The effects of spirulina supplementation on serum iron and ferritin, anemia parameters, and fecal occult blood in adults with ulcerative colitis: A randomized, double-blinded, placebo-controlled trial

Clinical Nutrition ESPEN - Tập 57 - Trang 755-763 - 2023
Sajjad Moradi1, Sahar Foshati2, Fariborz Poorbaferani3, Sepide Talebi4,5, Reza Bagheri6, Parsa Amirian7, Fatemeh Parvizi8, Michael Nordvall9, Alexei Wong9, Mehdi Zobeiri8
1Nutritional Sciences Department, School of Nutritional Sciences and Food Technology, Kermanshah University of Medical Sciences, Kermanshah, Iran
2Department of Clinical Nutrition, School of Nutrition and Food Sciences, Shiraz University of Medical Sciences, Shiraz, Iran
3Department of Clinical Nutrition, School of Nutrition and Food Science, Isfahan University of Medical Sciences, Isfahan, Iran
4Department of Clinical Nutrition, School of Nutritional Science, Tehran University of Medical Science, Tehran, Iran
5Students' Scientific Research Center (SSRC), Tehran University of Medical Sciences, Tehran, Iran
6Department of Exercise Physiology, University of Isfahan, Isfahan 8174673441, Iran
7General Practitioner, Kermanshah University of Medical Sciences (KUMS), Kermanshah, Iran
8Department of Internal Medicine, School of Medicine, Kermanshah University of Medical Sciences, Iran
9Marymount University, School of Health Sciences, Department of Health and Human Performance, Arlington, VA, USA

Tài liệu tham khảo

Santiago, 2022, Incidence trends of inflammatory bowel disease in a southern European country: a mirror of the western world?, Clin Transl Gastroenterol, 13, 10.14309/ctg.0000000000000481 Yangyang, 2017, Clinical presentation of Crohn's, ulcerative colitis, and indeterminate colitis: symptoms, extraintestinal manifestations, and disease phenotypes, 349 Ishihara, 2019, Irritable bowel syndrome-like symptoms in ulcerative colitis patients in clinical remission: association with residual colonic inflammation, Digestion, 99, 46, 10.1159/000494412 Chaubal, 2017, Anemia in patients with ulcerative colitis in remission: a study from western India, Indian J Gastroenterol, 36, 361, 10.1007/s12664-017-0791-z Khan, 2017, A novel model for predicting incident moderate to severe anemia and iron deficiency in patients with newly diagnosed ulcerative colitis, Dig Dis Sci, 62, 1295, 10.1007/s10620-017-4512-3 Bertani, 2021, Oral sucrosomial iron is as effective as intravenous ferric carboxy-maltose in treating anemia in patients with ulcerative colitis, Nutrients, 13, 608, 10.3390/nu13020608 Lamb, 2019, British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults, Gut, 68, s1, 10.1136/gutjnl-2019-318484 Nikkhah-Bodaghi, 2019, The effects of Nigella sativa on quality of life, disease activity index, and some of inflammatory and oxidative stress factors in patients with ulcerative colitis, Phytother Res, 33, 1027, 10.1002/ptr.6296 Rastegarpanah, 2015, A randomized, double blinded, placebo-controlled clinical trial of silymarin in ulcerative colitis, Chin J Integr Med, 21, 902, 10.1007/s11655-012-1026-x Nikkhah-Bodaghi, 2019, Zingiber officinale and oxidative stress in patients with ulcerative colitis: a randomized, placebo-controlled, clinical trial, Compl Ther Med, 43, 1, 10.1016/j.ctim.2018.12.021 Sadeghi, 2020, The effect of curcumin supplementation on clinical outcomes and inflammatory markers in patients with ulcerative colitis, Phytother Res, 34, 1123, 10.1002/ptr.6581 Samsamikor, 2016, Resveratrol supplementation and oxidative/anti-oxidative status in patients with ulcerative colitis: a randomized, double-blind, placebo-controlled pilot study, Arch Med Res, 47, 304, 10.1016/j.arcmed.2016.07.003 Amiri, 2019, Efficacy and safety of a standardized extract from Achillea wilhelmsii C. Koch in patients with ulcerative colitis: a randomized double blind placebo-controlled clinical