OBESITY AND ALTERED BODY composition are highly

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1 1092 ORIGINAL ARTICLE Body Composition Assessment in Taiwanese Individuals With Poliomyelitis Kwang-Hwa Chang, MD, Chien-Hung Lai, MD, PhD, Shih-Ching Chen, MD, PhD, Wen-Tien Hsiao, BS, Tsan-Hon Liou, MD, PhD, Chi-Ming Lee, MD ABSTRACT. Chang K-H, Lai C-H, Chen S-C, Hsiao W-T, Liou T-H, Lee C-M. Body composition assessment in Taiwanese individuals with poliomyelitis. Arch Phys Med Rehabil 2011;92: Objectives: To measure the changes in the total and regional body fat mass, and assess the clinical usefulness of the body mass index (BMI) in detecting overweight subjects with sequelae of poliomyelitis. Design: Prospective, cross-sectional study. Setting: General community. Participants: Subjects with poliomyelitis (n 17; age range, 42 57y; mean, 47y; 12 men, 5 women) and able-bodied people (n 17) matched by sex, age, body weight, and body height participated in the study. Interventions: Not applicable. Main Outcome Measures: Total and regional body composition was measured with dual-energy x-ray absorptiometry. Clinical characteristics such as blood pressure, serum biochemical studies, and habitual behaviors (daily cigarette smoking, alcohol consumption, and exercise regimen) of all participants were evaluated. Results: Compared with able-bodied controls, subjects with poliomyelitis had a 50% greater total body fat mass, significant increases in the regional fat mass in every part of the body, and had the greatest increase of fat mass in the thorax. Nearly all the subjects (94%) with poliomyelitis were obese according to standards of body composition. However, one third of them had a BMI value of less than 25.0kg/m 2. Conclusions: People with poliomyelitis have a higher prevalence of obesity and a significant increase in total and regional fat mass. Current BMI underestimates the total body fat mass percentage compared with the control; therefore, a populationspecific BMI should be used to address the prevalence of obesity in postpolio survivors. Key Words: Body composition; Body mass index; Absorptiometry, photon; Poliomyelitis; Rehabilitation by the American Congress of Rehabilitation Medicine From the Department of Physical Medicine and Rehabilitation, Wan Fang Hospital (Chang), Department of Physical Medicine and Rehabilitation, School of Medicine, College of Medicine (Chen), and Department of Physical Medicine and Rehabilitation, Shuang Ho Hospital (Liou), Taipei Medical University, Taipei, Taiwan; and Department of Physical Medicine and Rehabilitation (Lai, Chen), and Department of Diagnostic Radiology (Hsiao, Lee), Taipei Medical University Hospital, Taipei, Taiwan. Supported by the department funds of Taipei Medical University Hospital, Taipei Medical University. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Reprint requests to Shih-Ching Chen, MD, PhD, Dept of Physical Medicine and Rehabilitation, Taipei Medical University Hospital, Taipei Medical University, No. 252, Wuxing St, Taipei 11031, Taiwan, csc@tmu.edu.tw /11/ $36.00/0 doi: /j.apmr OBESITY AND ALTERED BODY composition are highly related to an increase in the prevalence of metabolic syndrome and cardiovascular diseases (CVDs). 1-3 In an extensive survey, Weil et al 4 found that people with physical disabilities have a higher prevalence of obesity than the general population. Moreover, a high body fat mass was found to increase the risk of mobility-associated disability by 2 to 3 times in a population-based study. 5 Thus, a vicious cycle involving physical disability and obesity develops. 6 Clinically, a body mass index (BMI) of 25.0 or greater is the standard defining the term overweight. 7,8 This condition is related to an increased risk of death in middle-aged people. 9 However, in other clinical populations, such as individuals with spinal cord injury (SCI), BMI tends to underestimate the percentage of total body fat mass (total body fat mass%) when compared with able-bodied controls. 10 Spungen et al 11 showed that individuals with SCI have a 13% greater total body fat mass compared with able-bodied controls with a corresponding BMI. A previous case study 12 found that subjects with poliomyelitis (polio) had abnormal fatty infiltration, accompanied by muscular atrophy, in their legs. These changes could result in increasing the total and leg body fat mass, which could alter both total and regional body fat mass% in polio survivors. Therefore, for disabled people, a useful BMI cutoff value for being overweight may differ from that of standardized norms. Identifying the correct BMI cutoff point for this population may be of clinical relevance in the prevention of other healthrelated secondary conditions. Gawne et al 13 declared that half of their polio subjects had 1 or more cardiac risk factors. Grimby et al 14 performed crosssectional computed tomography scans of the midthigh in a 4-year follow-up study and showed that the adipose tissue in polio survivors had increased by 12.1%. To our knowledge, only a few articles have reported body compositional changes in subjects with polio. 