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Results | PMC10349515 |
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Patient baseline characteristics | breast cancer | MPBC, BREAST CANCER | A total of 1412 older women with MpBC were included in this study. Patients were randomly divided into a training set (Clinicopathological characteristics of older women with metaplastic breast cancer | PMC10349515 |
Prognostic factors of survival | tumor, T stage, breast cancer | MPBC, TUMOR, BREAST CANCER | In the training set, the proportional sub-distribution hazard model was used to analyze the risk factors of CSM and OCM. The results showed that age, T stage, N stage, M stage, tumor size, surgery and radiotherapy were risk factors for CSM. In addition, age is a risk factor for OCM in older women with MpBC (Table The proportional sub-distribution risk model predict cancer-specific mortality older women with metaplastic breast cancer | PMC10349515 |
Development of the competitive risk model | MPBC | Based on the proportional sub-distribution hazard model analysis results, we incorporated risk factors affecting CSM in patients. We established a competitive risk model to predict 1-, 3-, and 5-year cancer-specific survival in older women with MpBC. As shown in Fig. Competitive risk model nomogram for predicting the 1-, 3-, and 5-year cancer-specific survival of MpBC | PMC10349515 |
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Validation of the competitive risk model | MPBC | We used a series of validation methods to validate the accuracy and discrimination of the model. The C-index of the model was 0.792 ( 95% CI: 0.763–0.821) in the training set and 0.744 ( 95% CI: 0.691–0.797) in the validation set. The calibration curves in the training and validation sets showed that the model’s predicted values were almost consistent with the actual observed values, which proved that the prediction model had good accuracy (Fig. The calibration curves for predicting the cancer-specific survival of older women with MpBC in the training set (ROC curve with AUC for cancer-specific survival in older women with MpBC. | PMC10349515 |
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Clinical application | MPBC | We used DCA to validate the practical clinical value of the model. The results showed that the prediction model showed good practical value in predicting 1-, 3-, and 5-year survival. And the predictive ability of the prediction model is better than the traditional TNM staging system (Fig. DCA of competitive risk model in the training and validation sets. K-M curves of older women with MpBC in training sets ( | PMC10349515 |
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Discussion | tumor, T stage, comorbidity, breast cancer | MPBC, TUMOR, LYMPH NODE METASTASIS, BREAST CANCER | MpBC is mainly composed of mesenchymal histological components and epithelial cells, a rare breast cancer type [Older breast cancer patients are a particular group. Compared with young women, they have different physiology, tumor biological behaviour and social dynamics [In this study, we reported the clinicopathological features and prognostic factors of older women with MpBC in the SEER database. This study found that marital status and race were not factors affecting cancer-specific survival in older women with MpBC. The pathological subtype of MpBC was also not significantly correlated with cancer-specific survival. Previous studies have shown that the lymph node metastasis rate of MpBC patients is about 22–31% [A previous study has reported that chemotherapy can improve the prognosis of MpBC patients [This study found that age, T stage, N stage, M stage, tumor size, surgery and radiotherapy were risk factors for cancer-specific survival in older patients with MpBC. We developed a competitive risk model nomogram based on these variables to predict 1-, 3-, and 5-year cancer-specific survival in older women with MpBC. The competitive risk model is a nomogram and a simple prediction tool. By accurately predicting the survival time of patients, it can help doctors make clinical decisions and improve patient compliance.There are still some limitations in this study. First, the study lacked essential variables such as comorbidity, chemotherapy regimen, endocrine therapy, radiation dose, and physiological status. However, this study included essential variables, such as tumor staging and treatment. Therefore, the prediction tool has good clinical value. Secondly, this study is retrospective, and there is still a selection bias that is difficult to adjust. Therefore, further prospective studies to confirm the study results are necessary. Finally, this study’s competitive risk prediction model only conducted internal cross-validation. Although the model was confirmed to have good accuracy, further external verification is still needed. | PMC10349515 |
Conclusion | death, tumor | MPBC, TUMOR | This study explored the competitive risk factors for cancer-specific death in older women with MpBC. Age, T stage, N stage, M stage, tumor size, surgery and radiotherapy were risk factors for cancer-specific death in older patients with MpBC. Based on these risk factors, we developed a competitive risk model to predict cancer-specific survival in older women with MpBC. The validation results of the model show that it is a very effective and reliable prediction tool. This predictive tool allows doctors and patients to make individualized clinical decisions. | PMC10349515 |
Acknowledgements | Not applicable. | PMC10349515 |
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Authors’ contributions | JT, DZ, and XP contributed to the conception and design. DZ and JT collected and analyzed the data. DZ and JT drew the figures and tables. JT and DZ wrote the draft. XP and JT contributed to manuscript writing and revision. All authors approved the final manuscript. | PMC10349515 |
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Funding | Not applicable. | PMC10349515 |
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Availability of data and materials | The data analyzed in this study is available at | PMC10349515 |
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Declarations | PMC10349515 |
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Ethics approval and consent to participate | The data of this study is obtained from the SEER database. The patients’ data is public and anonymous, so this study does not require ethical approval and informed consent. | PMC10349515 |
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Consent for publication | Not applicable. | PMC10349515 |
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Competing interests | The authors declare no competing interests. | PMC10349515 |
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References | PMC10349515 |
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PURPOSE: | toxicity | ADVANCED CANCER | The time spent in pursuing treatments for advanced cancer can be substantial. We have previously proposed a pragmatic and patient-centered metric of these time costs—which we term time toxicity—as any day with physical health care system contact. This includes outpatient visits (eg, bloodwork, scans, etc), emergency department visits, and overnight stays in a health care facility. Herein, we sought to assess time toxicity in a completed randomized controlled trial (RCT). | PMC10337749 |
METHODS: | Cancer | SECONDARY, COLORECTAL CANCER, CANCER | We conducted a secondary analysis of the Canadian Cancer Trials Group CO.17 RCT that evaluated weekly cetuximab infusions versus supportive care alone in 572 patients with advanced colorectal cancer. Initial results reported a 6-week improvement in median overall survival (OS) with cetuximab (6.1 | PMC10337749 |
RESULTS: | In the overall population, median time toxic days were higher in the cetuximab arm (28 | PMC10337749 |
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CONCLUSION: | toxicity | SECONDARY | This proof-of-concept feasibility study demonstrates that measures of time toxicity can be extracted through secondary analyses of RCTs. In CO.17, despite an overall OS benefit with cetuximab, home days were statistically similar across arms. Such data can supplement traditional survival end points in RCTs. Further work should refine and validate the measure prospectively. | PMC10337749 |
INTRODUCTION | toxicity | ONCOLOGY, ADVANCED CANCER | Despite progress over the past few decades, most individual treatments for advanced cancer are associated with modest survival benefits (often < 2 months as median).We have previously extracted and compared the time toxicity in clinical trials using trial publications and protocols.Clinical trials, the gold standard to prospectively assess and compare efficacy, provide a unique opportunity to compare the time toxicity of treatments. Oncology clinical trials already collect vast amounts of data. Cooperative group trials additionally often collect measures of resource utilization. | PMC10337749 |
METHODS | PMC10337749 |
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Study Background, Procedures, and Efficacy/Safety Data | Cancer | SECONDARY, CANCER | We conducted a secondary analysis of the Canadian Cancer Trials Group CO.17 open-label RCT (ClinicalTrials.gov identifier: A total of 572 patients were randomly assigned. Initial results published in 2007 reported a 6-week improvement in median OS with cetuximab (6.1 months | PMC10337749 |
