The Serum from Patients with Secondary Frozen Shoulder Following Rotator Cuff Repair Induces Shoulder Capsule Fibrosis and Promotes Macrophage Polarization and Fibroblast Activation

References

• Fermont AJ, Wolterbeek N, Wessel RN, Baeyens JP, de Bie RA. Prognostic factors for successful recovery after arthroscopic rotator cuff repair: a systematic literature review. J Orthop Sports Phys Ther. 2014;44(3):153–163. doi:10.2519/jospt.2014.4832
   PubMed Web of Science ®Google Scholar
• Papalia R, Franceschi F, Vasta S, Gallo A, Maffulli N, Denaro V. Shoulder stiffness and rotator cuff repair. Br Med Bull. 2012;104:163–174. doi:10.1093/bmb/lds006
   PubMed Web of Science ®Google Scholar
• Sun Y, Lin J, Luo Z, Chen J. Preoperative lymphocyte to monocyte ratio can be a prognostic factor in arthroscopic repair of small to large rotator cuff tears. Am J Sports Med. 2020;48(12):3042–3050. doi:10.1177/0363546520953427
   PubMed Web of Science ®Google Scholar
• Cho CH, Bae KC, Kim DH. Patients who have undergone rotator cuff repair experience around 75% functional recovery at 6 months after surgery. Knee Surg Sports Traumatol Arthrosc. 2020. doi:10.1007/s00167-020-06019-z
   Web of Science ®Google Scholar
• Blonna D, Fissore F, Bellato E, et al. Subclinical hypothyroidism and diabetes as risk factors for postoperative stiff shoulder. Knee Surg Sports Traumatol Arthrosc. 2017;25(7):2208–2216. doi:10.1007/s00167-015-3906-z
   PubMed Web of Science ®Google Scholar
• Harada GK, Arshi A, Fretes N, et al. Preoperative vitamin D deficiency is associated with higher postoperative complications in arthroscopic rotator cuff repair. J Am Acad Orthop Surg Glob Res Rev. 2019;3(7):e075. doi:10.5435/JAAOSGlobal-D-19-00075
   PubMedGoogle Scholar
• Erkus E, Aktas G, Atak BM, Kocak MZ, Duman TT, Savli H. Haemogram parameters in vitamin D deficiency. J Coll Physicians Surg Pak JCPSP. 2018;28(10):779–782.
   PubMed Web of Science ®Google Scholar
• Akbas EM, Gungor A, Ozcicek A, Akbas N, Askin S, Polat M. Vitamin D and inflammation: evaluation with neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio. Arch Med Sci. 2016;12(4):721–727. doi:10.5114/aoms.2015.50625
   PubMed Web of Science ®Google Scholar
• Cheng S, Hou G, Liu Z, et al. Risk prediction of in-hospital mortality among patients with type 2 diabetes mellitus and concomitant community-acquired pneumonia. Ann Palliat Med. 2020;9(5):3313–3325. doi:10.21037/apm-20-1489
   PubMed Web of Science ®Google Scholar
• Khaled SAA, NasrEldin E, Makarem YS, Mahmoud HFF. Value of platelet distribution width and mean platelet volume in disease activity score of rheumatoid arthritis. J Inflamm Res. 2020;13:595–606. doi:10.2147/JIR.S265811
   PubMed Web of Science ®Google Scholar
• He S, Mao X, Lei H, et al. Peripheral blood inflammatory-immune cells as a predictor of infertility in women with polycystic ovary syndrome. J Inflamm Res. 2020;13:441–450. doi:10.2147/JIR.S260770
   PubMed Web of Science ®Google Scholar
• Oner K, Okutan AE, Ayas MS, Paksoy AE, Polat F. Predicting postoperative pain with neutrophil/lymphocyte ratio after arthroscopic rotator cuff repair. Asia Pac J Sports Med Arthrosc Rehabil Technol. 2020;20:24–27. doi:10.1016/j.asmart.2020.03.001
   PubMed Web of Science ®Google Scholar
• Li M, Jiang M, Meng J, Tao L. Exosomes: carriers of pro-fibrotic signals and therapeutic targets in fibrosis. Curr Pharm Des. 2019;25(42):4496–4509. doi:10.2174/1381612825666191209161443
   PubMed Web of Science ®Google Scholar
• Kartika R, Purnamasari D, Pradipta S, Larasati RA, Wibowo H. Impact of low interferon-gamma and IL-10 levels on TNF-alpha and IL-6 production by PHA-induced PBMCs in type 2 diabetes mellitus. J Inflamm Res. 2020;13:187–193. doi:10.2147/JIR.S245064
   PubMed Web of Science ®Google Scholar
• Zhang H, Cao N, Yang Z, et al. Bilobalide alleviated dextran sulfate sodium-induced experimental colitis by inhibiting M1 macrophage polarization through the NF-kappaB signaling pathway. Front Pharmacol. 2020;11:718. doi:10.3389/fphar.2020.00718
   PubMed Web of Science ®Google Scholar
• Nie MF, Xie Q, Wu YH, et al. Serum and ectopic endometrium from women with endometriosis modulate macrophage M1/M2 polarization via the Smad2/Smad3 pathway. J Immunol Res. 2018;2018:6285813. doi:10.1155/2018/6285813
   PubMed Web of Science ®Google Scholar
• Sun Y, Wang H, Li Y, Liu S, Chen J, Ying H. miR-24 and miR-122 negatively regulate the transforming growth factor-beta/smad signaling pathway in skeletal muscle fibrosis. Mol Ther Nucleic Acids. 2018;11:528–537. doi:10.1016/j.omtn.2018.04.005
   PubMedGoogle Scholar
• Darmadi D, Ruslie RH. Association between serum interleukin (IL)-12 level and severity of non-alcoholic fatty liver disease (NAFLD). Rom J Intern Med. 2021;59:66–72.