12,14 Polio was a common cause of physical disability for people born in the 1950s and 1960s in Taiwan. Most of the subjects with polio are now middle aged and may be facing problems related to obesity. Compared with able-bodied controls, polio subjects have underdeveloped paralytic legs with flaccid muscle tone. We hypothesized that this characteristic may make a significant difference in the body composition between polio survivors and able-bodied controls. Little information exists on the amount and distribution of body fat mass and its relation to BMI for the polio population in Taiwan. This study was conducted to quantify the amount of total and regional body fat mass, and to assess the clinical BMI CVD DXA LBM SCI List of Abbreviations body mass index cardiovascular disease dual-energy x-ray absorptiometry lean body mass spinal cord injury

2 BODY COMPOSITION IN POSTPOLIO SURVIVORS, Chang 1093 usefulness of BMI in detecting obesity in subjects with polio in Taiwan. METHODS Participants A prospective study was conducted on middle-aged people who had experienced the onset of polio before 3 years of age. All of them had flaccid paralysis of 1 or both lower extremities and had no sphincter disturbances. Able-bodied people who were matched by sex, age ( 2y), body weight ( 5%), and body height ( 5%) were recruited as the controls. Those who had paralysis of the arm, were ventilator dependent, had signs of edema, had a metal implant in their bodies, were on diets or taking medications for weight loss, had a history of long-term use of glucocorticoid or other metabolism-related medications, or had a history of other neuromuscular diseases were excluded from the study. The institutional review board of a universityaffiliated hospital approved this study, and each participant signed an informed consent form before entering the study. Participant Demographics Eighteen pairs of polio (polio group) and able-bodied (control group) subjects were recruited between October 1, 2005, and September 30, 2006, in response to an advertisement. The advertisement, describing the study process as well as the inclusive and exclusive criteria for the study, appeared in the disability associations publications. One pair was excluded because the polio counterpart had had a minor stroke. Twelve men and 5 women in each group completed the study. Ages of the polio subjects ranged from 42 to 57 years, with both a median and mean age of 47 years. The duration of polio diagnosis on average was 45.4 years. Measurements After fasting for more than 6 hours and emptying their bladders, all subjects had their body composition measured with dual-energy x-ray absorptiometry (DXA; Norland XR-36, Version software). a The composition of the body comprises body fat mass, lean body mass (LBM), and bone mass individually. Weights of the body compositional variables of each body part were obtained from a whole-body scan. Body parts were subdivided into the head (above the chin), trunk, abdomen, both arms (distal to the shoulder girdles), and both legs (distal to the femoral trochanters) according to the Norland user s manual. The trunk included the thorax and abdomen. The region covering the abdomen was a polygonal shape (fig 1). Its upper border with the thorax was along the horizontal subcostal line. The upper line was chosen if 2 subcostal lines occurred in subjects with scoliosis. In this study, the demarcation between the thorax and abdomen was not related to the diaphragm because of technical limitations using DXA measurement. The body fat mass value of the thorax, including pericardial fat, was obtained by subtracting the value of the abdomen from that of the trunk. The LBM value of the thorax was obtained in the same way. The reported error, according to Norland Corporation, for total body fat mass estimates was less than 2%. With the use of these data obtained from DXA measurement, the total body fat mass%, the abdominal fat mass percentage, and the exercise burden index of body fat mass to LBM of each participant, as well as the relative difference of each poliocontrol pair, were calculated. The total body fat mass% is the ratio of whole-body fat mass to the body weight of a participant. Similarly, abdominal fat mass percent is the ratio of Fig 1. Diagram showing the results of a whole-body scan with DXA, delineating the 5 regions of the body, including the head, thorax, abdomen, both arms, and both legs. abdominal fat mass to the sum of body compositional variables of the abdomen. According to the literature, 