Using Serum Metabolomic Signatures to Investigate Effects of Acupuncture on Pain-Fatigue-Sleep Disturbance in Breast Cancer Survivors

Background/Objectives: Acupuncture is an efficacious integrative therapy for treating pain, fatigue, and sleep disturbance (the psychoneurological symptom cluster) in breast cancer survivors. However, the mechanisms underlying its effects remain unclear, and related metabolomics studies are limited....

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Main Authors: Hongjin Li, Ardith Z. Doorenbos, Yinglin Xia, Jun Sun, Hannah Choi, Richard E. Harris, Shuang Gao, Katy Sullivan, Judith M. Schlaeger
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Metabolites
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Online Access:https://www.mdpi.com/2218-1989/14/12/698
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author Hongjin Li
Ardith Z. Doorenbos
Yinglin Xia
Jun Sun
Hannah Choi
Richard E. Harris
Shuang Gao
Katy Sullivan
Judith M. Schlaeger
author_facet Hongjin Li
Ardith Z. Doorenbos
Yinglin Xia
Jun Sun
Hannah Choi
Richard E. Harris
Shuang Gao
Katy Sullivan
Judith M. Schlaeger
author_sort Hongjin Li
collection DOAJ
description Background/Objectives: Acupuncture is an efficacious integrative therapy for treating pain, fatigue, and sleep disturbance (the psychoneurological symptom cluster) in breast cancer survivors. However, the mechanisms underlying its effects remain unclear, and related metabolomics studies are limited. This study aimed to examine serum metabolite changes after acupuncture and their relationships to symptom improvement. Methods: Forty-two breast cancer survivors experiencing pain, fatigue, and sleep disturbance participated in a single-arm acupuncture trial. They received a 10-session acupuncture intervention over 5 weeks. Fasting blood samples and symptom surveys were collected before and after the acupuncture intervention, and untargeted metabolomics profiling was conducted on serum samples. Mixed-effects models adjusting for covariates (age, race, body mass index, and antidepressant use) were applied for analysis. Results: After acupuncture, there was a significant reduction in the psychoneurological symptom cluster (mean reduction = −6.2, <i>p</i> < 0.001).Bonferroni correction was applied to 40 independent metabolite clusters (α = 0.00125); cysteine-glutathione disulfide (<i>p</i> = 0.0006) significantly increased, and retinal (<i>p</i> = 0.0002) and cis-urocanate (<i>p</i> = 0.0005) were significantly decreased. Dimethyl sulfone (<i>p</i> = 0.00139) showed a trend towards reduction after acupuncture and its change (<i>p</i> = 0.04, β =1.97) was positively associated with reduction in the psychoneurological symptom cluster. Also, increased lauroylcarnitine (<i>p</i> = 0.0009) and decreased cytosine (<i>p</i> = 0.0008) can modulate the therapeutic effects of acupuncture. Conclusions: Acupuncture demonstrates beneficial effects on the psychoneurological symptom cluster in breast cancer survivors. Dimethyl sulfone may be a promising mediator in the relationship between acupuncture and psychoneurological symptoms, while acylcarnitine metabolism may modulate the therapeutic effect of acupuncture.
