The impact of Sambucus nigra L. extract on inflammation, oxidative stress and tissue remodeling in a rat model of lipopolysaccharide-induced subacute rhinosinusitis.


Journal

Inflammopharmacology
ISSN: 1568-5608
Titre abrégé: Inflammopharmacology
Pays: Switzerland
ID NLM: 9112626

Informations de publication

Date de publication:
Jun 2021
Historique:
received: 05 01 2021
accepted: 22 03 2021
pubmed: 22 4 2021
medline: 15 12 2021
entrez: 21 4 2021
Statut: ppublish

Résumé

Rhinosinusitis is a common disorder related to inflammation of paranasal sinuses and nasal cavity mucosa. Herbal medicines could be an option in the treatment of rhinosinusitis due to their anti-inflammatory and anti-oxidative properties. The study aims to investigate the effect of intranasal Sambucus nigra L. subsp. nigra (SN) extract against inflammation, oxidative stress, and tissue remodeling in nasal and sinus mucosa, but also in serum, lungs, and brain, in Wistar rat model of subacute sinonasal inflammation induced by local administration of lipopolysaccharides (LPS), from Escherichia Coli. The cytokines (TNF-α, IL-1β, IL-6) and oxidative stress (malondialdehyde) in nasal mucosa, blood, lungs, and brain were analyzed. In addition, a histopathological examination was performed, and NF-kB, MMP2, MMP9, TIMP1 expressions were also evaluated in nasal mucosa. Both doses of LPS increased the production of cytokines in all the investigated tissues, especially in the nasal mucosa and blood (p < 0.01 and p < 0.05), and stimulated their secretion in the lungs, and partially in the brain. Malondialdehyde increased in all the investigated tissues (p < 0.01 and p < 0.05). In parallel, upregulation of NF-kB and MMP2 expressions with downregulation of TIMP1, particularly at high dose of LPS, was observed. SN extract reduced the local inflammatory response, maintained low levels of IL-6, TNF-α, and IL-1β. In lungs, SN reduced all cytokines levels while in the brain, the protective effect was noticed only on IL-6. Additionally, SN diminished lipid peroxidation and downregulated NF-kB in animals exposed to a low dose of LPS, with increased TIMP1 expression, while in animals treated with a high dose of LPS, SN increased NF-kB, MMP2, and MMP9 levels. In conclusion, SN extract diminished the inflammatory response, reduced generation of reactive oxygen species (ROS) and, influenced MMPs expressions, suggesting the benficial effect of SN extract on tissue remodeling in subacute rhinosinusitis and on systemic inflammatory response.

Identifiants

pubmed: 33881685
doi: 10.1007/s10787-021-00805-y
pii: 10.1007/s10787-021-00805-y
doi:

Substances chimiques

Anti-Inflammatory Agents 0
Inflammation Mediators 0
Lipopolysaccharides 0
Plant Extracts 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

