Nephrol Dial Transplant (2002) 17: 1434–1439
Original Article
The prevalence of gastrointestinal symptoms in patients with chronic renal failure is increased and associated with impaired psychological general well-being Hans Strid1, Magnus Simre´n2, Ann-Cathrine Johansson3, Jan Svedlund4, Ola Samuelsson3 and Einar S. Bjo¨rnsson2 1
Department of Internal Medicine, Bora˚s Hospital, Bora˚s, Sweden, 2Department of Internal Medicine, 3Department of Nephrology and 4Institute of Clinical Neuroscience, Section of Psychiatry, Sahlgrenska University Hospital, Go¨teborg, Sweden
Abstract Background. Malnutrition occurs frequently in patients with end-stage renal disease (ESRD). Gastrointestinal (GI) symptoms may lead to reduced food intake, resulting in malnutrition and impaired well-being in these patients. The prevalence of GI symptoms in various chronic renal failure (CRF) groups is unexplored. We assessed the prevalence of GI complaints in patients on either haemodialysis (HD), peritoneal dialysis (PD), or in the pre-dialysis stage. Patients with and without diabetic nephropathy were also compared. Methods. A total of 233 patients with CRF (128 HD, 55 PD, and 50 pre-dialytic patients) completed two self-administered questionnaires: the Psychological General Well-Being (PGWB) index and the Gastrointestinal Symptom Rating Scale (GSRS), which measures GI symptoms. The values were compared with reference values obtained from the general population. The association between GI symptoms and serum (s-)albumin was also studied. Results. The total GSRS score in patients with CRF was significantly higher than the reference values (HD 2.14 (1.97–2.31), PD 2.24 (2.00 –2.48), and pre-dialytic patients 2.03 (1.82–2.25) vs controls 1.53 (1.50–1.55; P-0.001). When comparing CRF subgroups there was no overall difference between the groups, but PD patients had more severe reflux and eating dysfunction. In patients with diabetic nephropathy, only eating dysfunction was significantly more common than in the non-diabetic patients. There was a negative correlation between GI symptoms and psychological general well-being in CRF patients (Rhos 0.46, P-0.001) indicating that patients with a high GI
Correspondence and offprint requests to: Hans Strid, Department of Internal Medicine, SE-501 82 Bora˚s, Sweden. Email:
[email protected] #
symptom profile have impaired psychological general well-being. A negative correlation was found between eating dysfunction and s-albumin (Rhos–0.33, P-0.01). Conclusion. The prevalence of GI symptoms is high in patients with CRF and is associated with impairment in psychological general well-being. Presence of dialysis or not, type of dialysis, and presence or absence of diabetes mellitus seem to have limited impact on GI symptoms. Keywords: chronic renal failure; end-stage renal disease; gastrointestinal symptoms; Gastrointestinal Symptom Rating Scale; psychological general well-being; proton pump inhibitors
Introduction Malnutrition is associated with increased morbidity and mortality in patients with end-stage renal disease (ESRD) [1,2]. There is also an association between low serum (s-)albumin and risk of death in dialysis patients [1]. The pathogenesis of malnutrition is possibly multifactorial. Several factors seem to contribute to malnutrition in ESRD patients: inadequate intake of protein and calories, metabolic acidosis [3], uraemic toxins, medication, psychosocial factors, inadequate dialysis, metabolic disorders, and old age. Gastrointestinal (GI) symptoms can also contribute to decreased food intake resulting in malnutrition in these patients. Very limited data are available on the prevalence of GI symptoms in patients with chronic renal failure (CRF), although some previous studies have shown a high prevalence of GI symptoms in these patients [4–6]. However, these studies have not compared GI symptoms in different CRF groups: haemodialysis (HD) patients, peritoneal
2002 European Renal Association–European Dialysis and Transplant Association
GI symptoms associated with impaired psychological general well-being
dialysis (PD) patients, and pre-dialytic patients. Control groups were also missing in these studies. The relationship between GI symptoms and psychological well-being is not well documented. Our primary aim of this study was to assess the prevalence of GI symptoms in patients with CRF and make a comparison with values from the general population. We also wanted to assess GI complaints separately among patients on HD, PD, and before dialysis, and also compare patients with or without diabetic nephropathy, as gastroparesis is common among patients with diabetes mellitus [7]. Furthermore, secondary aims were to elucidate the impact of GI symptoms on quality of life assessed as psychological general well-being in these patients and to elucidate the relationship between the duration of dialysis and GI symptoms. The association between GI symptoms and body mass index (BMI) and s-albumin was also analysed.
