European Journal of Clinical Nutrition (2013) 67, 1271–1276 & 2013 Macmillan Publishers Limited All rights reserved 0954-3007/13 www.nature.com/ejcn

ORIGINAL ARTICLE

Nutritional status in patients with chronic pancreatitis BPM Verhaegh1, PLM Reijven2, MH Prins3, JHM Brouns2, AAM Masclee1 and YCA Keulemans1 OBJECTIVE: Chronic pancreatitis (CP) patients have an increased risk of malnutrition. Information about nutritional status of CP outpatients is scarce, and simple, sensitive methods to identify patients at risk are lacking. This explorative cross-sectional study was performed to survey the nutritional status of CP outpatients. SUBJECTS: Fifty patients with chronic or recurrent acute pancreatitis (RAP) had a nutritional assessment performed. Scores on nutritional screening tools and a quality of life questionnaire were assessed. General observations and relations between parameters were described. RESULTS: Thirty-nine patients had CP and eleven patients had RAP. According to the nutritional screening tools, 28–50% of the patients had a moderate or high risk of malnutrition. All domains of the Short Form Health Survey were significantly lowered in CP patients (all Pp0.001) compared with the Dutch norm values. A considerable number of patients scored below the 5th percentile on anthropometric measures. Mini Nutritional Assessment could not identify all patients with very low anthropometric scores. Substantial weight loss was not a sensitive indicator for functional impairment. CONCLUSION: CP outpatients are at risk of malnutrition. Currently used screening methods (for example, weight loss) are likely to be not sensitive enough to identify all patients with impaired body composition and restricted function. Therefore, some patients with objective decline in nutritional status will remain unidentified. An extended nutritional assessment is recommendable in CP patients. European Journal of Clinical Nutrition (2013) 67, 1271–1276; doi:10.1038/ejcn.2013.199; published online 16 October 2013 Keywords: chronic pancreatitis; outpatients; malnutrition; nutritional status; nutritional assessment; anthropometry

INTRODUCTION Chronic pancreatitis (CP) is an inflammatory condition of the pancreas that may ultimately lead to endocrine and exocrine insufficiency. This impairs digestive, absorptive and metabolic processes, enhancing the risk of malnutrition.1 Several reports have stated that malnutrition and weight loss are a consequence of CP rather than a cause.2,3 Midha et al.4 found that malnutrition and weight loss evidently progress after the onset of CP. The main factors contributing to the development of malnutrition among CP patients are an increased metabolic activity and a depletion of nutrients. The latter can be explained by several causes. First, pain may decrease appetite and nutrient intake. Second, compressing pseudocysts may impair food passage.1 Third, alcohol abuse is often accompanied by a disturbed diet, enhancing the risk of nutrient depletion. Fourth, exocrine insufficiency may lead to maldigestion and malabsorption of fat and proteins and is strongly associated with weight loss.4 Fifth, dietary restrictions to manage diabetes mellitus, whether or not caused by pancreatic dysfunction, also increase the risk of weight loss.5 The poor nutritional status will negatively affect the quality of life. Indeed, CP patients have impaired quality of life in all domains compared with healthy controls.6,7 Early detection of CP patients at risk of malnutrition is essential in order to improve nutritional status, physical functioning and quality of life. Global information about the nutritional status of CP outpatients is scarce and simple sensitive methods to identify CP outpatients at risk of malnutrition are lacking. In daily clinical routine, the screening on malnutrition in CP patients is based on

monitoring weight, pain and exocrine insufficiency. According to the recent ASPEN consensus, malnutrition is also associated with functional decline, changes in body composition and impaired energy intake.8 Therefore, the question arises whether the currently applied screening method is sensitive enough. The aim of this explorative cross-sectional study was to collect data on nutritional status of CP patients and to evaluate frequently used parameters for screening on malnutrition in CP patients. PATIENTS AND METHODS Patients All patients visited the Gastroenterology Outpatient Department of the Maastricht University Medical Center, a regional referral center for CP in the south of the Netherlands. The diagnosis CP had to be based on: (1) a typical medical history with recurrent attacks of acute pancreatitis, and/or (2) pancreatic calcifications, and/or pancreatic duct irregularities or dilation, and/or pancreatic duct stones, and/or pancreatic atrophy on imaging studies (that is, ultrasonography, computed tomography, endoscopic retrograde cholangiopancreaticography, magnetic resonance cholangiopancreaticography, endoscopic ultrasound).9 The diagnosis recurrent acute pancreatitis (RAP), as early-stage disease,10 was based on three or more recurrent attacks of proved