Measure of Time Toxicity | toxicity, toxicities | EVENTS, INFUSION REACTION | As previously described, we considered any day with physical health care system contact as a time toxic day.We calculated patient-level time toxicity (days with physical health care system contact) by analyzing treatment and follow-up forms and resource utilization assessment forms. The treatment and follow-up forms listed the dates of protocol-related health care contact (eg, bloodwork, infusions, imaging studies, etc). The resource utilization assessment form was completed every 28 days for each participant by trial staff, with the aim of collecting data on the number and type of medical resources consumed by each patient. The forms collected non–protocol-related office/clinic visits, outpatient procedures/treatments (such as imaging, transfusions, paracentesis, radiation, and chemotherapy), emergency department visits, hospitalizations, and admission to a facility (rehabilitation, long-term care, hospice, and others), along with the dates of each contact. If the exact date of an outpatient encounter was not recorded, we considered it to be on a separate day. The date(s) of an inpatient encounter (in hospital) were always available. For a time toxic day, we further classified the source of time toxicity as (1) planned and (2) unplanned, depending on if it was related to a per-protocol visit or an additional visit. If a day had both planned and unplanned time toxicities (eg, planned cetuximab leading to an infusion reaction leading to an emergency department visit), we treated it like planned time toxicity since it occurred first and was independent of future events.A day without physical health care contact was considered a home day. Thus, a day could either be a time toxic day or a home day. For an individual patient, OS was the sum of time toxic days and home days. The resource utilization assessment forms also collected visits by clinicians to patients' homes and procedures (eg, scans and thoracenteses) performed when a patient was inpatient. We excluded these visits from time toxicity analyses since they either did not require patient travel to a health care facility or the inpatient day was already included as a time toxic day. | PMC10337749 |
Statistical Analysis | We compared medians of time measures (time toxic days, home days, and proportion of home days alive) across arms by a Wilcoxon test and stratified results by | PMC10337749 |
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RESULTS | toxicity, Tumor, Toxicity | ONCOLOGY, TUMOR | All trial participants (n = 572) had data on time toxicity available and were included in the current analyses. The median age was 63 years, 64% of participants were men, and 77% had an Eastern Cooperative Oncology Group performance status of 0-1. Baseline characteristics were balanced between arms, and detailed data are available in prior publications.For the overall study population, median time toxic days were higher in the cetuximab arm (28, Time Toxicity Measures in CO.17 for the Overall Study PopulationResults stratified by Time Toxicity Measures in CO.17 Stratified by Tumor For patients with | PMC10337749 |
DISCUSSION | toxicity | DISEASE, SECONDARY | In this secondary analysis of the CO.17 trial, we demonstrate that a measure of patient-level time toxicity can be successfully extracted. In CO.17, despite a statistically significant OS benefit with cetuximab in the overall study population, the number of home days was similar across arms and patients receiving cetuximab spent three times as many days alive with health care contact compared with patients treated with supportive care alone. In the The primary objective of this work was to demonstrate the feasibility of collecting and comparing time toxicity from a completed RCT. We have previously calculated the estimated time toxicity of treatments from trial protocols and publications, but this work was limited by the lack of patient-level data.The primary finding of this work is that despite a statistically significant OS benefit with cetuximab, time toxicity eroded into its survival benefit. In the overall population, home days were similar across arms. Results were even more striking for patients with Patients receiving this treatment on average live 6 weeks longer.Patients receiving this treatment on average live 6 weeks longer. However, patients getting the treatment spend more time coming to clinic and in the hospital—almost one in every 5th day will be spent in the clinic or hospital. Overall, patients getting the treatment spend the same number of days at home as patients focusing on symptom control alone.For truly effective treatments, time toxicity data can support treatments. At the time that CO.17 was conducted (2003-2005) and when initial survival results were first published (2007), the impact of In addition to the overall time toxicity data, the source of time toxicity can provide valuable insights. We found that planned visits accounted for approximately 50% of all time toxicity (and two thirds of the time toxicity for people with This work has several limitations. First, the current measure itself is imperfect. It does not capture time toxicity when the patient is home (eg, telemedicine and home-based infusions), associated with care logistics (eg, time spent on the phone with insurance company), and for care partners. It does not differentiate between the source and quality of contact days. It assumes that all home days are equally good, and all time toxic days are equally bad. A more nuanced measure, perhaps a quality-weighted time toxic days, is appealing, but we must consider the complexity in collecting, calculating, collating, and communicating it. Measures such as Q-TWiST (quality-adjusted time without symptoms of disease or toxicity) face an uphill battle for routine adoption because of these reasons.In conclusion, we demonstrate that measures of time toxicity can be successfully extracted through secondary analyses of completed RCTs. Information on time toxicity can supplement traditional survival end point reporting in clinical trials. Future work should refine the time toxicity measure and explore how to deploy it prospectively in clinical trials. | PMC10337749 |
ACKNOWLEDGMENT | We thank the participants in the study for volunteering. | PMC10337749 |
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PRIOR PRESENTATION | We presented this work in abstract form at the 2022 ASCO Quality Care Symposium held in Chicago, IL (and virtually), September 30-October 1, 2022. | PMC10337749 |
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SUPPORT | Colorectal Cancer, Cancer | COLORECTAL CANCER, CANCER | Supported by the Canadian Cancer Society (Grant No. 707213). Arjun Gupta is supported by a grant from the Minnesota Colorectal Cancer Research Foundation. | PMC10337749 |
AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST | PMC10337749 |
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APPENDIX | Toxicity | Details of Unplanned Time Toxicity in CO.17 | PMC10337749 |
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REFERENCES | PMC10337749 |
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Abstract | PMC10278496 |
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Background | primary breast cancer | There has been steadily increasing use of bilateral mastectomy (BMX) in the treatment of primary breast cancer (BC). In this study, we utilized functional magnetic resonance imaging (fMRI) to examine the influence of emotion regulation on the decision of newly diagnosed BC patients to choose BMX rather than non‐BMX treatments. | PMC10278496 |
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Methods | We recruited 123 women with unilateral BC, 61 of whom received BMX and 62 of whom received non‐BMX treatments, and 39 healthy controls. While participants were in the fMRI scanner, we showed them BC‐related and non‐BC‐negative images. In one condition, they were instructed to watch the images naturally. In another, they were instructed to regulate their negative emotion. We compared the fMRI signal during these conditions throughout the brain. | PMC10278496 |
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Results | With non‐BC‐negative images as the baseline, BC patients showed greater self‐reported reactivity and neural reactivity to BC‐related images in brain regions associated with self‐reflection than did controls. Among the BC patients, the BMX group showed weaker activation in prefrontal emotion regulation brain regions during emotion regulation than did the non‐BMX group. | PMC10278496 |
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Conclusions | anxiety | BC patients are understandably emotionally hyper‐reactive to BC‐related stimuli and those who ultimately received BMX experience more difficulty in regulating BC‐related negative emotion than non‐BMX BC patients. These findings offer neuropsychological evidence that difficulty in managing anxiety related to the possibility of cancer recurrence is a factor in surgical treatment decision‐making and may be an intervention target with the goal of strengthening the management of cancer‐related anxiety by nonsurgical means. | PMC10278496 |
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Trial Registration | NCT03050463.
