preoperative cleansing, but others suggest that there is no need for any preparation.⁹⁶ The rationale for cleansing has been extrapolated from colonic surgery in humans, in whom reduction of bacterial numbers by preoperative oral antibiotics and mechanical cleansing has long been advocated as best practice. Recent prospective human studies of 380 and 329 patients^166,226 showed that there was no advantage to mechanical cleansing; in fact, 46.9% of those who underwent the procedure developed complications compared with 37.6% of those who only received perioperative antibiotics. Based on these results, there is no indication for bowel cleansing in dogs and cats. Indeed, their use is counterproductive because it turns fecal material into a liquid slurry within the colon, which is much more likely to leak and contaminate the abdominal cavity during surgery.⁹⁶

Antibiotic Prophylaxis

Use of perioperative antibiosis for colonic surgery has long been advocated in humans and small animals.39,96,148,149 Although still popular in human surgery, use of oral preparations, such as neomycin combined with erythromycin, has no clinical advantage over perioperative intravenous antibiotics. As a disadvantage, oral preparations must be administered 24 hours before surgery.¹⁹ Use of perioperative intravenous antibiotics, administered 1 hour before surgery, significantly reduces the risk of surgical site infection in colonic anastomosis in humans.¹⁰⁰ This is in line with the recent consensus document from the U.S. Medicare National Surgical Infection Prevention Project,¹⁹ which recommends that the “first antimicrobial dose should begin within 60 minutes before surgical incision and that prophylactic antimicrobial agents should be discontinued within 24 hours of the end of surgery.”¹⁹

Choice of antibiotic is based on the likely contaminants present: coliforms and anaerobes. Cefoxitin has been recommended for parenteral prophylaxis alone; given its half-life, a repeat dose should be given hourly during the procedure.19,96 Combination parenteral treatment may include cefazolin or cefuroxime and metronidazole;²⁶ if the procedure is prolonged, the cephalosporin should be given again after 2 hours. There is no indication for postoperative use of antibiotics after colonic surgery.