Abstract
Objective
This study aimed to investigate affected factors for subgroups of fatigue and the degree of fatigue in maintenance hemodialysis (MHD) patients.
Methods
This study included 120 MHD patients. Questionnaires, pre- and post-dialysis clinical data, bioimpedance spectroscopy, and ultrasound assessment were involved.
Results
The prevalence of fatigue in participants was 83%, including 54% of patients with fatigue worsened by dialysis, 13% with fatigue lessened by dialysis, and 16% with undifferentiated fatigue. Based on multi-nominal logistic regression analysis, age was associated with worsened fatigue by dialysis (odds ratio (OR) = 1.06, 95% confidence interval (CI) 1.01–1.11, p = 0.019), lower post-dialysis phosphorus was associated with lessened fatigue by dialysis (OR = 0.03, 95% CI 0.001–0.981, p = 0.049), and there was an increasing trend of patients experiencing undifferentiated fatigue as the extracellular water / intracellular water (E/I) level increased (p for trend = 0.020). Based on multi-ordinal logistic regression analysis, age was also a significant predictor for more severe fatigue (OR = 1.042, 95% CI 1.008–1.059, p = 0.015).
Conclusions
Different subgroups of fatigue in MHD patients have different affecting factors. Older patients were prone to worsened fatigue by dialysis, patients with lower post-dialysis phosphorus were prone to lessened fatigue by dialysis, and patients with higher E/I levels were prone to undifferentiated fatigue. Meanwhile, older patients are prone to suffer from more severe fatigue. However, more in-depth studies are needed to clarify the pathogenesis of fatigue in MHD patients.
Introduction
The critical role of patient-centeredness in the management of chronic kidney disease (CKD), including maintenance hemodialysis (MHD) patients, has gained increased recognition in the past decade [Citation1,Citation2] and highlighted the importance of effective symptom management [Citation3]. In MHD patients, fatigue symptoms are highly prevalent [Citation4], associated with the increasing risk of cardiovascular events and mortality and decreasing quality of life [Citation5–7]. Therefore, fatigue has been regarded as a crucial symptom in MHD patients, with a recent prioritization of identification, quantification, and further exploration [Citation8,Citation9]. Previous studies have investigated the pathophysiology or related factors of fatigue in non-dialysis CKD patients, suggesting that multiple abnormalities in demographic characteristics, comorbidities, and laboratory variables contribute to fatigue [Citation10,Citation11]. In contrast, the fatigue experienced by MHD patients is also a multidimensional, subjective experience that comprehensively reflects objective indicators, such as volume overload, fluid shifts during hemodialysis, uremia, anemia, inflammation, metabolic processes, mental health state, and other comorbid conditions [Citation12]. Hence, the fatigue of MHD patients is believed to be distinct from that of other non-hemodialysis patients and needs further exploration [Citation13]. Previous studies have mainly focused on post-dialysis fatigue (PDF), which is the most common type of fatigue in MHD patients, and have found some new factors related to it, such as higher post-dialysis lactic acid, the number of sleep hours before HD, and peridialytic serum cytokines [Citation14–16]. Besides PDF, fatigue symptoms can also occur before dialysis or continuously exist during a dialysis session and can be lessened or worsened by HD treatment. Moreover, these different fatigue symptoms may have different physio-pathological mechanisms. The current study assessed the degree of MHD patients’ fatigue using the SONG-HD Fatigue Scale [Citation8]. MHD patients were classified based on the relationship between fatigue aggravation/relief and HD treatment. In addition to dialysis parameters and demographic information, pre- and post-dialysis laboratory variables were collected, and ultrasound (US) and bioimpedance spectroscopy were used to measure volume load and nutrition-related indicators. This was done to identify objective factors associated with fatigue and explore clues for effective fatigue treatments in MHD patients.
Materials and methods
Patient inclusion
The study was conducted on MHD patients from two hemodialysis centers. Inclusion criteria: Patients must have been on hemodialysis therapy for at least three months, be over the age of 18, have the cognitive ability to answer questions correctly, and be able to provide informed consent. Exclusion criteria: Occurrence of inflammation (defined as acute inflammation such as acute infectious diseases, e.g., pneumonia, appendicitis, and sepsis, or acute stages of trauma, e.g., fracture and peri-operative phase), severe cardiovascular diseases such as acute myocardial infarction-related heart failure (cardiac function lower than Class II in the New York Heart Association Classification), acute myocardial injury with hemodynamic instability, and acute diarrhea. Given the limitations of bioimpedance spectroscopy, the study excluded patients with pacemakers or implanted defibrillators, amputations, and pregnant subjects. Given the limitations of ultrasonography, patients with known lung pathology, active pulmonary infections, recent thoracic or abdominal surgery, and a body mass index of more than 40 kg/m2 were also excluded. The study was approved by the Ethics Committee (IRB approval number K2021-09-046). All participants provided informed consent.