15,16 those men with a total body fat mass% of greater than 28% and those women with a total body fat mass% of greater than 40% were identified as being obese. The exercise burden index was calculated as the division of body fat mass to LBM and represents the load of body fat mass per unit of LBM. For example, the relative difference of abdominal fat mass was the ratio of the difference in abdominal fat mass between the subject with polio and the able-bodied control subject to the abdominal fat mass of the control. The difference in abdominal fat mass was equal to the abdominal fat mass of the polio subject minus that of his/her matched control. The relative difference in body fat mass and LBM in each region of the body was calculated in the same manner. The relative difference thus compared the weights of body fat mass and LBM between the 2 groups and presented the difference as a percentage of the control. After all subjects fasted overnight for more than 6 hours, an antecubital catheter was inserted in their arm and blood samples (10mL) were withdrawn to measure the values of serum

3 1094 BODY COMPOSITION IN POSTPOLIO SURVIVORS, Chang Fig 2. Percentage of total body fat mass (total body fat mass%) in relation to the BMI for (A) men and (B) women with polio and able-bodied controls. Regression lines are shown. Shadows mark the areas where obese people (total body fat mass% >28% in men and >40% in women) 15,16 had BMI values <25.0kg/m 2. All but 1 subject with polio were obese. Of these, 6 (37.5%) had BMIs in the shaded area. fasting glucose and a lipid profile (total cholesterol, high- and low-density lipoprotein, and triglyceride). Body weight was measured in a standing position on a standard hospital scale. For orthosis users, the total weight wearing the orthosis and the weight of the orthosis were separately measured. The orthotic weight was then subtracted from the total. Putting a standardized measuring board on the densitometer allowed the recumbent body height of each subject to be measured while lying on the board. Measurements were made from the vertex to the heel of each unflexed leg. The side with the longer leg was recorded as the body height. Manual muscle testing (grades 0 5) was performed to rate the muscular strength of bilateral hip flexors, knee extensors, and ankle dorsiflexors of each participant, according to the methods endorsed by the Medical Research Council of Great Britain. 17 With a standard hospital mercury sphygmomanometer, the subjects blood pressure was measured after they had been seated for 10 minutes. The lifestyle of all participants was assessed with a questionnaire. The questionnaire assessed daily cigarette smoking, daily alcohol consumption, and the amount of exercise. Those who exercised 3 hours or more on a weekly basis for at least 3 months were identified as active participants, whereas the others were identified as a sedentary group. Data Analysis Differences in age, body measurements, body compositions, and laboratory data in the polio and control groups were compared using a paired Student t test. Differences in body composition between 1-leg and 2-leg paralytic polio individuals, as well as between polio subjects with and without abnormal metabolic profile results, were compared using an independent t test. Relative differences were compared with zero using a 2-tailed Student t test. Categorical variables in the 2 groups were analyzed with the Fisher exact test. The data were analyzed using the Statistical Package for the Social Sciences. b Differences between groups were considered significant if P values were less than.05. RESULTS Subjects with polio had greater total body fat mass% values than able-bodied controls (fig 2), although both groups had similar ages and physical statures (table 1). Compared with able-bodied controls, polio subjects had greater body fat mass in every region and had an increase in total body fat mass of 8.6kg. This was 50% more than able-bodied controls (table 2). The percentage increase in total body fat mass per unit of BMI (fig 3) was greater in polio subjects (1.2%) than in able-bodied controls (0.8%). The percentage decrease in total LBM per unit of BMI was also greater in polio subjects ( 1.0%) than in able-bodied controls ( 0.7%). Table 1: Comparison of Age, Body Measurements, and Habitual Behaviors Between Subjects With Polio (n 17) and Able-Bodied Controls (n 17) Parameter Polio Control Age (y) Body weight (kg) Body height (m) BMI (kg/m 2 ) Waist circumference (cm) * Systolic blood pressure (mmhg) Diastolic blood pressure (mmhg) Habitual behavior Daily cigarette smoking 5 (29) 9 (53) Daily alcohol consumption 9 (53) 13 (76) Active participation 9 (53) 7 (41) NOTE. Values are mean SD or n (%). *P.005 (vs the control, paired t test); P.05 (vs the control, Fisher exact test).