1 Department of Gastroenterology, Maastricht University Medical Center, Maastricht, The Netherlands; 2Department of Dietetics, Maastricht University Medical Center, Maastricht, The Netherlands and 3Department of Epidemiology, Maastricht University, Maastricht, The Netherlands. Correspondence: BPM Verhaegh, Department of Gastroenterology, Maastricht University Medical Center, Universiteitssingel 40 (postvak 10), Postbox 616, 6200 MD Maastricht, The Netherlands. E-mail: [email protected] Received 12 June 2013; revised 30 August 2013; accepted 30 August 2013; published online 16 October 2013

Nutritional status in chronic pancreatitis BPM Verhaegh et al

1272 acute pancreatitis without typical features of CP on imaging studies.11 Patients were excluded if: aged o18 years, unproved diagnosis of CP or RAP, diagnosed with cystic fibrosis and if no nutritional assessment data were available. Patients were also excluded if the time interval between the most recent nutritional assessment and their last visit to the outpatient clinic exceeded 6 months. If assessment records stated a proper handgrip strength could not be performed because of manual comorbidities (for example, arthritis) on both dominant and non-dominant side, patients were excluded as well.

Statistical analysis To analyze the data, non-parametric statistics were applied. To standardize SF-36 scores, Dutch normative group reference values for the SF-36 were used.18 Differences from theDutch norm values were assessed by one sample T-test. Based on reference values, age- and gender-specific percentile scores were calculated for MAC, TSF, MAMC, FFMI, FMI, and HGS. These values were used for statistical analysis instead of raw data. All statistical evaluations were performed by PASW Statistics version 18.0 (SPSS Inc. 2009, Chicago, IL, USA).

Nutritional assessment Since 1 year, CP patients attending the gastroenterology outpatient clinic were standardly referred to the dietetic department for a general nutritional assessment to identify patients at risk of malnutrition. Assessments were performed by a well-trained physician (BV). The following data were recorded during the assessments: Three questionnaires were filled out preceding measurements: the Mini Nutritional Assessment (MNA), the 36-Item Short Form Health Survey (SF-36; both in Dutch) and the Malnutrition Universal Screening Tool (MUST). In addition, patients were asked whether they had experienced a decline in weight, muscle strength or physical endurance since the diagnosis CP. Patient’s usual weight before the diagnosis was listed. Height was recorded to the nearest centimeter using a Seca 222 telescopic scale (Seca GMBH, Hamburg, Germany); weight was measured to the nearest 0.1 kg using a Seca 707 digital personal scale (Seca GMBH). Midarm circumference (MAC) and wrist and calf circumferences were measured using a tailor’s measure, all in standing position on the dominant side. Triceps skin fold (TSF) was then measured using Holtain T/W Skin fold Calipers (Holtain LTD, Crymych, UK). The midarm muscle circumference (MAMC) was calculated using MAC and TSF data. All former measures were compared with reference values published by Frisancho.12 Handgrip strength (HGS) was measured using a Jamar hydraulic dynamometer (Sammons Preston Inc., Bolingbrook, IL, USA). Subjects were standing with their arms pending alongside the body, the dynamometer facing downwards. Three readings were made on both dominant and non-dominant side, alternating sides after every reading. The highest score was recorded in kilograms. The grip strength on the dominant side was compared with unpublished data of healthy Dutch subjects (n ¼ 1293, aged 18–89 years).13 Body composition was assessed by bioelectrical impedance analysis using the Xitron 4000B Complex Bioelectrical Impedance Spectrometer (Xitron Technologies, San Diego, CA, USA). Fat-free mass (FFM) was calculated using the Geneva-equation,14 based on the measured resistance and reactance at 50 kHz. Fat-mass, fatmass index (FMI) and FFM index (FFMI) were calculated and compared with reference to values published by Schutz et al.15

Ethical considerations All diagnostic tests were performed in the context of standard care. The study was approved by the Maastricht Medical Ethical Committee.

