Persicaria lanigera (Polygonaceae) leaf extract exhibits antiulcerogenic and antiproliferative activities against acetic acid-induced ulcerative colitis and cotton pellet-induced granuloma tissue in rats

Abstract

Objective: To assess the effect of leaf extract of Persicaria lanigera on cotton pellet-induced granuloma tissue formation and acetic acid-induced ulcerative colitis. Methods: Rats were randomly divided into six groups: normal control, negative control, positive control (dexamethasone or sulfasalazine) as well as Persicaria lanigera (100-600 mg/kg)-treated groups. The effects of the extracts on body weight, antioxidant, and hematological parameters, as well as mast cell proliferation, were assessed. In addition, a histological evaluation was conducted. Results: Persicaria lanigera extract significantly decreased the mean exudate amount and suppressed granuloma tissue formation in a concentration-dependent manner in rats (P<0.05). Additionally, the extract significantly increased body weight, improved hematological profile, reduced the disease activity index score and malondialdehyde level, as well as enhanced catalase and superoxide dismutase activities (P<0.05). Histological evaluation showed Persicaria lanigera extract alleviated acetic acid-induced colonic damages, as evidenced by decreased cell necrosis, edema, and inflammatory cell infiltration. Conclusions: Persicaria lanigera extract possesses antiproliferative, antioxidative, and anti-colitis activities. However, its underlying mechanisms of action need further investigation.

Keywords

Colitis / Persicaria lanigera / Antioxidant / Cotton pellets / Mast cells / Granuloma tissue formation

Conflict of interest statement

The authors declare that they have no conflict of interest.

Funding

The study received no extramural funding.

Data availability statement

The data supporting the findings of this study are available from the corresponding authors upon request.

Authors’ contributions

MAA, EO and EOA were involved in the conceptualization, design, definition of intellectual content, data acquisition, data analysis, manuscript preparation, interpretation, editing and review of the manuscript. MAA, EAA, RAA, and DA were involved in the experimental studies, literature search, collection of the plant materials, data analysis, statistical analysis, manuscript preparation, editing and review of the manuscript. MAA and AAK was involved in the execution of the ELISA work, editing and manuscript review. BA was involved in the histopathological analysis, editing and manuscript review.

Publisher’s note

The Publisher of the Journal remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

[1] Cristofori F, Dargenio VN, Dargenio C, Miniello VL, Barone M, Francavilla R. Anti-inflammatory and immunomodulatory effects of probiotics in gut inflammation: A door to the body. Front Immunol 2021; 12. doi: 10.3389/fimmu.2021.578386.

[2] Alfaro S, Acuña V, Ceriani R, Cavieres MF, Weinstein-Oppenheimer CR, Campos-Estrada C. Involvement of inflammation and its resolution in disease and therapeutics. Int J Mol Sci 2022; 23. doi: 10.3390/ijms231810719.

[3] Brusini R, Varna M, Couvreur P. Advanced nanomedicines for the treatment of inflammatory diseases. Adv Drug Deliv Rev 2020; 157: 161-178.

[4] Houglum JE, Harrelson GL, Seefeldt TM. Drugs for treating inflammation. In: Principles of pharmacology for athletic trainers. New York, USA: Routledge; 2024, p. 96-123.

[5] Obese E, Biney RP, Henneh IT, Anokwah D, Adakudugu EA, Woode E, et al. Antinociceptive effect of the hydroethanolic leaf extract of Calotropis procera (Ait) R. Br. (Apocynaceae): Possible involvement of glutamatergic, cytokines, opioidergic and adenosinergic pathways. J Ethnopharmacol 2021; 278. doi: 10.1016/j.jep.2021.114261.

[6] Santos WBDR, Guimarães JO, Pina LTS, Serafini MR, Guimarães AG. Antinociceptive effect of plant-based natural products in chemotherapy-induced peripheral neuropathies: A systematic review. Front Pharmacol 2022; 13. doi: 10.3389/fphar.2022.1001276.

[7] Obese E, Ameyaw EO, Biney RP, Henneh IT, Jackson N, Anokwah D, et al. A hydroethanolic leaf extract of Persicaria lanigera possesses antinociceptive activity through cytokine and glutamatergic pathways in vivo. Evid Based Complement Alternat Med 2021. doi: 10.1155/2021/5586789.

[8] Antwi-Adjei M, Obese E, Adakudugu EA, Henneh IT, Biney RP, Aboagye B, et al. Modulating effects of the hydroethanolic leaf extract of Persicaria lanigera R. Br. Soják (Polygonaceae) against acute inflammation. Sci World J 2023; 10(2023). doi: 10.1155/2023/5567410.

[9] Mohankumar R, Prakash SEL, Irfan N, Mohanraj S, Kumarappan C. Evaluation of analgesic, anti-inflammatory, and antipyretic activities of Ziziphus mauritania Lam leaves in animal models. Pharmacol Res 2022; 4. doi: 10.1016/j.prmcm.2022.100153.

