Mesenteric ischaemia in haemodialysis patients: a case/control study

Nader Bassilios1,, Victorio Menoyo1, Anne Berger3, Marie-France Mamzer4, Françoise Daniel1, Philippe Cluzel2, Claude Buisson1 and Frank Martinez1,5

1 CHPVR, AURA, 2 Radiology Department, CHU Pitié-Salpêtrière, 3 General Surgery Department, Hôpital Laënnec, 4 Nephrology and Intensive Care Departments, Hôpital Necker Enfants-Malades and 5 Nephrology Department, Hôpital Saint-Louis, Paris, France



   Abstract
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. Mesenteric ischaemia is not uncommon in dialysis patients and seems to have been increasing in the last decade. However, the risk factors for mesenteric ischaemia are unclear and prognosis of patients after this type of ischaemic accident is not well defined.

Methods. From January 1988 to June 1999, 15 haemodialysis patients (0.3% per patient-year) from a single institution presented with mesenteric ischaemia and the clinical, biological and radiological aspects of the ischaemia were described. To identify risk factors for mesenteric ischaemia, each ischaemic patient (case) was matched with two other haemodialysis patients not having ischaemia (controls). Survival curves were then established for the two groups.

Results. A marked hypotensive episode was present in seven out of 15 case patients (47%) during dialysis sessions that preceded mesenteric ischaemia. Abdominal pain, guarding, fever and hyperleucocytosis were all present in 13 out of 15 patients (87%). An abdominal computerized tomography scan with opaque enema enabled a rapid diagnosis for six patients. The caecum was the most frequently (47%) affected segment. Twelve patients were surgically treated and the remaining three were given medical support. The two groups (case and control) were not different in cardiovascular risk factors, comorbidity, administered drugs or main haemodialysis characteristics. The median survival of the case group was 600 days, whereas 80% of the control group survived beyond this period (P=0.0132). Eleven case patients survived >3 months after mesenteric ischaemia and had a median survival of 1500 days, which was identical to their matched control patients.

Conclusions. Mesenteric ischaemia should be systematically suspected in patients experiencing abdominal pain during or after dialysis sessions. Prompt diagnosis and treatment usually allow for a favourable prognosis.

Keywords: haemodialysis; mesenteric ischaemia; renal failure; risk factors; survival



   Introduction
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The small and large bowels may sustain hypoxic injury that is caused by various types of vascular insufficiency. Collectively, these lesions are designated as mesenteric ischaemia. The lesions of the colon are sometimes referred to as ischaemic colitis [1]. In non-haemodialysis adults, mesenteric ischaemia is rare with a frequency of 0.09–0.2% per patient-year [2,3]. In these patients, mesenteric ischaemia is predominantly an occlusive type, usually due to thrombosis formation over pre-existing atherosclerotic lesions in the proximal portion of the superior mesenteric artery. Mesenteric ischaemia in these patients leads to a high mortality rate, reaching 70% in two study groups that included 132 patients [4,5].

Mesenteric ischaemia may appear more frequently among dialysis patients than in the non-dialysis population. In an autopsy study of 78 haemodialysis patients, mesenteric ischaemia was found in 14% of cases [6] and in a recent study, the frequency was estimated to be as high as 1.9% per patient-year [7]. The non-occlusive type of mesenteric ischaemia is a predominant feature in haemodialysis patients [812] and is usually associated with circulatory failure secondary to acute heart failure, dehydration and arrhythmias [13]. A number of recent publications indicated that the frequency of mesenteric ischaemia is increasing in haemodialysis patients [7,12,14,15].

The aim of the present study was to describe mesenteric ischaemia cases observed in a single large dialysis institution during an 11 year period in order to specify comorbidities as well as predisposing risk factors and survival of affected patients.



   Subjects and methods
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Included in the study were haemodialysis patients that presented with mesenteric ischaemia confirmed by surgery and/or by colonoscopy, from January 1988 to June 1999. Patients were followed in three dialysis centres from a single institution: AURA (Association pour l'Utilisation du Rein Artificiel en Region Parisienne). In each of these 15 patients, we analysed clinical, biological and radiological aspects of mesenteric ischaemia. Demographical findings as well as methods of localizing lesions, including surgery or colonoscopy, were reported. We also analysed restoration of gastrointestinal tract continuity, relapse and the cause of death. A control group was established such that each patient presenting with mesenteric ischaemia was matched with two others according to age (±10 years), sex, length of time undergoing dialysis (±2 years) and the presence or absence of diabetes mellitus. For all patients (cases and controls) we studied the aetiology of end-stage renal failure, the past history of cardiovascular comorbidity and risk factors and the pertinent history of hepatic and digestive tract diseases. Also studied were medications given at the time of mesenteric ischaemia, haemodialysis treatment methods and blood pressure variations during the last four haemodialysis sessions before the mesenteric ischaemia episode. Finally, we assessed the cause of death and the survival rate of patients.