Biochemistry All CP patients were routinely screened (at least once a year) at the outpatient clinic for inflammation, exocrine insufficiency, endocrine insufficiency and nutrient deficits by blood and stool sampling. Most recent laboratory results at the moment of assessment were retrieved from patients’ medical charts. Elastase and steatocrit, as a measure for the degree of steatorrhea, were determined in feces samples. Exocrine pancreatic insufficiency was classified as fecal elastase levels of less than 200 mg/g feces.16 Endocrine pancreatic insufficiency was diagnosed in case of overt diabetes (classified as HbA1c448 mmol/mol or fasting glucose 47.0 mmol/l) secondary to pancreatic insufficiency because of CP.17 European Journal of Clinical Nutrition (2013) 1271 – 1276

RESULTS Subjects A total of 56 patients met the CP or RAP diagnostic criteria and had a nutritional assessment performed. Six patients appeared not to be able to perform proper handgrip dynamometry because of manual comorbidities and were excluded. Patient characteristics are listed in Table 1. The mean age was 57.1 years (range 20–81 years) and the mean age at the onset of pancreatitis was 50.9 years (range 13–76 years) with a mean duration of disease of 6.3 years (range 1.2–28.9 years). The diagnosis CP or RAP, based on earlier-mentioned criteria, was confirmed in, respectively, 39 (78.0%) and 11 (22.0%) patients. The etiology was alcohol abuse in 23 (46.0%) of all pancreatitis patients. At least 31 patients (62.0%) visited the dietician and 58.0% used oral pancreatic enzyme supplementation. Nutritional assessment data showed that body mass index (BMI) was significantly decreased compared with BMI at diagnosis (24.4 vs 26.1 kg/m2; Po0.001). None of the patients had a BMI o18.5 kg/m2 at the moment of diagnosis, compared with three patients at the moment of assessment. Questionnaires Table 2 shows the grouped MNA and MUST scores. The mean MNA score was 22.6±4.4 (range 10.5–29.0). No significant associations were found between MNAp23.5 or MUST X1 and the presence of calcifications on imaging studies, having one or more major comorbidities, having an alcoholic etiology of pancreatitis or present exocrine insufficiency; all indicators for a more severe disease. Data on self-reported weight loss, decline in muscle strength, and physical endurance since diagnosis are summarized in Table 2. A 410% weight loss was significantly associated with MUST X1 (P ¼ 0.015) and lower MNA scores (Po0.001). Age- and gender-specific MAC, TSF, FFMI and FMI percentile scores were all significantly lower (Pp0.01) in patients who reported 410% weight loss since diagnosis; a difference not observed for HGS (P ¼ 0.422) or any SF-36 domain (all P40.05). Patients who reported evident impairment in both muscle strength and physical endurance scored significantly lower on HGS (P ¼ 0.03) and on all eight SF-36 domains (all Po0.01) compared with patients who did not report any impairment in strength or endurance since diagnosis. Furthermore, functional impaired patients had a significantly lower MNA score (P ¼ 0.002) and were more often classified as ‘at risk of malnutrition’ or ‘malnourished’ (P ¼ 0.019). No association was found with MUST scores (P ¼ 0.85). Table 3 shows that the scale scores of all eight main domains of the SF-36 were significantly lower compared with the Dutch & 2013 Macmillan Publishers Limited

Nutritional status in chronic pancreatitis BPM Verhaegh et al

1273 Table 1.

Patient characteristics n ¼ 50

Male Caucasian Age (years) Age at onset (years) Duration of disease (years) Current body mass index (kg/m2) Body mass index at onset (kg/m2) Weight (kg) Chronic pancreatitis Recurrent acute pancreatitis

37 49 57.1 50.9 6.3 24.4 26.1 72.3 39 11

(74.0%) (98.0%) (53.8–60.4) (47.1–54.7) (4.8–7.8) (22.8–25.9) (24.6–27.7) (67.5–77.1) (78.0%) (22.0%)