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INTRODUCTION | primary breast cancer, anxiety | SURGICAL COMPLICATIONS, TREATMENT SIDE EFFECTS | While the use of unilateral mastectomies in the treatment of primary breast cancer (BC) has decreased, there has been steadily increasing use of bilateral mastectomy (BMX)BMX is an elective procedure for a unilateral BC, because it involves more surgery than is required for treatment. Given that BMX may have detrimental effects including surgical complications and associated costsEmotional responses are complex, coordinated phenomena that lead to behavioral, cognitive, and physiological changes, activate action tendencies, and modulate feelings.Thus, emotion dysregulation, involving anxiety, fear, and other negative emotions may be a major factor in decisions regarding BC faced by some 255,000 women in the United States every year. The desire to reduce understandable current anxiety by accepting major treatment side effects to avoid the future risk of regret may drive decisions that are inconsistent with actual risk reduction. We conducted a case–control study utilizing fMRI to better understand the influence of emotion regulation on the decision of newly diagnosed BC patients choosing BMX rather than unilateral mastectomies or breast‐conserving treatments (non‐BMX), with the ultimate goal of developing an intervention to enable the management of cancer‐related anxiety by nonsurgical means. The central hypotheses of the study are that: (1) BC patients choosing BMX rather than non‐BMX treatments would show more difficulty regulating the emotion elicited by unpleasant stimuli, in particular those relevant to BC, and, (2) BC patients would show greater emotional reactivity to stimuli with content relevant to BC than controls. | PMC10278496 |
METHODS | PMC10278496 |
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Participants | cancers, Stanford Cancer, cancer, substance/alcohol, psychosis, neurologic disease, bipolar disorder | OVARIAN CANCER, CANCERS, BREAST CANCER, CANCER, RECRUITMENT, HEARING IMPAIRMENT | We recruited a patient sample of 123 women diagnosed with BC within the preceding 12 months (mean 4.9 months; SD 3.5) with stage 0‐III unilateral breast cancer. We identified 33% of potential participants from Stanford Cancer Center records, 26% from the Army of Women website, 26% from social media, and the remaining 15% from other sources. Among the BC patients, 61 had undergone or later underwent BMX, and the other 62 had undergone or later received non‐BMX treatments. The recruitment of 39 healthy controls was monitored to maintain comparability in demographics. The controls were women with no history of cancer, no first‐degree relatives or 2 or more second‐degree relatives with a BC diagnosis, or any first‐ or second‐degree relatives with ovarian cancer. We identified 57% of potential control participants from a Stanford University volunteer pool, 33% from the Army of Women website, and the remaining 10% from other sources. All women (BC and control) were English‐proficient, willing to suspend intake of benzodiazepines and to undergo brain MRI, and with no contraindications to MRI imaging (e.g., ferromagnetic metal in their body). Exclusion criteria included other current or past cancers, any significant neurologic disease, current untreated psychosis or bipolar disorder, substance/alcohol abuse/dependence, current use of psychotropic medication, pregnancy, and hearing impairment. The research protocol was reviewed and approved by the Stanford Institutional Review Board (protocol number: 34959), and all subjects provided written informed consent. The details of functional and structural MRI acquisition and data preprocessing are presented in Data | PMC10278496 |
Emotion regulation task | During the task, participants viewed a series of pictures and were instructed to either respond naturally (“WATCH” condition) or to regulate their emotional response (“RETHINK” condition). Specifically, following the “WATCH” cue, they were instructed to look at and respond naturally to the picture without attempting to change their emotion. In WATCH trials, participants viewed either a neutral picture from the International Affective Picture System (IAPS),Trial structure of the emotion regulation task. A trial began with a fixation for 2–8 seconds (s), followed by a cue word “WATCH” or “RETHINK” for 2 s, a picture (neutral, IAPS‐negative, or BC‐negative) for 6 s, a blank screen for 2 s, and a rating window for 4 s. | PMC10278496 |
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Data analysis | The study is preregistered on the Open Science Framework, and its detail can be found in the wiki pages of each of the components ( | PMC10278496 |
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In the first‐level analysis, individual functional runs were modeled by a GLM with regressors representing the conditions including neutral‐watch, IAPS‐watch, BC‐watch, IAPS‐rethink picture, and BC‐rethink pictures (convolved with a double‐gamma function), and nuisance regressors (Data | PMC10278496 |
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Self‐report data | The self‐report negativity rating data of each participant were averaged across trials for each trial type. Following the preregistered analysis above (more details in Data | PMC10278496 |
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RESULTS | PMC10278496 |
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Sample characteristics | SD, breast cancer | POSITIVE, BREAST CANCER | The sample characteristics, including demographics, are presented in Table Sample characteristics. Data are presented in a format of Mean ± SD or number (percentage).Tumor status of breast cancer participants.Positive for a pathogenic variant. | PMC10278496 |
Mastectomies | Forty‐six (75.4%) of participants with BMX had their BMXs before their fMRI assessments (median of 173 days, interquartile range (IQR) 119.25, 252.5); and nine (14.5%) of non‐BMX participants had their unilateral mastectomies before their fMRI assessments (median of 84 days, IQR 34, 177) (Table | PMC10278496 |
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Chemotherapy | Fifteen (24.6%) of participants with BMX finished chemotherapy before their fMRI assessments (median of 128 days before the fMRI, IQR 69.5, 173.5). Seven (11.3%) of non‐BMX participants finished chemotherapy before their fMRI assessments (median of 121 days before the fMRI, IQR 1126.5). Six (9.8%) of participants with BMX were receiving chemotherapy at the time of their fMRI assessments (starting median of 86 days from the fMRI, IQR 80.5, 90.75). Twelve (19.4%) of non‐BMX participants were receiving chemotherapy at the time of their fMRI assessments (starting median of 87.5 days from the fMRI, IQR 22.25, 156.25) (Table | PMC10278496 |