753-769

Références

Ali MS, Hutton DA, Wilson JA, Pearson JP (2005) Major secretory mucin expression in chronic sinusitis. Otolaryngol Head Neck Surg 133:423–428
pubmed: 16143194
Alrumaihi F, Almatroudi A, Allemailem KS, Rahmani AH, Khan A, Khan MA (2020) Therapeutic effect of Bilsaan Sambucus nigra stem exudate, on the OVA-induced allergic asthma in mice. Oxid Med Cell Longev 2020:3620192
pubmed: 32617136 pmcid: 7313152
Al-Sayed AA, Agu RU, Massoud E (2017) Models for the study of nasal and sinus physiology in health and disease: a review of the literature. Laryngoscope Investig Otolaryngol 2:398–409
pubmed: 29299515 pmcid: 5743156
Álvarez CA, Barriga A, Albericio F, Romero MS, Guzmán F (2018) Identification of peptides in flowers of sambucus nigra with antimicrobial activity against aquaculture pathogens. Molecules 23:1033
pmcid: 6100021
Arnao MB, Cano A, Acosta M (2001) The hydrophilic and lipophilic contribution to total antioxidant activity. Food Chem 73:239–244
Baldea I, Costin GE, Shellman Y, Kechris K et al (2013) Biphasic pro-melanogenic and pro-apoptotic effects of all-trans-retinoic acid (ATRA) on human melanocytes: time-course study. J Dermatol Sci 72:168–176
pubmed: 23867358
Bartak M, Lange A, Słońska A, Cymerys J (2020) Antiviral and healing potential of Sambucus nigra extracts. Bionatura 5:1264–1670
Berger G, Kattan A, Bernheim J, Ophir D, Finkelstein Y (2000) Acute sinusitis: a histopathological and immunohistochemical study. Laryngoscope 110:2089–2094
pubmed: 11129027
Bhandari A, Takeuchi K, Suzuki S, Harada T, Hayashi S et al (2004) Increased expression of matrix metalloproteinase-2 in nasal polyps. Acta Otolaryngol 124:1165–1170
pubmed: 15768811
Biswas SK (2016) Does the interdependence between oxidative stress and inflammation explain the antioxidant paradox? Oxid Med Cell Longev. https://doi.org/10.1155/2016/5698931
doi: 10.1155/2016/5698931 pubmed: 26881031 pmcid: 4736408
Can IH, Ceylan K, Caydere M, Samim EE, Ustun H, Karasoy DS (2008) The expression of MMP-2, MMP-7, MMP-9, and TIMP-1 in chronic rhinosinusitis and nasal polyposis. Otolaryngol Head Neck Surg 139:211–215
pubmed: 18656717
Cao Y, Wu S, Zhang L, Yang Y, Cao S, Li Q (2018) Association of allergic rhinitis with obstructive sleep anea: a meta-analysis. Medicine (Baltimore) 97:e13783
Chang C, Yang M, Wen H, Cher J (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10:178–182
Chase AJ, Bond M, Crook MF, Newby AC (2002) Role of nuclear factor-kappa b activation in metalloproteinase-1, -3, and -9 secretion by human macrophages in vitro and rabbit foam cells produced in vivo. Arterioscler Thromb Vasc Biol 22:765–771
pubmed: 12006388
Ciocoiu M, Mirón A, Mares L, Tutunaru D, Pohaci C, Groza M, Badescu M (2009) The effects of Sambucus nigra polyphenols on oxidative stress and metabolic disorders in experimental diabetes mellitus. J Physiol Biochem 65:297–304
pubmed: 20119824
Conti M, Morand PC, Levillain P, Lemonnier A (1991) Improved fluorimetric determination of malondaldehyde. Clin Chem 37:1273–1275
pubmed: 1855301
Crascì L, Lauro MR, Puglisi G, Panico A (2018) Natural antioxidant polyphenols on inflammation management: anti-glycation activity vs metalloproteinases inhibition. Crit Rev Food Sci Nutr 58:893–904
pubmed: 27646710
David L, Danciu V, Moldovan B, Filip A (2019) Effects of in vitro gastrointestinal digestion on the antioxidant capacity and anthocyanin content of Cornelian cherry fruit extract. Antioxid Redox Signal 8:114
Domingues R, Zhang L, Rocchetti G, Lucini L, Pateiro M, Munekata PES, Lorenzo JM (2020) Elderberry Sambucus nigra L. as potential source of antioxidants. Characterization, optimization of extraction parameters and bioactive properties. Food Chem 330:127266
Eloy P, Poirrier AL, De Dorlodot C, Van Zele T, Watelet JB, Bertrand B (2011) Actual concepts in rhinosinusitis: a review of clinical presentations, inflammatory pathways, cytokine profiles, remodeling and management. Curr Allergy Asthma Rep 11:146–162
pubmed: 21274665 pmcid: 7089088
Enogieru AB, Haylett W, Hiss DC, Bardien S, Ekpo OE (2018) Rutin as a potent antioxidant: implications for neurodegenerative disorders. Oxid Med Cell Longev. https://doi.org/10.1155/2018/6241017
doi: 10.1155/2018/6241017 pubmed: 30050657 pmcid: 6040293
Erkan H, Aliseydi B, Keskin E, Abdullah E, Ali GM, Halis S, Zeynep S (2020) Effect of rutin on oxidative and proinflammatory damage induced by cisplatin in blood serum, ureter, bladder and urethra in rats. Biotechnol Biotechnol Equip 34:171–181
Filip A, Daicoviciu D, Clichici S, Bolfa P, Catoi C, Baldea I et al (2011) The effects of grape seeds polyphenols on SKH-1 mice skin irradiated with multiple doses of UV-B. J Photochem Photobiol B 105:133–142
