Introduction

In current clinical practice, patients with short bowel syndrome (SBS) are mostly monitored by clinical examination, general well-being, weight and simple biochemical tests. Body weight (BW) and observed weight changes are important parameters, but do not provide information of the distribution of fat-free mass (FFM) and fat mass (FM) (Kyle et al, 2001). Although anthropometric variables remain constant, a shift between the main compartments of the body may occur. Simple and accurate body composition methods are required to evaluate to what extent patients with SBS are malnourished or dehydrated. Such methods are also important to monitor the efficacy of nutritional and rehydration treatment. Kyle et al (2001) in a study on 995 patients at hospital admission found that a low FFM was present in almost one-third of patients with a normal BMI of 20–24.9 kg/m². They claimed that a body composition analysis based on bioelectrical impedance (BIA) was more sensitive than BMI to identify patients who were FFM depleted (Kyle et al, 2001). Methods for the determination of total body water (TBW) and assessment of fluid compartments as used in research are dominated by dilution techniques (Van Marken Lichtenbelt et al, 1994; Deurenberg et al, 1995; Heymsfield et al, 1996; Gudivaka et al, 1999). These techniques are cumbersome, require time for equilibration and involve extended laboratory facilities and calculations.

Moreover, the patient has to be in a stable condition with minimal fluid turnover. For these reasons, they are not suitable for monitoring the dynamic clinical course in the management of patients with a rapid fluid turnover and in dehydrated patients. Dilution methods may be inaccurate in patients with SBS due to rapid fluid changes and high stoma output, resulting in inadequate equilibration of the isotope (Chambrier et al, 2001).

The development of BIA measurements for clinical determination of TBW represents an interesting innovation. Particularly, with the use of the multiple-frequency technique (bioelectric impedance spectroscopy, BIS), allowing for a detailed analysis of water compartments, the potential clinical usefulness appears considerable (Van Loan and Mayclin, 1992; Van Marken Lichtenbelt et al, 1994; Gudivaka et al, 1999). Changes in the extracellular water/intracellular water (ECW/ICW) ratio may give important information about body water distribution and fluid shifts (Geerling et al, 1999). A supposed stability of tissue hydration makes it possible to use body fluid investigations for estimation of other compartments, such as FFM and further on FM (Wang et al, 1999a, 1999b).

The aim of the present study was to describe body composition in patients with SBS, as obtained by the use of BIS, and with data from DXA measurements and anthropometrically derived estimates.

Patients and methods

Patients (Table 1)

In all, 19 consecutive patients (F/M=11/8) with a mean (s. d.) age of 54 y (10.2), range 36–79, were recruited from the Short Bowel clinic. Among them, 16 patients had Crohn's disease (CD), one had ulcerative colitis (UC), one had been operated for mesenteric vascular occlusion and one for intestinal strangulation. All patients lived in the Western region of Sweden. All had undergone massive intestinal resections; the length of the remaining small intestine is depicted in Table 1. Details regarding diagnosis, type of operations and remaining length of the small intestine were collected from the medical records.

Table 1 - Patient characteristics (Mean and (s.d.) are shown).

Full table

Eight of the patients were on home parenteral nutrition (HPN) at the time of the study. The median time on HPN was 74 months, range 61–201 months. None of the patients had any inflammatory activity, as indicated by clinical history, physical examination and plasma CRP. Three patients were on steroids, prednisolone, 5–10 mg/day. One patient was treated with azathioprine. Two of the women menstruated. The menstrual cycle phase was not taken into consideration for the study. One of the women had oestrogen supplementation. No other drugs were taken by the patients during the study.

Urinary and sodium output differed between those with an ileostomy and those with a remaining colon. The ileostomy patients had a mean daily urine volume of 1.0 (0.47) l and those with remaining colon 2.2 (0.64) l. Urinary sodium output in patients with an ileostomy was 87 (51) mmol/24 h and for those with the remaining colon 180 (42) mmol/24 h. For clinical status, see Table 1.

Patients received verbal and written information on the design of the study and informed consent was obtained. The ethical committee of the Medical Faculty, University of Gothenburg approved the study protocol.

Body composition analysis

Patients reported to the SBS clinic at 0900 (n=9) or at 0100 p.m (n=10) after breakfast/lunch. The total time for investigations was 1.5 h. Patients did not eat or drink during that time. Six of the patients on HPN had finished the intravenous infusion >4 h before the body composition analysis and two did not have any infusion for 24 h before the investigations.

BW was measured to the nearest 0.1 kg with a portable platform digital scale (CL-300 BMI, Carl Lidén, Gothenburg, Sweden), with the patients in light clothing. Height was recorded using a wall-mounted stadiometer to the nearest cm. BMI was calculated from weight and height (kg/m²).