4 BODY COMPOSITION IN POSTPOLIO SURVIVORS, Chang 1095 Table 2: Weights of the Body Fat Mass and Lean Body Mass as Well as the Exercise Burden Indexes in Various Body Regions Between Polio Subjects (n 17) and Able-Bodied Controls (n 17) BFM (kg) LBM (kg) EBI Regions of Body Polio Control Polio Control Polio Control Thorax Abdomen * Arms * Legs Whole body NOTE. Values are mean SD; EBI, ratio of body fat mass to LBM. *P.05; P.005; P.001 (vs the control, paired t test). The greatest body fat mass difference between the polio and control groups occurred in the thorax (fig 4; mean SD: Relative difference 107.7% 73.5%; t 6.045, P.001). Other body fat mass differences were found in the legs (Relative difference 57.5% 39.3%; t 6.024, P.001), arms (Relative difference 39.7% 42.1%; t 3.889, P.005), and abdomen (Relative difference 26.3% 37.3%; t 2.903, P.05). Both groups had similar serum lipid profiles and glucose levels. In polio subjects, the glucose level and the data from the lipid profile were not relevant to the variables of the total and regional body fat mass, and BMI. All the polio subjects performed the activities of daily life independently and were community walkers. They had a mean SD hip flexor strength of grade , a knee extensor strength grade of , and an ankle dorsiflexor grade of Of these polio subjects, 11 (65%) had 2-leg involvement and 8 (47%) walked with an orthosis. Compared with 1-leg paralytic polio subjects, 2-leg subjects had a greater thoracic body fat mass% (mean difference SE: 3.27% 1.38%; t 2.371, P.05), with a reduction in LBM% in the legs ( 3.82% 1.40%; t 2.721, P.05) and abdomen ( 3.23% 1.45%; t 2.226, P.05). The body fat mass% and LBM% in other regions and for the entire body were not significantly different. DISCUSSION In our study, almost all the polio subjects were obese, based on the total body fat mass% criteria. 15,16 One third of them, however, did not meet the BMI criterion for being overweight. 7,8 BMI has been found to be inaccurate in subjects with SCI 10 as well as in adult Asians. 18 Subjects With Polio Had a High Rate of Obesity Using the total body fat mass% to detect obesity, 15,16 we found our polio subjects had a high rate of obesity. Compared with 29% (n 5) of able-bodied controls, 94% (n 16) of the polio subjects were obese (see fig 2). Women with polio had a higher mean total body fat mass% than the controls (mean SD: 49.1% 3.8% vs 37.4% 4.1%; t 6.896, P.005). Men with polio also had a higher mean total body fat mass% (39.8% 6.1% vs 25.1% 4.0%; t 8.404, P.001). Compared with able-bodied controls, the total and regional EBIs were higher in polio subjects (see table 2). This finding suggests that each unit of LBM in polio subjects carried a heavier working load. Body composition changes in our polio subjects, as reflected in an increase in the body fat mass and a decrease in the LBM (see fig 3), were similar to those with paraplegia Otherwise, our polio subjects had a greater mean total body fat mass% than those with an SCI (combined men and women, 30% 39%). 11,21,22 Gorgey and Dudley 23 claimed that muscular Fig 3. Percentage of total body fat mass and total LBM in relation to the BMI for subjects with polio and able-bodied controls. Regression lines are shown. (For polio subjects, the total body fat mass%.012 BMI.132, the total LBM%.010 BMI.788; for able-bodied controls, the total body fat mass%.008 BMI.090, the total LBM%.007 BMI.836). Polio subjects had a greater total body fat mass% but a lower total LBM% compared with able-bodied controls with corresponding BMI. Fig 4. Relative differences in the body fat mass (dark bar) and LBM (gray bar) in the total body and various regions of the body. Compared with able-bodied controls, subjects with polio had a significantly greater body fat mass in all regions of the body, and a lower LBM in the total body and the regions of the abdomen and legs. The relative difference in body fat mass (BFM of polio subject body fat mass of the matched control) body fat mass of the matched control. The relative difference in LBM was calculated in the same manner. Error bars show the 95% confidence intervals. *P<.05; **P<.01; P<.005; P<.001 (difference with zero, Student t test).

