With improvements in surgical methods and medical treatment for transplantation,1 clinical attention has shifted from maximizing short-term transplant recipient survival to optimizing long-term survival.2 Given the organ shortage, transplant recipient self-care management is essential to foster patient and graft survival.3 Accordingly, transplant recipients need to undertake a complex posttransplant self-care regimen that involves healthy lifestyle and behavior modifications.
A major lifestyle recommendation entails engagement in sufficient physical activity (PA) posttransplant to prevent cardiovascular disease and promote patient and graft survival. The primary cause of death for kidney recipients is cardiovascular disease.4-6 Reported 5-year mortality rates from cardiovascular disease in heart and kidney transplant recipients are 30% and 15% respectively.7 In hepatic and pancreatic transplant recipients, cardiovascular complications are the leading cause of death.8-11 Regular PA and exercise can effectively lower lipid profiles, blood pressure, and improve insulin sensitivity12 and are considered essential for cardiovascular risk prevention.13
Current international guidelines recommend at least 150 minutes of moderate intensity or 75 minutes at vigorous-intensity PA per week for healthy adults age 18–64 years.14 While official guidelines for PA in the transplant setting do not exist,4 guidelines for those with chronic diseases recommend similar levels of exercise guided by the individual’s exercise capacity.15 While organ transplant recipients generally do not meet recommended levels of PA in the immediate posttransplant period secondary their postsurgical state, prolonged bedrest, and compromised overall status, most can engage in PA after recovering from surgery. Yet, based on the US Surgeon General’s guidelines recommending moderate-intensity PA 3 or more times per week for at least 30 minutes, only 22%–50% of transplant recipients report being regularly physically active at 1–2 years posttransplant.16-18
A systematic review and meta-analysis focusing on exercise training after transplantation found that exercise training, particularly programs of longer duration, can improve exercise capacity in cardiac transplant recipients.7 Another systematic review suggests improvement in functional exercise capacity, skeletal muscle function, and lumbar bone mineral density in lung transplant recipients after structured exercise treatment.19 While supervised, exercise programs were examined in these reviews, little research has focused on PA in daily life. Given the established benefits of PA, identifying modifiable factors associated with inadequate PA following transplantation is important for designing interventions to encourage PA. In addition, better understanding the associations between low PA and various posttransplant outcomes will provide evidence to encourage clinicians to discuss the importance of PA in daily life and may help to influence attitudes and increase patients’ motivation to engage in PA following transpantation. This systematic review and meta-analysis aimed to examine the correlates and outcomes of low PA following solid organ transplantation in adult recipients.
MATERIALS AND METHODS
The systematic review was conducted following methodology described in the Center for Reviews and Dissemination handbook,20 and data reporting follows the PRISMA guidelines.21 This review was a part of the Brocher Foundation-funded grant to develop a solid organ transplant endpoint model on relationships between influencing factors and outcomes of transplant self-management (B-SERIOUS) research project, which aimed to assess the relationships between selected post-transplant behaviors (ie, low PA, medication nonadherence, smoking, and alcohol use), and correlate and outcomes in kidney, liver, lung, and heart transplant recipients, to develop a solid organ transplant endpoint model on relationships between possible influencing factors and outcomes of post-transplant self-management behaviors. The B-SERIOUS review protocol was registered in the PROSPERO database (registration number: CRD42015003333).22
Studies included in the review varied widely in their definition and measurement of PA. Thus, for the purpose of this review, we defined low PA as not meeting the individual study’s identified target for being physically active. For studies examining PA as a continuous variable and no specific cutoff was defined, lower PA was compared to higher PA.
We conducted systematic electronic literature searches of the PubMed, Embase, PsycINFO, and Ebscohost CINAHL databases to identify relevant studies published from inception until February 3, 2016. A PubMed search string (Table 1) was initially designed in collaboration with a health science librarian (M.L.K.) and was adapted to all databases searched (search strings are available from the researchers on request). All search strings combined controlled vocabulary (eg, MeSH terms) and free text words representing the concepts of PA and solid organ transplantation. In addition, the reference sections of all eligible articles were reviewed to identify additional articles. Four review authors (L.B., A.S.T., E.G., and C.K.) assessed titles and abstracts of all records retrieved. After consensus had been reached, 3 pairs of authors (L.B./A.S.T., E.G./T.G., and A.R./C.K.) independently reviewed all potentially relevant full-text articles using eligibility criteria described below. Disagreement was resolved by discussion between each pair of reviewers. A third author was consulted if consensus was not reached. No attempts were made to contact authors in instances of missing data.