trial, Compl Ther Med, 45, 262, 10.1016/j.ctim.2019.05.001 Gentscheva, 2023, 13, 845 Suliburska, 2016, Effect of Spirulina maxima supplementation on calcium, magnesium, iron, and zinc status in obese patients with treated hypertension, Biol Trace Elem Res, 173, 1, 10.1007/s12011-016-0623-5 Moradi, 2019, Effects of Spirulina supplementation on obesity: a systematic review and meta-analysis of randomized clinical trials, Compl Ther Med, 47, 10.1016/j.ctim.2019.102211 Bortolini, 2022, Functional properties of bioactive compounds from Spirulina spp.: current status and future trends, Food Chem: Mol Sci, 5 Wu, 2016, The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: an overview, Arch Toxicol, 90, 1817, 10.1007/s00204-016-1744-5 Bobescu, 2020, Are there any beneficial effects of spirulina supplementation for metabolic syndrome components in postmenopausal women?, Mar Drugs, 18, 651, 10.3390/md18120651 Neyrinck, 2017, Spirulina protects against hepatic inflammation in aging: an effect related to the modulation of the gut microbiota?, Nutrients, 9, 633, 10.3390/nu9060633 Moradi, 2021, Int J Clin Pract Kusmardi, 2017, Combination of sambiloto (Andrographis paniculata (Burm. F.) nees) extract and spirulina (Arthrospira platensis gomont) to prevent anemia in mice infected with Plasmodium berghei anka, Asian J Pharmaceut Clin Res, 10, 269, 10.22159/ajpcr.2017.v10i12.21231 Selmi, 2011, The effects of Spirulina on anemia and immune function in senior citizens, Cell Mol Immunol, 8, 248, 10.1038/cmi.2010.76 Emami, 2017, Effects of dietary supplementing of Spirulina platensis and Chlorella vulgaris microalgae on hematologic parameters in streptozotocin-induced diabetic rats, Iran J Ped Hemat Oncol, 7, 163 Simsek, 2009, Spirulina platensis feeding inhibited the anemia-and leucopenia-induced lead and cadmium in rats, J Hazard Mater, 164, 1304, 10.1016/j.jhazmat.2008.09.041 Marlina, 2020, The effectiveness of spirulina compared with iron supplement on anemia among pregnant women in Indonesia, Int J Caring Sci, 13, 1783 Niang, 2017, Spirulina supplementation in pregnant women in the Dakar region (Senegal), Open J Obstet Gynecol, 7, 147, 10.4236/ojog.2017.71016 Jowett, 2003, Defining relapse of ulcerative colitis using a symptom-based activity index, Scand J Gastroenterol, 38, 164, 10.1080/00365520310000654 Zeinalian, 2017, The effects of Spirulina Platensis on anthropometric indices, appetite, lipid profile and serum vascular endothelial growth factor (VEGF) in obese individuals: a randomized double blinded placebo controlled trial, BMC Compl Alternative Med, 17, 1 Mazokopakis, 2014, The hepatoprotective and hypolipidemic effects of Spirulina (Arthrospira platensis) supplementation in a Cretan population with non-alcoholic fatty liver disease: a prospective pilot study, Ann Gastroenterol: Quart Pub Hell Soci Gastroenterol, 27, 387 Rezaei, 2018, The protective effects of honey and spirulina platensis on acetic acid-induced ulcerative colitis in rats, Iran Red Crescent Med J, 20, 8, 10.5812/ircmj.62517 Dai, 2017, Effects of Jianpi Qingchang decoction on the quality of life of patients with ulcerative colitis: A randomized controlled trial, Medicine (Baltimore), 96, e6651, 10.1097/MD.0000000000006651 Naganuma, 2018, Efficacy of indigo naturalis in a multicenter randomized controlled trial of patients with ulcerative colitis, Gastroenterology, 154, 935, 10.1053/j.gastro.2017.11.024 Langmead, 2004, Randomized, double-blind, placebo-controlled trial of oral aloe vera gel for active ulcerative colitis, Aliment Pharmacol Therapeut, 19, 739, 10.1111/j.1365-2036.2004.01902.x Kamali, 2015, Efficacy of the Punica granatum peels aqueous extract for symptom management in ulcerative colitis patients. A randomized, placebo-controlled, clinical trial, Compl Ther Clin Pract, 21, 141, 10.1016/j.ctcp.2015.03.001 Committee, 2005 