Top

Pediatric Surgery International

Published in:

01-12-2024 | Original Article

Evaluation of the protective and therapeutic effects of extra virgin olive oil rich in phenol in experimental model of neonatal necrotizing enterocolitis by clinical disease score, ınflammation, apoptosis, and oxidative stress markers

Authors: Mustafa Tuşat, Recep Eroz, Ferhan Bölükbaş, Erkan Özkan, Hüseyin Erdal

Published in: Pediatric Surgery International | Issue 1/2024

Abstract

Background and aim

Necrotizing Enterocolitis (NEC) is an inflammation-associated ischemic necrosis of the intestine. To investigate the effects of extra virgin olive oil (EVOO) on inflammation, oxidative stress, apoptosis, and histological changes in NEC-induced newborn rats.

Materials and methods

24 rats were randomly divided into three groups: control, NEC and NEC + EVOO. NEC induction was performed using hypoxia–hyperoxia, formula feeding, and cold stress. The NEC + EVOO group received 2 ml/kg EVOO with high phenolic content by gavage twice a day for 3 days. 3 cm of bowel including terminal ileum, cecum, and proximal colon was excised.

Results

Weight gain and clinical disease scores were significantly higher in the NEC + EVOO group than in the NEC group (p < 0.001). EVOO treatment caused significant decreases in IL1β, IL6 levels (p = 0.016, p = 0.029 respectively) and EGF, MDA levels (p = 0.032, p = 0.013 respectively) compared to NEC group. Significant decreases were observed in IL6 gene expression in the NEC + EVOO group compared to the NEC group (p = 0.002). In the group NEC + EVOO, the number of Caspase-3 positive cells was found to be significantly reduced (p < 0.001) and histopathological examination revealed minimal changes and significantly lower histopathological scores (p < 0.001).

Conclusion

Phenol-rich EVOO prevents intestinal damage caused by NEC by inhibiting inflammation, oxidative stress, apoptosis.

Gupta A, Paria A (2016) Etiology and medical management of NEC. Early Hum Dev 97:17–23PubMedCrossRef

Wang K, Tao G, Sylvester KG (2019) Recent advances in prevention and therapies for clinical or experimental necrotizing enterocolitis. Dig Dis Sci 64(11):3078–3085PubMedCrossRef

Afrazi A, Sodhi CP, Richardson W, Neal M, Good M, Siggers R et al (2011) New insights into the pathogenesis and treatment of necrotizing enterocolitis: Toll-like receptors and beyond. Pediatr Res 69(3):183–188PubMedPubMedCentralCrossRef

Alganabi M, Lee C, Bindi E, Li B, Pierro A (2019) Recent advances in understanding necrotizing enterocolitis. F1000Res. https://doi.org/10.1268/f1000research.17228.1CrossRefPubMedPubMedCentral

Stark AH, Madar Z (2002) Olive oil as a functional food: epidemiology and nutritional approaches. Nutr Rev 60(6):170–176PubMedCrossRef

Martinez-Gonzalez MA, Estruch R (2004) Mediterranean diet, antioxidants and cancer: the need for randomized trials. Eur J Cancer Prev 13(4):327–335PubMedCrossRef

Miles EA, Zoubouli P, Calder PC (2005) Differential anti-inflammatory effects of phenolic compounds from extra virgin olive oil identified in human whole blood cultures. Nutrition 21(3):389–394PubMedCrossRef

Cicerale S, Lucas L, Keast R (2010) Biological activities of phenolic compounds present in virgin olive oil. Int J Mol Sci 11(2):458–479PubMedPubMedCentralCrossRef

Cicerale S, Conlan XA, Sinclair AJ, Keast RS (2008) Chemistry and health of olive oil phenolics. Crit Rev Food Sci Nutr 49(3):218–236CrossRef

10.

Abd Elmaksoud HA, Motawea MH, Desoky AA, Elharrif MG, Ibrahimi A (2021) Hydroxytyrosol alleviate intestinal inflammation, oxidative stress and apoptosis resulted in ulcerative colitis. Biomed Pharmacother 142:112073CrossRef

11.

Hidalgo M, Prieto I, Abriouel H, Villarejo AB, Ramirez-Sanchez M, Cobo A et al (2018) Changes in gut microbiota linked to a reduction in systolic blood pressure in spontaneously hypertensive rats fed an extra virgin olive oil-enriched diet. Plant Foods Hum Nutr 73(1):1–6PubMedCrossRef

12.

Takashima T, Sakata Y, Iwakiri R, Shiraishi R, Oda Y, Inoue N et al (2014) Feeding with olive oil attenuates inflammation in dextran sulfate sodium-induced colitis in rat. J Nutr Biochem 25(2):186–192PubMedCrossRef

13.