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Emotion regulation | PMC10278496 |
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A BMX versus non‐BMX group comparison revealed that, for the BC‐IAPS differential regulation, the non‐BMX recipients showed greater activation in dmPFC (clusterwise Group comparison between BMX and non‐BMX BC patients in the neural BC‐IAPS differential regulation. (A) Group comparison map of non‐BMX > BMX. The yellow regions indicate that non‐BMX recipients had greater activation for the BC‐IAPS differential regulation than BMX recipients. (B) Neural activation (There were no significant differences in the neural BC‐IAPS differential regulation between the control group and the patient group. There were no group differences between controls versus BC patients or BMX recipients versus non‐BMX recipients in other regulation contrasts (Data | PMC10278496 |
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Self‐report data | We compared emotion regulation between controls and BC patients and between BMX recipients and non‐BMX recipients (Figure | PMC10278496 |
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Emotional reactivity | PMC10278496 |
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A patient‐control group comparison revealed that, for the BC‐IAPS differential reactivity (Figure Group comparison between BC patients and controls in the neural BC‐IAPS differential reactivity. (A) Group comparison map of BC patients > controls. Yellow regions indicate where BC patients had greater activation for the BC‐IAPS differential reactivity than controls. (B) Neural activation (Within the patient group, there were no significant differences between the BMX and non‐BMX groups in the neural BC‐IAPS differential reactivity. There were no group differences between controls versus BC patients or BMX recipients versus non‐BMX recipients in other reactivity contrasts (Data | PMC10278496 |
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Self‐report data | As expected and consistent with the fMRI result, BC patients reported more similar emotional reactivity to BC‐related and general emotionally negative images (IAPS) than did controls, | PMC10278496 |
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DISCUSSION | The women who ultimately received BMX showed less activation in prefrontal brain regions that are associated with emotion regulation than those who received non‐BMX surgeries. Particularly, the non‐BMX group showed greater activation than the BMX group in the dmPFC and dlPFC during the application of reappraisal to regulate negative emotions elicited by BC‐related pictures.Consistent with our hypothesis, the self‐reported BC‐IAPS differential reactivity was significantly higher in BC patients than controls. It suggests that with IAPS pictures as a baseline, BC patients reported stronger relative emotional reactivity to BC‐related pictures than their healthy counterparts. The fMRI data further corroborated this finding. When comparing the neural differential BC‐IAPS reactivity, BC patients showed significantly stronger activation in regions within the default mode network (DMN), including vmPFC, PCC, and precuneus. These brain regions are typically involved in self‐reflection and self‐evaluation processes.It is interesting that the BC patient‐control group difference in neural reactivity did not appear in core limbic regions such as the amygdala, but was consistently evident in several DMN regions. The amygdala typically reflects low‐level aspects of emotional reactivity. The DMN, on the contrary, is typically involved in self‐referential cognitive processes.It is of clinical importance that greater activations of dmPFC and dlPFC during emotion regulation differentiate the non‐BMX and BMX groups. These components of the Executive Control Network (ECN) are crucial to emotion regulation, so their hypoactivation during the presentation of distressing visual stimuli, for cancer‐related images in particular, is consistent with a reduced ability to modulate negative emotion. | PMC10278496 |
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Limitations & future directions | anxiety | SECONDARY, BREAST CANCER | There are several limitations to the study. First, some of our BC participants underwent the fMRI assessment after undergoing their surgical treatment. Although our secondary analysis showed that including surgery timing as a covariate did not change the main finding, future studies would benefit from assessing emotion reactivity/regulation in BC patients before they experienced their surgical treatment. Second, a small number of the BC patients were receiving chemotherapy at the time of their fMRI assessments. Although this happened in both the BMX and the non‐BMX groups, we cannot exclude the possibility that undergoing chemotherapy could have influenced participants' emotion reactivity and regulation. Third, we used BC‐related pictures to induce negative emotion but not necessarily cancer‐related anxiety in particular. Also, pictures presented in a lab setting may not fully simulate real‐life experience of cancer‐related negative emotions, although they likely stimulate affect related to the experience of women with breast cancer. Future research is encouraged to employ other paradigms to assess real‐life cancer‐related anxiety directly. | PMC10278496 |
CONCLUSIONS | cancer, anxiety, breast cancer | CANCER, BREAST CANCER | Employing an fMRI experiment, we found that BC patients experienced greater negative emotion in response to BC‐related stimuli than their healthy counterparts. More importantly, those who chose BMX had less activation in prefrontal regions while regulating BC‐related negative emotion than did those who chose more conservative non‐BMX treatments. These findings offer neuropsychological evidence that difficulty in managing anxiety related to cancer is a crucial factor in surgical treatment decision‐making. Difficulty in emotion regulation may serve as an intervention target with the goal of improving breast cancer treatment decision‐making by enhancing the ability to regulate cancer‐related anxiety. | PMC10278496 |
AUTHOR CONTRIBUTIONS | PMC10278496 |
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CONFLICT OF INTEREST STATEMENT | The authors declare no potential conflicts of interest. | PMC10278496 |
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Supporting information |
Data S1.