pubmed: 21925895
Ganeshpurkar A, Saluja AK (2017) The pharmacological potential of rutin. Saudi Pharm J 25:149–164
pubmed: 28344465
Geng L, Wang S, Zhao Y, Hu H (2019) Gene expression profile in mouse bacterial chronic rhinosinusitis. Exp Ther Med 17:3451–3458
pubmed: 30988724 pmcid: 6447814
Giusti MM, Wrolstad RE (2001) Characterization and measurement of anthocyanins by UV-visible spectroscopy. In: Giusti MM, Wrolstad RE (eds) Current protocols in food analytical chemistry. John Wiley and Sons Inc, Hoboken, pp F1.2.1.–F1.2.13
Harokopakis E, Albzreh M, Haase E, Scannapieco F, Hajishengallis G (2006) Inhibition of proinflammatory activities of major periodontal pathogens by aqueous extracts from elder flower (Sambucus nigra). J Periodontol 77:271–279
pubmed: 16460254
Ismail C (2005) Pharmacology of sinupret. Recent results on the rational for the sinupret compound. HNO 53:S38–S42
pubmed: 15806393
Istratenco A (2019) Oxidative stress-related pathophysiology in chronic rhinosinusitis with nasal polyps: research challenges. Rom J Rhinol 9:71–77
Jung HJ, Zhang YL, Kim DK, Rhee CS, Kim DY (2019) The role of NF-κB in chronic rhinosinusitis with nasal polyps. Allergy Asthma Immunol Res 11:806–817
pubmed: 31552716 pmcid: 6761067
Khalid AN, Woodworth BA, Prince A, Quraishi SA, Antuneset MB et al (2008) Physiologic alterations in the murine model after nasal fungal antigenic exposure. Otolaryngol Head Neck Surg 139:695–701
pubmed: 18984266
Kim DH, Jeon E, Park SN, Park KH, Park YS, Yeo SW (2011) Effects of a tumor necrosis factor-α antagonist on experimentally induced rhinosinusitis. J Biomed Biotechnol. https://doi.org/10.1155/2011/360457
doi: 10.1155/2011/360457 pubmed: 22190856 pmcid: 3228682
Kim HY, Nam SY, Hong SW, Kim MJ, Jeong HJ, Kim HM (2015) Protective effects of rutin through regulation of vascular endothelial growth factor in allergic rhinitis. Am J Rhinol Allergy 29:e87-94
pubmed: 25975244
Kinoshita E, Hayashi K, Katayama H, Hayashi T, Obata A (2012) Anti-influenza virus effects of elderberry juice and its fractions. Biosci Biotechnol Biochem 76:1633–1638
pubmed: 22972323
Kittel B, Ruehl-Fehlert C, Morawietz G, Klapwijk J, Elwell MR, Lenz B et al (2004) Revised guides for organ sampling and trimming in rats and mice–Part 2: a joint publication of the RITA and NACAD groups. Exp Toxicol Pathol 55:413–431
pubmed: 15384248
Klein T, Bischoff R (2011) Physiology and pathophysiology of matrix metalloproteases. Amino Acids 41:271–290
pubmed: 20640864
Kong F (2009) Pilot clinical study on a proprietary elderberry extract: efficacy in addressing influenza symptoms. Online J Pharmacol Pharmacokin 5:32–43
Li X, Meng J, Qiao X, Liu Y, Liu F et al (2010) Expression of TGF, matrix metalloproteinases, and tissue inhibitors in Chinese chronic rhinosinusitis. J Allergy Clin Immunol 125:1061–1068
pubmed: 20392482
Lingappan K (2018) NF-kB in oxidative stress. Curr Opin Toxicol 7:81–86
pubmed: 29862377
Liu T, Zhang L, Joo D, Sun SC (2017) NF-κB signaling in inflammation. Signal Transduct Target Ther 2:17023
pubmed: 5661633 pmcid: 5661633
Lou H, Zhang N, Bachert C, Zhang L (2018) Highlights of eosinophilic chronic rhinosinusitis with nasal polyps in definition, prognosis, and advancement. Int Forum Allergy Rhinol 8:1218–1225
pubmed: 30296011 pmcid: 6282610
Magliulo G, Iannella G, Ciofalo A, Polimeni A, De Vincentiis M, Pasquariello B et al (2019) Nasal pathologies in patients with obstructive sleep apnoea. Acta Otorhinolaryngol Ital 39:250–256
pubmed: 30933181 pmcid: 6734203
Mahboubi M (2020) Sambucus nigra (black elder) as alternative treatment for cold and flu. Adv Tradit Med (ADTM). https://doi.org/10.1007/s13596-020-00469-z
doi: 10.1007/s13596-020-00469-z
Malinsky RR, Valera FCP, Cavallari FE, Küpper DS et al (2013) Matrix metalloproteinases and their impact on sinusal extension in chronic rhinosinusitis with nasal polyps. Eur Arch Oto-Rhino-L 270:1345–1348
Manicone AM, McGuire JK (2008) Matrix metalloproteinases as modulators of inflammation. Semin Cell Dev Biol 19:34–41
pubmed: 17707664
McQuibban GA, Gong JH, Wong JP, Wallace JL et al (2002) Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 100:1160–1167
pubmed: 12149192
Meltzer EO, Hamilos DL, Hadley JA et al (2004) Rhinisinusitis: establishing definition for clinical reseach and patient care. J Allergy Clin Immunol 114:155–212
pubmed: 15577865 pmcid: 7119142
Młynarczyk K, Walkowiak-Tomczak D, Łysiak GP (2018) Bioactive properties of Sambucus nigra L. as a functional ingredient for food and pharmaceutical industry. J Funct Foods 40:377–390
pubmed: 32362939
Mocan A, Vlase L, Raita O, Hanganu D, Paltinean R, Dezsi S, Gheldiu AM, Oprean R, Crisan G (2015) Comparative studies on antioxidant activity and polyphenolic content of Lycium barbarum L. and Lycium chinense Mill. leaves. Pak J Pharm Sci 28:1511–1515
