Abstract
Postoperative peritoneal adhesion (PPA) is a serious clinical condition that affects the high percentage of patients after abdominal surgery. In this review, we have tried to focus on pathophysiology and different underlying signal pathways of adhesion formation based on recent progress in the molecular and cellular mechanisms. Also, the strategies, developed based on traditional herbal and modern medicines, to prevent and treat the PPA via regulation of the molecular mechanisms were investigated. The search engines such as Google Scholar, PubMed, Scopus, and Science Direct have been used to evaluate the current literature related to the pathogenesis of adhesion formation and novel products. Recently, different mechanisms have been defined for adhesion formation, mainly categorized in fibrin formation and adhesion fibroblast function, inflammation, and angiogenesis. Therefore, the suppression of these mechanisms via traditional and modern medicine has been suggested in several studies. While different strategies with encouraging findings have been developed, most of the studies showed contradictory results and were performed on animals. The herbal products have been introduced as safe and effective agent which can be considered in future preclinical and clinical studies. Although a wide range of therapeutics based on traditional and modern medicines have been suggested, there is no agreement in the efficacy of these methods to prevent or treat adhesion formation after surgeries. Further basic and clinical researches are still needed to propose the efficiency of recommended strategies for prevention and treatment of PPA.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acun G et al (2018) The effect of single-dose intraperitoneal bevacizumab on peritoneal adhesion formation. Revista de Investigación Clínica 70:279–284
Akhtar T, Goodchild C, Boylan M (1992) Reversal of streptokinase induced bleeding with aprotinin for emergency cardiac surgery. Anaesthesia 47:226–228
Alexander ZE, Su’a B, Hill CTG, Lyndon MP, Singh PP, Hill AG (2016) The effect of oral simvastatin on fibrinolytic activity after colorectal surgery—a pilot study. Journal of Surgical Research 205:28–32. https://doi.org/10.1016/j.jss.2016.05.037
Alkharfy KM, Kellum JA, Matzke GR (2000) Unintended immunomodulation: part II. Effects of pharmacological agents on cytokine activity. Shock (Augusta, Ga) 13:346–360. https://doi.org/10.1097/00024382-200005000-00002
Arung W, Meurisse M, Detry O (2011) Pathophysiology and prevention of postoperative peritoneal adhesions. World J Gastroenterol 17:4545–4553. https://doi.org/10.3748/wjg.v17.i41.4545
Ashaari Z, Hadjzadeh MA, Hassanzadeh G, Alizamir T, Yousefi B, Keshavarzi Z, Mokhtari T (2018a) The flavone luteolin improves central nervous system disorders by different mechanisms: a review. Journal of Molecular Neuroscience: MN 65:491–506. https://doi.org/10.1007/s12031-018-1094-2
Ashaari Z et al (2018b) Luteolin reduced the traumatic brain injury-induced memory impairments in rats: attenuating oxidative stress and dark neurons of hippocampus. Acta Medica Iranica 56:570–563
Attari F et al (2015) Curcumin as a double-edged sword for stem cells: dose, time and cell type-specific responses to curcumin. DARU Journal of Pharmaceutical Sciences 23:33
Azizzadeh M, Soltani S, Dabiri R, Azadbar H, Pahlevan D (2017) A rare case of small bowel obstruction. Koomesh:248–251
Bagheri A et al (2017) The neuroprotective effects of flaxseed oil supplementation on functional motor recovery in a model of ischemic brain stroke: upregulation of BDNF and GDNF. Acta Medica Iranica:785–792
Basbug M et al (2011, 2011) The effect of antivascular endothelial growth factor on the development of adhesion formation in laparotomized rats: experimental study. Gastroenterol Res Pract:578691–578691. https://doi.org/10.1155/2011/578691
Başoğlu M, Kiziltunç A, Akcay F, Keleş S, Gündoğdu C, Durkaya Ö (1998) Tumor necrosis factor-\alpha and interleukin-6 in peritoneal adhesion formation. Turkish Journal of Medical Sciences 28:253–258
Bayhan Z et al (2016) Antiadhesive and anti-inflammatory effects of pirfenidone in postoperative intra-abdominal adhesion in an experimental rat model. Journal of Surgical Research 201:348–355. https://doi.org/10.1016/j.jss.2015.11.033
Belluco C, Meggiolaro F, Pressato D, Pavesio A, Bigon E, Donà M, Forlin M, Nitti D, Lise M (2001) Prevention of postsurgical adhesions with an autocrosslinked hyaluronan derivative gel. J Surg Res 100:217–221. https://doi.org/10.1006/jsre.2001.6248
