Nonocclusive Mesenteric Ischemia: A Lethal Complication in Peritoneal Dialysis Patients

Abstract

Nonocclusive mesenteric ischemia (NOMI) is a relatively uncommon disorder, seen primarily in elderly patients with cardiac disease, and is characterized by progressive intestinal ischemia leading to infarction, sepsis, and death. It is suspected of being the underlying cause in at least 20% – 30% of acute mesenteric ischemia patients.

End-stage renal disease patients are among the highest risk populations for developing this lethal complication; however, NOMI is not unique to hemodialysis and can occur in peritoneal dialysis patients as well. Unfortunately, the presentation of NOMI is very similar to that of peritonitis. The key to correct diagnosis is a high index of suspicion in predisposed patients. The high mortality rate is a clear reflection of failure to recognize the syndrome at an earlier, treatable stage.

We present our case experience and an extensive review of the literature regarding this dreadful complication that may be reversible if considered early as a possible etiology and the appropriate diagnostic maneuvers undertaken.

Keywords

Nonocclusive mesenteric ischemia gram-negative peritonitis

This case concerns a 76-year-old Caucasian female with end-stage renal disease (ESRD) due to hypertension. She commenced continuous ambulatory peritoneal dialysis (CAPD) in May 1998. Her medical history included chronic hypertension, paroxysmal atrial fibrillation, atherosclerosis of the carotids and the abdominal aorta, and chronic obstructive pulmonary disease. The patient's medication at the time of admission included clonidine 0.1 mg twice daily, amiodarone 200 mg twice daily, acetylsalicylic acid 100 mg once daily, pravastatin 40 mg, acenocoumarol, salbutamol inhaler, and a phosphate binder with meals three times per day.

In January of 2002 she was admitted to our clinic because of the development of nausea, vomiting, and mild, diffuse abdominal pain. In the month prior to admission, she had three fleeting episodes of abdominal pain, with normal serological studies and peritoneal dialysis (PD) fluid evaluation. Physical examination revealed a temperature of 37°C, pulse rate 98 per minute, with a supine blood pressure of 80/50 mmHg and respiratory rate of 20 per minute. Abdominal examination revealed decreased bowel sounds with mild tenderness to deep palpation, especially in the lower quadrants. There was a Toronto Western Hospital peritoneal catheter in place without evidence of exit-site abnormality. Stool examination for blood was negative. The peritoneal effluent was cloudy, while Gram stain of the fluid showed numerous leukocytes but no bacteria. Pertinent laboratory findings on admission included blood urea 110 mg/dL, serum creatinine 8.7 mg/dL, serum amylase 34 IU/L, hemoglobin 12.7 g/dL, and white blood cell count 13500/mL. The rest of her laboratory examination was within normal limits. The patient was initially treated with fluid resuscitation and intravenous vancomycin and gentamicin, while the oral anticoagulant treatment was stopped and replaced with subcutaneous low molecular weight heparin (Fraxiparine 9500 anti-Xa IU/mL, 0.6 mL subcutaneously twice daily; GlaxoSmithKline, Athens, Greece).

Her medical condition did not improve over the following days. On the fourth day post admission, she developed fever, severe hypotension (60/10 mmHg) with pulse rate 110/minute, respiratory rate 35/minute, and severe abdominal pain localized to the left abdomen. Abdominal examination revealed clinical signs of peritonitis. The peritoneal fluid had become very cloudy and at this point had numerous white cells and gram-negative rods. On that day, the peritoneal fluid amylase level was 65 IU/L. Cultures of the fluid that were obtained previously eventually grew Klebsiella pneumoniae as well as Escherichia coli. Her blood laboratory findings included white blood cell count 16 500 with a left shift and hemoglobin 11.5 g/dL. The patient was developing metabolic acidosis. Plain abdominal film in the erect position disclosed abdominal distention with multiple fluid levels of the large and the small intestine. No free air was noticed anywhere in the peritoneal cavity.