Click here for additional data file. | PMC10278496 |
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ACKNOWLEDGMENTS | Cancer | RECRUITMENT, CANCER | This work was supported by the National Cancer Institute (U01CA197282) and the National Center for Advancing Translational Science (NIH‐NCATS‐CTSA grant # 5UL1TR003142), National Institutes of Health. We thank our research participants for their time, wisdom, and willingness to participate, and the Dr. Susan Love Research Foundation's Love/Avon Army of Women Program for their assistance in recruitment. | PMC10278496 |
DATA AVAILABILITY STATEMENT | We share the neural and self‐report data on the Open Science Framework ( | PMC10278496 |
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REFERENCES | PMC10278496 |
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Background | cancer, disability, anxiety | CANCER | The use of graphic novels is a trending topic in health communication as a new form of visual storytelling which explores narratives of health care, cancer, healing, and disability. The objective of the present study was to evaluate - for the first time in the literature - the effect of graphic novels in reducing the anxiety of patients waiting for an incisional biopsy in an oral oncology setting. | PMC10635625 |
Material and Methods | Depression | DISORDERS | This open-label randomized clinical trial comprised 50 patients with a clinical suspicion of oral potentially malignant disorders. Twenty-five patients were randomly allocated to the test group, and a colourful graphic novel was provided. Subsequently, the Beck Depression Inventory and the Depression Anxiety Stress Scales-21 were administered to all 50 recruited patients, after which a biopsy was performed on each patient. | PMC10635625 |
Results | No statistically significant difference was observed between the test and control groups for the variables regarding the demographic data ( | PMC10635625 |
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Introduction | orofacial disorders, anxiety | DISEASE | Oral medicine is the main speciality, together with maxillofacial surgery, dealing with severe and on occasions life-threatening orofacial disorders or outcomes; it, therefore, elicits states of fear and anxiety in patients (Patients with a specific phobia often experience intense and immediate fear and/or anxiety prior to dental treatment and/or an oral biopsy. Their psychological state of stress and discomfort usually develops when they are in the waiting room, to possibly include negative intrusive thoughts (e.g., "it will hurt, I will be diagnosed with a terrible disease")(The term graphic medicine was coined by a group of researchers, clinicians, and artists with the aim of exploring this new subfield of research and practice (Researchers are becoming increasingly interested in graphic narratives, with which to convey persuasive public health messages (e.g., Centers for Disease Control and Prevention, 2011). Narratives with comics also continue to emerge as effective communication tools of public health (The visual narratives which can be considered most relevant to the study of graphic medicine are comic books in their various guises. Graphic medicine examines the use of sequential (but not always narratively linear) visual storytelling, with which to share health-related experiences or information (Consequently, graphic novels have been applied to several fields, including: oncology (The objective of the present study was to evaluate - for the first time in the literature - the efficacy of colourful graphic novels in reducing the anxiety of adult patients waiting for an incisional biopsy in an oral oncology setting. | PMC10635625 |
Material and Methods | Anxiety, anxiety, anhedonia, depression, subjects3, hyperactivity, P., OPMD, depressive, agitation, Post-biopsy, cognitive deficits, cognitive and motivational psychomotor, Depression, irritability | DISORDER, MAY, CAVITY | - Study designThis open-label randomized clinical trial (RCT) was approved by the local Institutional Ethics Committee of the P. Giaccone University Hospital of Palermo, Italy (approval #1/2022). The study was conducted according to the principles of the Declaration of Helsinki regarding experimentation involving human subjects, and written informed consent was obtained from all participants.The authors consecutively included all patients with a clinical suspicion of an oral potentially malignant disorder (OPMD), who had been referred to the Oral Medicine Unit at the P. Giaccone University Hospital in Palermo (Italy), from May to November 2022. Prior to the oral incisional biopsy, 50 patients were randomly allocated (i.e., computer-generated) to the test or control group; a graphic novel was provided to 25 patients in the test group.- Eligibility criteria1. age of patients ≥ 18 years2. absence of suspected or obvious pregnancy status in female subjects3. patients affected by OPMD4. agree to participate in the RCT, and the ability to read and understand informed consent5. patients not affected by any known psychological disorder.- Exclusion criteria1. patients with cognitive deficits, such that they cannot adequately complete the questionnaire and the visually impaired2. patients who are to undergo surgical treatment and/or biopsy, for reasons other than OPMD (e.g., salivary gland biopsy)3. patients using benzodiazepines or other psychotropic medications.- Oral graphic novel descriptionThe authors used a comic strip consisting of a sequence of 9 colourful vignettes, in which the procedure of an oral biopsy was described to the patient. (Fig. 1. A patient in the mirror is inspecting their oral cavity and they find something abnormal2. The patient seeks the clinical opinion of a physician3. The patient is examined by their dentist4. Thereafter, during the night, the patient ruminates as to what this abnormality might be5. Having been referred for diagnostic procedures, the patient is in the waiting room of the Oral Medicine Unit6. The Oral Medicine team greets the patient, and performs an OPMD biopsy7. Post-biopsy, the patient is leaving the Oral Medicine Unit while applying an ice pack after surgery8. The patient is requested (via a phone call) to return for the histology results9. An oral physician informs the patient of the histological findings.