Statistical analysis
Statistical analysis was performed using chi-square and Mann–Whitney analyses with Statistica Stat Soft version 5.0 (1996) software. We compared Kaplan–Meier survival curves with log-rank tests. P-values of <0.05 were considered significant.



   Results
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Three cases of mesenteric ischaemia were observed between 1988 and 1994, and 12 others occurred between 1995 and 1999. The period from the last haemodialysis session before mesenteric ischaemia to the beginning of clinical symptoms averaged 7.6±7 h with a maximum of 48 h. Eight patients (53%) presented with initial clinical symptoms during haemodialysis sessions. The clinical and laboratory features at the time of first suspected clinical diagnosis are reported in Table 1Go. Thirteen of the 15 patients (87%) showed concomitant abdominal pain, fever, striking leucocytosis and guarding.


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Table 1.  Clinical and biological features at the time of diagnosis of mesenteric ischaemia

 
Mesenteric ischaemia was initially diagnosed from clinical and radiological findings and was then confirmed by colonoscopy (four patients) or by laparotomy (11 patients). An abdominal computerized tomography (CT) scan combined with a water-soluble opaque enema provided a reliable test for establishing the diagnosis in six out of eight patients (75%). This CT scan method showed a thickening of fatty tissue infiltrations around the involved colonic segment as well as occasional gas in the colonic wall (Figure 1Go). Colonoscopy was performed in four patients (27%) and laparotomy established final diagnosis in 11 patients (73%). The period from the beginning of clinical symptoms to final diagnosis averaged 37±35 h.



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Fig. 1.  CT scan showing thickening of the fatty tissue infiltration around the colon and gastrointestinal colonic wall.

 
Multiple areas of the bowels were involved. The caecum was involved in seven patients (47%) and the sigmoid in only one patient (7%). The other seven patients had multiple lesions in different areas of the bowel. Twelve out of 15 patients were treated surgically (80%). During surgery, voluminous colonic ulcerations were present in four patients (27%), pre-perforating necrotic lesions were present in two (13%) and perforation was present in two patients. In all of the 12 operated patients, the superior and inferior mesenteric arteries were pulsatile. A necrosis of the mucosa was found in all patients and this extended to the submucosa in four patients (27%). Gastrointestinal tract continuity was restored in six out of the 12 operated patients. Four died between days 2 and 45 following surgery. The poor clinical condition of two patients did not allow restoration of gastrointestinal tract continuity. The mean hospitalization duration was 45 days (2–150 days).

Case/control analysis
According to the four matching criteria, there was no significant difference between patients who presented with mesenteric ischaemia (cases) and the control group (Table 2Go). There was also no difference between the two groups in aetiology of end-stage renal disease (ESRD). Diabetes mellitus, which provided one of the matching criteria, was present in 40% of all the patients. The case and control groups were not different in terms of cardiovascular risk factors and comorbidities, including smoking, hypercholesterolaemia, hypertension, arteritis, congestive heart failure, atrial arrhythmias, valvulopathies, prosthetic cardiac valve, coronary artery disease or cerebrovascular accidents.


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Table 2.  Characteristics of patients with mesenteric ischaemia from case patients and from controls

 
The medical treatments taken by the two groups (oral anticoagulants and antiplatelet drugs, vasodilators, antihypertensive medications, corticosteroids and erythropoietin) were not different.

Characteristics of the four dialysis sessions preceding mesenteric ischaemia were compared in both groups at the same date. In the two groups, the average haemodialysis session duration (4.2 vs 3.9 h), haemodialysis membrane, type and dose of anticoagulant administration and mean ultrafiltration volume (5.5±2 vs 4.7±2% of total body weight) were not statistically different.