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dysfunction is a question concerning early satiety, difficulties in eating normal portions, and post-prandially pain. The GSRS data are presented as a total score, as dimension scores, and as a separate score for eating dysfunction. The higher the scores, the more pronounced the symptoms. The questionnaire has been extensively validated previously [9].
2. Psychological general well-being. To measure psychological general well-being we used a generic selfadministered instrument, the Psychological General WellBeing index (PGWB index). This instrument was developed for the purpose of providing a self-reporting instrument that could be used to measure subjective well-being or distress [12]. It has been used extensively and its validity and reliability are well documented [9,11]. The PGWB index includes 22 items, divided into six dimensions: anxiety, depressed mood, positive well-being, self control, general health, and vitality. The subscales used to measure these states have three to five items, each using a six-grade Likert scale. Scores are calculated for each dimension and for an overall PGWB, with higher scores indicating greater well-being.
Subjects and methods Patient data Subjects A total of 277 patients with ESRD were invited to participate. The patients were recruited from the area around two cities, Gothenburg and Bora˚s in western Sweden, with a total population of 700 000. The dialysis patients came from four HD units and two PD units covering all dialysis patients in this particular region. The pre-dialytic patients were recruited from out-patient clinics in the area. The patients were given the questionnaires when they visited the hospitals for dialysis or during a visit to the out-patient clinic. The pre-dialytic patients had advanced renal insufficiency defined as a s-creatinine )300 mlumin anduor a glomerular filtration rate -25 mlumin, but were not yet on dialysis. As a control group, we used values from a previous study on the general population from the southern part of Sweden, including 2162 healthy people of different ages [8]. In this group 51% were men and the mean age was 51 years (range 19–84). In the patient groups and the control group the majority were Caucasians. The study was approved by the Ethics Committee of the University of Go¨teborg.
Patient data were collected from medical records. The following data were registered: disease leading to renal failure, height, weight, s-urea, s-albumin, duration of dialysis, dialysis efficacy (KtuV ), and consumption of drugs used for GI disorders.
Statistics Variable distribution is given as medians with interquartile ranges (IQR), except when comparing patients with healthy controls, where the results were expressed as a mean with a 95% confidence interval. For comparison of the three groups of CRF, the Kruskal–Wallis test was used and, if P-0.05, a post hoc analysis using the Mann–Witney U-test was performed. The non-parametric tests were also used when comparing other scores from the questionnaires in the study. The results were compared with reference values obtained from the general population [8]. Spearman’s correlation coefficient was used for correlation analyses of GI symptoms and psychological general well-being. Multiple regression analysis was used when studying diabetes mellitus impact on differences in GI symptoms in CRF subgroups.
Questionnaires 1. GI symptoms. To assess the presence and severity of GI symptoms, we used the self-administered version of the Gastrointestinal Symptom Rating Scale (GSRS) [9]. The GSRS was originally constructed as an interview-based rating scale designed to evaluate a wide range of GI symptoms and was later modified to become a self-administered questionnaire [10]. The questionnaire includes 15 items and uses a seven-grade Likert scale defined by descriptive anchors. A factor analysis was used to identify the following five dimensions: reflux syndrome (two items), abdominal pain syndrome (three items), constipation syndrome (three items), indigestion syndrome (four items), and diarrhoea syndrome (three items). One item, eating dysfunction, which was developed previously in a manner analogous to the GSRS [11], was also considered clinically relevant for this study and added to the original GSRS. Eating
Results Patient characteristics Completed questionnaires were returned by 233 patients, giving a response rate of 84%. Patients with severe illness, dementia, poor knowledge of the Swedish language, and unwillingness to participate in the study were excluded. The gender distribution was 158 men and 75 women. Among the participants, 128 were on HD, 55 on PD, and 50 were pre-dialytic. The mean age was 67 (54 –76) years (range 24 –86). The mean time on dialysis for HD patients was 25 (15– 48) months (range 7–84) and for PD patients was 18 (8–34) months (range 4 –48). Nineteen per cent of all patients
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Fig. 1. Total GSRS score for CRF patients compared with controls. HD patients (ns128) are shown in the striped bars, PD patients (ns55) in dotted bars, pre-dialytic patients (ns50) in white bars, and the controls in black bars. **P-0.001 compared with controls. Table 1. Different parameters in CRF patients