After retrieving all references and eliminating duplicates, titles and abstracts were reviewed. Articles were eligible for full-text review if they (1) reported the results of original quantitative research; (2) included adult (age 18+ years) kidney, liver, lung, or heart transplant recipients; (3) measured PA posttransplant; and (4) examined the associations between posttransplant PA and correlates/determinants and/or clinical, economic, or health-related quality of life outcomes of posttransplant PA. Articles were excluded if they: (1) did not report results from an original quantitative study (eg, case reports, reviews, books, consensus documents, letters to the editors); (2) focused on recipients undergoing combined transplants (eg, kidney-liver), tissue transplantation, or vascularized composite allotransplantation (eg, stem cell transplantation); (3) included children or adolescents (<18 years of age); or (4) examined PA that was a part of a study intervention.
Next, full text of all potentially eligible articles (ie, all articles judged by at least one reviewer to fulfill all initial inclusion criteria) were screened independently by two reviewers applying the following inclusion criteria: (1) reported in either English, Dutch, German, French, Portuguese, Italian, or Spanish; (2) full-text article available; (3) reported original research (not book chapter, case study, or case series with no descriptive data); (4) employed quantitative or mixed methods; (5) focused on adults or reported results separately for adult subjects; (6) results were reported for single organ kidney, liver, lung, or heart transplant recipients; (7) measured posttransplant PA; (8) empirically assessed the associations between predictors, correlates, or determinants of posttransplant PA and/or empirically assessed the associations between posttransplant PA and clinical, economic outcomes, and health-related quality of life; and (9) reported statistical data (eg, mean, standard deviation [SD], test-statistics, P values) necessary to calculate an effect size (at a minimum, the sample size and a P value less than or more than a specified value (eg, P < 0.05). Articles were included if both reviewers agreed that the article fulfilled all inclusion criteria. Disagreements were resolved by consensus discussion or consultation by a third reviewer.
Using a standardized data extraction database developed in Access (version 2007, Microsoft Corp., Redmond, WA), the following data were extracted from each included article: general information (eg, journal, year of publication, language of article, country and continent where the study was conducted, funding source, and organ type); study methodology (eg, study design, sample size, participants’ mean age, time since transplant, sex and race frequency distributions of participants); use of a theoretical framework; the method used to measure PA; the prevalence of low PA; and correlates and posttransplant outcomes examined in relation to PA or low PA. The World Health Organizations’ taxonomy for classifying correlates of medication nonadherence (eg, social/economic-related, patient-related, condition-related, treatment-related, and healthcare system-related correlates)23 was applied to classify the correlates of post-transplant low PA. Post-transplant outcomes included economic, clinical, and health-related quality-of-life outcomes. To be considered an outcome, a clinical condition (eg, diabetes, cardiovascular disease) needed to be diagnosed following transplant. Conditions known to be present before transplant were considered condition-specific correlates. Two reviewers independently extracted data from each study. Inconsistencies were resolved by discussion or through consultation with a third reviewer.
To assess the quality of included studies, we used an adapted checklist of 14 criteria.24,25 Each criterion was rated as reported (yes), not reported (no), partially reported or not applicable. The study sample size was considered adequate if it was formally calculated and reported a priori, at least 104+m subjects for bivariate analysis, where m is the number of independent variables evaluated, or 50 + 8m subjects for multivariate analysis.26 A study was considered reproducible if the methods (ie, sampling method, measurement of PA, outcomes and correlates, and data analysis) were described in enough detail that the study could be replicated. Two members of the research team independently rated the quality of all included studies. Any disagreements were resolved by discussion.
Study and participant characteristics were analyzed descriptively (frequency counts and percentages, means, SDs, and ranges, as applicable). For characteristics such as age and time since transplant when the mean and SD were reported in individual studies, a weighted mean and pooled SD were calculated. When there was a sufficient number of studies (ie, at least 5 independent studies) and with sufficient data to calculate an odds ratio (OR) and its 95% confidence interval (CI) for at least one correlate or outcome, the pooled OR for low PA was calculated across the included studies using a random-effects model.27 Comprehensive Meta-Analysis software (version 2.2, Biostat, Inc., Englewood, NJ)28 was used for the meta-analysis. For each statistically significant pooled effect size, we estimated the impact of publication bias by calculating the classic fail-safe N.29 The fail-safe N is the number of nonsignificant studies that would need to be included to make a significant pooled effect size nonsignificant. We calculated the Q statistic to determine whether there was significant variability in effect sizes among studies. Because the Q test has limited power to detect significant heterogeneity when the number of studies is small, we also calculated the T2 (the estimated variance of the true effect sizes) and I2 (the percentage of variations across studies due to heterogeneity rather than chance) indices to summarize the heterogeneity in effect sizes across the independent studies.29 Correlates and outcomes examined in fewer than five independent studies were excluded from the meta-analysis and the percentage of studies reporting statistical significance were summarized. Four of 11 studies that examined the relation between time since transplantation and low PA used single-group pretest-posttest design or repeated measures analysis. An OR and 95% CI could not be calculated for these studies. Consequently, they were not included in the meta-analysis, and their findings, along with the correlates and outcomes examined in fewer than 5 studies, were summarized in a tabular format.