The patient was taken to the operating room were an exploratory laparotomy was performed. Extensive gangrene involving the ascending, transverse, descending, and half of the sigmoid colon was found. There were no major occlusive lesions of the mesenteric vessels. The arteries were not thrombosed but had severe atheromatous changes. The mesocolon looked normal, without edema or hemorrhagic infiltration. A total colectomy with an ileorectal anastomosis was performed. Thereafter, despite intensive care including hemodialysis, the patient demonstrated severe sepsis syndrome. The patient's condition deteriorated and she died the same night. The findings at the time of exploratory laparotomy and the surgical pathology findings of the intestine were compatible with NOMI and will be discussed.

Discussion

Nonocclusive mesenteric ischemia, first described by Ende in 1958 (1), is one of the diseases that affect the vasculature of the intestine. NOMI has been defined as “intestinal gangrene in the presence of a patent arterial tree.”

The causes of mesenteric ischemia have been traditionally classified as either occlusive or nonocclusive, based on the underlying pathology. Occlusive causes of mesenteric ischemia comprise about 80% of all cases and include acute mesenteric arterial thrombosis or embolism, chronic mesenteric ischemia, mesenteric venous thrombosis, and strangulated bowel obstruction. Like NOMI, neonatal enterocolitis is classified as a non-occlusive type of mesenteric ischemia. Most studies have shown that 20% of all cases of mesenteric ischemia are nonocclusive in origin (2,3); however, it comprises the least understood mechanism of progression of mesenteric ischemia.

The overall incidence of NOMI is estimated to be approximately 1 case every 5000 hospital admissions (3). The mortality rate, despite being decreased from the shocking 80% 20 years ago, is still high, at approximately 50%. A major reason for this high mortality rate is delayed diagnosis and treatment initiation, which may range from 12 hours to 11 days (2,4 -6). Actually, in the majority of patients dying from NOMI there is no suspicion of intestinal infarction even at the time of the patient's death (7).

Despite a significant amount of work in the field of its pathogenesis, there is no unifying theory that has been accepted as the principal pathophysiologic basis for NOMI. Investigation of the regulatory mechanisms controlling the mesenteric circulation has revealed that mesenteric vasoconstriction in response to a number of systemic insults, intestinal hypoxia, and ischemia/reperfusion injury, together with increased intestinal metabolic demands and infection, contributes to the development of NOMI (8,9).

Risk factors include atherosclerosis, low cardiac output states (recent myocardial infarction, congestive heart failure, and arrhythmias), ESRD, and medications that are known to reduce splanchnic blood flow; for example, cyclosporine, propranolol and phenobarbital overdose, ergot derivatives, cocaine (8 -17). Furosemide has also been implicated in the pathogenesis of NOMI. The increased renal blood flow it causes results in decreased mesenteric perfusion. This is probably due to the furosemide-related activation of the rennin–angiotensin–aldosterone system with subsequently increased levels of angiotensin II (18). Other causes of mesenteric vasospasms are various forms of shock, septicemia, dehydration, and hypotension following heart surgery (cardiopulmonary bypass and repair of aortic coarctations) or major abdominal surgery (13,18).

The dialysis population, and in particular hemodialysis patients, are especially prone to the development of NOMI (19). The estimated incidence of mesenteric ischemia in this group is in the range of 0.3% – 1.9% per patient-year, in contrast to an up to 0.2% value for the general population. Incidence appears to be increasing steadily. This could be due in part to the increased number of published cases as well as the increased survival of ESRD patients, predisposing them to NOMI (20). The susceptibility of dialysis patients to NOMI is explained by the common encounter of known risk factors in this patient group: widespread atherosclerosis, advanced age, long-standing hypertension, diabetes mellitus, congestive heart failure, arrhythmias, and the use of mesenteric vasoconstrictor drugs are common (3,21,22). In addition, ESRD patients suffer from the so-called calcific uremic arteriolopathy. The presence of inappropriately high calcium–phosphorus product by the routine incorporation of calcium-based phosphate binders and high-dose vitamin D analogues, coupled to an active vascular smooth muscle cell process result in calcification of the intima and media layers of their arteries (22).