Alarcon de la Lastra C, Barranco MD, Martin MJ, Herrerias J, Motilva V (2002) Extra-virgin olive oil-enriched diets reduce indomethacin-induced gastric oxidative damage in rats. Dig Dis Sci 47(12):2783–2790PubMedCrossRef

14.

Yildiz Gulhan P, Eroz R, Ataoglu O, Ince N, Davran F, Öztürk CE et al (2022) The evaluation of both the expression and serum protein levels of Caspase-3 gene in patients with different degrees of SARS-CoV2 infection. J Med Virol 94(3):897–905PubMedCrossRef

15.

Tasdemir S, Eroz R, Dogan H, Erdem HB, Sahin I, Kara M et al (2016) Association between human hair loss and the expression levels of nucleolin, nucleophosmin, and UBTF genes. Genet Test Mol Biomark 20(4):197–202CrossRef

16.

Kabaklıoğlu M, Eroz R, Kaya M (2021) May argyrophilic nucleolar organizer regions be used as a biomarker for the detection of the degree of ischemic damage instead of tunel in testicular torsion? Medicina 57(11):1177PubMedPubMedCentralCrossRef

17.

Damar İH, Eroz R (2022) Argyrophilic nucleolar organizer regions as new biomarkers in ST-Elevation myocardial infarction. Journal of Cardiovascular Development and Disease 9(2):58PubMedPubMedCentralCrossRef

18.

Kaya M, Eroz R, Kabakliogli M (2022) Expression of nucleolin, nucleophosmin, upstream binding transcription factor genes and propolis in wound models. J Wound Care 31(Sup10):S28–S40PubMedCrossRef

19.

Acat M, Yıldız Gülhan P, Eröz R, Ertınmaz Özkan A, Koca O, Çınar C (2023) Evaluation of both expression and serum protein levels of caspase-8 and mitogen-activated protein kinase 1 genes in patients with different severities of COVID-19 infection. Mol Biol Rep 50(4):3241–3248PubMedPubMedCentralCrossRef

20.

Guven A, Gundogdu G, Vurucu S, Uysal B, Oztas E, Ozturk H et al (2009) Medical ozone therapy reduces oxidative stress and intestinal damage in an experimental model of necrotizing enterocolitis in neonatal rats. J Pediatr Surg 44(9):1730–1735PubMedCrossRef

21.

Khayyat LI (2021) Extra virgin olive oil protects the testis and blood from the toxicity of paracetamol (overdose) in adult male Rats. Biol (Basel) 10(10):1042

22.

Zani A, Cordischi L, Cananzi M, De Coppi P, Smith VV, Eaton S et al (2008) Assessment of a neonatal rat model of necrotizing enterocolitis. Eur J Pediatr Surg 18(6):423–426PubMedCrossRef

23.

Martal J, Djiane J, Dubois M, Wooding P, CullingCFA BG, Allison, RT and Barr, WT (1985) Cellular pathology Techniques. Butterworths, London

24.

Caplan MS, Hedlund E, Adler L, Hsueh W (1994) Role of asphyxia and feeding in a neonatal rat model of necrotizing enterocolitis. Pediatr Pathol 14(6):1017–1028PubMedCrossRef

25.

Kromhout D, Kok FJ (2004) Atherosclerosis: epidemiological studies on the health effects of a Mediterranean diet. Eur J Nutr 43(Suppl 1):2–5

26.

Pelucchi C, Bosetti C, Negri E, Lipworth L, La Vecchia C (2011) Olive oil and cancer risk: an update of epidemiological findings through 2010. Curr Pharm Des 17(8):805–812PubMedCrossRef

27.

Fernandes J, Fialho M, Santos R, Peixoto-Placido C, Madeira T, Sousa-Santos N et al (2020) Is olive oil good for you? A systematic review and meta-analysis on anti-inflammatory benefits from regular dietary intake. Nutrition 69:110559PubMedCrossRef

28.

Romani A, Ieri F, Urciuoli S, Noce A, Marrone G, Nediani C et al (2019) Health effects of phenolic compounds found in extra-virgin olive oil, by-products, and leaf of Olea europaea L. Nutrients 11(8):1776PubMedPubMedCentralCrossRef

29.

Armutcu F, Namuslu M, Yüksel R, Kaya M (2013) Zeytinyağı ve sağlık: Biyoaktif bileşenleri, antioksidan özellikleri ve klinik etkileri. Konuralp Medical Journal 5(1):60–68

30.

Parkinson L, Cicerale S (2016) The Health Benefiting Mechanisms of Virgin Olive Oil Phenolic Compounds. Molecules 21(12):1734PubMedPubMedCentralCrossRef

31.