The English version of the graphic novel, offered to the test group (with thanks to G. Piazza).- Description of tests used to assess anxietyAll the 50 recruited patients received the Beck Depression Inventory (BDI) and the Depression Anxiety Stress Scales-21 (DASS-21). Prior to the surgical procedures (i.e., oral biopsy), these questionnaires were administered anonymously in a mixed paper-pencil and QR Code mode. The administering psychologist (M.B.) was present for questions and clarification. Before filling out the BDI and DASS-21 questionnaires, patients were asked to answer some questions regarding their demographic data and medical history (e.g., smoking habits). The BDI is a self-administered instrument for assessing the severity of the affective, cognitive and motivational psychomotor, and the vegetative components of depression. It comprises 21 sets of statements, describing various and increasing levels of depressive symptomatology; each statement corresponds to a score, and these scores are totalled to produce a total score. Higher scores of BDI are correlated with major depressive state (The present study also used the psychometric properties of the Italian version of the DASS-21 to explore its use in an Italian context. The DASS-21 facilitates the identification of three constructs: depression, anxiety, and stress. Depression includes: dysphoria, hopelessness, devaluation of life, lack of interest/involvement in regulating daily life, anhedonia, and inertia. Anxiety relates to: autonomic nervous system arousal, skeletal muscle effects, situational anxiety, and the subjective experience of anxious effects. Stress relates to: the presence of chronic non-specific arousal levels, relaxation difficulties, nervous arousal, irritability, agitation, hyperactivity, and impatience (A digital platform, including the following, was created:1. a section with two separate BDI, DASS-21 tests/forms for patients, who completed them anonymously. And, in order to enhance the information collating process, a QR code was created for each test/form in such a way that patients could easily scan these with their cell phone camera and quickly complete each test/form2. an administrative section, including a Dashboard (providing an overview of the tests/forms, to be completed daily) and several subsections permitting the extrapolation of statistical data, each form being based on the answers provided by the patients. The React framework (for the front-end) and Php and MySql (for the back-end) was used to create the web platform.- Outcome MeasuresThe following data were recorded for each patient: demographic data, smoking habit, drug intake, the BDI scores according to the An Inventory for Measuring Depression (- Statistical AnalysisThe analysis was performed using the software R (R Core Team, 2022). Descriptive statistics were used to analyse the patients’ socio-demographic and physical characteristics. BDI and DASS-21 scores were summarized through mean value, standard deviation (SD), maximum, median and interquartile range (IQR). In order to analyse any significant statistical difference of anxiety between the test and control groups, the data were initially tested to ascertain if any socio-demographic or physical characteristics were associated with group membership by Chi-Square Test. The Mann-Whitney U test was used to evaluate the significant differences between treatment groups, with respect to BDI and DASS-21 scores. In order to quantify any statistically significant difference, the difference between BDI and DASS-21 scores in the groups was evaluated by the Hodges-Lehmann estimator. Any relation between BDI and DASS-21 scores was measured through a linear correlation coefficient. | PMC10635625 |
Results | The descriptive statistics relating to the patients’ socio-demographic and physical characteristics are displayed in
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Descriptive statistics relating to patient socio-demographic and physical characteristics. | PMC10635625 |
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Summary statistics of the BDI and DASS-21 scores. |
Boxplot describing the distribution and summary statistics of BDI and DASS-21 scores for the control and test groups.The results are shown in Each question of the BDI and DASS-21 questionnaires was also tested for differences between treatment groups. Thus far, a significant difference in BDI and DASS-21 scores has been observed between the test and control groups respectively. Indeed, a strong positive correlation was observed between the BDI and DASS-21 scores. The linear correlation coefficient generally equalled 0.78 (
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Mean and standard deviation, and Mann-Whitney U Test for each BDI question and total score. | PMC10635625 |
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Mean and standard deviation, and Mann-Whitney U Test for each DASS-21 question and total score. | PMC10635625 |
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Discussion | anger, anxiety, cancer, panic, OPMD, psychological distress, mental disorders, depression | CANCER, EVENT, SAID, BLIND, EVENTS | This study has proposed for the first time in the field of dentistry the use of a graphic novel, which is aimed at adults, that is, patients who are waiting for an incisional biopsy to ascertain the presence of OPMD. A further component of the study is to assesses its efficacy in reducing patient anxiety, as measured by BDI and DASS 21scores. It was observed that patients, who were offered a comic book while waiting to undergo an incisional biopsy were more informed about this subject than those who did not. They consequently experienced less anxiety (also in accordance with the theory of reasoned action) (There is an increasing need for new tools in the field of healthcare, with which to develop strategies of effective communication in medicine and dentistry. These include; the use of colour and ludic activities, infographic videos or leaflets (It has been demonstrated that combining pictures and text improves comprehension because reading and viewing activate different information-processing systems within the brain (In oral medicine, the dread of undergoing a biopsy is significant, leading to an unpleasant emotional state, which can affect the way a patient feels, thinks, and acts. Feelings of distress operate along a continuum, ranging from commonly-shared feelings (such as vulnerability, sadness, anger, and fear) to challenges which can quickly evolve into mental disorders (e.g., depression, anxiety, panic), social isolation, and existential and spiritual crises. The distress generated by the fear of having cancer typically negatively impacts a patient’s life, and it, therefore, plays a key role in diagnostic delay and assisting a patient to return to their before-the cancer diagnosis life (Such conditions of distress are strictly related to cognitive-behavioural theory, which considers emotions and behaviour to be closely intertwined. Specifically, thoughts can be said to influence emotions and behaviour, thus it is not the actual event which causes psychological distress (i.e., the oral biopsy), but one’s perception of that event. This implies that patients’ emotional and behavioural reactions can be determined by the way in which they interpret different situations and the attributed meaning of those events (The genre of the colourful graphic novel has been adapted to the field of oral medicine, after which it was necessary to evaluate its efficacy in reducing patient anxiety as they waiting for an incisional biopsy in presence of a possible OPMD.The results of the present study seem to confirm that the application of graphic medicine to a psychoeducational approach alleviates anxiety and distress of patients. In turn, this leads to a more accurate understanding of the risk, while facilitating communication with the patient. This study has provided an example of how this approach works and how it could be integrated into medical education and dental practice.- LimitationsThis RCT has been based on a small group of patients, and the context of administering the comic book reading and test completion is not considered to be particularly appropriate. On occasions, the target reader may not identify with the comic book character because the setting does not reflect their typical habits, expressions, type of language, and other aspects related to daily life. Regrettably, it was not possible to perform a blind RCT. | PMC10635625 |