5 1096 BODY COMPOSITION IN POSTPOLIO SURVIVORS, Chang spasticity can maintain muscular size in subjects with SCI. Because body fat mass offers one third of the resting energy expenditure of skeletal muscle (19 vs 55 kj kg 1 d 1 ), 24 the energy expenditure is reduced in polio subjects after replacing their skeletal muscle with body fat mass. 12 In addition, elderly people and inactive people both had lower levels of energy expenditure. 25 Compared with SCI subjects, our polio subjects were older, 11 had a longer duration of the disability or inactivity, and lacked spasticity. All of these factors could have lowered total energy expenditure and might have contributed to the greater mean total body fat mass% in our subjects with polio. Lipolysis related to hormone-sensitive lipase is greater in intra-abdominal adipose tissue than in subcutaneous adipose tissue. 26 Enevoldsen et al 27 showed that physical activity can increase both the sensitivity and the amount of hormonesensitive lipase in intra-abdominal adipose tissue. The study on lipolysis and hormone-sensitive lipase would be an interesting issue, worth further investigation in subjects with polio. Current Body Mass Index Criterion for Being Overweight Is Not Suitable for Subjects With Polio In a 22-year follow-up study, Heitmann et al 28 claimed that the risk of mortality was associated with the total body fat mass%, but not with the BMI. However, we found that the current BMI criterion of 25.0kg/m 2 for being overweight 7 might not be a suitable value for polio subjects. Six (37.5%) of our obese polio subjects had a BMI of less than 25.0kg/m 2 (see fig 2). This discrepancy did not occur in the control group. As mentioned above, our polio subjects had an increased body fat mass and a decreased LBM not only in their legs but also in their abdomens (see table 2). These findings suggest that muscular atrophy with fatty infiltration had also occurred in the abdominal region. For each BMI value, polio subjects had a higher total body fat mass% and a lower total LBM% than able-bodied controls (see fig 3). Because of the disproportionate increase in the fat mass fraction of the body weight, the total body fat mass% might have increased without an equivalent rise in the BMI value. Based on figure 2A, men with polio had a greater total body fat mass% by 10% to 14% at each corresponding BMI compared with controls. A large cohort study is warranted to identify population-specific BMI criteria. Therefore, identifying the correct BMI cutoff for this population may be of clinical importance in the prevention of other health-related problems. The Biggest Difference in Body Fat Mass Occurred in the Thorax Compared with able-bodied controls, our polio subjects had the greatest decrease in LBM in the legs (see fig 4; Relative difference 46.8% 12.3%; t , P.001) and abdomen (Relative difference 23.0% 21.1%; t 4.492, P.005). The increase in the body fat mass of polio subjects occurred in every region of the body (see table 2). Subjects with polio had similar levels of LBM but double the amount of body fat mass in the thorax compared with able-bodied controls (see fig 4). The major thoracic body fat mass is pericardial fat. 29 To assess the amount or percentage of pericardial fat, the use of the body fat mass value of the thorax may be more accurate than using the value for the entire trunk. Growing evidence suggests that thoracic body fat mass plays a role in the development of CVDs The increased thoracic and abdominal body fat mass found in our study suggest an increased risk of CVDs in polio subjects. However, unlike the assessment of abdominal fat mass with waist circumference, clinicians can seldom detect the extra accumulation of body fat mass in the thorax using simple clinical tools. Further investigation to discover such a useful tool is needed. Study Limitations This study has some limitations. First, DXA has 2 potential biases when measuring soft tissue mass. One is the shading effects of bones, such as the thoracic cage and spine For this reason, most previous studies explored body fat mass in the trunk rather than the thorax. Even so, they did not eliminate the existing bias in the thorax because it was included in the trunk. The other bias is a possible estimation error related to soft tissue hydration. 35 This error may increase as body size increases. 36 In our study, all participants had emptied their bladders and kept excessive water out of their bodies before the DXA test. However, the effects of a fluid shift were not considered. Nonetheless, we spent 5 to 10 minutes measuring the recumbent body height of our participants on the densitometer before conducting the DXA test, which partially reduced the effects of a fluid shift on measurements of body composition. In addition, the influence of body size might be close between the polio and control groups because both groups had similar physical stature and ages (see table 1). We thus used the relative difference instead of the absolute value and tried to subtract the influence of the biases from DXA, but we could not distinguish subcutaneous fat from visceral fat in either the abdominal or the thoracic region. The skin and its thickness in each pair of participants might not have been far apart because they had a similar physical stature and age. 37 With the aid of relative difference, we thus lessened the impact of subcutaneous fat and were able to assess the difference in body fat mass between polio and able-bodied subjects. However, we could not identify the amount of body fat mass in the breasts. Additionally, DXA assessment using Norland might overestimate the total body fat mass%, even though we used Norland XR-36 with version software, which is more accurate than the older model. 38 Using relative difference, we could also lower the bias between the 2 groups. Finally, another limitation of the study was the small number of subjects who participated. CONCLUSIONS People with polio have a higher prevalence of obesity and a significant increase in total and regional body fat mass. Current BMI underestimates the total body fat mass% compared with controls; therefore, a population-specific BMI should be used to address the prevalence of obesity in postpolio survivors. Further investigation is needed to compare the differences of total and regional body fat mass between ambulatory and nonambulatory, as well as between 1-leg and 2-leg, paralytic polio subjects. 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