Servili M, Sordini B, Esposto S, Urbani S, Veneziani G, Maio ID et al (2013) Biological activities of phenolic compounds of extra virgin olive oil. Antioxidants 3(1):1–23PubMedPubMedCentralCrossRef

32.

Surmeli Onay O, Korkmaz A, Yigit S, Yurdakok M (2020) Hypoxic-ischemic enterocolitis: a proposal of a new terminology for early NEC or NEC-like disease in preterm infants, a single-center prospective observational study. Eur J Pediatr 179(4):561–570PubMedCrossRef

33.

Neu J, Walker WA (2011) Necrotizing enterocolitis. N Engl J Med 364(3):255–264PubMedPubMedCentralCrossRef

34.

Hodzic Z, Bolock AM, Good M (2017) The Role of Mucosal Immunity in the Pathogenesis of Necrotizing Enterocolitis. Front Pediatr 5:40PubMedPubMedCentralCrossRef

35.

Neu J, Pammi M (2017) Pathogenesis of NEC: impact of an altered intestinal microbiome. In: Neu J, Pammi M (eds) Seminars in Perinatology. Elsevier

36.

Caplan M (2007) Is EGF the holy grail for NEC? J Pediatr 150(4):329–330PubMedCrossRef

37.

Kim JH Neonatal necrotizing enterocolitis: Pathology and pathogenesis. Up to Date. https://medilib.ir/uptodate/show/4991 Accessed June 2023 (2019).

38.

Eaton S, Rees CM, Hall NJ (2017) Current Research on the Epidemiology, Pathogenesis, and Management of Necrotizing Enterocolitis. Neonatology 111(4):423–430PubMedCrossRef

39.

Martinínez-Domínguez E, De la Puerta R, Ruiz-Gutiérrez V (2001) Protective effects upon experimental inflammation models of a polyphenol-supplemented virgin olive oil diet. Inflamm Res 50:102–106

40.

Karaosmanoglu H, Soyer F, Ozen B, Tokatli F (2010) Antimicrobial and antioxidant activities of Turkish extra virgin olive oils. J Agric Food Chem 58(14):8238–8245PubMedCrossRef

41.

Sodhi C, Richardson W, Gribar S, Hackam DJ (2008) The development of animal models for the study of necrotizing enterocolitis. Dis Model Mech 21(2–3):94–98CrossRef

42.

Yossuck P, Kraszpulski M, Salm AK (2006) Perinatal corticosteroid effect on amygdala and hippocampus volume during brain development in the rat model. Early Hum Dev 82(4):267–272PubMedCrossRef

43.

Rosignoli P, Fuccelli R, Fabiani R, Servili M, Morozzi G (2013) Effect of olive oil phenols on the production of inflammatory mediators in freshly isolated human monocytes. J Nutr Biochem 24(8):1513–1519PubMedCrossRef

44.

Hering NA, Fromm M, Schulzke JD (2012) Determinants of colonic barrier function in inflammatory bowel disease and potential therapeutics. J Physiol 590(5):1035–1044PubMedPubMedCentralCrossRef

45.

Qi W, Shen Q, Zhang L, Han LP, Wang S (2016) Study on the inflammatory intervention of erythropoietin on NEC. Exp Ther Med 11(6):2221–2224PubMedPubMedCentralCrossRef

46.

Sanchez-Fidalgo S, Cardeno A, Sanchez-Hidalgo M, Aparicio-Soto M, de la Lastra CA (2013) Dietary extra virgin olive oil polyphenols supplementation modulates DSS-induced chronic colitis in mice. J Nutr Biochem 24(7):1401–1413PubMedCrossRef

47.

Campolo M, Di Paola R, Impellizzeri D, Crupi R, Morittu VM, Procopio A et al (2013) Effects of a polyphenol present in olive oil, oleuropein aglycone, in a murine model of intestinal ischemia/reperfusion injury. J Leukoc Biol 93(2):277–287PubMedCrossRef

48.

Wang WC, Xia YM, Yang B, Su XN, Chen JK, Li W et al (2017) Protective Effects of Tyrosol against LPS-Induced Acute Lung Injury via Inhibiting NF-kappaB and AP-1 Activation and Activating the HO-1/Nrf2 Pathways. Biol Pharm Bull 40(5):583–593PubMedCrossRef

49.

Halliwell B (1997) Antioxidants and human disease: a general introduction. Nutr Rev 55:S44–S49PubMedCrossRef

50.

Romero FJ, Bosch-Morell F, Romero MJ, Jareno EJ, Romero B, Marin N et al (1998) Lipid peroxidation products and antioxidants in human disease. Environ Health Perspect 106(Suppl 5):1229–1234PubMedPubMedCentralCrossRef

51.