A recurrent theme described in both non-dialysis and dialysis populations is the presence of a relatively elevated red cell mass. This increased hematocrit leads to hyperviscosity and consequently a low flow state. The mechanism just described can be reproduced through the use of recombinant human erythropoietin (rHuEPO) (23,24). Studies in an in vitro and ex vivo model demonstrated that EPO also has a direct vasopressor effect on small mesenteric resistance vessels (25). In these studies, EPO caused endothelium-independent constriction of these vessels, suggesting that EPO acts directly on vascular smooth muscle. However, our patient did not have an elevated red cell mass nor was she on EPO therapy. Finally, hypoalbuminemia has also been considered a risk factor (22).

Hypotension, especially when there are repeated episodes, is the most important and immediate precipitating factor for NOMI in dialysis patients. However, hypotension is common in these patients and far outnumbers the NOMI cases, stressing the importance of other coexistent risk factors. In general, it seems that the combination of nondistensible, calcified mesenteric blood vessels and a dialysis-induced hypotension is the background upon which splanchnic hypoperfusion is liable to occur (20,22).

Despite its definite association with hemodialysis, NOMI has been reported only rarely in association with PD, due possibly to the lower occurrence of hypotensive episodes (3). Albeit, having a more stable blood pressure than patients on hemodialysis, PD patients may experience severe hypotensive episodes. Contributing factors are inappropriate use of dialysate resulting in excessive fluid removal, diuretics, and very low salt diet coupled to the tendency of dialysate to remove endogenous aldosterone, which is needed for adequate sodium absorption by the gastrointestinal tract (3). A literature review yielded 10 cases (9 PD patients, including our case, and 1 intermittent PD patient) (3,24,26 -30). As can be seen from these studies, predisposing conditions mirror those listed above, with hypotension and hypovolemia predominant. Mortality was very high (8 of 10 cases, 80%).

Preoperative diagnosis of NOMI in PD patients requires a high index of suspicion as well as early identification of patients at risk. The clinical presentation of NOMI is variable, depending on the length of the involved bowel, the rapidity of hypoxia onset, and the intrinsic resistance of bowel wall to ischemia and bacterial penetration. When present, pain is usually severe but may vary in intensity, character, and location. Usually it appears 8 to 12 hours after hemodialysis but may also appear during the course of it. The most common scenario is the initiation of right lower quadrant pain that progresses to peritoneal signs and guarding. However, in our case, the pain localized to the left abdomen. This is interesting since the pattern of intestinal involvement in NOMI is predominantly right, that is, the cecum and right colon are most commonly affected. During hypotensive episodes, a steeling phenomenon occurs on the superior mesenteric vessels. These collapse, but remain patent. In contrast, the left colon maintains a better collateral circulation due to the artery of Drummond and thus is more resistant to ischemia (20).

In the absence of pain, unexplained abdominal distention and gastrointestinal bleeding may be the earliest signs of ischemia and impending intestinal infarction. Fever, ileus, and diarrhea are common but nonspecific manifestations; however, this triple association along with leukocytosis strongly suggests intestinal ischemia (20). The peritoneal effluent may become cloudy but this implies transmural ischemia, which may not always be present (3). Diffuse or localized abdominal tenderness, rebound, and rigidity are ominous signs and usually herald transmural bowel infarction and peritonitis. Although studies have described a high incidence of abdominal guarding upon presentation, mild abdominal signs do not rule out this diagnosis. On the contrary, the finding of a “nonsurgical” abdomen when faced with a hypotensive hemodialysis or PD patient with severe abdominal pain, especially in the right iliac fossa, should alert the nephrologist to the very real possibility of NOMI (22).