Etiology Alcoholic Idiopathic Auto-immune Biliary Pancreas divisum Other Calcifications on imaging studies Pancreatic surgery Gastric/intestinal resection Pancreatic enzyme supplementation Reported consultation dietician Presence of pain Smokers Exocrine insufficiency Endocrine insufficiency Diabetes mellitus type 1 or 2

23 12 1 2 3 9 26 9 2 29 31 33 21 28 10 8

(46.0%) (24.0%) (2.0%) (4.0%) (6.0%) (18.0%) (52.0%) (18.0%) (4.0%) (58.0%) (62.0%) (66.0%) (42.0%) (56.0%) (20.0%) (16.0%)

Number of major comorbiditiesa None One More than one Extrapancreatic malignancy Coronary artery disease Other vascular disease Pulmonary disease Neurological disorders Musculoskeletal disorders

34 13 3 5 4 4 4 5 2

(68.0%) (26.0%) (6.0%) (10.0%) (8.0%) (8.0%) (8.0%) (10.0%) (4.0%)

a

Data are reported as frequencies and mean (95% CI). Extrapancreatic malignancy, coronary artery disease, vascular disease, pulmonary disease, neurological disorders, musculoskeletal disorders.

normative sample. This indicates an evident impairment of quality of life in CP patients.

Table 2. Data regarding nutritional screening tools and self-reported weight loss, impairment in muscle strength, and impairment in physical endurance since diagnosis n (%) MNA High risk (score o17) Medium risk (score 17–23.5) Low risk (score 423.5)

5 (10) 20 (40) 25 (50)

MUST High risk (score X2) Medium risk (score 1) Low risk (score 0)

6 (12) 8 (16) 36 (72)

Weight loss (%) 410 5–10 o5

22 (44) 8 (16) 20 (40)

Impaired muscle strength Strong Moderate Minimal/none

21 (42) 19 (38) 10 (20)

Impaired physical endurance Strong Moderate Minimal/none

32 (64) 12 (24) 6 (12)

Abbreviations: MNA, mini nutritional assessment; MUST, malnutrition universal screening tool.

Table 3.

Scale scores (0–100) of the SF-36 (n ¼ 50) Dutch normative group mean±s.d.

CP patients mean±s.d.

P-value

83.07±22.70

65.90±23.98

o0.001

84.15±22.30 76.56±36.14

59.25±29.75 31.00±40.90

o0.001 o0.001

82.45±32.75

58.67±43.41

o0.001

76.84±17.40 68.60±19.28 74.97±23.32 70.83±20.56

67.12±19.45 47.20±21.46 54.82±28.45 38.20±19.32

0.001 o0.001 o0.001 o0.001

Physical functioning Social functioning Role limitation physical Role limitation emotional Mental health Vitality Bodily pain General health

Abbreviation: CP, chronic pancreatitis.

Anthropometric measurements Uncorrected anthropometric and grip strength data are summarized in Table 4. Age- and gender-corrected data of MAMC, HGS and FFMI, showed scores below the 25th percentile in 31 (62.0%), 23 (46.0%) and 30 (60.0%) patients, respectively. The number of patients who scored below the 5th percentile on MAMC, HGS and FFMI was, respectively, 18 (36.0%), 10 (20.0%) and 14 (28.0%). Figure 1 indicates that a considerable number of patients with very low scores (op10) on muscle mass and muscle strengthrelated parameters were not identified as at risk of malnutrition by the MNA screening tool. Biochemistry Overall protein levels were only moderately decreased (Table 5). No patients had levels below the reference values for total serum protein and transferrin. One patient had hypoalbuminemia and one patient had a pre-albumin deficiency. None of the protein determinations showed any correlation with anthropometric parameters or MNA score. Copper and zinc deficiency were found & 2013 Macmillan Publishers Limited

Table 4.

