Quality of Life

Suboptimal long-term physical performance in children and young adults after pediatric allo-SCT

Abstract

We present a set of tests for physical performance used for annual prospective follow-up after a pediatric transplant. Of the 103 eligible patients transplanted at a mean age of 8.8 years, 94 were included. The results were divided into early, performed 1 (n=46) or 2 (n=12) years post transplant, and late tests (n=66), performed 4–16 (mean 6) years post transplant. A total of 30 patients had tests both at early and late time points (paired tests). The control subjects included 522 healthy age- and gender-matched schoolchildren. Using their test results, the s.d. score (SDS) was calculated for each patient and for each test individually. Both in the early and late tests, patients had the mean SDS for each test significantly lower (P<0.001) than controls, varying from −0.6 to −2.0 SDS. Specifically, tests measuring trunk muscles gave impaired results. In the group with paired tests, the results improved in four of six tests. In late tests, age at SCT, extensive chronic GVHD and being a sports club member correlated with the results. The potential beneficial effect of an exercise intervention program on impaired physical performance after pediatric SCT merits prospective studies.

Introduction

The possibilities for evaluating and the need to evaluate late effects and outcome after SCT have multiplied during the last 1–2 decades because of increasing survival rates and extended follow-up. Even if the majority of SCT survivors live a normal or near normal life, a number of late sequelae have been described.1, 2 Long-term impairment in physical performance has been suggested to be a significant contributor to a decreased quality of life among cancer patients.3, 4 Physical performance is associated with a number of factors, including cardio-vascular status, pulmonary function, nutritional status, musculoskeletal function and physical activity. Several methods have been used to evaluate physical performance during or after cancer therapy. The most common are a treadmill test,5, 6 peak oxygen uptake (VO2peak),7 muscle strength test with dynamometer,8, 9 functional mobility tests10, 11 and questionnaires.3

Impaired physical performance has been reported after cancer therapy, both among children and adults. Cancer-related fatigue and impairment in muscle function may constitute a serious and common problem.12 In adults, significant impairment in physical performance has been reported after high-dose chemotherapy, auto-SCT,5, 6 and after allo-SCT.13 Long-term follow-up studies focusing on physical ability or musculoskeletal function of transplanted children are few. According to a meta-analysis based on three articles, physical fitness measured by VO2peak tended to be reduced in survivors of childhood leukemia studied several years after treatment.7 Muscle strength was subnormal in a group of female survivors of childhood leukemia.8 Young adult survivors of childhood ALL had decreased muscle strength, associated with growth hormone deficiency and mobility deficits.11 A significant proportion of childhood cancer survivors treated on conventional protocols reported late effects that interfered with physical performance and restricted participation in daily activities.14 Limitations in physical performance were observed several years after pediatric SCT,3 in addition to increased coordination problems and muscle weakness compared with healthy siblings.

After SCT, children especially may be at risk for late musculoskeletal sequelae because of the effects of chemo- and radiotherapy on developing tissues. The aim of this study was to assess the physical fitness of transplanted children in a comprehensive manner, using a defined set of tests that are clinically safe, easily conducted and reproducible. We used these tests for prospective follow-up of transplanted children and young adults.

Patients and methods

This study was part of the follow-up program of patients treated with allo-SCT at the Hematology/Oncology unit of the Hospital for Children and Adolescents, University of Helsinki, Finland. Starting in December 1999, tests for physical ability were added to annual follow-up. Patients transplanted during the years 1990–2005 were included in the study. Eligibility criteria for this analysis were adherence to the post transplant follow-up program of the unit, age over 6 years during the tests and a relapse-free survival of at least 1-year post transplant. Children with antecedent neurological disorders and relapse of malignant disease were excluded.

Patients

Of the 103 eligible SCT patients, nine did not participate in the study. The reasons were severe pulmonary GVHD (n=1), severe joint problems due to chronic GVHD (cGVHD) (n=1), refusal (n=3) and lack of suitable time (n=4).

A total of 94 patients, 45 females and 49 males, transplanted at ages 1–19 (mean 8.8) years, were included. The underlying diagnoses were hematological malignancy (n=79), severe aplastic anemia (n=10), myelodysplastic syndrome (n=4) and chronic granulomatous disease (n=1). As conditioning for SCT, the patients had received high-dose chemotherapy with CY or cytarabine with (n=89) or without (n=5) TBI. Either HLA-identical sibling (n=45) or matched unrelated donor (n=49) grafts were used. The patients had regular follow-up visits at the outpatient clinic 1–6 times per month during the first follow-up year and subsequently with decreasing frequency, but at least once a year until 18–20 years of age. Routine measurements included height and weight, and calculation of body mass index (BMI, kg/m2). Relative heights in SDS were estimated from national Finnish growth charts.15

Designated early and late testing

Test results were categorized into early group and late group. The early group included the results of tests performed 1 year after transplantation. If these were not available, results of tests performed 2 years after transplantation were included in this group. The late group included test results obtained after a minimum of 4 years after transplantation. In the case in which there were several sets of tests belonging to the late group, results of the most recent tests were chosen.