At the beginning of the last haemodialysis session preceding the mesenteric ischaemia accident, systolic blood pressure (SBP) and diastolic blood pressure (DBP) were lower in the case group than in controls (P<0.05; Table 3Go). During this dialysis session, blood pressure values remained stable in the control group whereas SBP fell from 116±18 to 87.8±32 mmHg (P<0.05) and DBP from 59±18 to 49±28 mmHg (P<0.05) in the case group. Among case patients, seven out of 15 (47%) had a drop of >40 mmHg SBP compared with none in the control group. To determine whether this hypotensive response was chronic, we compared blood pressures in the two groups during the last three haemodialysis sessions but found no differences in either mean SBP or DBP.


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Table 3.  Mean blood pressures before and after the last haemodialysis session that preceded mesenteric ischaemia

 
Among the 15 mesenteric ischaemia patients, four (27%) died in the first 3 months of the post-operative period, with three of these (20%) from septic shock and one from cardiac arrhythmia. Among control patients, there were eight deaths caused by one myocardial infarction, three sepsis, one gastrointestinal bleeding and three unknown. In case patients, three out of four early deaths occurred when they were surgically treated at least 48 h following the onset of clinical symptoms. Figure 2Go shows the survival curves of the case patients and the control group. The log-rank test showed a clear difference in survival between the two groups (P=0.01). The median survival rate was 600 days for mesenteric ischaemia patients. Eighty per cent of control patients survived beyond that period. A comparison of survival rates of the 11 case patients who lived >3 months after the mesenteric ischaemia incidents with the 22 respective controls revealed no significant difference, with a median survival time of 1500 days (Figure 3Go).



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Fig. 2.  Survival curve of all patients (case and control) (Kaplan–Meier).

 


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Fig. 3.  Survival curve of the case who survived >3 months (Kaplan–Meier).

 



   Discussion
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The present report represents the largest case/control study of mesenteric ischaemia in haemodialysis patients to date. We analysed all publications between 1985 and 2000 that included more than four patients (a total of 98 patients in eight series, including our work) presenting with mesenteric ischaemia (Table 4Go). Based on the four largest series, the frequency of the mesenteric ischaemia was estimated to be between 0.3% (our series) and 1.9% per patient-year [7]. Despite this wide frequency range, mesenteric ischaemia appears to be much more frequent in dialysis than in non-dialysis patients [16]. In our study, 12 patients presented with ischaemic accidents between 1995 and 1999 vs only three patients between 1988 and 1994. Diagnosis in these first three patients permitted our group to be more aware of the presence of this pathology in haemodialysed patients. This increasing incidence may be due to the growing number of published cases, perhaps reflecting better diagnoses, to the increasing survival of haemodialysis patients which would increase the population prone to this type of ischaemic accident or to both causes [7,12,15,17]. Mesenteric ischaemia was found even in relatively younger patients (Table 4Go).


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Table 4.  Main characteristics of dialysis patients from study series presenting with mesenteric ischaemia

 
Mesenteric ischaemia can be difficult to diagnose [18]. The clinical presentation varies according to the severity, extent and rapidity of the ischaemic insult, as well as to the resistance of the bowel wall to hypoxia and its intrinsic ability to protect itself against bacterial invasion [19]. Pain is the only permanent symptom and usually appears 8–12 h after the last haemodialysis session [10,15,17]. In our series, pain appeared during haemodialysis in eight patients (53%). Pain usually begins in the right iliac fossa with diffuse guarding developing later [10,15]. Ileus as well as fever and diarrhoea appeared in 82% of patients [7,10,15].

In thirteen of our patients (87%), pain was present concomitantly with fever, guarding and hyperleucocytosis. Mesenteric ischaemia should be strongly suspected in the face of this quadruple association, especially when pain is located in the right iliac fossa.

The biological signs are not specific. In our series, a decrease in haematocrit of >5% was found in 40% of cases, a finding that has been described as unusual in previous studies [8,15]. Hyperphosphataemia, hyperkalaemia, acidosis and increases in CPK and LDH enzymes are classical signs of mesenteric ischaemia in non-haemodialysis patients. These laboratory data are difficult to interpret in the dialysis population [20]. As previously reported [14], serum lactate may be helpful as a biological marker for mesenteric ischaemia. Unfortunately, this parameter was not systematically measured in our patients and we cannot evaluate the importance of this measurement in our population.