Beyene RT, Kavalukas SL, Barbul A (2015) Intra-abdominal adhesions: anatomy, physiology, pathophysiology, and treatment. Curr Probl Surg 52:271–319. https://doi.org/10.1067/j.cpsurg.2015.05.001
Bianchi E, Boekelheide K, Sigman M, Lamb DJ, Hall SJ, Hwang K (2016a) Ghrelin ameliorates adhesions in a postsurgical mouse model. J Surg Res 201:226–234. https://doi.org/10.1016/j.jss.2015.10.044
Bianchi E, Boekelheide K, Sigman M, Lamb DJ, Hall SJ, Hwang K (2016b) Ghrelin inhibits post-operative adhesions via blockage of the TGF-β signaling pathway. PLoS One 11:e0153968. https://doi.org/10.1371/journal.pone.0153968
Boland GM, Weigel RJ (2006) Formation and prevention of postoperative abdominal adhesions. J Surg Res 132:3–12. https://doi.org/10.1016/j.jss.2005.12.002
Braun KM, Diamond MP (2014) The biology of adhesion formation in the peritoneal cavity. Semin Pediatr Surg 23:336–343. https://doi.org/10.1053/j.sempedsurg.2014.06.004
Brochhausen C, Schmitt VH, Planck CNE, Rajab TK, Hollemann D, Tapprich C, Krämer B, Wallwiener C, Hierlemann H, Zehbe R, Planck H, Kirkpatrick CJ (2012) Current strategies and future perspectives for intraperitoneal adhesion prevention. J Gastrointest Surg 16:1256–1274. https://doi.org/10.1007/s11605-011-1819-9
Brüggmann D, Tchartchian G, Wallwiener M, Münstedt K, Tinneberg H-R, Hackethal A (2010) Intra-abdominal adhesions: definition, origin, significance in surgical practice, and treatment options. Dtsch Arztebl Int 107:769–775. https://doi.org/10.3238/arztebl.2010.0769
Buckman RF Jr, Buckman PD, Hufnagel HV, Gervin AS (1976) A physiologic basis for the adhesion-free healing of deperitonealized surfaces. J Surg Res 21:67–76. https://doi.org/10.1016/0022-4804(76)90064-0
Cahill RA, Redmond HP (2008) Cytokine orchestration in post-operative peritoneal adhesion formation. World J Gastroenterol 14:4861–4866. https://doi.org/10.3748/wjg.14.4861
Cahill RA, Wang JH, Soohkai S, Redmond HP (2006) Mast cells facilitate local VEGF release as an early event in the pathogenesis of postoperative peritoneal adhesions. Surgery 140:108–112. https://doi.org/10.1016/j.surg.2006.01.020
Cashman J, Springate C, Winternitz C (2011) Pharmaceutical compositions and methods relating to inhibiting fibrous adhesions or inflammatory disease using low sulphate fucans. Google Patents
Charboneau AJ, Delaney JP, Beilman G (2018) Fucoidans inhibit the formation of post-operative abdominal adhesions in a rat model. PLoS One 13:e0207797. https://doi.org/10.1371/journal.pone.0207797
Chegini N (2008) TGF-beta system: the principal profibrotic mediator of peritoneal adhesion formation. Semin Reprod Med 26:298–312. https://doi.org/10.1055/s-0028-1082388
Chegini N et al (2002) Differential expression of matrix metalloproteinase and tissue inhibitor of MMP in serosal tissue of intraperitoneal organs and adhesions. BJOG: An International Journal of Obstetrics and Gynaecology 109:1041–1049
Cheong Y, Shelton J, Laird S, Richmond M, Kudesia G, Li T, Ledger W (2002) IL-1, IL-6 and TNF-α concentrations in the peritoneal fluid of women with pelvic adhesions. Hum Reprod 17:69–75
Cheung JPY, Tsang HHL, Cheung JJC, Yu HHY, Leung GKK, Law WL (2009) Adjuvant therapy for the reduction of postoperative intra-abdominal adhesion formation. Asian J Surg 32:180–186. https://doi.org/10.1016/S1015-9584(09)60392-4
Chiang SC, Cheng CH, Moulton KS, Kasznica JM, Moulton SL (2000) TNP-470 inhibits intraabdominal adhesion formation. J Pediatr Surg 35:189–196. https://doi.org/10.1016/s0022-3468(00)90008-3
Choi GJ, Park HK, Kim DS, Lee D, Kang H (2018) Effect of statins on experimental postoperative adhesion: a systematic review and meta-analysis. Sci Rep 8:1–10
Chung JH, Cosenza MJ, Rahbar R, Metson RB (2002) Mitomycin C for the prevention of adhesion formation after endoscopic sinus surgery: a randomized, controlled study. Otolaryngology—Head and Neck Surgery: Official Journal of American Academy of Otolaryngology-Head and Neck Surgery 126:468–474. https://doi.org/10.1067/mhn.2002.124705
Couto L, Donato J, Nucci GD (2004) Analysis of five streptokinase formulations using the euglobulin lysis test and the plasminogen activation assay. Brazilian Journal of Medical and Biological Research 37:1889–1894
Cubukçu A, Alponat A, Gönüllü NN, Ozkan S, Erçin C (2001) An experimental study evaluating the effect of mitomycin C on the prevention of postoperative intraabdominal adhesions. J Surg Res 96:163–166. https://doi.org/10.1006/jsre.2000.6059
Deng L et al (2016) P-glycoprotein mediates postoperative peritoneal adhesion formation by enhancing phosphorylation of the chloride channel-3. Theranostics 6:204–218. https://doi.org/10.7150/thno.13907
diZerega GS (1997) Biochemical events in peritoneal tissue repair. Eur J Surg Suppl:10–16