Wassertheil-Smoller, 2010, Statistical analysis of clinical trials, Semin Nucl Med, 40, 357, 10.1053/j.semnuclmed.2010.04.001 Wells, 2006, Effects of changes in hemoglobin level on quality of life and cognitive function in inflammatory bowel disease patients, Inflamm Bowel Dis, 12, 123, 10.1097/01.MIB.0000196646.64615.db Vegh, 2016, Association of extraintestinal manifestations and anaemia with disease outcomes in patients with inflammatory bowel disease, Scand J Gastroenterol, 51, 848, 10.3109/00365521.2016.1140807 Cucino, 2001, Cause of death in patients with inflammatory bowel disease, Inflamm Bowel Dis, 7, 250, 10.1097/00054725-200108000-00011 Guagnozzi, 2014, Anemia in inflammatory bowel disease: a neglected issue with relevant effects, World J Gastroenterol: WJG, 20, 3542, 10.3748/wjg.v20.i13.3542 Rr, 2015, Spirulina in combating protein energy malnutrition (PEM) and protein energy wasting (PEW)-A review, J Nutr Res, 3, 62 Nasirian, 2017, The effects of oral supplementation of spirulina platensis microalgae on hematological parameters in streptozotocin-induced diabetic rats, Am J Tourism Res, 9, 5238 Liu, 2002, Effect of spirulina platensis polysaccharide on hematopoietic recovery and related cytokines in mice with transplanted tumor treated by chemotherapy, Chin J Integr Tradit West Med, 8, 130, 10.1007/BF02934440 Ge, 2019, The efficacy of dietary Spirulina as an adjunct to chemotherapy to improve immune function and reduce myelosuppression in patients with malignant tumors, Transl Cancer Res, 8, 1065, 10.21037/tcr.2019.06.13 Anvar, 2021, Bioactive properties of spirulina: A review, Microb Bioact, 4, 134, 10.25163/microbbioacts.412117B0719110521 Kougia, 2023, Iron (Fe) biofortification of Arthrospira platensis: Effects on growth, biochemical composition and in vitro iron bioaccessibility, Algal Res, 70, 10.1016/j.algal.2023.103016 Chaouachi, 2023, A Review of the Health-Promoting Properties of Spirulina with a Focus on athletes’ Performance and Recovery, J Diet Suppl, 1 Liestianty, 2019, Nutritional analysis of spirulina sp to promote as superfood candidate García-Casal, 2000, β-carotene and inhibitors of iron absorption modify iron uptake by Caco-2 cells, J Nutr, 130, 5 Gao, 2019, Effect of microalgae as iron supplements on iron-deficiency anemia in rats, Food Funct, 10, 723, 10.1039/C8FO01834K Leal-Esteban, 2021, Spirulina supplementation: A double-blind, randomized, comparative study in young anemic Indian women, Clin Epid Glob Heal, 12 Kumar, 2023, Arthrospira platensis (Spirulina) fortified functional foods ameliorate iron and protein malnutrition by improving growth and modulating oxidative stress and gut microbiota in rats, Food Funct, 14, 1160, 10.1039/D2FO02226E Kapoor, 1998, Supplementary effect of spirulina on hematological status of rats during pregnancy and lactation, Plant Foods Hum Nutr, 52, 315, 10.1023/A:1008027408919 Madhubalaji, 2019, Improvement of vitamin B12 status with Spirulina supplementation in Wistar rats validated through functional and circulatory markers, J Food Biochem, 43 Abed, 2016, Impact of spirulina on nutritional status, haematological profile and anaemia status in malnourished children in the Gaza Strip: randomized clinical trial, Matern Pediatr Nutr, 110, 2 Batool, 2022, Comparative Effects of Spirulina with Iron Supplemented Sangobion Capsules among Anemic Females in Hafizabad, Pak J Med Heal Sci, 16, 957 Visiedo-García, 2020, Iron Metabolism in Obesity and Metabolic Syndrome, Int J Mol Sci, 21, 5529, 10.3390/ijms21155529 Nemeth, 2021, Hepcidin-Ferroportin Interaction Controls Systemic Iron Homeostasis, Int J Mol Sci, 22, 10.3390/ijms22126493 Bissinger, 2019, Oxidative stress, eryptosis and anemia: a pivotal mechanistic nexus in systemic diseases, The FEBS journal, 286, 826, 10.1111/febs.14606 Piovan, 2021, Pre-and early post-treatment with Arthrospira