A rapid radiological diagnosis is mandatory during clinical conditions that evoke mesenteric ischaemia [17]. Routine abdominal radiographs may show a dilated featureless colon and ‘thumbprinting’ signs that correspond to patchy submucosal oedema or haemorrhage [19]. These abdominal radiographs are of limited value [9,10,18]. Berger et al. [17] showed that opaque enema CT scans allowed early diagnosis of non-occlusive right colonic ischaemia in haemodialysis patients. This type of scan accurately defined involved colonic segments by showing characteristic thickenings. This feature was localized or was circumferential with continuous fatty tissue infiltrations around the involved segments [17]. When ischaemia was associated with parietal pneumatosis, this combination correlated with surgical and histological findings of necrosis and a rapid surgical intervention was necessary to produce 100% survival in the post-operative period [17]. In our series, the opaque enema CT scan allowed early diagnosis by showing the previously described radiological features in 75% of patients undergoing the test. In these six patients, surgical intervention was rapid with an average time of 21 vs 45 h for the other patients. Five out of these six patients survived >3 months after surgery.

In the general population, mesenteric ischaemia is of an occlusive type and the lesions usually affect the left colon and sigmoid [21]. In contrast, mesenteric ischaemia is usually non-occlusive in haemodialysis patients and lesions develop more frequently in the caecum and right colon [15,17]. In cases of severe hypotensive episodes, as can occur during haemodialysis, a steeling phenomenon affects the superior mesenteric vessels. These vessels collapse but remain permeable. In contrast, the left colon maintains a better collateral circulation due to the Drummond artery and is considered more resistant to ischaemia [22].

Angiography can be used to introduce vasodilator drugs, such as verapamil prostavasin, via the indwelling angiography catheter [14]. Angiography findings can confirm diagnosis in cases of arterial occlusion and indicate non-occlusive mesenteric injury when ‘beading’ and ‘defoliated tree’ signs are present [14]. Angiography should be performed long before the development of peritonitis [11]. A Doppler ultrasound of the mesenteric vessels has no value in the acute phase of ischaemic attacks and sensitivity is reduced due to the deep location of these vessels [23]. Magnetic resonance imaging (MRI) with gadolinium is also of no benefit in acute phases, but is better than ultrasound for visualizing the origin of the mesenteric vessels. In preliminary studies in 16 haemodialysis patients having coronary, iliac or carotid atherosclerosis, MRI showed an absence of significant stenosis in the mesenteric vessels. Colonoscopy is a sensitive exam which can estimate mucosal lesion location to allow performance of biopsies [19]. At early phases, the mucosa displays a ‘thumbprinting’ appearance followed by ulceration development [20]. Colonoscopy should be performed with great care because the insufflations involved in the procedure could lead to hyperpressure and induced new ischaemic lesions [24].

In non-dialysis patients, mesenteric ischaemia is usually due to atherosclerotic thrombosis of the superior mesenteric artery [16]. In contrast, haemodialysis patients show a non-occlusive type of mesenteric ischaemia that includes permeable mesenteric vessels as well as heart failure in some patients despite normal renal function [8,12,14,15,25]. This type of ischaemia occurs after dialysis-induced hypotensive episodes and can be due to myocardial infarction or acute worsening of a pre-existing aortic valve stenosis [14,18,19].

In our case patients with mesenteric ischaemia, dialysis onset blood pressure just before the ischaemic accident was lower than in controls. In seven out of 15 of these patients, an obvious fall in SBP was noted during that dialysis session (Table 3Go). Although it is difficult to clarify the exact role of these hypotensive episodes in mesenteric ischaemia, they represent an important factor in triggering mesenteric hypoperfusion and ischaemic insults.

The mechanisms underlying acute intradialytic hypotension remain poorly understood [26]. Possible compensatory mechanisms include the impaired ability of the heart to increase cardiac output, vascular abnormalities resulting in impaired compliance, reduced responsiveness to vasoconstrictor stimuli and autonomic neuropathy resulting in an abnormal cardiopulmonary receptor or baroreflex function [26]. The present data suggest that care should be taken with patients having a blood pressure of 120/50 mmHg at the beginning of a session. Bender et al. [7] found in patients with mesenteric ischaemia that 83% had atherosclerosis, 75% were hypertensive, 58% had a past history of angina pectoris and myocardial infarction and 16% had heart failure and cardiac arrhythmias.

In our series and in agreement with Diamond et al. [8], cardiovascular history and risk factors for cardiovascular disease were not different between patients with and without mesenteric ischaemia. In the study by John et al. [12], diabetes mellitus was present in 55% of patients and was cited as a predisposing condition for mesenteric ischaemia. Because diabetes mellitus was one of the matching criteria in the present study, we were unable to assess the importance of this parameter. However, of the 450 haemodialysis patients in our institution, only 19.5% were diabetic. The fact that 40% of the mesenteric ischaemia patients had diabetes mellitus also suggests a role for diabetes mellitus as a predisposing risk factor for this type of ischaemic accident.