All enrolled patients underwent hemodialysis three times per week for four hours per treatment. At 35.5–36.5 °C, all patients received heparin or low molecular heparin anticoagulant and standard carbonate dialysis fluid. Blood flow ranged from 200 to 300 mL/min with a 500 mL/min dialysis rate. Dialysis liquid ingredients were sodium (Na) 138–140 mmol/L, potassium (K) 2.0 mmol/L, calcium (Ca) 1.25–1.5 mmol/L, chlorine (Cl) 109–110 mmol/L, glucose (GLU) 0 mg/dL, and bicarbonate 35 mmol/L. All patients were treated with disposable synthetic biocompatible dialyzer membranes (polysulfone hollow fiber dialyzer membranes, Fresenius, Bad Homburg vor der Höhe, Germany). Dry weight was targeted for each patient during the HD session. Pre- and post-weight, blood measurements, lung US, inferior vena cava diameter (IVCD) US, and bioimpedance spectroscopy assessment were applied at the same first HD session of the week.
Laboratory measurements
Pre- and post-dialysis blood were sampled from the arterial bloodline at the first HD session of the week. The following parameters were tested: potassium, phosphorus, hemoglobin, hematocrit, urea nitrogen, and creatinine; other laboratory parameters (blood was collected in the morning after an overnight fast before dialysis within one month): albumin, prealbumin, cholesterol, triglycerides, serum ferrum, and parathormone, C-reactive protein, calcium, and sodium (Na).
Bioimpedance spectroscopy
All assessments were performed using the body composition monitor (BCM; Fresenius Medical Care, Bad Homburg vor der Höhe, Germany) at the same first HD session of the week. Pre-dialysis overhydration (OH), total body water (TBW), extracellular water (ECW), intracellular water (ICW), ECW/ICW (E/I), and post-dialysis muscle tissue index (LTI) and fat tissue index (FTI) were determined as previously described [Citation17]. After entering each patient’s age, weight, and height data, measurements were completed within 4 min.
Ultrasound
Pre- and post-dialysis lung USs, as well as pre-and post-dialysis IVCD, were also performed in our study. Although no significant factors from the US assessment were found in multivariate analysis, we would like to attach the relevant assessment and results in the Supplementary Materials (Table S1) for reference.
Questionnaire
The fatigue assessment of HD patients was conducted according to the SONG-HD Fatigue Scale by Ju et al. [Citation8]. A questionnaire was given to patients at their first dialysis session the following week to determine their fatigue symptoms. The person administering the questionnaire asked, ‘In the past week, 1. Did you feel tired? 2. Did you lack energy? 3. Did fatigue limit your usual activities?’ Each question was asked to specify the degree they experienced ‘not at all (score = 0), a little (score = 1), quite a bit (score = 2), or severely (score = 3).’ For each patient, the total score of these three questions was calculated. According to the total score, the degree of fatigue was classified as fatigue-free (total score = 0), mild (0 < total score ≤ 3), moderate (3 < total score ≤ 6), or severe (total score > 6). In order to classify MHD patients into different subgroups of fatigue, patients were asked to choose the effect of dialysis on fatigue during the prior week’s dialysis: ‘fatigue reduction or relief after dialysis, fatigue generation or aggravation after dialysis, undifferentiated fatigue.’ According to the answers, participants were divided into four groups: fatigue-free, fatigue lessened by dialysis, fatigue worsened by dialysis, and undifferentiated fatigue.
Statistical analysis
Statistical analysis was performed using SPSS 25.0 (IBM, Armonk, NY). Means ± standard deviation (SD) were used to express the continuous data with a normal distribution. A one-way ANOVA was used to compare groups. Comparisons between each fatigue group and the fatigue-free group were conducted by applying the Bonferroni correction. Categorical data were expressed as frequencies and percentages and analyzed using the Chi-square test. Multi-nominal logistic regression was applied for explore factors associated with each subgroup of fatigue using statistically significant variables as independent variables based on the results of variance analysis and cross-analysis. The continuous variable was transferred into a categorical variable according to quartile for tests for trend when necessary. Multi-ordinal logistic regression was applied for explore factors associated with the degree of fatigue using statistically significant variables as independent variables based on the results of variance analysis. The results were expressed as odds ratios (ORs) with 95% confidence intervals (CIs). p < 0.05 was used to determine statistical significance.