diZerega GS, Campeau JD (2001) Peritoneal repair and post-surgical adhesion formation. Hum Reprod Update 7:547–555. https://doi.org/10.1093/humupd/7.6.547
Dunn RC, Mohler M (1993) Effect of varying days of tissue plasminogen activator therapy on the prevention of postsurgical adhesions in a rabbit model. Journal of Surgical Research 54:242–245
Duron JJ (2007) Postoperative intraperitoneal adhesion pathophysiology. Colorectal Dis 9(Suppl 2):14–24. https://doi.org/10.1111/j.1463-1318.2007.01343.x
Dusre L, Covey JM, Collins C, Sinha BK (1989) DNA damage, cytotoxicity and free radical formation by mitomycin C in human cells. Chemico-Biological Interactions 71:63–78. https://doi.org/10.1016/0009-2797(89)90090-2
Ergul E, Korukluoglu B (2008) Peritoneal adhesions: facing the enemy. Int J Surg 6:253–260. https://doi.org/10.1016/j.ijsu.2007.05.010
Ersoy E, Ozturk V, Yazgan A, Ozdogan M, Gundogdu H (2009) Comparison of the two types of bioresorbable barriers to prevent intra-abdominal adhesions in rats. J Gastrointest Surg 13:282–286. https://doi.org/10.1007/s11605-008-0678-5
Falk K, BjÖrquist P, Falk P, Hedgren M, Ivarsson ML, Lanne B, Panfilov O, Holmdahl L (2003) Antifibrinolytic proCPU is present in the peritoneal cavity during surgery. Scand J Clin Lab Invest 63:287–296
Fang CC, Yen CJ, Chen YM, Shyu RS, Tsai TJ, Lee PH, Hsieh BS (2000) Pentoxifylline inhibits human peritoneal mesothelial cell growth and collagen synthesis: effects on TGF-beta. Kidney Int 57:2626–2633. https://doi.org/10.1046/j.1523-1755.2000.00123.x
Fang C-C, Lai M-N, Chien C-T, Hung K-Y, Tsai C-C, Tsai T-J, Hsieh B-S (2003) Effects of pentoxifylline on peritoneal fibroblasts and silica-induced peritoneal fibrosis. Peritoneal Dialysis International 23:228–236
Fielding CA et al (2014) Interleukin-6 signaling drives fibrosis in unresolved inflammation. Immunity 40:40–50. https://doi.org/10.1016/j.immuni.2013.10.022
Fletcher NM, Jiang ZL, Diamond MP, Abu-Soud HM, Saed GM (2008) Hypoxia-generated superoxide induces the development of the adhesion phenotype. Free Radic Biol Med 45:530–536. https://doi.org/10.1016/j.freeradbiomed.2008.05.002
Fletcher N, Juhani A, Abusamaan M, Diamond M, Saed G (2016) Human adhesion fibroblasts are characterized by a reduction in the level of pluripotency markers as compared to normal peritoneal fibroblasts. Fertil Steril 106:e13
Gao S, Liu Z, Li H, Little PJ, Liu P, Xu S (2012) Cardiovascular actions and therapeutic potential of tanshinone IIA. Atherosclerosis 220:3–10
Ghorbani R, Mokhtari T, Khazaei M, Salahshoor M, Jalili C, Bakhtiari M (2014) The effect of walnut on the weight, blood glucose and sex hormones of diabetic male rats. Int J Morphol 32
Gorvy DA, Herrick SE, Shah M, Ferguson MWJ (2005) Experimental manipulation of transforming growth factor-beta isoforms significantly affects adhesion formation in a murine surgical model. Am J Pathol 167:1005–1019. https://doi.org/10.1016/s0002-9440(10)61190-x
Greene AK et al (2005) Prevention of intra-abdominal adhesions using the antiangiogenic COX-2 inhibitor celecoxib. Ann Surg 242:140–146. https://doi.org/10.1097/01.sla.0000167847.53159.c1
Guan R et al (2016) Emodin ameliorates bleomycin-induced pulmonary fibrosis in rats by suppressing epithelial-mesenchymal transition and fibroblast activation. Sci Rep 6:35696. https://doi.org/10.1038/srep35696
Hasdemir PS, Ozkut M, Guvenal T, Uner MA, Calik E, Koltan SO, Koyuncu FM, Ozbilgin K (2017) Effect of pirfenidone on vascular proliferation, inflammation and fibrosis in an abdominal adhesion rat model. Journal of Investigative Surgery: the Official Journal of the Academy of Surgical Research 30:26–32. https://doi.org/10.1080/08941939.2016.1215578
Hashemzaei AM, Badrooze BA, Tabrizian CK, Iranshahi DM, Shahraki EMK, Khatibani FEA, Shahraki GJ (2016) Effects of luteolin on intra peritoneal adhesion bands in rat. Journal of Fundamental and Applied Sciences 8:1–11
Haslinger B, Goedde MF, Toet KH, Kooistra T (2002) Simvastatin increases fibrinolytic activity in human peritoneal mesothelial cells independent of cholesterol lowering. Kidney Int 62:1611–1619. https://doi.org/10.1046/j.1523-1755.2002.00601.x
Haslinger B, Kleemann R, Toet KH, Kooistra T (2003) Simvastatin suppresses tissue factor expression and increases fibrinolytic activity in tumor necrosis factor-α–activated human peritoneal mesothelial cells. Kidney International 63:2065–2074. https://doi.org/10.1046/j.1523-1755.2003.t01-2-00004.x
Hau T, Payne WD, Simmons RL (1979) Fibrinolytic activity of the peritoneum during experimental peritonitis. Surg Gynecol Obstet 148:415–418