The electronic searches returned 9888 references (Figure 1). After eliminating duplicates and adding one additional reference identified during screening of the reference list of included articles, 7401 (74.8%) unique references were identified. After screening for initial eligibility by title and abstract, 924 (12.5%) articles were identified for full-text review. Finally, 34 studies (3.7% of the screened full-text articles) were included in the qualitative synthesis (Table S1, SDC,https://links.lww.com/TP/B689) and 15 (1.6% of the screened full-text articles) were included in the quantitative synthesis (meta-analysis).
Study and Participant Characteristics
Characteristics of included studies are described in Table 2. Two studies reported their findings in two different articles each.30-33 Consequently, we included 34 studies reported in 36 articles. Slightly more than half of the studies (n = 18, 53%) were conducted among renal transplant recipients. Most studies were conducted in Europe (n = 21, 62%), followed by North America (n = 8, 24%). The mean sample size over all studies included was 99 (SD = 100.9), ranging from 8 to 540. Across studies, most participants were male (60%). Among studies reporting the participants’ ages, the weighted mean age was 50 years, ranging from 18 to 79 years. Eighteen studies reported the mean time since transplantation with the weighted mean across these studies being 53 months.
Methods Used to Measure PA
A variety of subjective and objective methods were used to measure and quantify PA, including self-report questionnaires (n = 27, 79.4%), objective measures (accelerometer or pedometer (n = 6, 17.6%), and a combination of self-report and objective measures (n = 3, 8.8%). As shown in Table S1, SDC,https://links.lww.com/TP/B689, fifteen studies (15/34; 44.1%) did not provide a definition of low PA. Of the studies that provided a definition, the definitions varied widely and none were based on current guidelines on PA in adults.14 Given the diversity of methods used to assess PA and its definition, we were unable to calculate overall prevalence rates of low PA.
Figure 2 reports the results of the quality assessment of the included studies. Most studies used and described appropriate data analysis methods (n = 30, 88.2%), reported the eligibility criteria used to select participants (n = 23, 67.6%), included a definition of low PA (n = 14, 41.2%), and reported when PA was assessed (n = 21, 61.8%). The quality criteria fulfilled by the fewest studies were comparison of the study sample to the overall transplant population (n = 3, 8.8%) and reproducibility of the study based on the key criteria reported (n = 6, 17.6%). No studies were excluded on the basis of the quality appraisal.
Correlates of Low PA
A total of 30 correlates of low PA were examined in the studies included in this systematic review. Correlates were classified as follows: condition (n = 11), social/economic (n = 9), patient (n = 4), healthcare system (n = 3), and treatment (n = 3) related. Only 4 correlates met our criteria for inclusion in a meta-analysis: age, posttransplant body mass index (BMI), sex, and time since transplantation. Their pooled ORs and 95% CIs are reported in Table 3 and displayed in the forest plot in Figure 3. None of the correlates examined in the meta-analyses were significantly related to low PA following solid organ transplantation. Except for sex, substantial heterogeneity was detected for the correlates examined, as evidenced by an I2 of 91.02% for age, 68.5% for posttransplant BMI, and 76.8% for time since transplant. There was less heterogeneity for sex (male); I2 was 33.9%. Time since transplantation (a treatment-related correlate) was examined in 8 studies where an effect size could be calculated. The pooled effect size for these studies was not significant (OR = 0.83; 95% CI, 0.47–1.47). However, this correlate was also examined in 4 single-group prospective studies that used pre-post or repeated measures analyses to examine its relationship with low PA. We were unable to identify a valid method to calculate an effect size estimate for these analytic approaches, and thus these studies were excluded from the meta-analysis. Three of the four found a significant inverse relationship between time since transplantation and low PA (ie, as time since transplant increased, the level of low PA decreased).34,51-53
Most correlates were examined in only 1 or 2 studies (Table 4), and many of the relationships were not significant. An exception was posttransplant blood pressure/hypertension, which was significantly related to low PA in 3 of the 4 studies examining this relationship.33,35,36,40
Outcomes of Low PA
Nineteen outcomes were reported. Only one outcome, physical health-related quality of life, was examined in 6 studies and, thus, had a pooled effect size calculated (Table 3 and Figure 3). There was a significant negative association between low PA and physical health-related quality of life (OR = 0.172, 95% CI, 0.08–0.37; I2 = 69.60%). Low PA was associated with worse physical health-related quality of life compared to being more physically active. Most of the other 18 outcomes were only examined in a single study and were significantly related to low PA (Table 4).