pubmed: 26431651
Moldovan B, Ghic O, David L, Chisbora C (2012) The influence of storage on the total phenols content and antioxidant activity of the cranberrybush (Viburnum opulus L.) fruits extract. Rev Chim 63:463–464
Moldovan B, Popa A, David L (2016) Effects of storage temperature on the total phenolic content of Cornelian cherry (Cornus mas L.) fruits extracts. J Appl Bot Food Qual 89:208–211
Naclerio RM, Bachert C, Baraniuk JN (2010) Pathophysiology of nasal congestion. Int J Gen Med 3:47–57
pubmed: 20463823 pmcid: 2866558
Noble JE, Bailey MJ (2009) Quantitation of protein. Meth Enzymol 463:73–95
NRCS, Natural Resources Conservation Service, United States Department Of Agriculture (2016) Classification for kingdom plantae down to genus sambucus L. http://plants.usda.gov/java/ClassificationServlet?source=display&classid=SAMBU 17 Noc 2016
Oberbaum M, Levine WZ, Saffer AJ, Koren N, Sarment D (2016) Inhibition of matrix metalloproteinase activity by a transmucosal patch containing botanical compounds. Dent Oral Craniofac Res 2:349–354
Okamoto T, Akuta T, Tamura F, Van Der Vliet A, Akaike T (2004) Molecular mechanism for activation and regulation of matrix metalloproteinases during bacterial infections and respiratory inflammation. Biol Chem 385:997–1006
pubmed: 15576319
Opris R, Tatomir C, Olteanu D, Moldovan R, Moldovan B, David L et al (2017) The effect of Sambucus nigra L. extract and phytosinthesized gold nanoparticles on diabetic rats. Colloids Surf B 150:192–200
Ozgul T, Selim SE, Halil K, Ozcan C (2008) Expression of metalloproteinases MMP-2 and MMP-9 in antrochoanal polyps. Am J Rhinol Allergy 22:339–342
Passali D, Passali GC, Bellussi LM, Sarafoleanu C, Loglisci M, Iosif C, Passalli FM (2018) Bromelain’s penetration into the blood and sinonasal mucosa in patients with chronic rhinosinusitis. Acta Otorhinolaryngol Ital 38:225–228
pubmed: 29984799 pmcid: 6036946
Pop CE, Pârvu M, Arsene AL, Pârvu AE, Vodnar DC, Tarcea M, Toiu AM, Vlase L (2017) Investigation of antioxidant and antimicrobial potential of some extracts from Hedera helix L. Farmacia 65:624–629
Rehl RM, Balla AA, Cabay RJ, Hearp ML, Pytynia KB, Joe SA (2007) Mucosal remodeling in chronic rhinosinusitis. Am J Rhinol 21:651–657
pubmed: 18201442
Rogerio AP, Kanashiro A, Fontanari C, Da Silva EV et al (2007) Anti-inflammatory activity of quercetin and isoquercitrin in experimental murine allergic asthma. Inflamm Res 56:402–408
pubmed: 18026696
Sidor A, Gramza-Michałowska A (2014) Advanced research on the antioxidant and health benefit of elderberry (Sambucus nigra) in food—a review. J Funct Foods 18B:941–958
Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Meth Enzymol 299:152–178
Sobol SE, Fukakusa M, Christodoulopoulos P et al (2003) Inflammation and remodeling of the sinus mucosa in children and adults with chronic sinusitis. Laryngoscope 113:410–414
pubmed: 12616188
Suh JD, Kennedy DW (2011) Treatment options for chronic rhinosinusitis. Proc Am Thorac Soc 8:132–140
pubmed: 21364231
Toiu A, Mocan A, Vlase L, Pârvu AE, Vodnar DC, Gheldiu AM, Moldovan C, Oniga I (2019) Comparative phytochemical profile, antioxidant, antimicrobial and in vivo anti-inflammatory activity of different extracts of traditionally used Romanian Ajuga genevensis L. and A. reptans L. (Lamiaceae). Molecules 24:1597
pmcid: 6515068
Ulbricht C, Basch E, Cheung L, Goldberg H, Hammerness P, Isaac R et al (2014) An evidence-based systematic review of elderberry and elderflower (Sambucus nigra) by the natural standard research collaboration. J Diet Suppl 11:80–120
pubmed: 24409980
Uslu C, Taysi S, Bakan N (2003) Lipid peroxidation and antioxidant enzyme activity in experimental maxillary sinusitis. Ann Clin Lab Sci 33:18–22
pubmed: 12661894
Van Bruaene N, Bachert C (2011) Tissue remodeling in chronic rhinosinusitis. Curr Opin Allergy Clin Immunol 11:8–11
pubmed: 21150430
Viapiana A, Wesolowski M (2017) The Phenolic contents and antioxidant activities of infusions of Sambucus nigra L. Plant Foods Hum Nutr 72:82–87
pubmed: 28084608 pmcid: 5325840
Wang S, Zhang H, Xi Z, Huang J, Nie J, Zhou B et al (2017) Establishment of a mouse model of lipopolysaccharide-induced neutrophilic nasal polyps. Exp Ther Med 14:5275–5282
pubmed: 29285053 pmcid: 5740573
Yoruk O, Gur FO, Uyanik H, Yasar M, Mutlu V, Altas E et al (2010) Antioxidant effects of Nigella Sativa in the treatment of experimentally induced rhinosinusitis. Maced J Med Sci 3:132–137
Ziegler A, Patadia M, Stankiewicz J (2018) Neurological Complications of Acute and Chronic Sinusitis. Curr Neurol Neurosci Rep 18:5
pubmed: 29404826