   PubMed Web of Science ®Google Scholar
• Suthanthiran M, Gerber LM, Schwartz JE, et al. Circulating transforming growth factor-beta1 levels and the risk for kidney disease in African Americans. Kidney Int. 2009;76(1):72–80. doi:10.1038/ki.2009.66
   PubMed Web of Science ®Google Scholar
• Xu L, Yang D, Zhu S, et al. Bleomycin-induced pulmonary fibrosis is attenuated by an antibody against KL-6. Exp Lung Res. 2013;39(6):241–248. doi:10.3109/01902148.2013.798056
   PubMed Web of Science ®Google Scholar
• Tamai K, Akutsu M, Yano Y. Primary frozen shoulder: brief review of pathology and imaging abnormalities. J Orthop Res. 2014;19(1):1–5. doi:10.1007/s00776-013-0495-x
   Google Scholar
• Akbar M, McLean M, Garcia-Melchor E, et al. Fibroblast activation and inflammation in frozen shoulder. PLoS One. 2019;14(4):e0215301. doi:10.1371/journal.pone.0215301
   PubMed Web of Science ®Google Scholar
• Wang D, Tan H, Lebaschi AH, et al. Kartogenin enhances collagen organization and mechanical strength of the repaired enthesis in a murine model of rotator cuff repair. Arthroscopy. 2018;34(9):2579–2587. doi:10.1016/j.arthro.2018.04.022
   PubMed Web of Science ®Google Scholar
• Dyrna F, Zakko P, Pauzenberger L, McCarthy MB, Mazzocca AD, Dyment NA. Human subacromial bursal cells display superior engraftment versus bone marrow stromal cells in murine tendon repair. Am J Sports Med. 2018;46(14):3511–3520. doi:10.1177/0363546518802842
   PubMed Web of Science ®Google Scholar
• Hamada K, Fukuda H, Mikasa M, Kobayashi Y. Roentgenographic findings in massive rotator cuff tears. A long-term observation. Clin Orthop Relat Res. 1990;254:92–96.
   Google Scholar
• Chung SW, Huong CB, Kim SH, Oh JH. Shoulder stiffness after rotator cuff repair: risk factors and influence on outcome. Arthroscopy. 2013;29(2):290–300. doi:10.1016/j.arthro.2012.08.023
   PubMed Web of Science ®Google Scholar
• Sun Y, Liu S, Chen S, Chen J. The effect of corticosteroid injection into rotator interval for early frozen shoulder: a randomized controlled trial. Am J Sports Med. 2018;46(3):663–670. doi:10.1177/0363546517744171
   PubMed Web of Science ®Google Scholar
• Richards RR, An KN, Bigliani LU, et al. A standardized method for the assessment of shoulder function. J Shoulder Elbow Surg. 1994;3(6):347–352. doi:10.1016/S1058-2746(09)80019-0
   PubMedGoogle Scholar
• Constant CR, Murley AH. A clinical method of functional assessment of the shoulder. Clin Orthop Relat Res. 1987;(214):160–164.