Body water was assessed by the use of two independent methods: BIS and DXA. For further comparison, a prediction of TBW (TBW-PRE) was calculated according to a formula suggested by Bruce (Bruce et al, 1980).

FFM was assessed by BIS and DXA. For comparison, a predicted value of FFM was calculated.

Technical equipment and techniques

Bioelectrical impedance spectroscopy (BIS)

A commercially available instrument (Xitron Hydra 4200, Xitron Technologies, San Diego, USA) was used. The impedance technique is based on the observation that the electric conductivity of the human body varies with the frequency of an alternating current, and that resistivity of intra- and extracellullar water compartments is different for different frequencies. The Xitron Hydra 4200 uses 50 frequencies between 5 kHz and 1 MHz. At the highest frequencies, the current is able to overcome most of the capacitance of cell membranes, and penetrates throughout virtually the entire body water pool, whereas, at lower frequencies, the current passes mainly through ECW For a detailed technical description, see the review by De Lorenzo et al (1997) and Chumlea and Guo, 1997. Patients were resting in the supine position for 10 min prior to assessment. Room temperature was 23°C, Electrodes were placed (according to the manufacturer's manual) on the dorsal surface of the right hand/wrist and the other on the right foot/ankle. Measurements were performed twice and the mean value was used. Error of precision was reported to be <2% (Ellis & Wong, 1998). Values for ECW and ICW compartments were obtained by using the instrument's software option for water compartment analysis after entering of gender, height and weight.

FFM values were obtained by using the formula

Dual-energy X-ray absorptiometry (DXA)

We used a LUNAR-DPX-IQ scanner (Scanexport Medical, Helsingborg, Sweden). The system used a constant-potential X-ray source and a K-edge filter to achieve a congruent beam of stable dual-energy radiation. Whole-body scans were performed at a scan speed suggested by the system for each subject. FM, lean tissue mass, total bone mineral content (BMC) and density were analysed using software, version 4.7°C.

FFM (DXA) was calculated as the sum:

TBW values were derived from the DXA analysis. For the present study, hydration of the FFM was assumed to be 0.732 and constant (Pace & Rathbun, 1945; Wang et al, 1999b).

Prediction of TBW

Predicted TBW (PRE) was calculated according to a modified formula derived by Bruce et al (1980). The formula uses body weight and height, sex and age and gives an estimate of TBW, r (male)=0.755, r (female)=0.773. The formula values were obtained in a healthy population (n=476) from a four-compartment model based on total body potassium and tritiated water (Bruce et al, 1980). The dilution technique using tritiated water overestimates TBW by 4–5% (Schoeller, 1992). The tritium-dilution space was therefore divided by 1.05, correcting for the exchange of tritium label with nonaqueous hydrogen in body solids (Schoeller, 1992). The modified formulas are:

Prediction of FFM

Predicted FFM (PRE) was calculated as:

Statistical analysis

All statistical analyses were executed using the SPSS 11.0. for Windows package (SPSS inc. Chicago, IL, USA). Descriptive statistics were reported as mean and s.d. Means were compared using paired and unpaired t-tests. A P-value <0.05 was considered significant. The Bland–Altman method was used to assess the degree of interchangeability between BIS, DXA and a predicted TBW (Bland & Altman, 1986). Calculation of regression was included, and Pearson's correlation coefficient and SEE were calculated. The limits of agreement between the two methods were defined as mean difference 2 s.d. (Bland & Altman, 1986).

Results

In one female patient with CD and an ilestomy and on HPN no values could be obtained when BIS measurement was attempted. This patient had a liver failure and ascites.

Body water

Mean (s.d.) of measurements of fluid compartments are given in Table 2. Considerable differences are observed. The difference between mean TBW (DXA) and TBW (BIS) was -1.1 l in women and -1.8 l in men. The difference was less pronounced between TBW (PRE) and TBW (BIS), with a mean difference of -0.7 l in male and +0.2 l in female patients. Figure 1 shows the graphical relation between TBW (DXA) and TBW (BIS) for all patients. The ECW/ICW ratio by BIS was 0.81 (0.15) for women and 0.70 (0.06) for men.

Figure 1.

Graphical relation between TBW (BIS) and TBW (DXA) in litres. The straight line represents identity.

Full figure and legend (18K)

Table 2 - Water compartments in SBS patients assessed by BIS, DXA and as predicted (see text).

Full table

Fat-free mass

FFM values are shown in Table 3. The difference between mean FFM (DXA) and FFM (BIS) was -1.7 kg in women and -2.5 kg in men. DXA returned lower values than BIS. This observation was concordant in male and female patients. FFM (PRE) differed from BIS with –1.2 kg in male and +0.1 kg in female patients.