All eligible patients were included in this study. However, when the tests were incorporated in the follow-up program, some patients were several years after SCT and, therefore, lacked data for early tests, and at the end of the study, some patients were still less than 4 years after SCT and hence lacked data for late tests.

Early tests involved a total of 58 patients, 26 females and 32 males, who were studied 1 (n=46) or 2 (n=12) years after transplantation. Patient characteristics are given in Table 1.

Table 1 Characteristics of the patients tested 1–2 years and/or 4 years after transplantation

Late tests involved a total of 66 patients, 33 females and 33 males, studied 4–16 (mean 6) years after transplantation (Table 1).

Paired tests

A total of 30 patients had tests conducted both at early (1 year n=22, 2 years n=8) and late time points, 4–8 (mean 5) years after transplant. They were analyzed separately as a group for a potential individual change between time points, in addition to being included in the early and late test groups.

Control subjects

Control subjects included 522 healthy age- and gender-matched schoolchildren tested in ordinary primary and secondary schools. There were 274 girls and 248 boys tested at the age of 6–18 (mean 12) years. The number of controls in each age group varied from 35 to 68 (mean 47). All pupils in each class were invited to participate and 75% underwent the tests. The main reason for nonparticipation was forgetting to ask parents’ permission, parental refusal or acute viral infection.

Tests for physical performance

The tests used were slightly modified from those widely used in healthy persons.16, 17, 18 The same physiotherapist (MK) tested all patients. She also instructed and supervised the physiotherapy students who ran the tests on control subjects at their schools. The patients were tested during their regular outpatient visits if they were at their baseline condition, that is, without symptoms of infectious disease, previous anesthesia, etc. The tests were conducted in the physiotherapy department. Muscular endurance, strength, flexibility and speed were investigated by different tests.

The following tests were used (Figure 1):

  1. 1

    Leg-lift test: This test measures speed endurance of the lower extremities, especially the hip flexors. The subject stands in front of a bench, which is adjusted for the height of the subject, with hip and knee being in 90° flexion, with one foot resting on the bench. The subject is asked to lift both feet alternatively onto the bench as quickly as possible for 30 s. The number of lifts is recorded.

  2. 2

    Repeated squatting test: This test measures the dynamic endurance of the lower extremities. The subject is asked to repeatedly squat down and stand up as many times as possible for 30 s. On each round and when squatting, he/she touches a marked spot on the floor with the fingers of the dominating hand and then rises up to touch an individually designated mark on the wall with the stretched hand. The number of rounds is recorded.

  3. 3

    Sit-up test: This test measures the dynamic muscular endurance of trunk flexors. The subject lies supine with the knees flexed at an angle of 90° and the hands with fingers interlocked on the back of the neck. The tester keeps the subject's heels in contact with the floor. The subject is then asked to rise to a sitting position until the elbows touch the knees as many times as possible for 30 s without a pause. The number of rounds is recorded.

  4. 4

    Sit-and-reach test: This test measures the flexibility of the lower back and the hamstring muscles. The subject sits on the floor and, while keeping the legs straight, bends forward as far as possible. Feet are placed with the soles flat against a stable box. Both knees are held flat against the floor by the tester. The subject slides the hands, with the palms facing down on the box, reaching forward as far as possible. The distance of the slide with hands is recorded (cm).

  5. 5

    Back-extension test: This test measures the dynamic endurance of trunk extensors .The subject lies prone on the bench with ankles supported and the trunk from the sacral spine upward unsupported when in horizontal position. He/she is asked to lower the trunk by bending the waist to a 45 degree angle and then lifting the trunk up to a horizontal position, and repeating this as many times as possible for 30 s. The number of rounds is recorded.

  6. 6

    Shuttle-run test: This test measures acceleration, maximal speed and speed differentiation. The subject makes a 10 × 5 meters shuttle run as fast as possible (both feet over the line when turning). The time (seconds) spent is recorded.

Figure 1
figure1

Tests for physical performance (see text for explanation).