Results
Demographics and clinical characteristics
A summary of clinical indicators and comparisons among groups are listed in . A total of 120 MHD patients were included. There were 61 HD patients on Monday, Wednesday, and Friday (MWF) schedules and 59 HD patients on Tuesday, Thursday, and Saturday (TTS) schedules. All of our MHD patients underwent hemodialysis in morning or afternoon sessions. Among them, 100 (83%) MHD patients experienced fatigue, including 65 (54%) with fatigue worsened by dialysis, 16 (13%) with fatigue lessened by dialysis, and 19 (16%) with undifferentiated fatigue. The most frequent fatigue was fatigue worsened by dialysis. There were significant differences between the three fatigue subgroups and the fatigue-free group in age (p = 0.013), Kt/v (p = 0.019), post-dialysis phosphorus (p = 0.011), post-dialysis creatinine (p = 0.025), OH (p = 0.005), E/I (p = 0.011), and FTI (p = 0.019). However, the four groups did not significantly differ in dialytic age, vascular access, dialysis mode, pre- and post-dialysis blood pressure, and dialysis arrangements. Several factors such as age, post-dialysis phosphorus, and E/I were found significant, at least in one subgroup (Table S2).
Table 1. Demographics and clinical characteristics.
Factors associated with each subgroup of fatigue
The independent variables included in the multi-nominal regression analysis were age, post-dialysis phosphorus, and E/I. The reference category of the dependent variable was set as ‘fatigue-free group’. As a result, age was associated with worsened fatigue by dialysis (OR = 1.06, 95% CI 1.01–1.11, p = 0.019). With per 1-year increase in age, the probability of suffering from worsened fatigue by dialysis increases by 6%. Meanwhile, lower post-dialysis phosphorus was associated with lessened fatigue by dialysis (OR = 0.03, 95% CI 0.001–0.981, p = 0.049). With per 1 mmol/L decrease in post-dialysis phosphorus, the probability of achieving lessened fatigue by dialysis increases by 97%. Moreover, as the E/I level increases, the likelihood of patients experiencing undifferentiated fatigue shows an increasing trend. The trend test p for trend = 0.020 indicates that this upward trend is statistically significant ().
Table 2. Factors associated with each subgroup of fatigue (n = 120).
Factors associated with the degree of fatigue
The independent variables included in the multi-ordinal regression analysis were gender (p < 0.001), age (p = 0.002), height (p < 0.001), pre-dialysis hemoglobin (p = 0.030), post-dialysis hemoglobin (p = 0.011), post-dialysis creatinine (p = 0.027), TBW (p = 0.025), ICW (p = 0.004), E/I (p = 0.002), LTI (p = 0.016), and FTI (p = 0.011) (). As a result, age has a significant effect on the degree of fatigue (p = 0.015) (). With one year increase in age, the OR value of worse fatigue grows by 1.042 times compared to the initial value.
Table 3. Comparison of characteristics among different degree of fatigue (n = 120).
Table 4. Factors associated with the degree of fatigue (n = 120).
Discussion
Our study aimed to investigate affected factors for subgroups of fatigue and the degree of fatigue in MHD patients. Therefore, laboratory indicators and dialysis parameters were detected in a dialysis session pre- and post-dialysis. Moreover, BCM was used to detect the pre-dialysis volume load, post-dialysis muscle, and fat index. According to the relationship between fatigue and hemodialysis treatment, MHD patients are subdivided into four subgroups. The results showed a high incidence of fatigue in MHD patients (83%) while mostly with fatigue worsened by dialysis (65%), consistent with previous studies [Citation18,Citation19]. Based on multi-nominal regression analysis, age was associated with worsened fatigue by dialysis (p = 0.021), suggesting that older patients were prone to suffer from worsened fatigue by dialysis. Previous study also found that patients with PDF are older [Citation20]. Older patients are more prone to comorbidities, malnutrition, and poor heart function than younger patients. Therefore, older patients are less tolerant of HD treatment, more likely to experience adverse reactions such as intradialytic hypotension (IDH) and suffer PDF [Citation21]. Based on multi-ordinal regression analysis, age was also a significant predictor for more severe fatigue (p = .015). In a recent study on older MHD patients, fatigue was considered one of the most burdensome symptoms [Citation22]. Hence, more attention should be paid to older MHD patients with fatigue. Considering that age is an irreversible factor, it is essential to reveal more potential mechanisms under age and to figure out what can be done to relieve the fatigue of older patients. Some clinical researchers found that the nutritional intervention program could improve nutritional status, reduce the risk of developing heart disease, and improve the quality of life in older patients with CKD [Citation23]. However, whether older MHD patients can also benefit from nutritional intervention to reduce fatigue is unknown. Some studies highlighted physical activity on fatigue reduction [Citation24], while less physical activity might increase the IDH in old MHD patients [Citation25]. Nevertheless, more efforts are still needed to improve the fatigue of older MHD patients.