Hematologic and serologic abnormalities are frequently detected during the course of acute mesenteric insufficiency but, unfortunately, they are nonspecific. Apart from hemoconcentration, other laboratory clues can raise early suspicion toward the diagnosis of NOMI. These include an unexplained leukocytosis and/or lactic acidosis closely following a hemodialysis session. Rising serum lactate levels have been proposed as an indication for second-look surgery (22). Other notable abnormalities include hyperphosphatemia and elevated amylase levels in the serum or peritoneal fluid (31). Despite the fact that hyperamylasemia is common in asymptomatic PD patients, a major increase in amylase, in serum (>600 U/L) or peritoneal effluent (>100 U/L), should raise suspicion (3). A rise in serum levels of glutamic oxaloacetic transaminase, lactate dehydrogenase, or creatine phosphokinase occurs late in the course of intestinal ischemia and often signifies nonreversible ischemia or infarction.

Plain abdominal x rays are useful in excluding other causes of abdominal pain, such as perforated viscus or bowel obstruction. A normal plain film in a patient with pain out of proportion to physical findings is suggestive of early acute mesenteric ischemia and should prompt consideration of diagnostic arteriography. Occasionally, abdominal films will show “thumb printing” of the bowel wall, intramural air, portal venous air, or free intraperitoneal air, all of which are found in patients with mesenteric ischemia. Unfortunately, most of these findings indicate bowel infarction and a late stage in the course of the disease. Furthermore, positive findings on plain films are present in only 20% – 60% of cases (8).

Controversy exists regarding the clinical significance of free intra-abdominal air in PD patients. Although air can enter the abdomen innocently via the peritoneal catheter, it does not appear to be a common finding. In one study of 572 chest x rays in PD patients, free air was found in 26 patients, usually in association with catheter manipulation, tubing changes, or cycler dialysis (32). In the absence of these circumstances, only 4 patients were found to have free air, 3 of whom had bowel perforation. In our patient, there was no free air present.

Bacteriology of the peritoneal fluid also provides clues for the diagnosis. The presence of gram-negative rods in the peritoneal effluent is suggestive of a bowel source of contamination (33). Enterobacteriaceae peritonitis is thought to be due to colitis, bacterial translocation, or chronic constipation, apart from exit-site infection or touch contamination (33). Also, gram-negative bacteria, fungi, and polymicrobial peritonitis have been correlated with enteric contamination (34).

Further, peritonitis that fails to improve after the administration of the appropriate antibiotics should raise the concern of an abdominal catastrophe (34).

Klebsiella species peritonitis comprises approximately 3% – 4% of cases in PD patients (33,35). The antibiotic resistance of Klebsiella and Escherichia has emerged as the most important issue in the management of peritonitis in PD patients. However, there are no reports of worst outcomes for resistant isolates compared to the nonresistant species, except for Serratia marcescens (33,35).

Initial treatment should address correction of any underlying cause. It should be stressed that prompt resuscitation of the patient must be instituted before any diagnostic or therapeutic tests are performed. Patients who are hypotensive or hypovolemic, whatever the etiology, demonstrate mesenteric vasoconstriction on angiography even in the absence of NOMI. However, if a patient's abdominal symptoms persist after volume resuscitation, nasogastric tube decompression should be performed and a Swan–Ganz catheter should be placed. A broad-spectrum intravenous antibiotic should be administered to all patients in whom the diagnosis of NOMI is entertained. Plain abdominal radiographs should be obtained to exclude the presence of an alternate diagnosis. If the plain films fail to show another cause for the pain, immediate angiography is advisable.

