Fitness testing of pediatric liver transplant recipients

Fitness testing of pediatric liver transplant recipients

Fitness Testing of Pediatric Liver Transplant Recipients Viswanath B. Unnithan,* Suzanne H.E. Veehof,* Philip Rosenthal,† Christine Mudge,† Teresa H. ...

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Fitness Testing of Pediatric Liver Transplant Recipients Viswanath B. Unnithan,* Suzanne H.E. Veehof,* Philip Rosenthal,† Christine Mudge,† Teresa H. O’Brien,‡ and Patricia Painter§ Liver transplantation is accepted as the standard management for end-stage liver disease in children. Pediatric heart and heart-lung transplant recipients have shown significantly diminished exercise capacities compared with age-matched, able-bodied, control subjects. The primary aim of this study is to compare the fitness levels of a group of pediatric liver transplant (LT) recipients (LT group, 20 boys, 9 girls; age, 8.9 ⴞ 4.8 years; 56 ⴞ 35 months posttransplantation) with a group of able-bodied control subjects (22 boys, 12 girls; age, 8.4 ⴞ 3.8 years). The secondary aim is to compare the performance of the LT group against the Fitnessgram criterion standards. We assessed muscular endurance by means of a partial curlup, flexibility by means of the back-saver sit and reach, and cardiorespiratory fitness by means of the progressive aerobic cardiovascular endurance run (PACER). The only significant (P < .05) difference between the 2 groups was the number of shuttles run in the PACER (control, 16.8 ⴞ 9.8 v LT, 11.5 ⴞ 8.4 shuttles). Other differences between the 2 groups were not significant. With regard to satisfying the Fitnessgram criterion standards, only 35% of the LT group achieved the standards for the partial curl-up, 88% of the LT group achieved the criterion standards for flexibility, and 0% achieved the standards for the PACER. These results indicate that the LT group has diminished exercise capacity. The origins of exercise limitations deserve further investigation. (Liver Transpl 2001;7: 206-212.)


ransplantation is the accepted therapy for endstage organ failure. Thirty five thousand individuals received organ transplants in 1998, and this number is growing. One of the major reasons for this increase over previous years is the better long-term prognosis for these individuals.1 Common to all adult liver transplant (LT) candidates is an impaired physical performance level before transplantation.2-4 It is expected that im-

paired exercise capacity affects the performance of adults in their daily recreational activities and inhibits the accomplishment of simple physical tasks. Although improved physical functioning is assumed after transplantation, limited information exists regarding the physical functioning of adult and pediatric transplant recipients.2 The limited cross-sectional data that exist in pediatric heart, heart-lung, and lung transplant recipients showed significant (43% to 64%) reductions in physical work capacity compared with able-bodied control subjects.5 The limitations to exercise performance more likely stem from central limitations in heart and heartlung transplant recipients and pretransplantation exercise intolerance. Both reduced exercise tolerance on a treadmill walking test6 and reduced cardiorespiratory fitness (maximal oxygen consumption [VO2max]) on a cycle ergometer7 compared with able-bodied control subjects have been shown in adolescent renal transplant recipients. Reductions in VO2max compared with agematched healthy individuals8 and limitations in daily functioning were noted in adult LT recipients.9-11 To the best of our knowledge, no research has been conducted on the assessment of fitness levels in pediatric LT recipients. The purpose of this study is to use simple field tests of the basic components of physical fitness (cardiorespiratory fitness and muscular endurance, specifically abdominal and flexibility) to (1) compare the fitness level of pediatric LT recipients with able-bodied control subjects and (2) assess the proportion of pediatric LT recipients capable of achieving able-bodied pediatric criterion fitness standards.

Materials and Methods From *Exercise and Sport Science, University of San Francisco; †Pediatric Liver Transplant Program and §Department of Physiological Nursing, University of California at San Francisco; and the ‡Department of Kinesiology, San Francisco State University; San Francisco, CA. Supported by a Faculty Development Research Grant from the University of San Francisco. Address reprint requests to Viswanath B. Unnithan, PhD, Exercise and Sport Science, University of San Francisco, 2130 Fulton St, San Francisco, CA 94117-1080. Telephone: 415-422-5624; FAX: 415422-5671; E-mail: [email protected] Copyright © 2001 by the American Association for the Study of Liver Diseases 1527-6465/01/0703-0010$35.00/0 doi:10.1053/jlts.2001.22324


Subjects Sixty-three subjects volunteered for the study (Table 1). Written informed consent was obtained from a parent or guardian, and each child gave verbal assent. The Committee on Human Research at the University of California, San Francisco, gave ethical approval for this study. Before the commencement of testing, each child completed a pretest questionnaire to assess their current physical and health status.