[10] Zeng Y, Song J, Zhang M, Wang H, Zhang Y, Suo H. Comparison of in vitro and in vivo antioxidant activities of six flavonoids with similar structures. Antioxidants 2020; 9(8). https://doi.org/10.3390/antiox9080732.

[11] Yousra M, Elsherbiny NM, El-Shafey M, Said E. The interplay of the inhibitory effect of nifuroxazide on NF-κB/STAT3 signaling attenuates acetic acid-induced ulcerative colitis in rats. Environ Toxicol Pharmacol 2020; 79. doi: 10.1016/j.etap.2020.103433.

[12] Adakudugu EA, Ameyaw EO, Obese E, Biney RP, Henneh IT, Aidoo DB, et al. Protective effect of bergapten in acetic acid-induced colitis in rats. Heliyon 2020; 6(8). doi: 10.1016/j.heliyon.2020.e04710.

[13] Kimball ES, Palmer JM, D’Andrea MR, Hornby PJ, Wade PR. Acute colitis induction by oil of mustard results in later development of an IBS-like accelerated upper GI transit in mice. Am J Physiol Gastrointest Liver Physiol 2005; 288(6): G1266-G1273.

[14] Caballero-Sánchez N, Alonso-Alonso S, Nagy L. Regenerative inflammation: When immune cells help to re-build tissues. FEBS J 2024; 291: 1597-1614.

[15] Lu K, Yang CY, Yan ZH. Analgesic and anti-inflammatory activity of Cotinus coggygria Scop. extracts in vivo. Asian Pac J Trop Biomed 2024; 14(6): 225-235.

[16] Rafiyan M, Sadeghmousavi S, Akbarzadeh M, Rezaei N. Experimental animal models of chronic inflammation. Curr Res Immunol 2023; 4. doi: 10.1016/j.crimmu.2023.100063.

[17] Akhtar MA. Anti-inflammatory medicinal plants of Bangladesh-A pharmacological evaluation. Front Pharmacol 2022; 13. doi: 10.3389/fphar.2022.809324.

[18] Ahmad RM, Ibrahim OMS. Anti-inflammatory activity of clove (Syzygium aromaticum) oil extract against chronic inflammation in rat. Adv Anim Vet Sci 2024; 12(1): 77-84.

[19] Chitsaza R, Zarezadeha A, Asgarpanah J, Najafizadeha P, Mousavi Z. Rubiadin exerts an acute and chronic anti-inflammatory effect in rodents. Braz J Biol 2021; 83. doi: 10.1590/1519-6984.243775.

[20] Ashagrie G, Abebe A, Umer S. Analgesic and anti-inflammatory activities of 80% methanol extract and solvent fractions of Ehretia cymosa Thonn (Boraginaceae) leaves in rodents. J Exp Pharmacol 2023; 15: 63-79.

[21] Basavarajaiah SC, Pawar TA, Ramappa H, Setty V. Anti-arthritic and anti-inflammatory activity of ayurvedic polyherbal formulation in laboratory animals. Pharmacognosy Res 2023; 16(1): 110-117.

[22] Amoateng OE, Amoateng P, Ossei SPP, Fenteng AE, Amponsah KI, William Gilbert Ayibor GW, et al. An acute and sub-acute toxicological assessment of Reissantia indica plant extract in male Sprague-Dawley rats: Hematological, serum biochemical and histopathology. Sci African 2024; 23. doi: 10.1016/j.sciaf.2024.e02089.

[23] Okwakpam NF, Ken-Ezihuo US, Ajie P, Amadi AB. Effects of graded doses of ethanolic extract of Pausinystalia Yohimbe stem bark on biochemical and hematological indices in the kidneys of female wistar rats. Biochem Res Rev 2023; 32(4): 23-36.

[24] Miaffo D, Ankang NE, Maidadi B, Gode BA. Prophylactic effects of Combretum molle boughs on changes in the hematological, biochemical, and histological parameters in dexamethasone-induced insulin-resistant rats. Phytomed Plus 2024; 4(2). doi: 10.1016/j.phyplu.2024.100544.

[25] Riaz B, Sohn S. Neutrophils in inflammatory diseases: Unraveling the impact of their derived molecules and heterogeneity. Cells 2023; 12(22). doi: 10.3390/cells12222621.

[26] Okoben FC, Ejiofor II, Mbagwu IS, Ajaghaku DL, Anowi FC. Effects of methanolic leaf extract and fractions of Irvingia gabonensis on hematological parameters in wistar rats with splenomegaly. Sci Pharm 2024; 3(1): 9-17.

[27] Mishra NK, Panda RK, Mishra G, Rajakumar V, Kumar S, Tejonidhi K. Screening of anti-inflammatory activity and dose selection of Mollugo pentaphylla by using cotton pellet-induced granuloma in rats. Int J Pharma Life Sci 2011; 2(6): 791-796.

[28] Antwi-Adje M, Obese E, Owusu G. Cytokine Inhibition of IL-6 and TNF-α accounts for the amelioration of cotton pellet-induced tissue granuloma formation in Sprague-Dawley rats by the aqueous ethanolic stem bark extract of Bombax costatum Pellegr and Viullet (Bombacaceae). Int J Phar Pharmaceut Res 2022; 25(3): 424-436.