Hellebrekers BWJ, Kooistra T (2011) Pathogenesis of postoperative adhesion formation. Br J Surg 98:1503–1516. https://doi.org/10.1002/bjs.7657
Hellebrekers BWJ, Trimbos-Kemper TCM, Trimbos JBMZ, Emeis JJ, Kooistra T (2000) Use of fibrinolytic agents in the prevention of postoperative adhesion formation. Fertil Steril 74:203–212. https://doi.org/10.1016/S0015-0282(00)00656-7
Hellebrekers BWJ et al (2009) Preoperative predictors of postsurgical adhesion formation and the prevention of adhesions with plasminogen activator (PAPA-study): results of a clinical pilot study. Fertil Steril 91:1204–1214. https://doi.org/10.1016/j.fertnstert.2008.01.052
Higgins CF (1995) P-glycoprotein and cell volume-activated chloride channels. J Bioenerg Biomembr 27:63–70. https://doi.org/10.1007/bf02110332
Hills BA (1996) Lubrication of visceral movement and gastric motility by peritoneal surfactant. J Gastroenterol Hepatol 11:797–803. https://doi.org/10.1111/j.1440-1746.1996.tb00083.x
Hill-West JL, Dunn RC, Hubbell JA (1995) Local release of fibrinolytic agents for adhesion prevention. J Surg Res 59:759–763. https://doi.org/10.1006/jsre.1995.1236
Hoffmann EK, Holm NB, Lambert IH (2014) Functions of volume-sensitive and calcium-activated chloride channels. IUBMB Life 66:257–267. https://doi.org/10.1002/iub.1266
Holmadhl L, Al-Jabreen M, Xia G, Risberg B (1994) The impact of starch-powdered gloves on the formation of adhesions in rats. Eur J Surg 160:257–261
Holmdahl L, Ivarsson ML (1999) The role of cytokines, coagulation, and fibrinolysis in peritoneal tissue repair. Eur J Surg 165:1012–1019. https://doi.org/10.1080/110241599750007810
Holmdahl L, Eriksson E, Al-Jabreen M, Risberg B (1996) Fibrinolysis in human peritoneum during operation. Surgery 119:701–705. https://doi.org/10.1016/s0039-6060(96)80196-6
Holmdahl L, Kotseos K, Bergström M, Falk P, Ivarsson M-L, Chegini N (2001a) Overproduction of transforming growth factor-β1 (TGF-b1) is associated with adhesion formation and peritoneal fibrinolytic impairment. Surgery 129:626–632. https://doi.org/10.1067/msy.2001.113039
Holmdahl L, Kotseos K, Bergström M, Falk P, Ivarsson ML, Chegini N (2001b) Overproduction of transforming growth factor-beta1 (TGF-beta1) is associated with adhesion formation and peritoneal fibrinolytic impairment. Surgery 129:626–632. https://doi.org/10.1067/msy.2001.113039
Holschneider C, Cristoforoni P, Ghosh K, Punyasavatsut M, Abed E, Montz F (1997) Endogenous versus exogenous IL-10 in postoperative intraperitoneal adhesion formation in a murine model. Journal of Surgical Research 70:138–143
Honjo K et al (2017) Plasminogen activator inhibitor-1 regulates macrophage-dependent postoperative adhesion by enhancing EGF-HER1 signaling in mice. FASEB J 31:2625–2637. https://doi.org/10.1096/fj.201600871RR
Hoshino A et al (2007) Inhibition of CCL1-CCR8 interaction prevents aggregation of macrophages and development of peritoneal adhesions. J Immunol 178:5296–5304. https://doi.org/10.4049/jimmunol.178.8.5296
Hosseini A, Akhavan S, Menshaei M, Feizi A (2018) Effects of streptokinase and normal saline on the incidence of intra-abdominal adhesion 1 week and 1 month after laparotomy in rats. Adv Biomed Res 7:16. https://doi.org/10.4103/abr.abr_225_16
Ichimura A et al (2013) A small molecule inhibitor to plasminogen activator inhibitor 1 inhibits macrophage migration. Arteriosclerosis, Thrombosis, and Vascular Biology 33:935–942. https://doi.org/10.1161/atvbaha.113.301224
Ipatova AY, Koerner PH, Miller RT, Staskon F, Radi M (2019) Retrospective analysis of medication utilization and clinical outcomes in patients with idiopathic pulmonary fibrosis treated with nintedanib or pirfenidone. Clin Med Insights Circ Respir Pulm Med 13:1179548419834922. https://doi.org/10.1177/1179548419834922
Jafari-Sabet M, Shishegar A, Saeedi A-R, Ghahari S (2015) Pentoxifylline increases antiadhesion effect of streptokinase on postoperative adhesion formation: involvement of fibrinolytic pathway. Indian J Surg 77:837–842. https://doi.org/10.1007/s12262-013-1025-y
Javaherzadeh M, Shekarchizadeh A, Kafaei M, Mirafshrieh A, Mosaffa N, Sabet B (2016) Effects of intraperitoneal administration of simvastatin in prevention of postoperative intra-abdominal adhesion formation in animal model of rat. Bulletin of Emergency & Trauma 4:156
Jennings DL, Williams CT, Morgan JA (2013) Pentoxifylline for the treatment of hemolytic anemia in a patient who developed recurrent gastrointestinal bleeding while on continuous-flow left ventricular assist device support. ASAIO Journal (American Society for Artificial Internal Organs: 1992) 59:526–527. https://doi.org/10.1097/MAT.0b013e31829f0eb1