Tests All tests were performed at the annual picnic for pediatric LT recipients and families. The order of the tests was randomized

Liver Transplantation, Vol 7, No 3 (March), 2001: pp 206-212

Fitness and Transplantation

Table 1. Physical Characteristics of Pediatric LT Recipients and Able-Bodied Controls

Age (yr) Stature (cm) Body mass (kg) Sum of skinfolds (mm)

LT (n ⫽ 29)

Control (n ⫽ 34)

8.9 ⫾ 4.8 127.8 ⫾ 22.8 31.2 ⫾ 15.8 23.5 ⫾ 13.9

8.4 ⫾ 3.8 132.3 ⫾ 22.5 35.4 ⫾ 21.3 24.8 ⫾ 12.6

NOTE. Values expressed as mean ⫾ SD. Differences are not significant.

for each child. Protocols for all test items were taken from the Fitnessgram Test Administration Manual.12 The selected test items were chosen because the motor skill requirements in these tests were minimal, thus minimizing a practice effect for the children. Consequently, this obviated the need for extensive practice for each of the tests. Subjects completed a physical activity questionnaire modified from Bar-Or.13 The questionnaire required the children to estimate their physical activity levels against those of their healthy peers. Stature was measured with a portable stadiometer to the nearest centimeter. Mass was measured with the Detecto Scale (Cardinal Scale Manufacturing, Webb City, MO) to the nearest kilogram. Body composition consists of different types of tissue (skeletal, muscle, fat, and residual mass). Fat mass, normally assessed through simple skinfold measurements, has often been related to health problems and regarded as a potential health risk factor.14 Body composition was estimated by taking skinfold measurements of the triceps and calf (calipers from Lange Country Technology, Gays Mills, WI). The triceps and calf skinfolds were selected because of the ease of measurement and high correlation with percentage of body fat.15-17 Validity of this test has been documented to be 0.76 to 0.83 for boys and girls aged 6 to 16 years.18 A laboratory measure of VO2max is generally considered the best measure of aerobic power.19,20 However, this approach requires specialized expensive equipment and a laboratory environment. In the present study, aerobic power was measured with the progressive aerobic cardiovascular endurance run (PACER). This field test for cardiorespiratory fitness has shown strong reliability and validity against directly measured VO2max.21 Validity of this test has been documented to be 0.70 for boys and girls aged 8 to 19 years.22 Reliability was 0.89 for boys and girls aged 6 to 16 years.23 The rationale for selection of the PACER was its applicability for all ages and ease of administration. Details of the PACER protocol can be found in the Fitnessgram Test Administration Manual.12 One week after the picnic, a small group of children who had received LTs (n ⫽ 5) came to an indoor sports center to perform the test to confirm the test-retest reliability of the test.


Pearson’s correlation coefficient of 0.91 was obtained for testretest reliability. Muscular endurance is defined as the ability of specific muscle groups to sustain muscular force through repeated contractions to a point of fatigue.24 Abdominal muscle endurance can be evaluated using repeated curl-ups performed to exhaustion. The curl-up was selected because it does not involve the assistance of the hip flexor muscles and minimizes compression in the spine compared with a full sit-up with the feet held.25 All subjects had 5 minutes of standardized explanation and practice time; the protocol is described in the Fitnessgram Test Administration Manual.12 Objectivity and reliability of the test has been documented to be 0.99 and 0.88 for children and adolescents, respectively.26 Flexibility is defined as the range of linear limb motion around a specific joint.27 Flexibility of the lower back and hamstrings muscles was tested with the back-saver sit and reach. This test is very similar to the traditional sit and reach except that the measurement is performed on 1 side at a time; therefore, subjects are not encouraged to hyperextend. Validity of this test has been documented to be between 0.96 and 0.99 for boys and girls aged 11 to 15 years on both sides of the body. Reliability in the same study28 was 0.99.

Statistical Analysis Unpaired t-tests were used to determine the differences between the LT and control subjects in age, mass, stature, and results for the back-saver sit and reach, curl-up, and PACER tests. Comparisons were considered significant at P less than .05. To compare the LT group and the control group against Fitnessgram standards, we used the percentages of children who were able to reach the criterion-referenced standard for their age. Pearson’s product-moment correlation coefficients were used to assess the test-retest reliability of the PACER, association between months posttransplantation and both curl-up and PACER performance, and the association between serum hemoglobin levels and PACER performance. Microsoft Excel 97 (Microsoft Corp, Redmond, WA) was used to analyze the data.