In previous studies, mesenteric ischaemia occurred in patients taking digitalis [27], Glypressin® (terlipressin) [28] and ergotamine [29]. None of our patients received these drugs. In our study, the percentage of mesenteric ischaemia patients treated with erythropoietin (Epo) was slightly higher than in controls (80 vs 53%; P=0.08). Although a previous study showed that Epo causes mesenteric vessel vasoconstriction [30], these findings are insufficient to establish a role for Epo in inducing mesenteric ischaemia and this area will require further investigation. In the four largest studies of haemodialysis patients with mesenteric ischaemia (Table 4Go), the authors did not analyse the role of the haemodialysis membrane, the duration of the session nor the type of anticoagulants involved in mesenteric ischaemia prevalence [7,8,12,15]. In our series, an analysis of these parameters revealed no differences between the two groups. Although mesenteric ischaemia has been reported in peritoneal dialysis patients, we did not find this association in our series. This may be due to reduced haemodynamic variations caused by the present method for blood epuration [31].

Mesenteric ischaemia is usually treated by surgery. In three previous series [7,10,15], all of the 28 haemodialysis patients (Table 4Go) had resection of the ischaemic areas, but failed to report whether digestive tract continuity had been re-established. A short delay between the beginning of clinical symptoms and surgery was associated with better survival. In the study by Charra et al. [15], mortality was limited to 15% of patients when 75% of these were surgically treated in the first 24 h. Bender et al. [7] experienced a higher mortality rate (45%) when surgery was delayed to after the first 24 h vs no death when this interval was reduced to below this critical period. From our experience, the four patients (27%) that died in the first 3 months had a poor prognosis because surgical treatment had been delayed for up to 48 h. In our series, three patients had medical treatment that consisted of a broad spectrum of antibiotics and a low-residue diet. The other 12 patients had surgical treatment. Relapse after mesenteric ischaemic accidents has varied from 8% [10] to 60% [15], although most studies have not properly examined this parameter. None of our 15 patients experienced mesenteric ischaemia relapse during the 11 years of our study period. However, three of our case patients died from unknown aetiology and mesenteric ischaemia relapse could not be absolutely excluded as a cause of death in these cases.

The main causes of early death are extensions of the ischaemic lesions [7] and septic shock [15]. To eliminate these extensions some authors recommend performing a second look operation at 24 h following the first procedure [14].

The number of patients surviving after surgery varied among the analysed studies (Table 4Go). In our experience, an early death in four patients explained why the overall survival of the case patients presenting with mesenteric ischaemia was shorter than in the control group. If these four patients are excluded, the survival of the other 11 is identical to their 22 respective controls. There are at least two possible explanations for this finding: first, the absence of a difference in cardiovascular comorbidity between the two groups and second, the absence of a relapse of mesenteric ischaemia.

In conclusion, mesenteric ischaemia is not uncommon in haemodialysis patients and seems to have increased in the last decade. Mesenteric ischaemia is a surgical emergency with non-specific symptoms. An early diagnosis before transmural necrosis formation is difficult to establish. A definite diagnosis is usually late and ischaemic lesions can be gangrenous at this stage. Mesenteric ischaemia should be systematically diagnosed when abdominal pains appear in haemodialysis patients. In addition, a severe hypotensive episode during dialysis should be considered as a risk factor for mesenteric ischaemia. The opaque enema CT scan can visualize thickening of affected colonic segments. Mesenteric ischaemia patients present with high early mortality rates: >25% of the patients died in the first 3 months. Beyond this period, the mortality rate of these patients is equal to that of the control group. Therefore, a rapid diagnosis of mesenteric ischaemia is needed in the first 24 h in order to allow early surgical treatment for a better prognosis.



   Acknowledgments
 
We wish to thank the physicians of Centre Henri Kuntziger, Centre Pasteur Vallery-Radot and Centre d'Entrainement pour l'Hémodialyse à Domicile, Paris and Dr N. Bishai, English Language and Literature PhD, London.



   Notes
 
Correspondence and offprint requests to: Dr Nader Bassilios, Réseau Nephropar, Hôpital Necker 149, rue de Sèvres, F-75743 Paris Cedex 15, France. Email: nbassilios{at}hotmail.com Back



   References
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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Received for publication: 7.11.01
Accepted in revised form: 8.10.02





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