Statistical methods

SPSS software (SPSS Inc, Chicago, IL, USA) was used in statistical analyses. The mean value and s.d. of each test for controls per gender and age group was calculated by the 3-year-cohort (moving average) method, that is, by pooling the results of each age group in years, together with those of the previous and the next group. Using these control values, the s.d. score (SDS) was calculated for each patient and for each test individually (difference between the actual patient value and the mean value of the age- and sex-matched control group, divided by the s.d. of the control group). In the shuttle-run test, the worse results were higher in seconds and thus gave positive SDS values as compared with the other tests, in which poor results gave negative SDS. To unify the results, the SDS of the shuttle-run test was multiplied by −1. In addition to the SDS for each test, a designated personal muscle sum score was determined for each patient by calculating the mean SDS value for the five muscle tests (leg-lift, repeated squatting, sit-up, back-extension and shuttle-run tests). The personal muscle sum score was calculated separately for early and late time points. The SDS values of patients were used for analyses. The significance of differences in the early and late groups was calculated by the unpaired two-tailed t-test. The paired t-test was used for the group with both early and late tests. Independent samples t-test and one-way ANOVA (analysis of variance) were used to study the effect of cGVHD and exercise activity. Spearman's correlation coefficient test was used for the effect of age at SCT, height (s.d.) and BMI during the study and length of follow-up. A P-value of <0.05 was considered as statistically significant.

Results

Safety and feasibility

Of the patients invited to the study, only three refused to undergo tests. All patients were highly motivated and participated actively in the testing, which took 30 min. No adverse reactions or injuries were observed.

Early tests (1–2 years after SCT)

The mean SDS value for each test was significantly lower (P<0.001) in the 58 patients tested 1 or 2 years after SCT as compared with that of healthy controls, varying from −0.6 to −2.0 SDS (Table 2). The difference was highly significant, even if the four patients with a poor Karnofsky score (<80) were omitted. The percentage of patients with very poor results, that is, <−2 SDS, was 19% in leg-lift, 24% in repeated squatting, 48% in sit-up, 10% in sit-and-reach, 43% in back-extension and 19% in shuttle-run tests. Gender did not correlate with test results. Individual test results for female patients, both in early and late tests, are illustrated as compared with that of healthy controls in Figure 2. The mean value of muscle sum scores was −1.4 SDS (s.d. 1.0). It correlated with the Karnofsky/Lansky score (P=0.041) but not with gender, age at SCT, cGVHD or BMI.

Table 2 Results of physical performance tests in SDS (mean+s.d.) (that is, compared with healthy age and gender-matched controls, see: Statistical methods) in the patient groups investigated 1–2 years and/or 4 years after transplantation
Figure 2
figure2

Results of female patients in six different tests evaluating physical performance 1 or 2 years (early group) and 4 years (late group) after SCT. The hatched area represents results of the normal healthy age-matched girls (mean±1 s.d.).

Late tests (4 years after SCT)

The mean value of SDS for each test was also significantly lower (P0.001) in the 66 patients tested 4 years after SCT as compared with that in healthy controls, varying from −0.6 to −1.8 SDS (Table 2). The difference between patients and controls was highly significant, even if the four patients with a poor Karnofsky score (<80) were omitted. The proportion of patients with <−2 SDS was 10% in leg-lift, 19% in repeated squatting, 46% in sit-up, 18% in sit-and-reach, 23% in back-extension and 19% in shuttle-run tests. Gender, again, did not correlate with test results. The mean value of muscle sum scores was −1.1 SDS (s.d. 1.2). It correlated with the Karnofsky/Lansky score (P<0.001), age at SCT (P=0.002), extensive cGVHD (P=0.015) and membership in a sports club (P=0.03), but not with gender, follow-up time after SCT or BMI (Figure 3).

Figure 3
figure3

The muscle sum score at late evaluation (4 years after SCT) in designated subgroups defined by chronic GVHD, age at SCT, the Karnofsky/Lansky score and being a sports club member. Box plots showing the 10th, 25th, 50th, 75th and 90th percentiles are given.

Paired tests

An improvement in results (SDS) from early to late time points was found in four of six tests in the group of 30 patients with paired tests. Improvement was shown in leg-lift (P=0.002), repeated squatting (P=0.027), sit-up (P<0.001) and back-extension (P<0.001) tests. In sit-and-reach and shuttle-run tests, no significant change was observed. The change between early and late testing in individual SDS values of the different tests is illustrated in Figure 4. The muscle sum score in the group of patients with paired tests improved significantly between early and late testing, the mean values being −1.5 and −0.6, respectively (P<0.001).