This systematic review examined the relationship between low PA correlates and outcomes following single kidney, liver, lung, and heart transplant in adults. Overall, relatively few studies examined correlates and outcomes associated with PA in posttransplant recipients. Among the 30 correlates that were investigated, only 4 were examined in a sufficient number of studies to perform meta-analyses—age, gender, posttransplant BMI, and time since transplant, and none were significantly related to low PA. While we did not find a statistically significant relationship between time since transplant and low PA, we excluded 4 studies from the meta-analysis because we were unable to calculate an effect size. Inclusion of these studies in the meta-analysis may have changed the results. Most of the other correlates were examined in only 1 or 2 studies. Additional research is needed to examine the association between these characteristics and PA following solid organ transplantation.
Nineteen studies assessed the association between PA and posttransplant outcomes, but only one, physical health-related quality of life, was examined in enough studies to conduct a meta-analysis. Low PA was associated with poorer physical health-related quality of life in comparison with higher levels of activity. This is consistent with the findings of systematic reviews in other chronically ill populations.66-68 Most outcomes were not assessed in at least 5 studies, so no meta-analysis could be performed. Surprisingly, no studies investigated the impact of low PA on mortality or graft survival, pointing to a gap in the evidence base, given that evidence from other chronically ill populations show that low PA has a negative impact on hard outcomes.69,70 Although the number of studies that assessed clinical outcomes is small, data are suggestive that PA might be associated with a lower likelihood of a metabolic syndrome, better cardiovascular fitness, and lower risk of osteoporosis and better mineral bone density33,36,57-59,61-63 in selected solid organ transplant recipients. These findings should be confirmed by further research.
A strength of this review is the focus on PA as a part of individuals’ normal daily activities. While structured exercise programs can play an important role in early posttransplant rehabilitation, and later care for select patients, they are generally of limited duration and potentially costly. Lifestyle change in terms of increased PA may not be sustained by such programs. Given that most beneficial effects of PA depend on sustained engagement, it is important to examine the effects of PA that is a part of individuals’ normal daily activities.
The methodological quality of the included studies varied widely. All studies were observational which is to be expected given that the focus of the review was on PA that participants engaged in during their daily lives. However, most studies used cross-sectional designs which further limit the ability to infer causal relationships between low PA and the correlates and outcomes measured. The methods used to measure PA varied across studies with the majority using self-report.
There are limitations to this review. Despite the extensive and rigorous search process used to identify published studies, relevant articles may have been missed. We included published studies and may have missed studies that were not published in peer-reviewed databases. While we included articles published in 7 languages, 17 articles were excluded because they did not meet our language-related criteria. The methodology and the methodological quality of the included studies varied widely. Not all authors provided a definition of PA. The reported definitions differ among studies as well as methods used to measure PA. The majority used (nonvalidated) self-report measures. Most studies used a cross-sectional design not allowing one to infer causal relationships between low PA and the correlates and outcomes. Reported statistical data varied in completeness and some effect size estimates were highly estimated (eg, based only on P values and sample sizes). For most of the correlates and the outcome with sufficient studies to perform meta-analysis, there was a substantial degree of heterogeneity based on I2 values. While random-effects analysis was appropriately used during meta-analysis, the small number of studies available for each of the correlates and the outcomes examined precluded our ability to conduct sensitivity or subgroup analysis to identify potential sources of the heterogeneity. Most studies were conducted in European settings and most of the study participants were renal transplant recipients. This may limit the generalizability of our findings to other settings and other organ transplant recipients.
Recommendations for Clinical Practice
Clinicians should motivate and educate patients on the importance of regular PA for their health and well-being. Transplant recipients should be encouraged to meet current PA guidelines for individuals with chronic disorders15 as their capacity permits. PA should be regularly assessed as a part of routine posttransplant follow-up, preferably by activity monitors instead of self-report to gain a more objective insight in what patients are doing in their daily lives. For patients whose exercise capacity is markedly limited, the best initial approach is a structured and monitored exercise program. Gaining insight in barriers of low PA might help to delineate further avenues for tailored supportive interventions.