BMI (kgum2) s-albumin (gul) s-urea (mmolul) Kt uV
Total
HD patients (ns127)
PD patients (ns55)
Pre-dialytic patients (ns50)
25 (22–27) 35 (32–39) 22.6 (18.6–27.6) 1.46 (1.23–1.86)
24 (22–27) 36 (33–39) 23.6 (20.6–28.0) 1.33 (1.15–1.52)
25 (22–28) 33 (28–36) 19.0 (16.0 –24.0) 1.94 (1.80 –2.26)
25 (23–26) 38 (34 – 41) 21.0 (18.0 –28.0) –
Values are given as medians and IQR. Kt uV measures adequacy of renal replacement therapy. Normal values: HD patients )1.2,
had diabetic nephropathy: 15% of HD patients, 33% of PD patients, and 13% of the pre-dialytic patients. Values for BMI, s-albumin, s-urea, and Kt uV are given in Table 1. GI symptoms The mean total GSRS score for all patients with CRF was clearly higher than the reference values (controls) (Figure 1). In all GSRS domains, except for reflux, the scores were higher in all the patients groups than in the general population (Figure 2). Only PD patients had significantly higher reflux symptoms than controls (Figure 2). Comparing the three different groups with PD patients had more severe reflux and eating dysfunction than the other two groups (Table 2). Multivariate analysis showed that these differences were not due to the different percentage of diabetics in CRF subgroups (data not shown). In patients with diabetic nephropathy, only eating dysfunction was significantly more common compared with non-diabetic patients (Table 3). A negative correlation was found between the GSRS total symptom score and the PGWB index in the patients with CRF (Rhos 0.46, P-0.001). This means that the more symptoms the patients had, the less the psychological general well-being. We found a negative correlation between eating dysfunction and s-albumin (Rhos 0.33, P-0.01). The duration of
dialysis did not correlate with the prevalence of GI symptoms, except for reflux, where patients with long dialysis duration showed a lower reflux score. Gender and age had no impact on symptoms in CRF patients (data not shown). In the control group there was no significant difference in total GSRS score between the age groups [8]. Psychological general well-being Body weight and duration of dialysis did not have any impact on psychological general well-being in patients with CRF. Patients with s-albumin less than normal (-35 gul) had lower general health (P-0.03), but did not differ in the other dimensions of the PGWB index. We also studied differences between the three groups of CRF and found that patients on HD had significantly less psychological general well-being compared with pre-dialytic patients, especially in the positive well-being, general health, and vitality dimensions (Table 4). There was no statistical difference in the PGWB index when comparing HD patients with PD patients, PD patients with pre-dialytic patients, and PD and pre-dialytic patients with controls (Table 4). Patients with diabetic nephropathy had lower psychological general well-being than the other CRF patients (data not shown). Gender did not have any impact on the PGWB index.
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Fig. 2. Comparison of the different GSRS domain scores for CRF patients and the general population (controls). HD patients (ns128) are shown in striped bars, PD patients (ns55) in dotted bars, pre-dialytic patients (ns50) in white bars, and the controls in black bars. *P-0.05, **P-0.001 compared with controls. Table 2. Comparsion of GSRS scores between different groups of CRF GSRS
HD patients (ns128)
PD patients (ns55)
Pre-dialytic patients (ns50)
Total Reflux Abdominal pain Constipation Indigestion Diarrhoea Eating dysfunction
1.93 1.00 1.67 1.67 2.00 1.67 1.00
2.07 1.50 2.00 2.00 2.00 1.67 2.00
1.84 1.00 1.50 1.67 2.12 1.67 1.00
(1.40 –2.67) (1.00 –1.50) (1.00 –2.33) (1.00 –2.33) (1.25–3.25) (1.00 –3.33) (1.00 –2.00)
(1.48–3.08) (1.00 –2.50)* (1.08–3.29) (1.00 –2.33) (1.56–3.00) (1.08–3.67) (1.00 – 4.00)*
(1.47–2.67) (1.00 –1.50) (1.00 –3.33) (1.00 –2.00) (1.50 –3.00) (1.00 –3.67) (1.00 –2.00)
Values are given as medians and IQR group comparisons. *P-0.01. PD vs HD patients and pre-dialytic patients. Table 3. Comparsion of GSRS scores between patients with diabetic nephropathy and patients with other causes of CRF
Table 4. Comparsion of the PGWB index between different groups of CRF
GSRS
Diabetic (ns43)**
Non-diabetic (ns185)**
PGWB
HD patients (ns127)
Total Reflux Abdominal pain Constipation Indigestion Diarrhoea Eating dysfunction
2.07 1.00 2.00 1.67 2.00 1.67 2.00
1.93 1.00 1.67 1.67 2.00 1.67 1.00
Total Anxiety Depressed mood Positive well-being Self-control
93 24 15 13 15
(1.53–3.04) (1.00 –2.50) (1.00 –3.00) (1.00 –2.58) (1.75–3.25) (1.00 –3.33) (1.00–4.00)*
(1.40 –2.64) (1.00 –1.50) (1.00 –2.33) (1.00 –3.00) (1.75–3.00) (1.00 –3.33) (1.00–2.00)
Values are given as medians and IQR. *Group comparison: P-0.05. **Group comparison: in five patients, the aetiology of nephropathy was somewhat unclear, explaining that the sum of patients here is not 233.
