{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,4]],"date-time":"2026-09-04T14:28:10Z","timestamp":1788532090933,"version":"build-2803163510"},"reference-count":42,"publisher":"American Chemical Society (ACS)","issue":"9","license":[{"start":{"date-parts":[[2026,8,10]],"date-time":"2026-08-10T00:00:00Z","timestamp":1786320000000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2026,8,10]],"date-time":"2026-08-10T00:00:00Z","timestamp":1786320000000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2026,8,10]],"date-time":"2026-08-10T00:00:00Z","timestamp":1786320000000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-045"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,9,4]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Opioid analgesia shows substantial interindividual variability in cancer patients, yet the underlying serum inflammatory alterations remain poorly characterized. This study collected plasma samples from 44 cancer pain patients before and after opioid initiation, quantifying 92 immunoinflammation proteins by Olink proteomics. Cross-sectional analysis identified nine differentially expressed proteins between responders and nonresponders. A five-protein nomogram involving TGF-\u03b1, EN-RAGE, CASP-8, ST1A1, and IL-10RA demonstrated superior predictive performance for opioid efficacy (AUC 0.902) compared to traditional CRP (AUC 0.625). Longitudinal analysis of this population revealed upregulation of \u03b2-NGF, MCP-4, IL-1alpha, and IL-13, and downregulation of CD6, IL-12beta, and SCF after treatment. STRING analysis clustered these proteins into three functional groups: efficacy-related (NGF), bowel-inflammation-related (IL-12\/IL-13), and CD6-related. Notably, expression of IL-12\u03b2 showed a significant efficacy\u2013constipation interaction: constipation completely reversed the efficacy-IL-12 association, and higher IL-12 levels predicted favorable response only in nonconstipated patients. These findings established a pretreatment protein signature for predicting opioid efficacy and revealed systemic immune reprogramming following opioid therapy.<\/jats:p>","DOI":"10.1021\/acs.jproteome.6c00052","type":"journal-article","created":{"date-parts":[[2026,8,10]],"date-time":"2026-08-10T13:02:10Z","timestamp":1786366930000},"page":"4589-4598","source":"Crossref","is-referenced-by-count":0,"title":["Inflammatory\nSerum Olink Proteomics in Cancer-Related\nPain Treated with Opioids: A Pilot Cross-Sectional and Longitudinal\nStudy"],"prefix":"10.1021","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6470-7780","authenticated-orcid":true,"given":"Zihui","family":"Li","sequence":"first","affiliation":[{"name":"Affiliated Hospital of Jianghan University , , , ,","place":["Wuhan, Hubei Province, China, 430033"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Deng","sequence":"additional","affiliation":[{"name":"Affiliated Hospital of Jianghan University , , , ,","place":["Wuhan, Hubei Province, China, 430033"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fei","family":"Yan","sequence":"additional","affiliation":[{"name":"Affiliated Hospital of Jianghan University , , , ,","place":["Wuhan, Hubei Province, China, 430033"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Liu","sequence":"additional","affiliation":[{"name":"Affiliated Hospital of Jianghan University , , , ,","place":["Wuhan, Hubei Province, China, 430033"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanling","family":"Ma","sequence":"additional","affiliation":[{"name":"Affiliated Hospital of Jianghan University , , , ,","place":["Wuhan, Hubei Province, China, 430033"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianhai","family":"Sun","sequence":"additional","affiliation":[{"name":"Affiliated Hospital