Table 3 - Fat-free mass in SBS patients as assessed by DXA, and estimated from BIS and predicted (see text).

Full table

Hydration of FFM

An indirect estimation of hydration of FFM using TBW (BIS)/FFM (DXA) gave a mean of 0.75. (0.08) for all SBS patients and men: 0.77 (0.06), women: 0.74 (0.09). The corresponding figure for the HPN patients was 0.75 (0.07).

Subgroups: patients on HPN and ileostomy patients

TBW and FFM in subgroups of patients, as determined with the three methods, are compared in Table 4. There were no statisitical differences for TBW and FFM between HPN patients and non-HPN patients, as well as between ileostomates and those with a remaining colon.

Table 4 - Body composition analysis using three techniques in subgroups of SBS patients.

Full table

Comparison between methods

The limits of agreement (Bland–Altman) between TBW (DXA) and TBW (BIS), TBW (PRE) and TBW (BIS ) and FFM (DXA) and FFM (BIS) are shown in Table 5. The limits of agreement were wide, indicating that methods are not interchangeable.

Table 5 - Comparison of means in SBS patients between methods (n=18).

Full table

Discussion

Patients with SBS are threatened by malnutrition and excessive fluid losses. The severity depends on both the length and function of the residual small bowel and whether or not the water-absorbing capacity of the large bowel is intact. Assessment of body composition is important in follow-up.

With a long-term perspective, the most interesting components to assess are the fluid content and the working cell mass (body cell mass—BCM). The main components of BCM are mainly muscle and the parenchymatous internal organs. If the relations between all compartments of the body were constant, BW would be the ideal and sufficient method for assessment of body composition, and could be performed with a high precision. As the relation between magnitude of the various body compartments is highly variable, and particularly so in patients with SBS, it is important to go into more detail.

In using DXA for body composition analysis, a two-compartment model can be designed: FM and FFM. The FFM constitutes BMC and the hydrated lean tissue mass. The lean tissue mass does reflect BCM, but is sensitive to shifts of fluids between the ECN and ICN compartments as well as the variation of hydration of the FFM. By combining DXA and BIS to assess ECW and ICW, it is possible to get an estimate of the composition of FFM by adding information about water distribution between the ECW and ICW compartments.

Determination of body water with BIS has practical advantages. The equipment is relatively inexpensive and requires limited operator training and maintenance. The method is quick and noninvasive. The accuracy of the method in different clinical settings has been questioned, for example, reduced accuracy has been described in obese subjects (Cox-Reijven & Soeters, 2000), cirrhotic patients (Lehnert et al, 2001) and children (Ellis et al, 1999). In one of our female patients with liver failure and ascites, no values were obtained from BIS because the software was unable to perform the calculations.

DXA has been used and validated against other methods in large groups. DXA compares well with other more complicated techniques, particularly in lean subjects. Previous studies have shown that DXA detects small changes in weight and resolves the changes in lean and fat components (Going et al, 1993; Tjellesen et al, 1997). However, DXA software is based on the assumption that hydration of FFM remains constant. Therefore, an abnormal state of hydration might infer an error in the calculation. There are also systematic differences between different manufacturers of the DXA equipment (Tjellesen et al, 1998; Kyle et al, 2001). On the other hand, DXA is well tolerated by patients and does not require any equilibration time.

Total body water

In the present study, we found that BIS overestimated TBW compared to DXA by 1. 2 l and limits of agreement between methods to assess TBW were wide (Table 5). Haderslev and Staun (2000) found that the mean TBW by BIA was overestimated by 1.9–3.1 l compared with dilution in underweight patients, when prediction equations for normal-weight subjects were used. This is consistent with the data reported by others (Royall et al, 1994).

However, BIS underestimated TBW compared to deuterium in a study on renal transplant patients. The mean TBW difference was 0.7 l, limits of agreement were -3.4 and +4.8 l (van den Ham et al, 1999). The patients had a mean BMI of 24.8 kg/m², which was similar to our previous study on ileostomates with a BMI of 25.4 kg/m² were BIS also underestimated TBW compared to tritiated water (van den Ham et al, 1999; Carlsson et al, 2002).

Fat-free mass

The mean difference for FFM between DXA and BIS for all patients was –1. 6 kg and limits of agreement were between –10.7 and +7.4 kg. DXA returned lower values than BIS, which is in concert with our previous study on healthy ileostomates (Carlsson et al, 2002). Royall et al (1994) found that BIS underestimated FFM compared to DXA, with a mean difference of 1.8 kg in malnourished patients with Crohn's disease after 3 weeks of enteral nutrition. Haderslev and Staun (2000) compared DXA, tritium dilution, total body potassium and skinfold measurements with BIA in the assessment of FFM in underweight patients with chronic gastrointestinal disease. Results obtained by DXA were not significantly different from tritium dilution, but differed significantly from BIA (Haderslev & Staun, 2000). Van den Ham et al (1999) concluded in a study of renal transplant patients that the reliability in the assessment of FM and FFM by BIS compared to DXA was questionable. Egger et al (1999) evaluated BIA in the determination of FFM in 38 patients on HPN. The limits of agreement between the results of FFM obtained by BIA and anthropometry were between –9.4 and +8 kg (Egger et al, 1999). Ward et al (2000) evaluated FFM using a new BIA instrument, the Soft tissue analyser, with DXA in 205 healthy adult subjects. Again, the limits of agreement between methods were poor, –7.5 and +9.9 kg, almost the same range as in the present study.

Hydration of FFM

The water content or hydration of FFM of 0.73 is among the best known and most widely applied of the body-composition constants (Pace & Rathburn, 1945; Wang et al, 1999b). Studies have shown that the hydration is influenced by growth, ageing, adiposity, gender, acute or chronic catabolic illness and malnutrition (Wang et al, 1999a).

The hydration of FFM in the SBS patients was 0.75 as for HPN patients, which is in concert with a group of healthy ileostomates, 0.77 (Carlsson et al, 2002).

The hydration was higher than in the study by Geerling in patients with long standing CD, 0.71 (Geerling et al, 1999). Christie et al (1990) compared TBW with tritiated water in two groups, 14 patients with an ileostomy and 20 patients with an ileal pouch with controls, and no group presented with chronic dehydration. Hydration for ileal pouch patients was 0.76 compared to 0.73 for ileostomy patients.

Changes in the extracellular and intracellular (E/I) ratio may give important information about water distribution and fluid shifts. For this purpose, BIS could be useful for repeated measurements and in a longitudinal setting. An increase in the E/I ratio may be caused by, for example, obesity, acquired immunodeficiency syndrome chronic renal failure, malnutrition and sepsis with oedema (Wang et al, 1999a). Conversely, diseases or conditions associated with dehydration may decrease the E/I ratio (Wang et al, 1999a). Three patients in the present study were on steroids (prednisolone). Treatment with glucocorticoids may expand ECW. However, since inflammation may also expand ECW, the anti-inflammatory effect of glucocorticoids may help in reducing ECW expansion. Thus, the net effect of glucocorticoids on ECW in inflammatory disorders is difficult to predict.

Two of the women menstruated, and the others were in menopause. The menstrual cycle phase was not taken into consideration for the studies. Deurenberg et al (1998) found changes in body impedance during the menstrual cycle to be small.

The E/I ratio in the present study was 0.81 in women and 0.70 in men. The corresponding figures in healthy ileostomates were 0.79 for females and 0.75 for males (Carlsson et al, 2002). Geerling et al (1999) suggested that the increased E/I ratio 0.86 observed in females with long-standing CD compared to 0.75 in males may be the result of a decreased intracellular water volume, suggesting a decreased metabolically active BCM.

Results of FFM and TBW determined by DXA and BIS did not agree in our patient population (Table 5). We also have a similar experience from a study in healthy ileostomates using BIS, DXA and dilution techniques, and observed differences that precluded free interchangeability between methods (Carlsson et al, 2002). In the present study, six patients had intravenous infusion >4 h before investigation, and changes in fluid balances could be one explanation for the lack of agreement between methods (Egger et al, 1999).

The wide limits of agreement associated with DXA and BIS, as shown in the present study and by others (Cox-Reijven & Soeters, 2000; Lehnert et al, 2001; Carlsson et al, 2002), limits its clinical utility.

Smith et al (2002) described a new method for calculating TBW in measuring the fraction of deuterium in the water contained in single-breath exhalations: flowing afterglow-mass spectrometry (FA-MS) and compared with BIS. TBW with FA-MS enables an immediate calculation of TBW and the accuracy is established close to 1% (Spanel & Smith, 2001). It was suggested that using dilution methods (e.g. FA-MS) seems to be a logical next step to derive individual algorithms for BIS measurements, particularly in patients with SBS, where there is a need for more precise and accurate body composition measures than those presently used today.

In conclusion, we have observed that most of our patients with SBS were maintained in a stable clinical condition within the normal limits of BW and BMI. FFM did not appear to be substantially altered in ileostomates or those on HPN. We have not observed any differences in TBW in subgroups. Further studies could be performed to investigate the clinical usefulness with BIS by repeated and longitudinal measurements in patients with SBS.

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Acknowledgements

This investigation was supported by grants from the Swedish Medical Research Council (17X-03117), Göteborgs Läkarsällskap, and IB och A Lundbergs Forskningsstiftelse.