Consumption of GI drugs Table 5 shows the use of GI-acting drugs among the patients with CRF in this study. Patients taking proton pump inhibitors (PPI) had significantly
PD patients (ns55)
Pre-dialytic patients (ns50)
(76–103)** 100 (79–113) 104 (92–112) (20 –28) 24 (20 –29) 26 (24–28) (12–17) 16 (13–18) 16 (14–17) (11–17)** 15 (11–18) 16 (13–17) (13–17) 16 (12–17) 16 (14–17)
Values are given as medians and IQR. **Group comparisons: P-0.01. HD vs pre-dialytic patients.
higher total GSRS scores than the rest of the group (2.33 (1.70–3.07) vs 1.72 (1.33–2.47), P-0.001), especially in the following domains: pain (2.33 (1.33–3.67) vs 1.33 (1.00–2.00), P-0.0001), eating dysfunction (2.00 (1.00–4.00) vs 1.00 (1.00–2.00), P-0.001), and indigestion (2.50 (1.75–3.62) vs 2.00 (1.25–2.75), P-0.01). The group ‘others’ consisted of other GI drugs, and in this group laxatives dominated.
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Table 5. Use of GI-acting drugs among CRF patients GI drug
Number (ns216)
Per cent (%)
PPI Motility-stimulating drugs Anti-diarrhoea drugs Others
68 10 16 52
31.5 4.6 7.4 24.1
Discussion In the present study we have demonstrated a high prevalence of GI symptoms among patients with CRF. The data are in agreement with previous results in HD patients [4–6]. In our study, PD patients suffered more from reflux symptoms and eating dysfunction than the other two groups of CRF. No major differences were observed between patients with renal dysfunction due to diabetes mellitus and the rest of the patients with CRF. The level of GI symptoms was inversely correlated with psychological general wellbeing. Furthermore, we found a high consumption of GI drugs, especially PPIs. We could not detect any differences in symptom scores between men and women. Previous studies have shown that GI symptoms are common in dialysis patients, with values ranging from 32 to 79% among these patients [4–6]. In one of the studies, the method of assessment was not described very well, which makes the validity uncertain [4]. In none of the studies was a comparison performed with GI complaints in the general population. In our study, we used two validated and reproducible measuring instruments, PGWB index and GSRS, to assess GI symptoms and psychological general well-being. The results were compared with reference values from a general population study [8]. The mean age in the controls was lower than in the patients, but age had little impact on general well-being and GI symptoms in the control group. All previous studies were performed using HD patients only [4,5]. This study found similiar high prevalence values among patients with PD as well as in pre-dialytic patients with advanced renal insufficiency. Malnutrition is common in patients with CRF and strongly correlated with increased morbidity and mortality [1,2]. Several factors—such as metabolic acidosis, uraemic toxins, medication, psychosocial factors, inadequate dialysis, and old age—have been proposed as contributing to malnutrition in patients with CRF. Recently, GI symptoms have been identified as a possible contributing factor. Nausea and vomiting are common in uraemia and it has been suggested that delayed gastric emptying is part of the pathogenesis behind these symptoms. Previous studies have shown conflicting results, some demonstrating delayed gastric emptying [6,13] although others have not been able to confirm this and have reported normal gastric emptying in these patients [14]. Only a few of these studies
have shown a correlation between GI symptoms and delayed gastric emptying [6,13]. In one study in nondiabetic patients, the treatment of gastroparesis with pro-kinetic drugs resulted in an improved nutritional state reflected as increased s-albumin levels [13]. In a recent study by van Vlem et al. [6] a correlation between dysmotility-like dyspepsia and gastric emptying was reported in patients on HD. They also found an inverse correlation between s-albumin and gastric emptying, implicating an impact of GI symptoms on malnutrition. In the present study, we found that in all symptom domains of GSRS, except reflux, scores were higher in all the patient groups than in the general population. This indicates a multifactorial pathogenesis to the GI symptoms in patients with CRF. In our study, we compared GI symptoms in CRF patients with normal controls, but we did not make a comparison with another population with chronic illness. Chronic diseases often lead to a high consumption of drugs, which is frequently associated with secondary effects as GI symptoms. Symptoms in chronic illnesses often influence several organ systems including the GI tract. It cannot be excluded that the higher prevalence of GI symptoms in CRF patients compared with normal could be partly due to the fact that the patients suffer from a chronic illness. It can be speculated that