Jeong BY, Uddin MJ, Park JH, Lee JH, Lee HB, Miyata T, Ha H (2016) Novel plasminogen activator inhibitor-1 inhibitors prevent diabetic kidney injury in a mouse model. PLoS One 11:e0157012. https://doi.org/10.1371/journal.pone.0157012
Jin X, Ren S, Macarak E, Rosenbloom J (2016) Pathobiological mechanisms of peritoneal adhesions: the mesenchymal transition of rat peritoneal mesothelial cells induced by TGF-β1 and IL-6 requires activation of Erk1/2 and Smad2 linker region phosphorylation. Matrix Biology 51:55–64
Johnson KE, Wilgus TA (2014) Vascular endothelial growth factor and angiogenesis in the regulation of cutaneous wound repair. Adv Wound Care (New Rochelle) 3:647–661. https://doi.org/10.1089/wound.2013.0517
Jones JM et al (2020) Hyaluronan derived nanoparticle for simvastatin delivery: evaluation of simvastatin induced myotoxicity in tissue engineered skeletal muscle. Biomaterials Science 8:302–312
Kaidi AA, Nazzal M, Gurchumelidze T, Ali MA, Dawe EJ, Silva YJ (1995) Preoperative administration of antibodies against tumor necrosis factor-alpha (TNF-alpha) and interleukin-1 (IL-1) and their impact on peritoneal adhesion formation. Am Surg 61:569–572
Kaleli B, Ozden A, Aybek Z, Bostanci B (1998) The effect of L-arginine and pentoxifylline on postoperative adhesion formation. Acta Obstetricia et Gynecologica Scandinavica 77:377–380
Kaya T, Guvenal T, Karadas B, Cetin A, Soydan AS (2002) Effects of 5-nitro-2-(3-phenylpropylamino) benzoic acid, anthracene-9-carboxylate, and zaprinast on endothelin-1-induced contractions of pregnant rat myometrium. European Journal of Obstetrics, Gynecology, and Reproductive Biology 105:114–119. https://doi.org/10.1016/s0301-2115(02)00149-5
Khazaei M, Nematollahi-Mahani SN, Mokhtari T, Sheikhbahaei F (2018) Review on Teucrium polium biological activities and medical characteristics against different pathologic situations. J Contemp Med Sci 4
Kim S, Lee S, Greene AK, Arsenault DA, le H, Meisel J, Novak K, Flynn E, Heymach JV, Puder M (2008) Inhibition of intra-abdominal adhesion formation with the angiogenesis inhibitor sunitinib. J Surg Res 149:115–119. https://doi.org/10.1016/j.jss.2007.10.010
Kim H, Choi YH, Park SJ, Lee SY, Kim SJ, Jou I, Kook KH (2010) Antifibrotic effect of pirfenidone on orbital fibroblasts of patients with thyroid-associated ophthalmopathy by decreasing TIMP-1 and collagen levels. Investigative Ophthalmology & Visual Science 51:3061–3066. https://doi.org/10.1167/iovs.09-4257
Koca SS, Ozgen M, Sarikaya M, Dagli F, Ustundag B, Isik A (2014) Ghrelin prevents the development of dermal fibrosis in bleomycin-induced scleroderma. Clinical and Experimental Dermatology 39:176–181. https://doi.org/10.1111/ced.12195
Koninckx PR, Gomel V, Ussia A, Adamyan L (2016) Role of the peritoneal cavity in the prevention of postoperative adhesions, pain, and fatigue. Fertil Steril 106:998–1010. https://doi.org/10.1016/j.fertnstert.2016.08.012
Krielen P et al (2020) Adhesion-related readmissions after open and laparoscopic surgery: a retrospective cohort study (SCAR update). Lancet 395:33–41. https://doi.org/10.1016/S0140-6736(19)32636-4
Kucuk HF et al (2007) The role of simvastatin on postoperative peritoneal adhesion formation in an animal model. European Surgical Research Europaische chirurgische Forschung Recherches chirurgicales europeennes 39:98–102. https://doi.org/10.1159/000099156
Lai HS, Chu SY, Chen Y, Wu CH, Lin LT (1994) Effect of pentoxifylline on intraperitoneal adhesions after intestinal resection in rats. J Formos Med Assoc 93:911–915
Lai HS, Chen Y, Chang KJ, Chen WJ (1998) Tissue plasminogen activator reduces intraperitoneal adhesion after intestinal resection in rats. J Formos Med Assoc 97:323–327
Lévesque LE, Brophy JM, Zhang B (2005) The risk for myocardial infarction with cyclooxygenase-2 inhibitors: a population study of elderly adults. Annals of Internal Medicine 142:481–489. https://doi.org/10.7326/0003-4819-142-7-200504050-00113
Li NYK, Chen F, Dikkers FG, Thibeault SL (2014) Dose-dependent effect of mitomycin C on human vocal fold fibroblasts. Head Neck 36:401–410. https://doi.org/10.1002/hed.23310
Liakakos T, Thomakos N, Fine PM, Dervenis C, Young RL (2001) Peritoneal adhesions: etiology, pathophysiology, and clinical significance. Recent advances in prevention and management. Dig Surg 18:260–273. https://doi.org/10.1159/000050149
Liu B et al (2019) Effect of Bletilla striata on the prevention of postoperative peritoneal adhesions in abrasion-induced rat model. Evid Based Complement Alternat Med 2019