Definitive diagnosis of NOMI requires expeditious arteriographic study of the aorta and mesenteric vessels. The study is invaluable in the assessment of mesenteric vasospasm and in determining other causes of acute mesenteric ischemia. If time allows, arteriography should be considered in order to help formulate the most appropriate intraoperative strategy, even when a decision to explore the patient has been made. Oral contrast studies should be avoided if arteriography is contemplated in patients suspected of having NOMI.

Siegelman et al. (36) have described four reliable arteriographic criteria for the diagnosis of mesenteric vasospasm: (1) narrowing of the origin of multiple branches of the superior mesenteric artery; (2) alternate dilatation and narrowing of the intestinal branches, the “string-of-sausages” sign; (3) spasm of the mesenteric arcades; and (4) impaired filling of the intramural vessels. In addition to these findings, delayed arterial emptying of mesenteric veins may also be associated with ischemia. Once the diagnosis is confirmed, an intra-arterial infusion of papaverine is begun through a catheter in the superior mesenteric artery (37). Frequent repetitive abdominal examination every 4 hours and sequential angiography every 12 – 24 hours are important in following the efficacy of this treatment. Using this vigorous approach, Boley and co-workers (37) reported a mortality rate of 40% in their subset of patients with NOMI and, in those who survived, 85% had normally functioning gastrointestinal tracts. Angiography was not done in the current case due to lack of the proper equipment in our hospital.

If the peritoneal signs fail to resolve with papaverine infusion and evidence exists of mounting leukocytosis, gastrointestinal bleeding, or free or intramural air, immediate celiotomy is indicated. The aims of the operation are to assess bowel viability, to resect obviously infracted bowel segments, and to determine whether a second-look procedure at 24 hours is necessary. Nonviable bowel is dull gray or black in color, edematous, distended, and lacking in peristaltic activity.

Intestinal continuity is restored after enterectomy if the margins are unequivocally viable; otherwise, exteriorization is advised. Decision for a second-look procedure at 24 hours is made at the time of the initial celiotomy. If marginally viable intestinal segments are allowed to remain, the decision to re-explore should be upheld irrespective of clinical improvement during the immediate postoperative period.

In our case, at the time of exploratory laparotomy, the whole colon was noted to be necrotic except the cecum and the distal sigmoid. The surgical pathology demonstrated extensive necrosis in the large intestine. In some sections, the necrotic changes were minimal and limited to the superficial mucosa. In other sections, there was evidence of transmural necrosis. Finally, throughout the entire specimen, numerous small resistance vessels within the submucosa were occluded by fresh thrombi. These surgical pathologic findings represent the classic description of the NOMI entity.

The desire to avoid second-look operations has prompted the use of a large number of techniques to evaluate the viability of ischemic intestine. Sheridan et al. (38) pointed out the futility of clinical criteria when he showed that, by using intestinal color, arterial pulsations, and peristalsis, he could correctly predict intestinal viability with only 57.7% accuracy. A number of other techniques have been described, such as Doppler ultrasound (39 -41), fluorescein fluorescence (40 -43), and laser flow Doppler (38). The most commonly used techniques for assessment of bowel viability are clinical criteria, Doppler ultrasound, and fluorescein fluorescence. Mann et al. (40) compared the fluorescein fluorescence technique to Doppler ultrasound experimentally in a canine mesenteric circulation model. They found the Doppler device to be unreliable in the determination of intestinal viability. Fluorescein, on the other hand, was found to be a much more reliable indicator than either clinical criteria or Doppler ultrasound.

In conclusion, despite its rarity, NOMI should always be suspected in the differential diagnosis of abdominal pain in PD patients. The diagnosis of NOMI should be strongly considered in every patient who has peritoneal signs and risk factors associated with the development of this complication, especially if there have been hypotensive episodes during treatment. Laboratory and radiological examinations are neither sensitive nor specific, and the decision to proceed with arteriography is based on clinical criteria since early diagnosis and treatment initiation is the cornerstone of survival. Although surgery is feasible in the context of advanced infarction, it usually does not prevent the dreadful outcome.

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