the high prevalence of GI symptoms may have an impact on eating behaviour in these patients. The higher prevalence of reflux and eating dysfunction in PD patients compared with other CRF patients is in line with previous studies aimed at elucidating the pathophysiology of GI symptoms [15]. Recent studies from Belgium have demonstrated that gastric emptying is delayed in the presence of glucose-based dialysate in the abdomen [16]. Acute hyperglycaemia has been found to effect gastroduodenal motility in both diabetics [7] and healthy individuals [17] and inhibits contractile activity in the upper gut, which might possibly contribute to reflux and eating dysfunction. These results support the conclusion of van Vlem et al. [16]. In our study, diarrhoea was commonly reported in all the different groups of patients with CRF. The reason for the high prevalence of diarrhoea is unknown. In some of our patients, a diagnostic workup had been performed previously without revealing any specific aetiology of the diarrhoea although most patients were not investigated for that particular symptom. Surprisingly no major differences were observed between non-diabetic and diabetic patients with CRF. Although the distribution of diabetic nephropathy in the three patient groups was different, the GSRS scores were similar. It was only the eating dysfunction item in the GSRS that the patients with diabetic nephropathy had significantly higher scores. The reason for this could be gastroparesis, which is common in patients with diabetes mellitus, the explanation being neuropathy or hyperglyacaemia [7]. The lack of difference in symptoms between the two groups
GI symptoms associated with impaired psychological general well-being
may reflect the complex pathophysiology behind GI symptoms in CRF patients. Patients with diabetic nephropathy had a lower PGWB index than the other patients. This could be explained partly by other complications associated with diabetes mellitus. The negative correlation between the GSRS score and the PGWB index indicates that a high prevalence of GI symptoms has a major impact on daily life for these patients without implicating a direct cause. Other causes related to the illness, and its treatment, also have a major impact on daily life in this patient group. Previous reports have shown that HD patients often either have to restrict their participation in many activities or give them up entirely because of the medical regimen and poor health [18]. This could be one of the reasons for the lower psychological general well-being of HD patients compared with pre-dialytic patients and controls. PD patients and pre-dialytic patients had PGWB indexes similar to the controls, indicating a rather good level of psychological well-being among these patients. The use of acid-suppressant drugs was very common and over 30% of the patients took PPIs. The high consumption of PPIs in our study was more prevalent among CRF patients with high scores in the GSRS domains pain, reflux, and eating dysfunction. These findings are in line with the results of previous studies in which patients with CRF have been reported to have a high prevalence of superficial gastritis, duodenitis, and peptic ulceration [19] associated with increased circulating gastrin values and upper GI haemorrhage [20]. This may partly explain the consumption of acid secretion inhibitors, although there is probably a certain degree of overuse in this patient group. Further investigations are needed to evaluate the indications for the use of acid-suppressant drugs in these patients. In our study, the duration of dialysis did not influence the prevalence of GI symptoms and this is in line with a previous study [5]. A low s-albumin has been demonstrated as a marker of morbidity in CRF [1]. The low s-albumin in these patients is partly due to chronic inflammation. In our study, patients with low s-albumin had significantly more eating dysfunction symptoms. This finding might imply that the burden of illness with increased inflammation, may contribute to decreased food intake leading to poor nutritional status in some CRF patients. We conclude that the prevalence of GI symptoms is high in patients with CRF and is associated with impairment in psychological general well-being. No major differences were observed between patients with renal dysfunction due to diabetes mellitus and to a non-diabetic underlying disease. The high consumption of PPIs in this patient group might reflect the unknown pathogenesis behind the GI symptoms. Further studies of the pathophysiology of upper GI symptoms are required.
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Acknowledgements. This study was supported by the Swedish Medical Research Council (Grants 8288 and 13409), and the Faculty of Medicine, University of Go¨teborg.
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