of Jianghan University , , , ,","place":["Wuhan, Hubei Province, China, 430033"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,8,10]]},"reference":[{"issue":"7","key":"2026090409131058300_cit1","doi-asserted-by":"publisher","DOI":"10.6004\/jnccn.2025.0032","article-title":"Adult\nCancer Pain, Version 2.2025, NCCN Clinical Practice Guidelines In\nOncology","volume":"23","author":"Swarm","year":"2025","journal-title":"J. Natl. Compr Canc Netw"},{"issue":"3","key":"2026090409131058300_cit2","doi-asserted-by":"publisher","first-page":"286","DOI":"10.3322\/caac.21823","article-title":"Opioid analgesics for nociceptive cancer pain: A comprehensive\nreview","volume":"74","author":"Abdel Shaheed","year":"2024","journal-title":"Ca-Cancer J. Clin."},{"issue":"3","key":"2026090409131058300_cit3","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/S0304-3959(01)00324-4","article-title":"Symptoms during cancer pain treatment following WHO-guidelines: a\nlongitudinal follow-up study of symptom prevalence, severity and etiology","volume":"93","author":"Meuser","year":"2001","journal-title":"Pain"},{"key":"2026090409131058300_cit4","doi-asserted-by":"publisher","first-page":"113871","DOI":"10.1016\/j.biopha.2022.113871","article-title":"Pharmacological\nmanagement of cancer pain: Novel therapeutics","volume":"156","author":"Virgen","year":"2022","journal-title":"Biomed. Pharmacother."},{"issue":"4","key":"2026090409131058300_cit5","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1097\/FPC.0000000000000032","article-title":"Genetic, pathological\nand physiological determinants of transdermal fentanyl pharmacokinetics\nin 620 cancer patients of the EPOS study","volume":"24","author":"Barratt","year":"2014","journal-title":"Pharmacogenet.\nGenomics"},{"issue":"1","key":"2026090409131058300_cit6","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.brainresrev.2007.06.006","article-title":"Listening\u2033\nand \u2033talking\u2033 to neurons: implications of immune activation\nfor pain control and increasing the efficacy of opioids","volume":"56","author":"Watkins","year":"2007","journal-title":"Brain Res. Rev."},{"issue":"Pt A","key":"2026090409131058300_cit7","doi-asserted-by":"publisher","first-page":"111142","DOI":"10.1016\/j.intimp.2023.111142","article-title":"The bidirectional relationship\nbetween opioids and\nthe gut microbiome: Implications for opioid tolerance and clinical\ninterventions","volume":"125","author":"Taboun","year":"2023","journal-title":"Int. Immunopharmacol."},{"issue":"3","key":"2026090409131058300_cit8","doi-asserted-by":"publisher","first-page":"713","DOI":"10.3390\/biomedicines11030713","article-title":"Inflammatory Blood\nSignature Related to Common Psychological\nComorbidity in Chronic Pain","volume":"11","author":"Karshikoff","year":"2023","journal-title":"Biomedicines"},{"issue":"2","key":"2026090409131058300_cit9","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1515\/sjpain-2018-0340","article-title":"Detection of systemic\ninflammation in severely impaired chronic pain\npatients and effects of a multimodal pain rehabilitation program","volume":"19","author":"Hysing","year":"2019","journal-title":"Scand J. Pain"},{"issue":"8031","key":"2026090409131058300_cit10","doi-asserted-by":"publisher","first-page":"S28","DOI":"10.1038\/d41586-024-03004-1","article-title":"Could biomarkers mean better pain treatment?","volume":"633","author":"Mitchell Crow","year":"2024","journal-title":"Nature"},{"issue":"1","key":"2026090409131058300_cit11","doi-asserted-by":"publisher","first-page":"S37","DOI":"10.1097\/j.pain.0000000000001529","article-title":"Deconstructing\nbiomarkers for chronic\npain: context- and hypothesis-dependent biomarker types in relation\nto chronic