Figure 4
figure4

Change in the results (s.d. score, SDS) of physical performance tests in individual patients during post transplant follow-up. (a) Tests performed 1 or 2 years after SCT. (b) Tests performed 4 years after SCT. *Improvement was statistically significant in leg-lift, repeated squatting, sit-up and back-extension tests.

Age at SCT

The age at SCT varied from 1 to 19 (mean 8.8) years. During early testing, age at SCT correlated with leg-lift results (Spearman's correlation coefficient 0.36, P=0.006), but not with other tests. During late testing, age at SCT correlated with all test results, except with those of sit-and-reach tests (correlation coefficients varying from 0.29 to 0.48, P-values <0.001–0.019). The muscle sum score correlated with age at SCT during late (P=0.002) but not early testing. The length of follow-up after SCT did not correlate with test results.

Chronic GVHD

In the early tests, patients (n=11) with extensive cGVHD had inferior results in all tests compared with other patients, but the difference was statistically significant only in the sit-and-reach test (−1.4 vs −0.4 SDS, P=0.013). Moreover, in late tests, patients (n=10) with extensive cGVHD had inferior results in all tests: repeated squatting (−1.6 vs −0.7, P=0.041), sit-up (−3.2 vs −1.5, P=0.001), sit-and-reach (−1.9 vs −0.7, P=0.005) and shuttle-run (−2.9 vs −0.8, P=0.001) tests. In leg-lift and back-extension tests, the difference was not significant. The muscle sum score correlated with extensive cGVHD during late (−2.0 vs −0.9, P=0.015) but not early testing (Figure 3).

Height and BMI

In early tests, the relative height (s.d.) correlated with sit-up test results (Spearman's correlation coefficient 0.344, P=0.008) but not with those of other tests. In late tests, neither height (s.d.) nor BMI correlated with any test result.

Exercise activity

During early testing, only six patients reported physical exercise at least once a week, and five patients reported membership in a sports club. Exercise activity did not correlate with the test results. During late testing, patients who were sports club members (n=15) had better results than did others in all tests, with statistical significance in sit-up (−0.7 vs −2.1, P=0.004), sit-and-reach (0.0 vs −1.2, P=0.002), back-extension (−0.5 vs −1.3, P=0.007) and shuttle-run (−0.3 vs −1.4, P=0.036) tests, and also in the muscle sum score (−0.4 vs −1.1, P=0.03) (Figure 3).

Discussion

In this study, a simple, quantitative and reproducible method to measure physical performance post transplant is described. Furthermore, by using these tests and the muscle sum score, individual physical performance could easily and reliably be translated into numerical values. Individual test results were transformed to SDS by comparing them with age- and gender-matched healthy controls. To define the general muscle performance of a given individual, a sum score for muscle tests was calculated. The good correlation of the muscle sum score with the Karnofsky/Lansky scores supports the validity of our physical performance test.

These physical performance tests were used in the post transplant follow-up of children and young adults. According to our results, transplanted patients had impaired results in all tests when compared with healthy controls. Impaired results were shown not only in the tests performed early, that is, 1 or 2 years after SCT, but also in those performed several years after SCT, even if some improvement was observed in the latter. No systematic exercise program was recommended to patients.

The tests performed were derived from a set of tests widely used in Finland for many years to evaluate physical fitness in healthy schoolchildren and young adults.16 Each test was planned to be suitable for and easily performed by patients of various ages and conditions during regular outpatient visits. In our experience, the lower age range for proper testing was 6–7 years. Safety is important when patients with suboptimal muscle strength and balance are investigated. In addition to physical components, psychological aspects are also important when motivating adolescents to achieve optimal results in fitness tests. As even small changes in conducting the tests may cause differences in results, it is optimal to have, as we did, the same tester supervising the tests each time. Moreover, with healthy controls of the same age and sex, exactly the same tests and preferably the same tester are essential. Our controls were a sizable group of pupils from ordinary schools with no special preference for sports. About one-fourth of those invited did not perform the tests for various reasons. Although possible, we consider it unlikely that their participation would have essentially influenced our reference values.

In this study, all transplanted patients over 6 years of age, in remission and with regular follow-up visits were invited to participate. In total, 2 of 103 patients were excluded because of severe cGVHD, and 3 refused to participate. Thus, the tested patients well represent a general pediatric post transplant cohort. This is also reflected by the activity status of patients (Karnofsky/Lansky) when mild-to-moderate restriction was found in about 20%, well comparable with EBMT data.19

Dynamic muscular endurance was impaired in all muscle groups studied. Specifically, the muscle groups needed to support the body, that is, the abdominal muscles in the sit-up test and the back muscles in the back-extension test, gave poor results. Among the patients investigated several years after SCT, 12 of 66 could not perform any sit-ups (Figure 2). The difference is striking when compared with healthy controls in whom 6 of 522 were unable to perform sit-ups (data not shown). The inferiority of muscle endurance of the lower extremities was significant, but less remarkable. It is possible that the walking needed in everyday life supports muscle strength of the lower extremities, whereas abdominal and back muscles do not necessarily have as much exercise without special intervention.