Kasdallah-Grissa A, Nakbi A, Koubaa N, El-Fazaa S, Gharbi N, Kamoun A et al (2008) Dietary virgin olive oil protects against lipid peroxidation and improves antioxidant status in the liver of rats chronically exposed to ethanol. Nutr Res 28(7):472–479PubMedCrossRef

52.

Mokhtari T, Hussein Osman HE, El-Meghawry El-Kenawy A, Dashti N (2020) Ameliorative effect of virgin olive oil against nephrotoxicity following sub-chronic administration of ethephon in male rats. J Tradit Complement Med 10(5):487–495PubMedCrossRef

53.

Egan CE, Sodhi CP, Good M, Lin J, Jia H, Yamaguchi Y et al (2016) Toll-like receptor 4-mediated lymphocyte influx induces neonatal necrotizing enterocolitis. J Clin Invest 126(2):495–508PubMedCrossRef

54.

Elgebaly HA, Mosa NM, Allach M, El-Massry KF, El-Ghorab AH, Al Hroob AM et al (2018) Olive oil and leaf extract prevent fluoxetine-induced hepatotoxicity by attenuating oxidative stress, inflammation and apoptosis. Biomed Pharmacother 98:446–453PubMedCrossRef

55.

Visioli F, Galli C, Galli G, Caruso D (2002) Biological activities and metabolic fate of olive oil phenols. Eur J Lipid Sci Technol 104(9–10):677–684CrossRef

56.

Khalatbary AR, Mohammadnegad B, Goudarzi G, Fazlollahpour Balef A (2017) Immunohistochemical and electron microscopic study of the inhibitory effects of olive oil polyphenol on dexamethasone-induced apoptosis. Iran J Pathol 12(1):45–52PubMedPubMedCentralCrossRef

57.

Isani MA, Delaplain PT, Grishin A, Ford HR (2018) Evolving understanding of neonatal necrotizing enterocolitis. Curr Opin Pediatr 30(3):417–423PubMedCrossRef

58.

Warner BW, Warner BB (2005) Role of epidermal growth factor in the pathogenesis of neonatal necrotizing enterocolitis. In: Warner BW, Warner BB (eds) Seminars in Pediatric Surgery. Elsevier

59.

Khailova L, Dvorak K, Arganbright KM, Williams CS, Halpern MD, Dvorak B (2009) Changes in hepatic cell junctions structure during experimental necrotizing enterocolitis: effect of EGF treatment. Pediatr Res 66(2):140–144PubMedPubMedCentralCrossRef

60.

Millman J, Okamoto S, Kimura A, Uema T, Higa M, Yonamine M et al (2020) Metabolically and immunologically beneficial impact of extra virgin olive and flaxseed oils on composition of gut microbiota in mice. Eur J Nutr 59(6):2411–2425PubMedCrossRef

61.

Millman JF, Okamoto S, Teruya T, Uema T, Ikematsu S, Shimabukuro M et al (2021) Extra-virgin olive oil and the gut-brain axis: influence on gut microbiota, mucosal immunity, and cardiometabolic and cognitive health. Nutr Rev 79(12):1362–1374PubMedPubMedCentralCrossRef

Title: Evaluation of the protective and therapeutic effects of extra virgin olive oil rich in phenol in experimental model of neonatal necrotizing enterocolitis by clinical disease score, ınflammation, apoptosis, and oxidative stress markers
Authors: Mustafa Tuşat
Recep Eroz
Ferhan Bölükbaş
Erkan Özkan
Hüseyin Erdal
Publication date: 01-12-2024
Publisher: Springer Berlin Heidelberg
Published in: Pediatric Surgery International / Issue 1/2024
Print ISSN: 0179-0358
Electronic ISSN: 1437-9813
DOI: https://doi.org/10.1007/s00383-024-05669-1

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Evaluation of the protective and therapeutic effects of extra virgin olive oil rich in phenol in experimental model of neonatal necrotizing enterocolitis by clinical disease score, ınflammation, apoptosis, and oxidative stress markers

Abstract

Background and aim

Materials and methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background and aim

Materials and methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2024

Commentary to “Advantages of single-site laparoscopic orchiopexy for palpable undescended testes in children: a prospective comparison study”

The role of the early video-assisted thoracoscopic surgery in children with pleural empyema

Long-gap esophageal atresia: gastric transposition or esophageal lengthening with delayed primary anastomosis? A systematic review

Transanal fistula repair for the treatment of rectovestibular fistula with normal anus in female children: a 5-year single-center experience

Risk factors for and developmental relation of delayed oral nutrition in infants with congenital diaphragmatic hernia

Diagnostic and prognostic value of the gut microbiota and its metabolite butyrate in children with biliary atresia