Structural and functional measures of nutritional status Male n ¼ 37

BMI (kg/m2) MAC (cm) TSF (mm) MAMC (mm) FFM (kg) FFMI (kg/m2) FM (kg) FMI (kg/m2) HGS dominant (kg) HGS non-dominant (kg)

24.1 30.0 16.9 24.6 56.5 18.2 18.1 5.9 41.6 40.1

(22.2–26.0) (28.3–31.6) (14.2–19.6) (23.3–26.0) (53.5–59.6) (17.3–19.2) (15.0–21.2) (4.8–6.9) (38.2–44.9) (36.6–43.5)

Female n ¼ 13 25.1 30.0 26.4 21.7 42.5 16.2 23.3 8.9 27.9 25.7

(22.1–28.2) (27.5–32.6) (21.8–31.0) (20.2–23.2) (39.0–46.1) (15.1–17.4) (17.7–28.9) (6.9–10.9) (24.9–31.0) (22.9–28.5)

Abbreviations: BMI, body mass index; FFM(I), fat-free mass (index); FM(I), fat mass (index); HGS, handgrip strength; MAC, midarm circumference; MAMC, midarm muscle circumference; TSF, triceps skin fold thickness. All means and 95% confidence intervals of raw data.

European Journal of Clinical Nutrition (2013) 1271 – 1276

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Figure 1. MNA-score plotted against age- and gender-corrected percentile scores for MAC (midarm circumference), MAMC (midarm muscle circumference), FFMI (fat-free mass index) and HGS (handgrip strength). Reference lines are drawn at MNA ¼ 23.5 (risk of malnutrition) and the 10th percentile.

Table 5.

Biochemical parameters Reference value

CRP (mg/l) Total serum protein (g/l) Albumin (g/l) Pre-albumin (g/l) Transferrin (g/l) Ferritin (mg/l) Zinc (mmol/l) Copper (mmol/l) Selenium (mmol/l) Fecal steatocrit (%) Fecal elastase (mg/g)

2.0 70.4 44.1 0.27 2.4 108.5 11.2 16.4 0.75 10.0 164

(0.0–5.0) (67.7–74.0) (40.6–46.9) (0.21–0.31) (2.2–2.6) (68.3–154.3) (10.2–12.4) (13.8–17.9) (0.60–0.97) (5.7–16.5) (56–500 þ )

o10 mg/l 60.0–80.0 g/l 32.0–47.0 g/l 0.15–0.40 g/l 1.5–3.5 g/l 30–400 mg/l 10.0–18.0 mmol/l 10.0–18.0 mmol/l 0.80–1.40 mmol/l o10% 4200 mg/g

Abbreviation: CRP, C-reactive protein. All concentrations are reported as median (interquartile range).

in one patient. Selenium levels were decreased in 55.8% of the patients. Sixteen (37.2%) patients had elastase levels o100 mg/g, indicating severe exocrine insufficiency. DISCUSSION Our present study shows that there is an evident risk of malnutrition in CP/RAP outpatients. Many patients experienced weight loss during the course of their disease and frequently reported a moderate to strong decline in muscle strength and physical endurance. This contributed to remarkably low scores on all SF-36 domains, resembling the results of other studies.6,7 Furthermore, a considerable number of patients scored low or very low on anthropometric measures. These results indicate a nutritional problem in this population. On the outpatient clinic percentage of weight loss, BMI, laboratory results and indicators for disease severity are commonly applied to trace and monitor malnutrition. However, European Journal of Clinical Nutrition (2013) 1271 – 1276

some of these markers have shortcomings when used as single screening tools.19 Our data are likely to confirm this. Patients indicated as having a more severe disease based on clinical data did not score worse on nutritional screening tools, implicating that attention should be paid to patients with less severe disease as well. Screening on protein levels may not be indicative either, as protein deficiency was rather uncommon. With regard to BMI, body mass indices of less than 18.5 kg/m2 are commonly used as cutoff point for malnutrition. In our population, a BMI of less than 18.5 kg/m2 was only observed in three patients, whereas many more patients experienced both subjective and objective functional impairment. Regarding percentage of weight loss, patients who reported more than 10% weight loss since diagnosis scored worse on nutritional screening tools and had significantly lower scores on anthropometric measures, although function measures (HGS and SF-36) were not significantly impaired. Physical functioning, however, is an essential part of nutritional assessment. Loss of function is correlated with worse clinical outcome and is indicative for loss of lean body mass.20 Recently published definitions of malnutrition recommend including deterioration of function in the diagnosis.8,21 CP patients who reported strong decline in both muscle strength and physical endurance scored significantly lower on SF-36 domains, had decreased MNA scores and performed worse on HGS measurements. Remarkably, only about half of these functional impaired patients had experienced strong weight loss. A BMI of less than 20 kg/m2 was rarely observed in the functional impaired group. Changes in body composition could be an explanation for this discrepancy, for example, loss of FFM combined with an increase of FM. Determination of body composition-related parameters is therefore essential in screening for malnutrition. When evaluating the nutritional assessment results we found remarkably low percentile scores of muscle mass-related parameters such as FFMI and MAMC. Recent literature indicates that a decreased FFMI is related to worse outcome after surgery,22 a higher mortality in chronic obstructive pulmonary disease23 and a & 2013 Macmillan Publishers Limited