Our results showed that lower post-dialysis phosphorus was associated with lessened fatigue by dialysis (p = 0.045). Since no significant differences were found in pre-dialysis phosphorus among different subgroups (p = 0.095), the improvement of fatigue might benefit from more clearance of serum phosphorus by dialysis in this subgroup. Considering that phosphorus represent a stubborn ‘uremic’ toxin, the results implied that those MHD patients with more successful phosphorus-removal were prone to have less fatigue. While serum phosphorus can rise back to a high level before the next dialysis session, more clearance of serum phosphorus by dialysis also means more fluctuation of serum phosphorus during dialysis intervals. Therefore, high level and the wide fluctuation of serum phosphorus might both affect fatigue in this subgroup. Few studies discussed the relationship between serum phosphorus and fatigue in MHD patients. Exploring possible mechanisms for serum phosphorus-associated fatigue in MHD patients would be meaningful.
Our results showed an increasing trend of patients experiencing undifferentiated fatigue as the E/I level increased (p for trend = 0.020), which suggested that MHD patients with higher E/I levels were prone to undifferentiated fatigue. ECW represents the sum of interstitial fluid and blood plasma in the extracellular space, whereas ICW reflects muscle cell mass [Citation26]. Therefore, an increase in the E/I ratio indicates a relative decrease in muscle mass [Citation27]. Previous studies have provided evidence of a relationship between an increased E/I ratio and decreased strength [Citation27,Citation28]. Furthermore, a loss of strength can lead to continuous fatigue. Moreover, considering that MHD patients frequently undergo volume overload, fluid volume imbalance might be another potential explanation for increased E/I [Citation29]. Noticeably, the undifferentiated fatigue group accounts for the highest proportion of post-dialysis B lines (>5) in lung US assessment (Table S1), which implied that pulmonary interstitial edema could be one of the manifestations of the increased proportion of extracellular fluid. There are some clinical studies committed to evaluating the pulmonary interstitial edema of MHD patients in the US and to adjusting the ultrafiltration strategy according to B lines, which were confirmed to decrease ambulatory BP levels effectively and safely in the long term [Citation30] and decrease cardiac chamber dimensions and LV filling pressure [Citation31]. However, it is unknown whether reducing pulmonary interstitial edema will relieve undifferentiated fatigue by lowering the E/I ratio. Further studies with larger sample sizes are needed (the interval of 95% CI was relatively wide may be due to the relatively small sample size in the current study) to validate the role of E/I and explore effective treatment strategies for undifferentiated fatigue in MHD patients.
Other studies have linked fatigue in MHD patients to gender, dialysis vintage [Citation32], increased serum Ca, and PTH [Citation33], but our results did not demonstrate these relationships. In our study, different factors affected different subgroups of fatigue in MHD patients, suggesting that different subgroups of fatigue may have different causes. The influenced factors in different subgroups could provide clues for clinical strategies to relieve fatigue symptoms in MHD patients.
There are some limitations to this study. First, it was a cross-sectional study focusing only on one dialysis session with Chinese HD patients in two-centers. More long-term cohort studies with larger multi-center samples are needed to provide more evidence for the pathogenesis of each fatigue. Second, our patients have more homogeneity on dialysis parameters, so our study has limitations in verifying the effect of dialysis parameters on HD patients’ fatigue, such as hydraulic or molecular flux, dialysis session duration, ultrafiltration rates, etc., which were independently associated with HD fatigue [Citation34,Citation35]. Third, our study mainly focuses on the dialysis day to collect objective values during a dialysis session. Moreover, more research is needed to explore potential fatigue-related factors on the non-dialysis day. Fourth, the psychometric properties of the SONG-HD Fatigue were confirmed in hemodialysis patients in the United Kingdom, Australia, and Romania [Citation8]. Furthermore, validation of the Chinese version of SONG-HD Fatigue in over 400 HD patients is conducted in China and has achieved ideal results. In order to explore the application of the SONG-HD Fatigue Score, we classified the degree of fatigue into four levels based on the SONG-HD Fatigue Score. However, more studies are needed to prove the validity of the statements.
In MHD patients, fatigue is closely related to a poor prognosis, which cannot be ignored. Although its mechanism is not completely clear, we must explore the fatigue of MHD patients and pursue effective treatment strategies for them.
Ethical approval
All procedures performed in studies involving human participants followed the institutional and/or national research committee at which the studies were conducted (IRB approval number K2021-09-046) with the 1964 Helsinki Declaration and its later amendments and comparable ethical standards.
Consent form
Informed consent was obtained from all participants.
Author contributions
All authors have made a significant contribution to the study. Methodology and writing original draft were done by ZXY; formal analysis and writing original draft by ZZH; resources and data curation by CYM and YQ; methodology and data curation by XB and LBC; conceptualization, financial support, and manuscript revision by HLT. All authors approved the final manuscript.
Supplemental Material
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No potential conflict of interest was reported by the author(s).
Data availability statement
All data generated or analyzed during this study are included in this published article.
Additional information
Funding
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