Conclusions | P., anxiety | SAID, DISEASES | Comics can be said to communicate concepts by telling stories with relevant characters, settings, and situations; they are also accessible, even for patients with different educational levels. Graphic novels are a recently-created, original and creative way of informing patients about diseases or medical procedures. In the scenario outlined in this paper, a graphic novel has been demonstrated to improve the ability to tolerate anxiety while waiting for an invasive examination, such as an oral biopsy. With the present study, the authors aspire to attract attention to the possible role of graphic novel in dealing with patient anxiety, thereby becoming an invaluable tool to the medical practitioner in the field of oral medicine.Ackcnowledgements The authors would like to thank Giorgia Piazza for her instrumental role in drafting the test graphic novel, which was used in this research. The authors also thank J O Davies for the positive contribution to language editing.Authors contributions Conceptualization, M.B. and G.C.; methodology, M.B., R.M. and G.C.; investigation, M.B.; data curation, M.B. and G.M.; writing—original draft preparation, M.B. and G.M.; writing—review and editing, R.M. and G.C.; visualization, R.M.; supervision, G.C. All authors have read and agreed to the published version of the manuscript.Ethics This open-label randomized clinical trial (RCT) was approved by the local Institutional Ethics Committee of the P. Giaccone University Hospital, Palermo, Italy (approval #1/2022).Conflicts of interest The authors declare that there are no conflicts of interest.Funding None declared. | PMC10635625 |
Background | cancer | CANCER, DYSFUNCTION, COMPLICATIONS | Patients undergoing hematopoietic cell transplantation (HCT) are at high risk of chronic health complications, including frailty and physical dysfunction. Conventional exercise programs have been shown to improve frailty in other cancer populations, but these have largely been based out of rehabilitation facilities that may act as geographic and logistical barriers. There is a paucity of information on the feasibility of implementing telehealth exercise interventions in long-term HCT survivors. | PMC10150529 |
Methods | We conducted a pilot randomized trial to assess the feasibility of an 8-week telehealth exercise intervention in 20 pre-frail or frail HCT survivors. Participants were randomized to either a telehealth exercise (N = 10) or delayed control (N = 10). We administered a remote physical function assessment at baseline, followed by an 8-week telehealth exercise intervention (30-60 min/session, 3 sessions/week), and post-intervention. The primary endpoint was feasibility as determined by 1) > 70% of participants completing all remote physical functional assessments, and 2) > 70% of participants in the exercise group completing > 70% (17/24) of the prescribed exercise sessions. Exploratory outcomes included changes in gait speed, handgrip strength, and short physical performance battery. | PMC10150529 |
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Results | fatigue | The mean [standard deviation] age at study enrollment was 64.7 [9.1] years old. Twelve had undergone allogenic and 8 had undergone autologous HCT at an average of 17 years from study enrollment. Both feasibility criteria were achieved. Nineteen patients (95%) completed all remote study outcome assessments at baseline and post-intervention, and nine participants in the exercise group completed > 70% of prescribed exercise sessions. Overall, no significant group x time interaction was observed on handgrip strength, fatigue, body mass index, and short physical performance battery test (P < 0.05). However, there were significant within-group improvements in four-meter gait speed (+ 13.9%; P = 0.004) and 5-minute gait speed (+ 25.4%; P = 0.04) in the exercise group whereas non-significant changes in four-meter gait speed (-3.8%) and 5-minute gait speed (-5.8%) were observed after 8 weeks. | PMC10150529 |
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Conclusion | cancer | CANCER | Implementing an 8-week telehealth exercise intervention for long-term HCT survivors was feasible. Our findings set the stage for innovative delivery of supervised exercise intervention that reduces the burden of frailty in HCT survivors as well as other at-risk cancer survivors. | PMC10150529 |
Trial registration | The protocol and informed consent were approved by the institutional IRB (IRB#20731) and registered (ClinicalTrials.gov NCT04968119; date of registration: 20/07/2021). | PMC10150529 |
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Keywords | PMC10150529 |
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Background | cancer | CANCER, HEMATOLOGICAL MALIGNANCIES | Advances in hematopoietic cell transplantation (HCT) have led to marked improvements in the survival of patients with hematological malignancies [Exercise is an established strategy to decrease the risk of frailty in conventionally-treated cancer patients [In the general population, there is increased recognition about the importance of telehealth exercise interventions that can provide real-time supervision, goal setting, and performance feedback during exercise sessions [The purpose of this trial was to evaluate the feasibility of a supervised telehealth exercise intervention aimed at improving physical function in prefrail or frail HCT survivors. We hypothesized that an 8-week telehealth exercise intervention would be feasible and improve physical function in the telehealth exercise group. | PMC10150529 |
Methods and analysis | hematologic malignant diseases | BLOOD, APLASTIC ANEMIA | Study participants were identified from the Blood or Marrow Transplant Survivor Study (BMTSS), which is a retrospective cohort study of patients who received HCT at City of Hope (COH), University of Minnesota, or University of Alabama at Birmingham (UAB) for hematologic malignant diseases, or severe aplastic anemia, and survived at least 2 years after HCT [ | PMC10150529 |
Study procedures | CVD, BLOOD, CARDIOVASCULAR DISEASE | Information on frailty status was obtained from questionnaires completed by BMTSS participants [
Study schemaAbbreviations: BMTSS: Blood or Marrow Transplant Survivor Study; COH: City of Hope; CVD: Cardiovascular disease, UAB: University of Alabama Birmingham | PMC10150529 |
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Remote assessments of frailty and physical function | hand dynamometer, fatigue | SECONDARY, CHRONIC ILLNESS | The primary endpoint was feasibility as determined by 1) > 70% of participants completing all remote physical functional assessments, and 2) > 70% of participants in the exercise group completing > 70% (17/24) of the prescribed telehealth exercise sessions. Study participants were mailed a set of 3 gait sensors (for hip, right foot, and left foot), a hand dynamometer, measuring tape, and five exercise elastic bands that varied by resistance level. They completed an initial technology instructional support session via video conferencing. We used the telehealth exercise platform developed by Moerum Technologies (moterum.com, Salt Lake City, UT), which enables implementation of remote exercise strategies accessible through digital platforms (e.g. real-time video conferencing on smart phones or tablets) and customizable to individual needs.The secondary endpoint was frailty characteristics as assessed using a 5-scale frailty index before and after the 8-week period: body mass index (BMI), fatigue (13-item Functional Assessment of Chronic Illness Therapy [FACIT] fatigue scale), [ | PMC10150529 |
Exercise intervention | The 8-week telehealth exercise intervention (> 30 min per session; 3 sessions/week for 8 weeks) began within 3 weeks of baseline study assessments. Exercise programs were individualized and prescribed based on participants’ baseline assessment, physical limitations, and exercise preferences. Exercise intensity progression was achieved by altering the color of resistance bands. If a participant reached a band color with the max resistance, an additional band was added, allowing them to use up to all 5 bands at once. Each exercise session consisted of exercises targeting four essential components (dynamic balance, strength, core stability and postural control) [ | PMC10150529 |
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Sample size and statistical analysis | The sample size was evaluated using the statistical recommendation for the standardized effect size of 0.8 in 10 participants each arm [ | PMC10150529 |
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Results | MM, CML, AML, MDS, SD, HL, Hodgkin’s lymphoma, Non-Hodgkin’s lymphoma, ALL, NHL | ACUTE LYMPHOCYTIC LEUKEMIA, CLL, ACUTE MYELOID LEUKEMIA, AML, CHRONIC MYELOID LEUKEMIA, MULTIPLE MYELOMA, CML, MYELODYSPLASTIC SYNDROMES, CHRONIC LYMPHOCYTIC LEUKEMIA, NHL, BLOOD | There were 137 self-reported prefrail/frail HCT survivors identified in the BMTSS cohort. Of the 75 self-reported prefrail/frail survivors who were successfully contacted, 17 refused the referral, and 16 were deemed ineligible; Fig.