A possible change in test results with follow-up was evaluated in those patients who had paired tests from both early and late time points. Significant improvement was observed in all muscle endurance tests, but, nevertheless, the late test results still remained impaired. Our finding of improvement in muscle tests with time is in accordance with the report by Hogarty et al. showing an improvement in cardiopulmonary exercise tests. They showed an increase in maximal oxygen consumption and maximum work studied at 1.6 and 6.1 years after pediatric SCT, but the values remained inferior compared with controls. They hypothesized that increased oxygen extraction at the level of the exercising muscle would explain the improved aerobic capacity.20

There are many different factors that explain subnormal physical performance after SCT. It may be a direct effect of chemotherapy and radiotherapy on developing muscle and nerve tissues, or it may be an indirect consequence of treatment of malignant disease and SCT through other mechanisms, such as decreased growth hormone secretion,21 cGVHD, or combined physical or psychosocial effects. In a previous study, no association between muscular endurance strength and height or BMI was observed among leukemia survivors.8

Young children have been shown to be more sensitive than older ones to the adverse late effects of SCT, at least regarding growth and neuro-cognitive functions.22, 23 There are no reports on the effect of age at SCT on the subsequent physical performance. A correlation between poorer test results and younger age at SCT was shown in this study. The sensitivity of growing muscle and nervous tissue to irradiation may be one explanation. Young transplanted children constitute a special group for follow-up.

We show that cGVHD was associated with impaired physical performance. Stiffness is a common symptom of cGVHD and thus inferior results in the sit-and-reach test were expected. Inferior results in patients with extensive cGVHD were also observed in all other tests at the late time point, indicating a long-lasting debilitating effect of cGVHD on children and young adults. A strong association of muscle weakness and cGVHD was also shown in a previous study on the basis of a self-reported questionnaire.24

The question may arise whether intervention with a physical exercise program would make a difference, not only for physical performance but also for general health and quality of life. Regarding healthy children and those with conventional therapy for ALL, an increasing amount of data have been published on the beneficial effects of physical activity on weight control, type II diabetes, blood pressure, osteoporosis, psychological well being and fatigue, with many of them being a special risk for transplanted children.25 Adult long-term survivors of childhood ALL were more likely to be physically inactive than was the general population.26 In our study, among the patients tested for 4 or more years after SCT, the sports club members had better results in all tests when compared with others. There are several studies of transplanted adults advocating the beneficial effect of physical exercise intervention.4, 9, 13, 27 There are hardly any studies on the effect of an exercise program in children. In a small group of children, 12 months post transplant, the experience of physical and overall health benefits after an 8-week exercise training program was reported.28

A direct correlation between muscle strength and physical well being after SCT has not been reported, but an association between physical participation restriction and performance limitation was reported among childhood SCT survivors.3 A poor performance status can easily lead to less physical activity, thus functioning as a vicious cycle. It is obvious that muscle strength of the lower extremities is needed for walking and running, and the abdominal and back muscles are essential in everyday life to support the trunk and spine, thus having an effect on balance and preventing falling and spinal distress. The potential beneficial effects of physical exercise and a good physical performance status on multiple known late post transplant sequelae, such as primarily metabolic syndrome and osteoporosis, remain to be shown.

We present a set of tests for physical performance that are easy, reliable and reproducible, with the results being translatable into numerical values. When applied to transplanted patients, children and young adults had impaired physical performance up to several years after SCT when compared with healthy controls. Extensive cGVHD and young age at SCT were risk factors. An exercise intervention program might have beneficial effects on physical performance, general health and quality of life, but that factor remains to be shown in prospective studies.

Conflict of interest

The authors declare no conflict of interest.

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Acknowledgements

This study was supported by the Nona and Kullervo Väre Foundation.

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Correspondence to L Hovi.

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Hovi, L., Kurimo, M., Taskinen, M. et al. Suboptimal long-term physical performance in children and young adults after pediatric allo-SCT. Bone Marrow Transplant 45, 738–745 (2010). https://doi.org/10.1038/bmt.2009.221

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Keywords

  • physical performance
  • children
  • transplantation
  • late effect
  • muscle tests

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