Results Twenty-nine children (20 boys, 9 girls) had undergone liver transplantation. Two of these children (1 boy, 1 girl) had received combined liver-kidney transplants. Mean age at transplantation was approximately 52 months (LT group; 51.6 ⫾ 48.3 months [SD]), and all children underwent 1 protocol liver biopsy posttransplantation. Thirty-four children (22 boys, 12 girls) served as able-bodied controls. As listed in Table 1, the 2 groups had similar age, stature, body mass, and sum of skinfold measurements. Causes of the disease conditions that led to liver transplantation were as follows: 11 children had biliary atresia; 3 children, ␣1-antitrypsin deficiency; 2 chil-


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Table 2. Activity Characteristics of Pediatric LT Recipients and Able-Bodied Controls LT (n ⫽ 22) Control (n ⫽ 21) As active as friends More active than friends Less active than friends Comparison too difficult

11 (50%) 2 (9%) 8 (36%)

10 (48%) 8 (38%) 2 (10%)

1 (5%)

1 (5%)

dren, primary hyperoxaluria (both received combined liver-kidney transplants); 2 children, Alagille syndrome; 2 children, familial cholestatic liver disease; and 2 children, fulminant hepatic failure. The other children had glycogen storage disease type 1-B, NiemannPick disease, hepatitis (of unknown origin), sclerosing cholangitis, methylmalonic acidemia, cryptogenic cirrhosis, and ornithine transcarbamylase deficiency. The transplant recipients were 56.3 ⫾ 35.5 (SD) months posttransplantation. The LT group was on multiple medication regimens. The major medications administered were antibacterial agents, antisecretory compounds (gastric acid suppressors), and immunosuppressive agents. The major antibacterial agent was a combination drug of trimethoprim and sulfamethoxazole (15 subjects). Seven subjects were administered omeprazole as the major antisecretory agent. The remaining subjects were not administered an antibacterial or antisecretory compound. The immunosuppressives administered were cylosporine (17 subjects), FK506 (9 subjects), and prednisone (3 subjects). After transplantation, the discharge recommendation for all patients was to encourage them to participate in walking, but no specific exercise prescription was given. No preexisting hepaticpulmonary complications existed in the children tested. Serum hemoglobin values were obtained from all pediatric LT recipients at a clinic visit before the fitness testing session. Sixty children participated in the PACER, 59 children participated in flexibility testing, and all control subjects completed flexibility testing. However, 2 children in the LT group and 1 child in the control group were unwilling to perform the PACER test despite encouragement from the researchers. Four subjects from the LT group did not perform the flexibility testing despite encouragement from the researchers. Fiftythree subjects completed the curl-up. However, 6 children in the LT group and 4 children in the control group did not take part in the testing because they were

unwilling to perform the protocol (despite encouragement) and also were unable to maintain appropriate form to achieve a valid curl-up. The mean completion rate for all tests was 92%. There were no statistically significant differences with regard to the physical characteristics described in Table 1. Seventy percent of the subjects completed the questionnaire (22 children, LT group; 21 children, control group). The primary reason for not completing the questionnaire was the young age of some of the subjects. Approximately equal numbers of subjects from both groups rated their activity levels similar to those of their friends. However, only 2 children from the LT group rated their activity level to be more active than their friends compared with 8 children in the control group. Eight children in the LT group rated themselves less active than their peers compared with only 2 children in the control group (Table 2). One control and one LT subject who took the questionnaire found the comparison too difficult to make. The only statistically significant difference (P ⬍ .05) between the LT and control groups in the fitness testing was the number of shuttles completed in the PACER (Table 3). Control subjects completed a significantly greater number of shuttles than the LT group. Using criterion-referenced standards (Tables 4 and 5), Fitnessgram has established a range of performance that able-bodied children are expected to meet to be in the healthy fitness zone (HFZ). The LT and control groups were assessed for the proportion of children who achieved this HFZ. For the test of abdominal strength and endurance (curl-up), only 35% of the LT group (8 of 23 children) were within the HFZ. Seventy percent of the control group (21 of 30 children) achieved

Table 3. Comparison of Fitness Results Between LT and Control Groups

Back-saver sit and reach (in.) Left side Right side Curl-up (no. performed) PACER (no. of shuttles run)



10.3 ⫾ 2.1 (n ⫽ 25) 10.4 ⫾ 1.8 (n ⫽ 25) 12.0 ⫾ 16.5 (n ⫽ 23) 11.5 ⫾ 8.4 (n ⫽ 27)

10.2 ⫾ 1.6 (n ⫽ 34) 10.3 ⫾ 1.7 (n ⫽ 34) 15.0 ⫾ 16.1 (n ⫽ 30) 16.8 ⫾ 9.8* (n ⫽ 33)

NOTE. Values expressed as mean ⫾ SD. * P ⬍ .05.