[29] Owusu G, Obiri DD, Ainooson GK, Osafo N, Antwi AO, Duduyemi BM, et al. Acetic acid-induced ulcerative colitis in Sprague Dawley rats is suppressed by hydroethanolic extract of Cordia vignei leaves through reduced serum levels of TNF-α and IL-6. Int J Chronic Dis 2020; 2020. doi: 10.1155/2020/8785497.

[30] Shahid M, Raish M, Ahmad A, Bin Jardan YA, Ansari MA, Ahad A, et al. Sinapic acid ameliorates acetic acid-induced ulcerative colitis in rats by suppressing inflammation, oxidative stress, and apoptosis. Molecules 2022; 27(13). doi: 10.3390/molecules27134139.

[31] Rehman NU, Ansari MN, Palla AH, Karim A, Imam F, Raish M, et al. Myrica salicifolia Hochst. ex A. Rich. suppress acetic acid-induced ulcerative colitis in rats by reducing TNF-alpha and interleukin-6, oxidative stress parameters and improving mucosal protection. Hum Exp Toxicol 2022; 41. doi: 10.1177/09603271221102518.

[32] Albalawi GA, Albalawi MZ, Alsubaie KT, Albalawi AZ, Elewa MAF, Hashem KS, et al. Curative effects of crocin in ulcerative colitis via modulating apoptosis and inflammation. Int Immunopharmacol 2023; 118. doi: 10.1016/j.intimp.2023.110138.

[33] Alsharif IA, Fayed HM, Abdel-Rahman RF, Abd-Elsalam RM, Ogaly HA. Miconazole mitigates acetic acid-induced experimental colitis in rats: Insight into inflammation, oxidative stress and Keap1/Nrf-2 signaling crosstalk. Biology (Basel) 2022; 11(2). doi: 10.3390/biology11020303.

[34] Olojo FO, Akinrinde AS, Ogundairo SA, Ubochi VC. Argania spinosa essential oil ameliorates colonic damage and extraintestinal alterations in a rat model of acetic acid-induced colitis by suppressing oxidative stress and inflammation. Adv Tradit Med 2024; 24(2): 459-474.

[35] Fokam Tagne MA, Kom B, Foyet Fondjo A, Noubissi PA, Talom Tangue B, Gaffo EF, et al. Evaluation of anticolitis and antioxidant properties of Bixa orellana (Bixaceae) leaf hydroethanolic extract on acetic acid-induced ulcerative colitis in rats. Curr Ther Res Clin Exp 2022; 97. doi: 10.1016/j.curtheres.2022.100685.

[36] Otu-Boakye SA, Yeboah KO, Boakye-Gyasi E, Oppong-Kyekyeku J, Okyere PD, Osafo N. Acetic acid-induced colitis modulating potential of total crude alkaloidal extract of Picralima nitida seeds in rats. Immun Inflamm Dis 2023; 11(5). doi: 10.1002/iid3.855.

[37] Sammari H, Jedidi S, Selmi H, Jridi M, Ayari A, Sebai H. Phytochemical properties of Crataegus azarolus berries decoction extract and evaluation of its protective activity against acetic acid-induced ulcerative colitis in rats. Dose Response 2024; 22(1). doi: 10.1177/15593258241226890.

[38] Jedidi S, Sammari H, Selmi H, Karim Hosni K, Rtibi K, Aloui F, et al. Strong protective effects of Salvia officinalis L. leaves decoction extract against acetic acid-induced ulcerative colitis and metabolic disorders in rat. J Funct Foods 2021; 79. doi: 10.1016/j.jff.2021.104406.

[39] Parisio C, Lucarini E, Micheli L, Toti A, Khatib M, Mulinacci N, et al. Pomegranate mesocarp against colitis-induced visceral pain in rats: Effects of a decoction and its fractions. Int J Mol Sci 2020; 21(12). doi: 10.3390/ijms21124304.

[40] Vona R, Pallotta L, Cappelletti M, Severi C, Matarrese P. The impact of oxidative stress in human pathology: Focus on gastrointestinal disorders. Antioxidants 2021; 10(2). doi: 10.3390/antiox10020201.

[41] Bejeshk MA, Aminizadeh AH, Rajizadeh MA, Rostamabadi F, Bagheri F, Khaksari M, et al. Ameliorating effects of Acacia arabica and Ocimum basilicum on acetic acid-induced ulcerative colitis model through mitigation of inflammation and oxidative stress. Heliyon 2023; 9(11). doi: 10.1016/j.heliyon.2023.e22355.

[42] Liu J, Han X, Zhang T, Tian K, Li Z, Luo F. Reactive oxygen species (ROS) scavenging biomaterials for anti-inflammatory diseases: from mechanism to therapy. J Hematol Oncol 2023; 16(1): 116. doi: 10.1186/s13045-023-01512-7.

[43] Jafri S, Khalid Z, Khan M, Jogezai N. Evaluation of phytochemical and antioxidant potential of various extracts from traditionally used medicinal plants of Pakistan. Open Chem 2022; 20: 1337-1356.