pain","volume":"160","author":"Reckziegel","year":"2019","journal-title":"Pain"},{"issue":"5","key":"2026090409131058300_cit12","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1016\/j.neuron.2019.02.019","article-title":"Composite\nPain Biomarker Signatures\nfor Objective Assessment and Effective Treatment","volume":"101","author":"Tracey","year":"2019","journal-title":"Neuron"},{"issue":"7","key":"2026090409131058300_cit13","doi-asserted-by":"publisher","first-page":"811","DOI":"10.1111\/anae.16011","article-title":"Risk factors\nand prediction modelling for chronic post-surgical pain after breast\ncancer surgery","volume":"78","author":"Shanthanna","year":"2023","journal-title":"Anaesthesia"},{"issue":"12","key":"2026090409131058300_cit14","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1007\/s00520-023-08144-0","article-title":"Nomogram for predicting opioid-induced\nnausea and vomiting for cancer pain patients","volume":"31","author":"Kong","year":"2023","journal-title":"Support Care Cancer"},{"issue":"7","key":"2026090409131058300_cit15","doi-asserted-by":"publisher","first-page":"3488","DOI":"10.3390\/ijms23073488","article-title":"Machine-Learning Analysis\nof Serum Proteomics in Neuropathic Pain after Nerve Injury in Breast\nCancer Surgery Points at Chemokine Signaling via SIRT2 Regulation","volume":"23","author":"Lotsch","year":"2022","journal-title":"Int. J. Mol. Sci."},{"issue":"1","key":"2026090409131058300_cit16","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1038\/s41398-023-02627-8","article-title":"Multivariate\nanalyses of immune markers\nreveal increases in plasma EN-RAGE in first-episode psychosis patients","volume":"13","author":"Korhonen","year":"2023","journal-title":"Transl. Psychiatry"},{"key":"2026090409131058300_cit17","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1016\/j.psyneuen.2017.02.029","article-title":"Inflammatory markers in late pregnancy\nin association with postpartum depression-A nested case-control study","volume":"79","author":"Brann","year":"2017","journal-title":"Psychoneuroendocrinology"},{"issue":"14","key":"2026090409131058300_cit18","doi-asserted-by":"publisher","first-page":"2717","DOI":"10.1111\/bph.13750","article-title":"Opioids and the\nimmune system - friend or foe","volume":"175","author":"Plein","year":"2018","journal-title":"Br. J. Pharmacol."},{"issue":"1","key":"2026090409131058300_cit19","doi-asserted-by":"publisher","first-page":"260","DOI":"10.3390\/curroncol31010017","article-title":"Impact of Opioid Use\non Duration of Therapy and Overall Survival for Patients with Advanced\nNon-Small Cell Lung Cancer Treated with Immune Checkpoint Inhibitors","volume":"31","author":"Young","year":"2024","journal-title":"Curr. Oncol"},{"issue":"1","key":"2026090409131058300_cit20","doi-asserted-by":"publisher","DOI":"10.1111\/cns.70216","article-title":"C3\/C3aR Bridges Spinal\nAstrocyte-Microglia Crosstalk\nand Accelerates Neuroinflammation in Morphine-Tolerant Rats","volume":"31","author":"Peng","year":"2025","journal-title":"CNS Neurosci. Ther."},{"issue":"10","key":"2026090409131058300_cit21","doi-asserted-by":"publisher","first-page":"104607","DOI":"10.1016\/j.jpain.2024.104607","article-title":"Comparison of Morphine\nand Endomorphin Analog ZH853 for Tolerance and Immunomodulation in\na Rat Model of Neuropathic Pain","volume":"25","author":"Hunter","year":"2024","journal-title":"J. Pain"},{"key":"2026090409131058300_cit22","doi-asserted-by":"publisher","first-page":"3009","DOI":"10.3389\/fimmu.2019.03009","article-title":"Cytokines in Pain:\nHarnessing Endogenous Anti-Inflammatory\nSignaling for Improved Pain Management","volume":"10","author":"Vanderwall","year":"2019","journal-title":"Front.\nImmunol."