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Table 4. Fitnessgram Standards for the HFZ in Boys

Age (yr)

PACER (minimum laps)

PACER (maximum laps)

Curl-Up (minimum)

Curl-Up (maximum)

Sit and Reach* (in.)

5 6 7 8 9 10 11 12 13 14 15 16 17 17⫹

† † † † † 23 23 32 41 41 51 61 61 61

† † † † † 61 72 72 72 83 94 94 94 94

2 2 4 6 9 12 15 18 21 24 24 24 24 24

10 10 14 20 24 24 28 36 40 45 47 47 47 47

8 8 8 8 8 8 8 8 8 8 8 8 8 8

* Inability to reach 8 in. constitutes failure of the test. † HFZ for PACER was not created for boys aged younger than 10 years. Modified and reprinted with permission from The Cooper Institute for Aerobics Research, 1999, FitnessGram:test administration manual, 2nd ed. (Champaign, IL: Human Kinetics), 38-39.

the HFZ. For flexibility of the hamstrings and lower back, most subjects were within the HFZ (left side: LT, 88% [22 of 25 children] v control, 87% [29 of 34 children]; right side: LT, 88% [22 of 25 children] v control, 88% [30 of 34 children]). In the PACER, none of the LT subjects (0 of 8 children) and only 36% of the control subjects (4 of 11 children) achieved the HFZ.

Fewer children were used in this comparison because the criterion-referenced standard for the PACER is only for children aged 10 years or older. Statistically significant (P ⬍ .05) Pearson’s correlation coefficients of 0.51 (curl-up) and 0.37 (PACER) were obtained for their associations with months posttransplantation. Mean serum hemoglobin value for the

Table 5. Fitnessgram Standards for the HFZ in Girls

Age (yr)

PACER (minimum laps)

PACER (maximum laps)

Curl-Up (minimum)

Curl-Up (maximum)

Sit and Reach* (in.)

5 6 7 8 9 10 11 12 13 14 15 16 17 17⫹

† † † † † 15 15 23 23 23 23 32 41 41

† † † † † 41 41 41 51 51 51 61 61 61

2 2 4 6 9 12 15 18 18 18 18 18 18 18

10 10 14 20 22 26 29 32 32 32 35 35 35 35

9 9 9 9 9 9 10 10 10 10 12 12 12 12

* Inability to reach the score in inches at each age group constitutes failure of the test. † HFZ for PACER not created for girls aged younger than 10 years. Modified and reprinted with permission from The Cooper Institute for Aerobics Research, 1999, FitnessGram:test administration manual, 2nd ed. (Champaign, IL: Human Kinetics), 38-39.


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LT group was 13.1 ⫾ 3.9 (SD) g/dL. No association was found between serum hemoglobin values and number of shuttles run on the PACER (r ⫽ – 0.08) for the LT group.

Discussion The 3 major findings from this study are: (1) based on the PACER, the LT group showed reduced cardiorespiratory fitness compared with the control group; (2) despite the lack of difference between the 2 groups for abdominal strength and endurance, only 35% of the LT group achieved the HFZ for the curl-up; and (3) no significant differences between the 2 groups were noted for flexibility of the lower back and hamstrings. In addition, a mean completion rate of 92% across all tests implies that psychological motivation to perform each task was not a significant issue for these children. Time posttransplantation has been implicated as a possible factor in reduced cardiorespiratory fitness and work capacity in pediatric transplant recipients. Nixon et al5 showed a significant relationship (r ⫽ 0.73) between physical work capacity on the cycle ergometer and days posttransplantation in pediatric lung transplant recipients. The range of time posttransplantation for these patients was 52 to 4,170 days. These data seem to indicate that exercise tolerance might improve with time posttransplantation. However, Hsu et al29 reported no significant difference in cardiorespiratory fitness in pediatric heart transplant recipients tested 1 and 3 years after transplantation. In the present study, a lower level of cardiorespiratory fitness (measured by the PACER) was noted for the LT group; however, its association with time posttransplantation, although significant, was limited (r ⫽ 0.37). The average time posttransplantation for the group in the present study was 1,680 days. Because of the cross-sectional nature of the present study design; it is not possible to determine whether this lower level of cardiorespiratory fitness represents an improvement from the period immediately posttransplantation or a constant deficit present from the time immediately posttransplantation. Another factor that may have a role in the reduced cardiorespiratory fitness of the LT group is the effect of medication. Most of the LT group were administered multiple medications, making it difficult to determine the effects of any 1 medication. However, the primary medication for all the children was immunosuppressives, specifically cyclosporine. Many of the medications administered to the LT group also have the potential to cause myalgia (antibacterials), muscle weakness, and fatigue (glucocorticoids), factors that