Recommendations for Future Research
This systematic review has important implications for future research. First, while there are published guidelines for PA in adults 18–65 years of age and adults age 55 and older with other chronic conditions,14,15 there is an urgent need for a consensus definition on what sufficient PA entails for transplant populations. Existing recommendations on PA can be used as a starting point in this regard.14,15 Standardization of definition would facilitate comparison of studies and will allow to identify the evidence gaps as well as the implications for clinical practice.15
Second, researchers are encouraged to use activity monitors to document PA. If this is not possible, researchers should only use valid self-report instruments for use in transplant populations. Third, correlates and risk factor of low PA should be assessed in a more comprehensive way and attention should be given to multilevel factors. Studies now only investigate one or a few risk factors, often not theory based. Using a theory-based approach fuels the evidence base to identify which variables, or a combination thereof, are most promising to be targeted for intervention. Prospective studies will contribute to establish causal relations between risk factors and PA on the one hand and between PA and outcome on the other hand. Intervention research is needed as this will provide the basis for true change in clinical practice. The quality of reporting studies can be enhanced by adhering to publication guidelines such as STROBE or CONSORT depending on the type of study.
We found a relatively small number of studies examining correlates and outcomes associated with low PA in solid organ transplant recipients. Most studies were conducted in kidney transplant recipients. The vast majority of correlates and outcomes were assessed in only one or two studies. The combined effect size estimates for the meta-analysis of age, sex, posttransplant BMI, and time since transplantation were not significant. We were only able to perform meta-analysis of one of the outcomes, physical health-related quality of life. Transplant recipients with low PA reported lower health-related quality of life than those who were more physically active.
The authors would like to thank Tracy Glass and Amy Disharoon for their contributions in the data abstraction phase.
B-SERIOUS consortium: Lut Berben, PhD, RN, Institute of Nursing Science, Department Public Health University of Basel, Switzerland; Isabelle Binet, MD, Nephrology and Transplantation Medicine, Cantonal Hospital St. Gallen, Switzerland; Hanna Burkhalter, PhD, RN, Centre of Sleep Medicine, Hirslanden Group Zürich, Switzerland; Sabina M. De Geest, PhD, RN, Institute of Nursing Science, Department Public Health University of Basel, Switzerland & Academic Centre for Nursing and Midwifery, KU Leuven—University of Leuven, Belgium; Paolo De Simone, MD, PhD, Hepatobiliary surgery and liver Transplantation, University of Pisa Medical School Hospital, Italy; Kris Denhaerynck, PhD, RN, Institute of Nursing Science, University of Basel, Switzerland; Fabienne Dobbels, Msc, PhD, Academic Centre for Nursing and Midwifery, KU Leuven—University of Leuven, Belgium & Institute of Nursing Science, University of Basel, Switzerland; Gerda Drent, RN, PhD, Department of Gastroenterology and Hepatology, University Medical center Groningen, Groningen, the Netherlands; Nathalie Duerinckx, PhD, RN, Academic Centre for Nursing and Midwifery, KU Leuven—University of Leuven, Belgium & Heart Transplantation Program, University Hospitals Leuven, Belgium; Sandra J. Engberg Sandra, PhD, School of Nursing, University of Pittsburgh, United States; Tracy Glass, PhD, Department of Biostatistics, Swiss Tropical and Public Health Institute, University of Basel, Switzerland; Elisa J. Gordon, PhD, MPH, Center for Healthcare Studies and Comprehensive Transplant Center, Northwestern University Feinberg School of Medicine, Chicago, United States; Monika Kirsch, PhD, RN, Department of Anesthesiology, University Hospital of Basel, Switzerland; Mary-Lou Klem, PhD, MLIS, Health Sciences Library System, University of Pittsburgh, United States; Christiane Kugler, PhD, RN Institute of Nursing Science, Medical Faculty, University of Freiburg, Germany; Stacee Lerret, PhD, RN, Department of Pediatric Gastroenterology and Transplant Surgery, Medical College of Wisconsin, United States; Anja Rossmeissl, MD, Departement für Sport, Bewegung und Gesundheit, University Hospital of Basel, Switzerland; Cynthia L. Russell, RN, PhD, School of Nursing and Health Studies, University of Missouri-Kansas City, United States; Arno Schmidt-Trucksäss, MD, PhD, Departement für Sport, Bewegung und Gesundheit, University of Basel, Switzerland; Susan M. Sereika, PhD, MPH, School of Nursing and Graduate School of Public Health, University of Pittsburgh, United States.
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