   PubMed Web of Science ®Google Scholar
• Ge Y, Chen S, Chen J, Hua Y, Li Y. The development and evaluation of a new shoulder scoring system based on the view of patients and physicians: the Fudan University shoulder score. Arthroscopy. 2013;29(4):613–622. doi:10.1016/j.arthro.2012.11.009
   PubMed Web of Science ®Google Scholar
• Hong J, Mao Y, Chen X, et al. Elevated preoperative neutrophil-to-lymphocyte ratio predicts poor disease-free survival in Chinese women with breast cancer. Tumour Biol. 2016;37(3):4135–4142. doi:10.1007/s13277-015-4233-1
   PubMedGoogle Scholar
• Moser HL, Doe AP, Meier K, et al. Genetic lineage tracing of targeted cell populations during enthesis healing. J Orthop Res. 2018;36(12):3275–3284. doi:10.1002/jor.24122
   PubMed Web of Science ®Google Scholar
• Oki S, Shirasawa H, Yoda M, et al. Generation and characterization of a novel shoulder contracture mouse model. J Orthop Res. 2015;33(11):1732–1738. doi:10.1002/jor.22943
   PubMed Web of Science ®Google Scholar
• Sun Y, Chen W, Hao Y, et al. Stem cell-conditioned medium promotes graft remodeling of midsubstance and intratunnel incorporation after anterior cruciate ligament reconstruction in a rat model. Am J Sports Med. 2019;47(10):2327–2337. doi:10.1177/0363546519859324
   PubMed Web of Science ®Google Scholar
• Feeley BT, Liu M, Ma CB, et al. Human rotator cuff tears have an endogenous, inducible stem cell source capable of improving muscle quality and function after rotator cuff repair. Am J Sports Med. 2020;48(11):2660–2668. doi:10.1177/0363546520935855
   PubMed Web of Science ®Google Scholar
• Yang R, Deng H, Hou J, et al. Investigation of salmon calcitonin in regulating fibrosis-related molecule production and cell-substrate adhesion in frozen shoulder synovial/capsular fibroblasts. J Orthop Res. 2020;38(6):1375–1385. doi:10.1002/jor.24571
   PubMed Web of Science ®Google Scholar
• Chen W, Sun Y, Gu X, et al. Conditioned medium of mesenchymal stem cells delays osteoarthritis progression in a rat model by protecting subchondral bone, maintaining matrix homeostasis, and enhancing autophagy. J Tissue Eng Regen Med. 2019;13(9):1618–1628. doi:10.1002/term.2916
   PubMed Web of Science ®Google Scholar
• Reed M, Luissint AC, Azcutia V, et al. Epithelial CD47 is critical for mucosal repair in the murine intestine in vivo. Nat Commun. 2019;10(1):5004. doi:10.1038/s41467-019-12968-y
   PubMedGoogle Scholar
• Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest. 2007;117(3):524–529. doi:10.1172/JCI31487
   PubMed Web of Science ®Google Scholar
• Weiskirchen R, Weiskirchen S, Tacke F. Organ and tissue fibrosis: molecular signals, cellular mechanisms and translational implications. Mol Aspects Med. 2019;65:2–15. doi:10.1016/j.mam.2018.06.003
   PubMed Web of Science ®Google Scholar
• Entezari V, Lazarus M. Surgical considerations in managing osteoporosis, osteopenia, and vitamin D deficiency during arthroscopic rotator cuff repair. Orthop Clin North Am. 2019;50(2):233–243. doi:10.1016/j.ocl.2018.10.006
   PubMed Web of Science ®Google Scholar
• Feng J, Dong C, Long Y, et al. Elevated Kallikrein-binding protein in diabetes impairs wound healing through inducing macrophage M1 polarization. Cell Commun Signal. 2019;17(1):60. doi:10.1186/s12964-019-0376-9
   PubMed Web of Science ®Google Scholar
• Yin K, You Y, Swier V, et al. Vitamin D protects against atherosclerosis via regulation of cholesterol efflux and macrophage polarization in hypercholesterolemic swine. Arterioscler Thromb Vasc Biol. 2015;35(11):2432–2442. doi:10.1161/ATVBAHA.115.306132
   PubMed Web of Science ®Google Scholar
• Lee JS, Kim NY, Na SH, Youn YH, Shin CS. Reference values of neutrophil-lymphocyte ratio, lymphocyte-monocyte ratio, platelet-lymphocyte ratio, and mean platelet volume in healthy adults in South Korea. Medicine. 2018;97(26):e11138. doi:10.1097/MD.0000000000011138
   PubMed Web of Science ®Google Scholar
• Pujani M, Chauhan V, Singh K, Rastogi S, Agarwal C, Gera K. The effect and correlation of smoking with platelet indices, neutrophil lymphocyte ratio and platelet lymphocyte ratio. Hematol Transfus Cell Ther. 2020. doi:10.1016/j.htct.2020.07.006
   PubMedGoogle Scholar
• Villa-Camacho JC, Okajima S, Perez-Viloria ME, et al. In vivo kinetic evaluation of an adhesive capsulitis model in rats. J Shoulder Elbow Surg. 2015;24(11):1809–1816. doi:10.1016/j.jse.2015.06.015
   PubMed Web of Science ®Google Scholar
• Kanno A, Sano H, Itoi E. Development of a shoulder contracture model in rats. J Shoulder Elbow Surg. 2010;19(5):700–708. doi:10.1016/j.jse.2010.02.004
   PubMed Web of Science ®Google Scholar
• Yunna C, Mengru H, Lei W, Weidong C. Macrophage M1/M2 polarization. Eur J Pharmacol. 2020;877:173090. doi:10.1016/j.ejphar.2020.173090
   PubMed Web of Science ®Google Scholar
• Tang PM, Nikolic-Paterson DJ, Lan HY. Macrophages: versatile players in renal inflammation and fibrosis. Nat Rev Nephrol. 2019;15(3):144–158.