platensis (Spirulina) extract impedes lipopolysaccharide-triggered neuroinflammation in microglia, Front Pharmacol, 2426 Mohammadi, 2022, Spirulina platensis protein hydrolysates: Techno-functional, nutritional and antioxidant properties, Algal Res, 65, 10.1016/j.algal.2022.102739 Hu, 2019, Reactive oxygen species and Nrf2: functional and transcriptional regulators of hematopoiesis, Oxid Med Cell Longev, 2019, 10.1155/2019/5153268 Mahdavi, 2022, The effect of the Dietary Approaches to Stop Hypertension (DASH) diet on body composition, complete blood count, prothrombin time, inflammation and liver function in haemophilic adolescents, Br J Nutr, 128, 1771, 10.1017/S0007114521004839 Cheng-Wu Z. Effects of polysaccharide and phycocyanin from spirulina on peripheral blood and hematopoietic system of bone marrow in mice. in Proc. Of 2nd asia pacific conf. On algal biotech Garland Publishers, NY1994. Othoo, 2021, Impact of Spirulina corn soy blend on Iron deficient children aged 6–23 months in Ndhiwa Sub-County Kenya: a randomized controlled trial, BMC nutr, 7, 1, 10.1186/s40795-021-00472-w Fitriningsih, 2021, The effect of consuming seaweed capsules of Spirulina on hemoglobin levels of pregnant women at Batua Public health Center of Makassar, Enfermeria Clinica, 31, S697, 10.1016/j.enfcli.2021.07.019 Barennes, 2022, Spirulina as a daily nutritional supplement of young pre-school Cambodian children of deprived settings: a single-blinded, placebo-controlled, cross-over trial, BMC Pediatr, 22, 1, 10.1186/s12887-022-03766-5 Thaakur, 2007, Influence of spirulina on the phenytoin induced haematological changes, Ancient Sci Life, 26, 9 Abdel-Daim, 2018, Antagonistic effects of Spirulina platensis on diazinon-induced hemato-biochemical alterations and oxidative stress in rats, Environ Sci Pollut Control Ser, 25, 27463, 10.1007/s11356-018-2761-0 Gargouri, 2019, Potential protective effects of the edible alga Arthrospira platensis against lead-induced oxidative stress, anemia, kidney injury, and histopathological changes in adult rats, Appl Physiol Nutr Metabol, 44, 271, 10.1139/apnm-2018-0428 Gargouri, 2020, Protective effects of spirulina against hemato-biochemical alterations, nephrotoxicity, and DNA damage upon lead exposition, Hum Exp Toxicol, 39, 855, 10.1177/0960327120903490 Sachdeva, 2004, Effect of supplementation of Spirulina on the haematological profile and intellectual status of school girls (7-9 years), J Hum Ecol, 15, 105 Kaur, 2009, Effect of spirulina supplementation on the nutrient adequacy and health status of non-insulin-dependent diabetes mellitus (NIDDM) male subjects, Stud Ethno-Med, 3, 119, 10.1080/09735070.2009.11886348 Matondo, 2016, Spirulina supplements improved the nutritional status of undernourished children quickly and significantly: experience from Kisantu, the Democratic Republic of the Congo, Int J Pediatr, 2016, 10.1155/2016/1296414 Patel, 2018, Management of anemia in patients with inflammatory bowel disease (IBD), Curr Treat Options Gastroenterol, 16, 112, 10.1007/s11938-018-0174-2 Morsy, 2019, Protective effect of Spirulina platensis extract against dextran-sulfate-sodium-induced ulcerative colitis in rats, Nutrients, 11, 2309, 10.3390/nu11102309 Wang, 2022, Spirulina platensis aqueous extracts ameliorate colonic mucosal damage and modulate gut microbiota disorder in mice with ulcerative colitis by inhibiting inflammation and oxidative stress, J Zhejiang Univ - Sci B, 23, 481, 10.1631/jzus.B2100988 Abdel-Daim, 2015, Anti-inflammatory and immunomodulatory effects of Spirulina platensis in comparison to Dunaliella salina in acetic acid-induced rat experimental colitis, Immunopharmacol Immunotoxicol, 37, 126, 10.3109/08923973.2014.998368 Borges, 2018, Fecal occult blood: a comparison of chemical and immunochemical tests, Arq Gastroenterol, 55, 128, 10.1590/s0004-2803.201800000-22