CONSORT diagram of telehealth exercise interventionAbbreviations: BMTSS: Blood or Marrow Transplant Survivor Study; COH: City of Hope; UAB: University of Alabama BirminghamBaseline characteristics are presented in Table
Baseline Participant Characteristics
MaleFemale10 (50)10 (50)4 (40)6 (60)6 (60)4 (40)
AllogeneicAutologous12 (60)8 (40)6 (60)4 (40)6 (60)4 (40)
Non-Hispanic whiteHispanic whiteAfrican AmericanAsian/Pacific Islander13 (65)2 (10)2 (7)0 (0)7 (70)1 (10)0 (0)1 (10)6 (60)1 (10)2 (14)1 (10)
ALLAMLCLLCMLMMMDSHLNHL1 (5)3 (15)1 (5)3 (15)1 (5)2 (10)2 (10)7 (35)1 (10)2 (20)0 (0)2 (20)0 (0)1 (10)1 (10)3 (30)0 (0)1 (10)1 (10)1 (10)1 (10)1 (10)1 (10)4 (40)
YesNo9 (45)11 (55)5 (50)5 (50)4 (40)6 (60)
FrailPre-frail18 (90)2 (10)9 (90)1 (10)9 (90)1 (10)Note. Data are presented as No. (%) in each column unless otherwise indicated. Abbreviations: ALL, Acute lymphocytic leukemia; AML, Acute myeloid leukemia; CLL, Chronic lymphocytic leukemia; CML, Chronic myeloid leukemia; MM, Multiple myeloma, MDS, Myelodysplastic syndromes; HL, Hodgkin’s lymphoma; NHL, Non-Hodgkin’s lymphoma, SD, standard deviation | PMC10150529 |
Study assessments and adherence to prescribed exercise sessions | ADVERSE EVENTS | Nineteen patients (95%) successfully completed all remote physical function assessments at pre- and post-intervention, and nine participants (90%) in the exercise group completed > 70% prescribed exercise sessions. The mean adherence to the 24 prescribed sessions for 10 patients in the exercise group was 94.2% (226/240 sessions); 9 of 10 participants attended at least 23 of 24 sessions. Although we remained flexible with scheduling and adapted to participants’ availability including weekends, most participants chose to perform exercise on weekdays (e.g. Monday/Wednesday/Friday or Tuesday/Thursday/Friday), except 2 participants who chose to include one weekend day for each week. No serious adverse events or unintended effects were associated with the exercise intervention during the 8 weeks. | PMC10150529 |
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Physical function outcomes | Frailty | Table
Frailty Characteristics
Telehealth ExerciseDelayed Control10.0 (2.0)8.2 (2.4)10.4 (2.2)7.8 (3.8)0.630.69
Telehealth ExerciseDelayed Control0.86 (0.22)0.78 (0.27)0.98 (0.25)0.75 (0.23)
0.11
Telehealth ExerciseDelayed Control0.63 (0.30)0.68 (0.24)0.79 (0.24)0.64 (0.27)
0.13
Telehealth ExerciseDelayed Control28.7 (11.7)26.6 (6.7)30.3 (14.0)23.9 (10.6)0.150.51
Telehealth ExerciseDelayed Control28.9 (12.2)23.9 (10.7)29.6 (11.6)22.5 (10.2)0.480.70
Telehealth ExerciseDelayed Control39.2 (6.6)31.7 (11.3)40.7 (5.6)31.3 (9.9)0.190.69
Telehealth ExerciseDelayed Control29.3 (6.9)27.1 (6.7)29.7 (9.7)26.5 (6.4)0.890.08 | PMC10150529 |
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Gait speed | Four-meter gait speed was significantly improved (0.86 ± 0.22 to 0.98 ± 0.25 m/s; P = 0.004) in the exercise group, while there was no significant change in the delayed control group (0.78 ± 0.27 to 0.75 ± 0.23 m/s, P = 0.11). However, there was no group x time interaction between the two groups before and after 8 weeks (P > 0.05). Notably, 8 out of 10 patients in the exercise group increased gait speed > 0.1 m/s, whereas only one participant in the delayed control group increased gait speed by > 0.1 m/s. Five-minute gait speed, as measured by gait sensors, also increased significantly in the exercise group (0.63 ± 0.30 to 0.79 ± 0.24 m/s: P = 0.04), and there was no significant change in the control group (0.68 ± 0.24 to 0.64 ± 0.27 m/s: P = 0.13). | PMC10150529 |
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Handgrip strength | There was no group x time interaction between the two groups before and after 8 weeks. Overall, there was a slight improvement in dominant arm handgrip strength in the exercise group, but it did not reach statistical significance (28.7 ± 11.7 to 30.3 ± 14.0 kg; P = 0.15). However, 5 out of 10 participants increased > 1 kg of handgrip strength (dominant arm) following the 8-week exercise training, compared to one participant in the control group. There was no significant change in the control group (P > 0.05). | PMC10150529 |
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SPPB | At baseline, mean SPPB score was 10.0 ± 2.0 for the exercise group and 8.2 ± 2.4 for the delayed control group. There was no significant mean difference between the two groups before and after 8 weeks. Of note, among 4 participants who had an SPPB score < 10 at baseline in the exercise group, 3 participants increased SPPB ( | PMC10150529 |
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Fatigue | There was no significant mean difference between the two groups before and after 8 weeks in the exercise (39.3 ± 6.6 to 40.7 ± 5.6) and control (31.7 ± 11.3 to 31.3 ± 9.9) groups; P > 0.05. | PMC10150529 |
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Acknowledgements | Not applicable. | PMC10150529 |
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Author Contribution | Conceptualization (All authors); Methodology (KL, JS, LL, ER, LH, MSS, RN, SJF, FLW, SB, SA); Writing Original Draft (all authors); Writing Review & Editing (All authors); Resources (KL, SB, SA); Supervision (KL). All authors read and approved the final manuscript. | PMC10150529 |
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Funding | Leukemia Lymphoma, Cancer | CANCER | This study was supported by the Conrad N. Hilton Foundation Pilot Award; the National Cancer Institute (R01 CA078938, U01 CA213140); the Leukemia Lymphoma Society (R6502-16). | PMC10150529 |
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