Lucas PA, Warejcka DJ, Young HE, Lee BY (1996) Formation of abdominal adhesions is inhibited by antibodies to transforming growth factor-β1. Journal of Surgical Research 65:135–138. https://doi.org/10.1006/jsre.1996.0355
Maciver AH, McCall M, James Shapiro AM (2011) Intra-abdominal adhesions: cellular mechanisms and strategies for prevention. International Journal of Surgery 9:589–594. https://doi.org/10.1016/j.ijsu.2011.08.008
Mais V (2014) Peritoneal adhesions after laparoscopic gastrointestinal surgery. World J Gastroenterol 20:4917–4925. https://doi.org/10.3748/wjg.v20.i17.4917
Menzies D, Ellis H (1990) Intestinal obstruction from adhesions—how big is the problem? Ann R Coll Surg Engl 72:60–63
Michailova KN, Usunoff KG (2006) Serosal membranes (pleura, pericardium, peritoneum). Normal structure, development and experimental pathology. Adv Anat Embryol Cell Biol 183:i
Molinas CR, Campo R, Elkelani OA, Binda MM, Carmeliet P, Koninckx PR (2003) Role of hypoxia inducible factors 1alpha and 2alpha in basal adhesion formation and in carbon dioxide pneumoperitoneum-enhanced adhesion formation after laparoscopic surgery in transgenic mice. Fertil Steril 80(Suppl 2):795–802. https://doi.org/10.1016/s0015-0282(03)00779-9
Molinas CR, Binda MM, Koninckx PR (2006) Angiogenic factors in peritoneal adhesion formation. Gynecological Surgery 3:157–167. https://doi.org/10.1007/s10397-006-0236-7
Moraloglu Ö, Işık H, Kılıç S, Şahin U, Çaydere M, Üstün H, Batıoglu S (2011) Effect of bevacizumab on postoperative adhesion formation in a rat uterine horn adhesion model and the correlation with vascular endothelial growth factor and Ki-67 immunopositivity. Fertil Steril 95:2638–2641
Myśliwski A, Kubasik-Juraniec J, Koszałka P, Szmit E (2004) The effect of angiogenesis inhibitor TNP-470 on the blood vessels of the lungs, kidneys and livers of treated hamsters. Folia Morphologica 63:5–9
Oshio T et al (2014) Chemokine receptor CCR8 is required for lipopolysaccharide-triggered cytokine production in mouse peritoneal macrophages. PLoS One 9:e94445. https://doi.org/10.1371/journal.pone.0094445
Ouaïssi M, Gaujoux S, Veyrie N, Denève E, Brigand C, Castel B, Duron JJ, Rault A, Slim K, Nocca D (2012) Post-operative adhesions after digestive surgery: their incidence and prevention: review of the literature. J Visc Surg 149:e104–e114. https://doi.org/10.1016/j.jviscsurg.2011.11.006
Ozbilgin K, Üner MA, Ozkut M, Hasdemir PS (2017) The effects of pirfenidone on T helper cells in prevention of intraperitoneal adhesions. The Kaohsiung Journal of Medical Sciences 33:271–276. https://doi.org/10.1016/j.kjms.2017.03.011
Pavan R, Jain S, Shraddha, Kumar A (2012) Properties and therapeutic application of bromelain: a review. Biotechnol Res Int 2012:976203. https://doi.org/10.1155/2012/976203
Pennison M, Pasche B (2007) Targeting transforming growth factor-beta signaling. Curr Opin Oncol 19:579–585. https://doi.org/10.1097/CCO.0b013e3282f0ad0e
Qin F et al (2015) Efficacy and mechanism of tanshinone IIA liquid nanoparticles in preventing experimental postoperative peritoneal adhesions in vivo and in vitro. Int J Nanomedicine 10:3699–3716. https://doi.org/10.2147/IJN.S81650
Reijnen MMPJ, Bleichrodt RP, van Goor H (2003) Pathophysiology of intra-abdominal adhesion and abscess formation, and the effect of hyaluronan. Br J Surg 90:533–541. https://doi.org/10.1002/bjs.4141
Rodrigues-Díez R et al (2014) IL-17A is a novel player in dialysis-induced peritoneal damage. Kidney International 86:303–315. https://doi.org/10.1038/ki.2014.33
Roohbakhsh Y et al (2020) Evaluation of the effects of peritoneal lavage with Rosmarinus officinalis extract against the prevention of postsurgical-induced peritoneal adhesion. Planta Med. https://doi.org/10.1055/a-1118-3918
Rout UK, Oommen K, Diamond MP (2000) Altered expressions of VEGF mRNA splice variants during progression of uterine-peritoneal adhesions in the rat. Am J Reprod Immunol 43:299–304. https://doi.org/10.1111/j.8755-8920.2000.430509.x
Rout UK, Saed GM, Diamond MP (2005) Expression pattern and regulation of genes differ between fibroblasts of adhesion and normal human peritoneum. Reprod Biol Endocrinol 3:1–1. https://doi.org/10.1186/1477-7827-3-1
Saed GM, Zhang W, Diamond MP (2001) Molecular characterization of fibroblasts isolated from human peritoneum and adhesions. Fertil Steril 75:763–768. https://doi.org/10.1016/s0015-0282(00)01799-4
Saed GM, Zhao M, Diamond MP, Abu-Soud HM (2006) Regulation of inducible nitric oxide synthase in post-operative adhesions. Hum Reprod 21:1605–1611. https://doi.org/10.1093/humrep/dei500
Sahbaz A, Aynioglu O, Isik H, Ozmen U, Cengil O, Gun BD, Gungorduk K (2015) Bromelain: a natural proteolytic for intra-abdominal adhesion prevention. International Journal of Surgery 14:7–11. https://doi.org/10.1016/j.ijsu.2014.12.024
Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S (2011) The pro-and anti-inflammatory properties of the cytokine interleukin-6. Biochimica et Biophysica Acta (BBA)-Molecular Cell Res 1813:878–888
Shavell VI, Saed GM, Diamond MP (2009) Review: cellular metabolism: contribution to postoperative adhesion development. Reprod Sci 16:627–634. https://doi.org/10.1177/1933719109332826
Shay JES, Celeste Simon M (2012) Hypoxia-inducible factors: crosstalk between inflammation and metabolism. Seminars in Cell & Developmental Biology 23:389–394. https://doi.org/10.1016/j.semcdb.2012.04.004
Smaniotto B, Biondo-Simões MLP, Artigas GV, Silva APG, Collaço LM, Ramasco GV (1997) Effect of streptokinase in the prevention of intra-abdominal adhesions in the rat. Acta Cirurgica Brasileira 12:240–245
Soleimani A, Asgharzadeh F, Rahmani F, Avan A, Mehraban S, Fakhraei M, Arjmand MH, Binabaj MM, Parizadeh MR, Ferns GA, Ryzhikov M, Afshari AR, Naghinezhad J, Sayyed-Hosseinian SH, Khazaei M, Hassanian SM (2020) Novel oral transforming growth factor-β signaling inhibitor potently inhibits postsurgical adhesion band formation. J Cell Physiol 235:1349–1357. https://doi.org/10.1002/jcp.29053
Soltani S, Foruzesh Fard M, Danaie N (2005) The effect of mitomycin and dexamethasone on peritoneal adhesion formation after abdominal surgery in rat. Koomesh 6:297–304
Strowitzki MJ et al (2017) Pharmacological HIF-inhibition attenuates postoperative adhesion formation. Sci Rep 7:13151–13151. https://doi.org/10.1038/s41598-017-13638-z
Sukhova GK, Williams JK, Libby P (2002) Statins reduce inflammation in atheroma of nonhuman primates independent of effects on serum cholesterol. Arteriosclerosis, Thrombosis, and Vascular Biology 22:1452–1458. https://doi.org/10.1161/01.atv.0000030360.72503.56
Sulaiman H, Dawson L, Laurent GJ, Bellingan GJ, Herrick SE (2002) Role of plasminogen activators in peritoneal adhesion formation. Biochem Soc Trans 30:126–131
Sun GX et al (2015) Ghrelin attenuates renal fibrosis and inflammation of obstructive nephropathy. The Journal of Urology 193:2107–2115. https://doi.org/10.1016/j.juro.2014.11.098
Tabibian N, Swehli E, Boyd A, Umbreen A, Tabibian JH (2017) Abdominal adhesions: a practical review of an often overlooked entity. Ann Med Surg (Lond) 15:9–13. https://doi.org/10.1016/j.amsu.2017.01.021
Takeda R et al (2006) Ghrelin improves renal function in mice with ischemic acute renal failure Journal of the American Society of Nephrology. JASN 17:113–121. https://doi.org/10.1681/asn.2004080626
Tarhan OR, Barut I, Sutcu R, Akdeniz Y, Akturk O (2006) Pentoxifylline, a methyl xanthine derivative, reduces peritoneal adhesions and increases peritoneal fibrinolysis in rats. The Tohoku Journal of Experimental Medicine 209:249–255. https://doi.org/10.1620/tjem.209.249
Tsai JM et al (2019) Neutrophil and monocyte kinetics play critical roles in mouse peritoneal adhesion formation. Blood Adv 3:2713–2721. https://doi.org/10.1182/bloodadvances.2018024026
Tsukada K, Katoh H, Shiojima M, Suzuki T, Takenoshita S, Nagamachi Y (1993) Concentrations of cytokines in peritoneal fluid after abdominal surgery. The European Journal of Surgery = Acta Chirurgica 159:475–479
Türkoğlu A, Gül M, Yuksel HK, Alabalik U, Ülger BV, Uslukaya O, Avci Y (2015) Effect of intraperitoneal curcumin instillation on postoperative peritoneal adhesions. Medical Principles and Practice 24:153–158
Urkan M, Özerhan İH, Ünlü A, Can MF, Öztürk E, Günal A, Yağcı G (2017) Prevention of intraabdominal adhesions: an experimental study using mitomycin-C and 4% icodextrin. Balkan Med J 34:35–40. https://doi.org/10.4274/balkanmedj.2015.1359
Uyama N et al (2019) Anti-interleukin-6 receptor antibody treatment ameliorates postoperative adhesion formation. Sci Rep 9:17558. https://doi.org/10.1038/s41598-019-54175-1
van der Wal JBC, Jeekel J (2007) Biology of the peritoneum in normal homeostasis and after surgical trauma. Colorectal Dis 9(Suppl 2):9–13. https://doi.org/10.1111/j.1463-1318.2007.01345.x
Villarroel LAH, Fernandez H, Cesin L (2017) Meloxicam decreases the formation of peritoneal adhesions in an experimental surgical model in rats. International Journal of Medical Students 5:6–13
Wang C, Li X, Meng X, Zhou J, Qin F, Hou L (2014) Prevention of experimental postoperative peritoneal adhesions through the intraperitoneal administration of tanshinone IIA. Planta Med 80:969–973
Wang Q et al (2020) Regulation and function of IL-22 in peritoneal adhesion formation after abdominal surgery. Wound Repair and Regeneration: Official Publication of the Wound Healing Society [and] the European Tissue Repair Society 28:105–117. https://doi.org/10.1111/wrr.12740