Nutritional status in chronic pancreatitis BPM Verhaegh et al

1275 prolonged length of hospitalization.24 Perhaps FFMI might be a relevant measure for risk of malnutrition in CP outpatients as well. Although whole body composition techniques (for example, bioelectrical impedance analysis) are preferred above anthropometric parameters,25 routine application in the outpatient clinic is, however, limited. With regard to the MAMC, this parameter has been found to be a better predictor of malnutrition than BMI in chronic obstructive pulmonary disease patients.26,27 The value of MAMC in the prediction of the risk of malnutrition in CP has never been assessed. The value of HGS as a screening tool for malnutrition is unclear.28 Despite the fact that 20% of the patients in the present study scored below the 5th percentile on HGS, we did not found HGS to be significantly lower in people who experienced 410% weight loss nor to be correlated with FFMI percentile scores. Decline in muscle strength may not only occur due to loss of muscle mass. Other factors may have a role in muscle strength as well, for example, muscle energy status could be affected by disease. As previously described, low serum protein levels were uncommon in our population, as were low zinc and copper levels. There is some evidence that zinc and copper deficiencies can occur in CP, but they are rather uncommon.29 An observation worth to notice is that we observed a remarkable number of patients with low selenium levels. Van Gossum et al.30 made the same observations in their population of CP patients (n ¼ 35). As selenium has a role in anti-oxidant functioning, van Gossum et al. suggest that low plasma levels of selenium may reflect increased metabolic requirements associated with long-term exposure to factors that enhance production of oxygen radicals, such as alcohol consumption. However, results of the present study did not show selenium levels to be significantly lower in patients with an alcoholic etiology of CP. A significant positive correlation was observed between selenium levels and muscle-related parameters (MAMC, FFMI and HGS) and MNA score. We cannot clarify these findings, but it is hypothesized that selenium levels are somehow related to body composition, in particular to muscle mass. Limitations of this explorative cross-sectional study are the heterogeneity of patients studied and the considerable number of patients with major comorbidities. Besides, data were retrieved from a referral center population, meaning that the disease may be more severe or complicated. Another disadvantage was the unavailability of essential information regarding dietary intake and energy balances. Finally, all results were based on single moment measurements. Follow-up data were not yet available. In summary, the results of this explorative cross-sectional study indicate that not only weight, but also function and muscle mass may be significantly impaired in CP outpatients. This implies an evident risk of malnutrition and a generally impaired quality of life. Current, frequently used methods of monitoring weight, protein levels and disease course may not be the optimal parameters to identify those patients at risk of malnutrition as body composition and function are not taken into account. Widely used nutritional screening tools are unlikely to identify all patients with a decreased lean body mass and restricted function. Extensive nutritional assessment includes all malnutrition determinants and is therefore recommendable in CP patients. Simple questions regarding selfreported decline in muscle strength and physical endurance seem to be meaningful predictors for objective functional impairment. Inclusion of these questions in the screening of CP outpatients might be valuable to improve current screening methods, which are often based on weight and BMI only. Longitudinal data regarding nutritional status of CP patients are, however, needed to assess useful screening tools and to study the changes in body composition and function in CP patients over time.

REFERENCES

The authors declare no conflict of interest.

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Nutritional status in patients with chronic pancreatitis.

Chronic pancreatitis (CP) patients have an increased risk of malnutrition. Information about nutritional status of CP outpatients is scarce, and simpl...
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