could negatively affect cardiorespiratory fitness and muscle strength.30 The pretransplantation status of the child may also have a role in posttransplantation exercise performance. Low oxidative capacity of the working muscles as a result of the preexisting condition or physical deconditioning may have a major role in limiting the child’s exercise capacity after transplantation.5 The LT group generally rated their physical activity levels to be of a similar magnitude to those of their peers; only 2 children in the LT group rated their levels of physical activity greater than those of their peers. In addition, 8 children in the LT group perceived their levels of physical activity to be less than those of their peers. These 2 pieces of evidence seem to indicate either real or misplaced perceptions of deficits in the level of physical activity in the LT group. In able-bodied children, limited evidence exists to support the relationship between habitual physical activity and cardiorespiratory fitness.31 However, no data exist to confirm or refute this relationship in pediatric LT recipients. In the present study, no absolute differences were noted between the LT and control groups for abdominal strength and endurance; however, only 35% of the LT group achieved the able-bodied criterion-referenced standards for their age. Therefore, a lack of absolute differences between the groups should not mask the age-specific deficit in abdominal strength and endurance seen in the LT group. The surgical procedure for whole-organ liver transplantation is based on the techniques described by Ghobrial et al.32 This procedure involves entering the abdomen through a bilateral subcostal incision that can be extended up to the superior xyphoid process. The surgical procedure certainly would seem to affect abdominal muscle function, which could also impact on aerobic exercise performance.33 Therefore, the need to characterize abdominal muscle endurance becomes a significant issue. In adolescents, weak abdominal muscle strength has also been directly linked to low levels of habitual physical activity and an increased incidence of lower back pain.34 These weaknesses in abdominal strength can be overcome by increased physical activity and specialized training.35,36 No significant differences were noted between the 2 groups for flexibility, and a high proportion of both groups achieved the Fitnessgram criterion-referenced standards. Limited evidence exists to confirm the efficacy and significance of flexibility in clinical populations. Koch et al37 showed a 25% improvement in lower-limb flexibility and improvements in neck flexion and hamstring and lower-back flexibility in children who had undergone surgery to rectify congenital heart

Fitness and Transplantation

disease. Improvement in flexibility potentially can help improve activities of daily living. Fitnessgram established criterion-referenced standards rather than normative values for their fitness standards. The major limitation of using normative data is that the exercise performance of 1 child is compared directly against another child of a similar chronological age. It has been documented that factors that contribute to physical fitness and performance in exercise tests steadily improve with biological age, but the rate of this increase does not parallel increases in chronological age. Therefore, performance on exercise tasks is more closely related to the biological age of the child than the chronological age.38 Therefore, a comparison of fitness data against normative values (based on chronological age) could be considered invalid. Many pediatric LT recipients are stunted in their growth pretransplantation, further limiting such age-matched scores. To the best of our knowledge, this study is the first of its kind to characterize the fitness levels of pediatric LT recipients. The metabolic and muscular origins of the deficits in aerobic fitness and abdominal muscle strength and endurance seen in the LT group warrant further laboratory investigation. Efforts should be made to optimize increased function through increased physical activity.







12. 13.

14. 15.

Acknowledgment The authors thank the undergraduate students in the Exercise and Sport Science Department at the University of San Francisco for help in data collection; Jean-Paul Verhees (Women’s Soccer Coach at University of San Francisco), Laurie Carlson, Erin Rogers, John McDermott, and Diane Valmassoi for help at the annual pediatric liver transplant picnic; and Joanne Krasnoff (University of California at San Francisco) for reviewing the manuscript.

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