},{"issue":"14","key":"2026090409131058300_cit23","doi-asserted-by":"publisher","first-page":"2726","DOI":"10.1111\/bph.13903","article-title":"Influence of opioids on immune function\nin patients\nwith cancer pain: from bench to bedside","volume":"175","author":"Boland","year":"2018","journal-title":"Br.\nJ. Pharmacol."},{"key":"2026090409131058300_cit24","doi-asserted-by":"publisher","first-page":"2994","DOI":"10.3389\/fimmu.2018.02994","article-title":"CD6, a Rheostat-Type\nSignalosome That Tunes T Cell Activation","volume":"9","author":"Goncalves","year":"2018","journal-title":"Front.\nImmunol."},{"issue":"12","key":"2026090409131058300_cit25","doi-asserted-by":"publisher","first-page":"2589","DOI":"10.3390\/cells9122589","article-title":"Soluble CD5 and CD6: Lymphocytic\nClass I Scavenger Receptors as Immunotherapeutic Agents","volume":"9","author":"Velasco-de Andres","year":"2020","journal-title":"Cells"},{"issue":"1","key":"2026090409131058300_cit26","doi-asserted-by":"publisher","DOI":"10.1136\/jitc-2019-000172","article-title":"Multifaceted effects of soluble human CD6 in experimental\ncancer models","volume":"8","author":"Simoes","year":"2020","journal-title":"J. Immunother Cancer"},{"key":"2026090409131058300_cit27","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.phrs.2018.07.019","article-title":"Targeting\nneurotrophin signaling in cancer: The renaissance","volume":"135","author":"Griffin","year":"2018","journal-title":"Pharmacol. Res."},{"issue":"10","key":"2026090409131058300_cit28","doi-asserted-by":"publisher","first-page":"2210","DOI":"10.1097\/j.pain.0000000000001625","article-title":"Nerve growth\nfactor antibody for\nthe treatment of osteoarthritis pain and chronic low-back pain: mechanism\nof action in the context of efficacy and safety","volume":"160","author":"Schmelz","year":"2019","journal-title":"Pain"},{"issue":"1","key":"2026090409131058300_cit29","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1186\/s12871-016-0242-x","article-title":"Anti-nerve\ngrowth factor antibody attenuates chronic morphine treatment-induced\ntolerance in the rat","volume":"16","author":"Cheppudira","year":"2015","journal-title":"BMC Anesthesiol."},{"key":"2026090409131058300_cit30","doi-asserted-by":"publisher","first-page":"1744806916644928","DOI":"10.1177\/1744806916644928","article-title":"Impacts of\nanti-nerve growth factor\nantibody on pain-related behaviors and expressions of opioid receptor\nin spinal dorsal horn and dorsal root ganglia of rats with cancer-induced\nbone pain","volume":"12","author":"Yao","year":"2016","journal-title":"Mol. Pain"},{"issue":"4","key":"2026090409131058300_cit31","doi-asserted-by":"publisher","first-page":"765","DOI":"10.1097\/ALN.0000000000004880","article-title":"Nerve Growth Factor\/Tyrosine\nKinase A Receptor Pathway Enhances Analgesia in an Experimental Mouse\nModel of Bone Cancer Pain by Increasing Membrane Levels of delta-Opioid\nReceptors","volume":"140","author":"Kan","year":"2024","journal-title":"Anesthesiology"},{"issue":"16","key":"2026090409131058300_cit32","doi-asserted-by":"publisher","first-page":"5617","DOI":"10.1523\/JNEUROSCI.5296-09.2010","article-title":"Nerve growth\nfactor-regulated emergence of functional delta-opioid receptors","volume":"30","author":"Bie","year":"2010","journal-title":"J. Neurosci."},{"key":"2026090409131058300_cit33","doi-asserted-by":"publisher","first-page":"1597922","DOI":"10.3389\/fnins.2025.1597922","article-title":"Molecular and cellular basis of mu-opioid\nreceptor\nsignaling: mechanisms underlying tolerance and dependence development","volume":"19","author":"Swingler","year":"2025","journal-title":"Front. Neurosci."