   PubMed Web of Science ®Google Scholar
• Xu HT, Lee CW, Li MY, Wang YF, Yung PS, Lee OK. The shift in macrophages polarisation after tendon injury: a systematic review. J Orthop Translat. 2020;21:24–34. doi:10.1016/j.jot.2019.11.009
   PubMed Web of Science ®Google Scholar
• Shapouri-Moghaddam A, Mohammadian S, Vazini H, et al. Macrophage plasticity, polarization, and function in health and disease. J Cell Physiol. 2018;233(9):6425–6440. doi:10.1002/jcp.26429
   PubMed Web of Science ®Google Scholar
• Hettrich CM, DiCarlo EF, Faryniarz D, Vadasdi KB, Williams R, Hannafin JA. The effect of myofibroblasts and corticosteroid injections in adhesive capsulitis. J Shoulder Elbow Surg. 2016;25(8):1274–1279. doi:10.1016/j.jse.2016.01.012
   PubMed Web of Science ®Google Scholar
• Liu F, Qiu H, Xue M, et al. MSC-secreted TGF-beta regulates lipopolysaccharide-stimulated macrophage M2-like polarization via the Akt/FoxO1 pathway. Stem Cell Res Ther. 2019;10(1):345. doi:10.1186/s13287-019-1447-y
   PubMed Web of Science ®Google Scholar
• Wang L, Li Y, Wang X, et al. GDF3 protects mice against sepsis-induced cardiac dysfunction and mortality by suppression of macrophage pro-inflammatory phenotype. Cells. 2020;9(1):120.
   PubMed Web of Science ®Google Scholar
• Bunker TD, Reilly J, Baird KS, Hamblen DL. Expression of growth factors, cytokines and matrix metalloproteinases in frozen shoulder. J Bone Joint Surg Br. 2000;82(5):768–773. doi:10.1302/0301-620X.82B5.0820768
   PubMedGoogle Scholar
• Andronic O, Ernstbrunner L, Jungel A, Wieser K, Bouaicha S. Biomarkers associated with idiopathic frozen shoulder: a systematic review. Connect Tissue Res. 2020;61(6):509–516. doi:10.1080/03008207.2019.1648445
   PubMed Web of Science ®Google Scholar
• Kim YS, Kim JM, Lee YG, Hong OK, Kwon HS, Ji JH. Intercellular adhesion molecule-1 (ICAM-1, CD54) is increased in adhesive capsulitis. J Bone Joint Surg Am. 2013;95(4):e181–188. doi:10.2106/JBJS.K.00525
   PubMedGoogle Scholar
• Park HB, Gwark JY, Kam M, Jung J. Association between fasting glucose levels and adhesive capsulitis in a normoglycemic population: a case-control study. J Shoulder Elbow Surg. 2020;29(11):2240–2247. doi:10.1016/j.jse.2020.03.017
   PubMed Web of Science ®Google Scholar
• Park HB, Gwark JY, Jung J, Jeong ST. Association between high-sensitivity C-reactive protein and idiopathic adhesive capsulitis. J Bone Joint Surg Am. 2020;102(9):761–768. doi:10.2106/JBJS.19.00759
   PubMed Web of Science ®Google Scholar
• Wijsenbeek MS, Kool M, Cottin V. Targeting interleukin-13 in idiopathic pulmonary fibrosis: from promising path to dead end. Eur Respir J. 2018;52(6):1802111. doi:10.1183/13993003.02111-2018
   PubMed Web of Science ®Google Scholar
• Wulff BC, Pappa NK, Wilgus TA. Interleukin-33 encourages scar formation in murine fetal skin wounds. Wound Repair Regen. 2019;27(1):19–28. doi:10.1111/wrr.12687
   PubMed Web of Science ®Google Scholar
• Chen HP, Wang XY, Pan XY, et al. Circulating neutrophil-derived microparticles associated with the prognosis of patients with sepsis. J Inflamm Res. 2020;13:1113–1124. doi:10.2147/JIR.S287256
   PubMed Web of Science ®Google Scholar
• Martellucci S, Orefice NS, Angelucci A, Luce A, Caraglia M, Zappavigna S. Extracellular vesicles: new endogenous shuttles for miRNAs in cancer diagnosis and therapy? Int J Mol Sci. 2020;21:18.
   Web of Science ®Google Scholar