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spelling doaj-art-7baec0cbbaad460eb0c870c0727bd4a12025-08-20T02:00:35ZengMDPI AGMetabolites2218-19892024-12-01141269810.3390/metabo14120698Using Serum Metabolomic Signatures to Investigate Effects of Acupuncture on Pain-Fatigue-Sleep Disturbance in Breast Cancer SurvivorsHongjin Li0Ardith Z. Doorenbos1Yinglin Xia2Jun Sun3Hannah Choi4Richard E. Harris5Shuang Gao6Katy Sullivan7Judith M. Schlaeger8College of Nursing, University of Illinois Chicago, 845 S. Damen Avenue, Chicago, IL 60612, USACollege of Nursing, University of Illinois Chicago, 845 S. Damen Avenue, Chicago, IL 60612, USACollege of Medicine, University of Illinois Chicago, 1853 W Polk St, Chicago, IL 60612, USAUniversity of Illinois Cancer Center, 818 South Wolcott Ave, Chicago, IL 60612, USACollege of Nursing, University of Illinois Chicago, 845 S. Damen Avenue, Chicago, IL 60612, USASusan Samueli Integrative Health Institute, School of Medicine, University of California at Irvine, 856 Health Sciences Rd Suite 2600, Irvine, CA 92617, USACollege of Medicine, University of Illinois Chicago, 1853 W Polk St, Chicago, IL 60612, USACollege of Nursing, University of Illinois Chicago, 845 S. Damen Avenue, Chicago, IL 60612, USACollege of Nursing, University of Illinois Chicago, 845 S. Damen Avenue, Chicago, IL 60612, USABackground/Objectives: Acupuncture is an efficacious integrative therapy for treating pain, fatigue, and sleep disturbance (the psychoneurological symptom cluster) in breast cancer survivors. However, the mechanisms underlying its effects remain unclear, and related metabolomics studies are limited. This study aimed to examine serum metabolite changes after acupuncture and their relationships to symptom improvement. Methods: Forty-two breast cancer survivors experiencing pain, fatigue, and sleep disturbance participated in a single-arm acupuncture trial. They received a 10-session acupuncture intervention over 5 weeks. Fasting blood samples and symptom surveys were collected before and after the acupuncture intervention, and untargeted metabolomics profiling was conducted on serum samples. Mixed-effects models adjusting for covariates (age, race, body mass index, and antidepressant use) were applied for analysis. Results: After acupuncture, there was a significant reduction in the psychoneurological symptom cluster (mean reduction = −6.2, <i>p</i> < 0.001).Bonferroni correction was applied to 40 independent metabolite clusters (α = 0.00125); cysteine-glutathione disulfide (<i>p</i> = 0.0006) significantly increased, and retinal (<i>p</i> = 0.0002) and cis-urocanate (<i>p</i> = 0.0005) were significantly decreased. Dimethyl sulfone (<i>p</i> = 0.00139) showed a trend towards reduction after acupuncture and its change (<i>p</i> = 0.04, β =1.97) was positively associated with reduction in the psychoneurological symptom cluster. Also, increased lauroylcarnitine (<i>p</i> = 0.0009) and decreased cytosine (<i>p</i> = 0.0008) can modulate the therapeutic effects of acupuncture. Conclusions: Acupuncture demonstrates beneficial effects on the psychoneurological symptom cluster in breast cancer survivors. Dimethyl sulfone may be a promising mediator in the relationship between acupuncture and psychoneurological symptoms, while acylcarnitine metabolism may modulate the therapeutic effect of acupuncture.https://www.mdpi.com/2218-1989/14/12/698acupuncturebreast cancerfatiguemetabolomicspainpsychoneurological symptom cluster
spellingShingle Hongjin Li
Ardith Z. Doorenbos
Yinglin Xia
Jun Sun
Hannah Choi
Richard E. Harris
Shuang Gao
Katy Sullivan
Judith M. Schlaeger
Using Serum Metabolomic Signatures to Investigate Effects of Acupuncture on Pain-Fatigue-Sleep Disturbance in Breast Cancer Survivors
Metabolites
acupuncture
breast cancer
fatigue
metabolomics
pain
psychoneurological symptom cluster
title Using Serum Metabolomic Signatures to Investigate Effects of Acupuncture on Pain-Fatigue-Sleep Disturbance in Breast Cancer Survivors
title_full Using Serum Metabolomic Signatures to Investigate Effects of Acupuncture on Pain-Fatigue-Sleep Disturbance in Breast Cancer Survivors
title_fullStr Using Serum Metabolomic Signatures to Investigate Effects of Acupuncture on Pain-Fatigue-Sleep Disturbance in Breast Cancer Survivors
title_full_unstemmed Using Serum Metabolomic Signatures to Investigate Effects of Acupuncture on Pain-Fatigue-Sleep Disturbance in Breast Cancer Survivors
title_short Using Serum Metabolomic Signatures to Investigate Effects of Acupuncture on Pain-Fatigue-Sleep Disturbance in Breast Cancer Survivors
title_sort using serum metabolomic signatures to investigate effects of acupuncture on pain fatigue sleep disturbance in breast cancer survivors
topic acupuncture
breast cancer
fatigue
metabolomics
pain
psychoneurological symptom cluster
url https://www.mdpi.com/2218-1989/14/12/698
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