Ward BC, Panitch A (2011) Abdominal adhesions: current and novel therapies. J Surg Res 165:91–111. https://doi.org/10.1016/j.jss.2009.09.015
Wei G, Wu Y, Gao Q, Zhou C, Wang K, Shen C, Wang G, Wang K, Sun X, Li X (2017) Effect of emodin on preventing postoperative intra-abdominal adhesion formation. Oxid Med Cell Longev 2017:1740317–1740317. https://doi.org/10.1155/2017/1740317
Wei G et al (2018) Gallic acid attenuates postoperative intra-abdominal adhesion by inhibiting inflammatory reaction in a rat model. Med Sci Monit 24:827–838. https://doi.org/10.12659/MSM.908550
Witowski J, Książek K, Jörres A (2004) Interleukin-17: a mediator of inflammatory responses. Cellular and Molecular Life Sciences CMLS 61:567–579
Wu R, Dong W, Zhou M, Zhang F, Marini CP, Ravikumar TS, Wang P (2007) Ghrelin attenuates sepsis-induced acute lung injury and mortality in rats. American Journal of Respiratory and Critical Care Medicine 176:805–813. https://doi.org/10.1164/rccm.200604-511OC
Wu Y et al (2019) Danhong injection alleviates postoperative intra-abdominal adhesion in a rat model. Oxid Med Cell Longev 2019:4591384–4591384. https://doi.org/10.1155/2019/4591384
Wu F, Liu W, Feng H, Long L, Hou L, Hou C (2020) Application of traditional Chinese medicines in postoperative abdominal adhesion. Evid Based Complement Alternat Med 2020:8073467. https://doi.org/10.1155/2020/8073467
Xu X-F et al (2018) Respective roles of the mitogen-activated protein kinase (MAPK) family members in pancreatic stellate cell activation induced by transforming growth factor-β1 (TGF-β1). Biochem Biophys Res Commun 501:365–373. https://doi.org/10.1016/j.bbrc.2018.04.176
Yagmurlu A, Barlas M, Gursel I, Gokcora I (2003) Reduction of surgery-induced peritoneal adhesions by continuous release of streptokinase from a drug delivery system. European Surgical Research 35:46–49
Yan S, Yue Y, Zeng L, Jiang C, Li W, Li H, Qian Y (2019) Ligustrazine nanoparticles nano spray's activation on Nrf2/ARE pathway in oxidative stress injury in rats with postoperative abdominal adhesion. Ann Transl Med 7:379–379. https://doi.org/10.21037/atm.2019.07.72
Yang Y-L et al (2018) Pentoxifylline decreases post-operative intra-abdominal adhesion formation in an animal model. PeerJ 6:e5434
Yao L, Liu F, Hong L, Sun L, Liang S, Wu K, Fan D (2011) The function and mechanism of COX-2 in angiogenesis of gastric cancer cells. J Exp Clin Cancer Res 30:13–13. https://doi.org/10.1186/1756-9966-30-13
Yildiz MK et al (2014) Effect of orally administered simvastatin on prevention of postoperative adhesion in rats. Int J Clin Exp Med 7:405–410
Zarghi A, Arfaei S (2011) Selective COX-2 inhibitors: a review of their structure-activity relationships. Iran J Pharm Res 10:655–683
Zhang Z, Ni J, Chen L, Yu L, Xu J, Ding J (2012) Encapsulation of cell-adhesive RGD peptides into a polymeric physical hydrogel to prevent postoperative tissue adhesion. J Biomed Mater Res B Appl Biomater 100:1599–1609. https://doi.org/10.1002/jbm.b.32728
Zhang H, Song Y, Li Z, Zhang T, Zeng L (2016) Evaluation of breviscapine on prevention of experimentally induced abdominal adhesions in rats. The American Journal of Surgery 211:1143–1152. https://doi.org/10.1016/j.amjsurg.2015.05.037
Zhao M et al (2019) HuoXueTongFu formula alleviates intraperitoneal adhesion by regulating macrophage polarization and the SOCS/JAK2/STAT/PPAR-γ signalling pathway mediators. Inflamm 2019:1769374–1769374. https://doi.org/10.1155/2019/1769374
Zhong J et al (2020) NPPB prevents postoperative peritoneal adhesion formation by blocking volume-activated Cl(−) current. Naunyn Schmiedebergs Arch Pharmacol 393:501–510. https://doi.org/10.1007/s00210-019-01740-0
Zhou YF, Mori T, Kudo H, Asakai R, Sassa S, Sakamoto S (2003) Effects of angiogenesis inhibitor TNP-470 on the development of uterine adenomyosis in mice. Fertil Steril 80(Suppl 2):788–794. https://doi.org/10.1016/s0015-0282(03)00988-9
Author information
Authors and Affiliations
Contributions
SS conceived and designed research. SS wrote the manuscript. SS read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The author declares that she has no conflict of interest.
Ethical approval
None.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Soltany, S. Postoperative peritoneal adhesion: an update on physiopathology and novel traditional herbal and modern medical therapeutics. Naunyn-Schmiedeberg's Arch Pharmacol 394, 317–336 (2021). https://doi.org/10.1007/s00210-020-01961-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00210-020-01961-8