},{"issue":"24","key":"2026090409131058300_cit34","doi-asserted-by":"publisher","first-page":"5203","DOI":"10.1016\/j.cell.2023.10.029","article-title":"Molecular basis\nof opioid receptor signaling","volume":"186","author":"Che","year":"2023","journal-title":"Cell"},{"issue":"14","key":"2026090409131058300_cit35","doi-asserted-by":"publisher","first-page":"7999","DOI":"10.3390\/ijms25147999","article-title":"Opioid Use\nand Gut Dysbiosis in Cancer Pain Patients","volume":"25","author":"Coluzzi","year":"2024","journal-title":"Int.\nJ. Mol. Sci."},{"key":"2026090409131058300_cit36","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1111\/j.1749-6632.2003.tb03144.x","article-title":"Effects of\nin vitro and in vivo opioids on the production of IL-12 and IL-10\nby murine macrophages","volume":"992","author":"Sacerdote","year":"2003","journal-title":"Ann. N.Y. Acad. Sci."},{"issue":"5","key":"2026090409131058300_cit37","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1023\/A:1019766602138","article-title":"Endomorphin-2 modulates\nproductions of TNF-\u03b1, IL-1beta, IL-10,\nand IL-12, and alters functions related to innate immune of macrophages","volume":"26","author":"Azuma","year":"2002","journal-title":"Inflammation"},{"issue":"8","key":"2026090409131058300_cit38","doi-asserted-by":"publisher","first-page":"4999","DOI":"10.4049\/jimmunol.175.8.4999","article-title":"Chronic morphine\ntreatment promotes specific Th2 cytokine production by murine T cells\nin vitro via a Fas\/Fas ligand-dependent mechanism","volume":"175","author":"Greeneltch","year":"2005","journal-title":"J. Immunol."},{"issue":"11","key":"2026090409131058300_cit39","doi-asserted-by":"publisher","first-page":"4393","DOI":"10.7150\/thno.96184","article-title":"Intestinal\nepithelial damage-derived mtDNA activates STING-IL12 axis in dendritic\ncells to promote colitis","volume":"14","author":"Cai","year":"2024","journal-title":"Theranostics"},{"issue":"5","key":"2026090409131058300_cit40","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1016\/j.cmet.2025.01.007","article-title":"Synergistic role of\ngut-microbial L-ornithine in enhancing ustekinumab\nefficacy for Crohn\u2019s disease","volume":"37","author":"Wang","year":"2025","journal-title":"Cell Metab."},{"issue":"5","key":"2026090409131058300_cit41","doi-asserted-by":"publisher","first-page":"CD007572","DOI":"10.1002\/14651858.CD007572.pub4","article-title":"Anti-IL-12\/23p40 antibodies for induction\nof remission in Crohn\u2019s disease","volume":"2025","author":"Hasskamp","year":"2025","journal-title":"Cochrane\nDatabase Syst. Rev."},{"issue":"7","key":"2026090409131058300_cit42","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1038\/s41575-023-00768-1","article-title":"IL-12 and IL-23 pathway inhibition in inflammatory\nbowel disease","volume":"20","author":"Verstockt","year":"2023","journal-title":"Nat. Rev. Gastroenterol. Hepatol."}],"container-title":["Journal of Proteome Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.jproteome.6c00052","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/jprobs\/article-pdf\/25\/9\/4589\/66471201\/acs.jproteome.6c00052.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/jprobs\/article-pdf\/25\/9\/4589\/66471201\/acs.jproteome.6c00052.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,4]],"date-time":"2026-09-04T14:05:13Z","timestamp":1788530713000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/jprobs\/article\/25\/9\/4589\/5251097\/Inflammatory-Serum-Olink-Proteomics-in-Cancer"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,10]]},"references-count":42,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,8,10]]},"published-print":{"date-parts":[[2026,9,4]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.jproteome.6c00052","relation":{},"ISSN":["1535-3893","1535-3907"],"issn-type":[{"value":"1535-3893","type":"print"},{"value":"1535-3907","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,10]]}}}