Auteurs

C N Tiboc Schnell (CN)

Department of Pediatrics, "Iuliu Hatieganu" University of Medicine and Pharmacy, 400006, Cluj-Napoca, Romania.

Gabriela Adriana Filip (GA)

Department of Physiology, "Iuliu Hatieganu" University of Medicine and Pharmacy, Clinicilor Street, No. 1-3, 400006, Cluj-Napoca, Romania. adrianafilip33@yahoo.com.

N Decea (N)

Department of Physiology, "Iuliu Hatieganu" University of Medicine and Pharmacy, Clinicilor Street, No. 1-3, 400006, Cluj-Napoca, Romania.

R Moldovan (R)

Department of Physiology, "Iuliu Hatieganu" University of Medicine and Pharmacy, Clinicilor Street, No. 1-3, 400006, Cluj-Napoca, Romania.

R Opris (R)

Department of Physiology, "Iuliu Hatieganu" University of Medicine and Pharmacy, Clinicilor Street, No. 1-3, 400006, Cluj-Napoca, Romania.

S C Man (SC)

Department of Pediatrics, "Iuliu Hatieganu" University of Medicine and Pharmacy, 400006, Cluj-Napoca, Romania.

B Moldovan (B)

Faculty of Chemistry and Chemical Engineering, "Babes-Bolyai" University, 400028, Cluj-Napoca, Romania.

L David (L)

Faculty of Chemistry and Chemical Engineering, "Babes-Bolyai" University, 400028, Cluj-Napoca, Romania.

F Tabaran (F)

Department of Pathology, University of Agricultural Sciences and Veterinary Medicine, 400035, Cluj-Napoca, Romania.

D Olteanu (D)

Department of Physiology, "Iuliu Hatieganu" University of Medicine and Pharmacy, Clinicilor Street, No. 1-3, 400006, Cluj-Napoca, Romania.

A M Gheldiu (AM)

Department of Pharmaceutical Botany, Faculty of Pharmacy, Iuliu Hatieganu University of Medicine and Pharmacy, 400337, Cluj-Napoca, Romania.

I Baldea (I)

Department of Physiology, "Iuliu Hatieganu" University of Medicine and Pharmacy, Clinicilor Street, No. 1-3, 400006, Cluj-Napoca, Romania.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH