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Source and amount of carbohydrate in the diet and inflammation in women with polycystic ovary syndrome

  • Luigi Barrea (a1), Paolo Marzullo (a2), Giovanna Muscogiuri (a1), Carolina Di Somma (a3), Massimo Scacchi (a4), Francesco Orio (a5), Gianluca Aimaretti (a6), Annamaria Colao (a1) and Silvia Savastano (a1)...

Abstract

High carbohydrate intake and low-grade inflammation cooperate with insulin resistance and hyperandrogenism to constitute an interactive continuum acting on the pathophysiology of polycystic ovary syndrome (PCOS), the most common endocrine disorder in women of reproductive age characterised by oligo-anovulatory infertility and cardiometabolic disorders. The role of insulin in PCOS is pivotal both in regulating the activity of ovarian and liver enzymes, respectively involved in androgen production and in triggering low-grade inflammation usually reported to be associated with an insulin resistance, dyslipidaemia and cardiometabolic diseases. Although an acute hyperglycaemia induced by oral glucose loading may increase inflammation and oxidative stress by generating reactive oxygen species through different mechanisms, the postprandial glucose increment, commonly associated with the Western diet, represents the major contributor of chronic sustained hyperglycaemia and pro-inflammatory state. Together with hyperinsulinaemia, hyperandrogenism and low-grade inflammation, unhealthy diet should be viewed as a key component of the ‘deadly quartet’ of metabolic risk factors associated with PCOS pathophysiology. The identification of a tight diet–inflammation–health association makes the adoption of healthy nutritional approaches a primary preventive and therapeutic tool in women with PCOS, weakening insulin resistance and eventually promoting improvements of reproductive life and endocrine outcomes. The intriguing nutritional–endocrine connections operating in PCOS underline the role of expert nutritionists in the management of this syndrome. The aim of the present review is to provide an at-a-glance overview of the possible bi-directional mechanisms linking inflammation, androgen excess and carbohydrate intake in women with PCOS.

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Corresponding author

*Corresponding author: Dr Luigi Barrea, email luigi.barrea@unina.it

References

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1. Goodarzi, MO & Azziz, R (2006) Diagnosis, epidemiology, and genetics of the polycystic ovary syndrome. Best Pract Res Clin Endocrinol Metab 20, 193205.
2. Dunaif, A (1997) Insulin resistance and the polycystic ovary syndrome: mechanism and implications for pathogenesis. Endocr Rev 18, 774800.
3. Plymate, SR, Matej, LA, Jones, RE, et al. (1988) Inhibition of sex hormone-binding globulin production in the human hepatoma (Hep G2) cell line by insulin and prolactin. J Clin Endocrinol Metab 67, 460464.
4. Nestler, JE, Jakubowicz, DJ, de Vargas, AF, et al. (1998) Insulin stimulates testosterone biosynthesis by human thecal cells from women with polycystic ovary syndrome by activating its own receptor and using inositolglycan mediators as the signal transduction system. J Clin Endocrinol Metab 83, 20012005.
5. Altieri, P, Cavazza, C, Pasqui, F, et al. (2013) Dietary habits and their relationship with hormones and metabolism in overweight and obese women with polycystic ovary syndrome. Clin Endocrinol (Oxf) 78, 5259.
6. Di Sarra, D, Tosi, F, Bonin, C, et al. (2013) Metabolic inflexibility is a feature of women with polycystic ovary syndrome and is associated with both insulin resistance and hyperandrogenism. J Clin Endocrinol Metab 98, 25812588.
7. O’Reilly, MW, Taylor, AE, Crabtree, NJ, et al. (2014) Hyperandrogenemia predicts metabolic phenotype in polycystic ovary syndrome: the utility of serum androstenedione. J Clin Endocrinol Metab 99, 10271036.
8. Glueck, CJ, Dharashivkar, S, Wang, P, et al. (2005) Obesity and extreme obesity, manifest by ages 20–24 years, continuing through 32–41 years in women, should alert physicians to the diagnostic likelihood of polycystic ovary syndrome as a reversible underlying endocrinopathy. Eur J Obstet Gynecol Reprod Biol 122, 206212.
9. Wong, BW, Meredith, A, Lin, D, et al. (2012) The biological role of inflammation in atherosclerosis. Can J Cardiol 28, 631634.
10. Escobar-Morreale, HF, Luque-Ramírez, M & González, F (2011) Circulating inflammatory markers in polycystic ovary syndrome: a systematic review and metaanalysis. Fertil Steril 95, 10481058.
11. Minihane, AM, Vinoy, S, Russell, WR, et al. (2015) Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr 114, 9991012.
12. Shivappa, N, Hebert, JR, Marcos, A, et al. (2017) Association between dietary inflammatory index and inflammatory markers in the HELENA study. Mol Nutr Food Res 61, 10.1002/mnfr.201600707.
13. Nasef, NA, Mehta, S & Ferguson, LR (2017) Susceptibility to chronic inflammation: an update. Arch Toxicol 91, 11311141.
14. Neale, EP, Batterham, MJ & Tapsell, LC (2016) Consumption of a healthy dietary pattern results in significant reductions in C-reactive protein levels in adults: a meta-analysis. Nutr Res 36, 391401.
15. Hotamisligil, GS (2006) Inflammation and metabolic disorders. Nature 444, 860867.
16. Chawla, A, Nguyen, KD & Goh, YP (2011) Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol 11, 738749.
17. Galland, L (2010) Diet and inflammation. Nutr Clin Pract 25, 634640.
18. Aravindhan, V & Madhumitha, H (2016) Metainflammation in diabetic coronary artery disease: emerging role of innate and adaptive immune responses. J Diabetes Res 2016, 6264149.
19. Shah, MS & Brownlee, M (2016) Molecular and cellular mechanisms of cardiovascular disorders in diabetes. Circ Res 118, 18081829.
20. Calder, PC, Yaqoob, P, Thies, F, et al. (2002) Fatty acids and lymphocyte functions. Br J Nutr 87, Suppl. 1, S31S48.
21. Calder, PC, Ahluwalia, N, Brouns, F, et al. (2011) Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr 106, Suppl. 3, S5S78.
22. Paniagua, JA (2016) Nutrition, insulin resistance and dysfunctional adipose tissue determine the different components of metabolic syndrome. World J Diabetes 7, 483514.
23. Cousin, B, Munoz, O, Andre, M, et al. (1999) A role for preadipocytes as macrophage-like cells. FASEB J 13, 305312.
24. Charrière, G, Cousin, B, Arnaud, E, et al. (2003) Preadipocyte conversion to macrophage. Evidence of plasticity. J Biol Chem 278, 98509855.
25. Skurk, T, Alberti-Huber, C, Herder, C, et al. (2007) Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 92, 10231033.
26. Nishimura, S, Manabe, I, Nagasaki, M, et al. (2009) CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15, 914920.
27. Hill, AA, Reid Bolus, W & Hasty, AH (2014) A decade of progress in adipose tissue macrophage biology. Immunol Rev 262, 134152.
28. Cinti, S, Mitchell, G, Barbatelli, G, et al. (2005) Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 46, 23472355.
29. Weisberg, SP, McCann, D, Desai, M, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112, 17961808.
30. Xu, H, Barnes, GT, Yang, Q, et al. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112, 18211830.
31. Harman-Boehm, I, Blüher, M, Redel, H, et al. (2007) Macrophage infiltration into omental versus subcutaneous fat across different populations: effect of regional adiposity and the comorbidities of obesity. J Clin Endocrinol Metab 92, 22402247.
32. Mohanty, P, Hamouda, W, Garg, R, et al. (2000) Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes. J Clin Endocrinol Metab 85, 29702973.
33. Ceriello, A (2012) The emerging challenge in diabetes: the “metabolic memory”. Vascul Pharmacol 57, 133138.
34. Siti, HN, Kamisah, Y & Kamsiah, J (2015) The role of oxidative stress, antioxidants and vascular inflammation in cardiovascular disease (a review). Vascul Pharmacol 71, 4056.
35. Ceriello, A (1997) Acute hyperglycaemia and oxidative stress generation. Diabet Med 14, Suppl. 3, S45S49.
36. Lugrin, J, Rosenblatt-Velin, N, Parapanov, R, et al. (2014) The role of oxidative stress during inflammatory processes. Biol Chem 395, 203230.
37. Dröge, W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82, 4795.
38. Zuo, T, Zhu, M & Xu, W (2016) Roles of oxidative stress in polycystic ovary syndrome and cancers. Oxid Med Cell Longev 2016, 8589318.
39. Alfadda, AA & Sallam, RM (2012) Reactive oxygen species in health and disease. J Biomed Biotechnol 2012, 936486.
40. Parthasarathy, S, Steinberg, D & Witztum, JL (1992) The role of oxidized low-density lipoproteins in the pathogenesis of atherosclerosis. Annu Rev Med 43, 219225.
41. Buyken, AE, Goletzke, J, Joslowski, G, et al. (2014) Association between carbohydrate quality and inflammatory markers: systematic review of observational and interventional studies. Am J Clin Nutr 99, 813833.
42. Pahwa, R & Jialal, I (2016) Hyperglycemia induces Toll-like receptor activity through increased oxidative stress. Metab Syndr Relat Disord 14, 239241.
43. Soeki, T & Sata, M (2016) Inflammatory biomarkers and atherosclerosis. Int Heart J 57, 134139.
44. Teeman, CS, Kurti, SP, Cull, BJ, et al. (2016) Postprandial lipemic and inflammatory responses to high-fat meals: a review of the roles of acute and chronic exercise. Nutr Metab (Lond) 13, 80.
45. Güray, U, Erbay, AR, Güray, Y, et al. (2004) Levels of soluble adhesion molecules in various clinical presentations of coronary atherosclerosis. Int J Cardiol 96, 235240.
46. Esposito, K, Nappo, F, Marfella, R, et al. (2002) Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 106, 20672072.
47. Wolever, TM, Jenkins, DJ, Jenkins, AL, et al. (1991) The glycemic index: methodology and clinical implications. Am J Clin Nutr 54, 846854.
48. Wolever, TM, Vuksan, V, Eshuis, H, et al. (1991) Effect of method of administration of psyllium on glycemic response and carbohydrate digestibility. J Am Coll Nutr 10, 364371.
49. Sheard, NF, Clark, NG, Brand-Miller, JC, et al. (2004) Dietary carbohydrate (amount and type) in the prevention and management of diabetes: a statement by the American Diabetes Association. Diabetes Care 27, 22662271.
50. Rizkalla, SW, Taghrid, L, Laromiguiere, M, et al. (2004) Improved plasma glucose control, whole-body glucose utilization, and lipid profile on a low-glycemic index diet in type 2 diabetic men: a randomized controlled trial. Diabetes Care 27, 18661872.
51. Ebbeling, CB, Leidig, MM, Sinclair, KB, et al. (2005) Effects of an ad libitum low-glycemic load diet on cardiovascular disease risk factors in obese young adults. Am J Clin Nutr 81, 976982.
52. Brynes, AE, Mark Edwards, C, Ghatei, MA, et al. (2003) A randomised four-intervention crossover study investigating the effect of carbohydrates on daytime profiles of insulin, glucose, non-esterified fatty acids and triacylglycerols in middle-aged men. Br J Nutr 89, 207218.
53. Venn, BJ & Green, TJ (2007) Glycemic index and glycemic load: measurement issues and their effect on diet–disease relationships. Eur J Clin Nutr 61, Suppl. 1, S122S131.
54. Cordain, L, Eaton, SB, Sebastian, A, et al. (2005) Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 81, 341354.
55. Steckhan, N, Hohmann, CD, Kessler, C, et al. (2016) Effects of different dietary approaches on inflammatory markers in patients with metabolic syndrome: a systematic review and meta-analysis. Nutrition 32, 338348.
56. Feliciano Pereira, P, das Graças de Almeida, C & Alfenas Rde, C (2014) Glycemic index role on visceral obesity, subclinical inflammation and associated chronic diseases. Nutr Hosp 30, 237243.
57. Esposito, K & Giugliano, D (2006) Diet and inflammation: a link to metabolic and cardiovascular diseases. Eur Heart J 27, 1520.
58. Diamanti-Kandarakis, E, Papalou, O, Kandaraki, EA, et al. (2017) Mechanisms in Endocrinology: Nutrition as a mediator of oxidative stress in metabolic and reproductive disorders in women. Eur J Endocrinol 176, R79R99.
59. Hu, Y, Block, G, Norkus, EP, et al. (2006) Relations of glycemic index and glycemic load with plasma oxidative stress markers. Am J Clin Nutr 84, 7076.
60. Levitan, EB, Cook, NR, Stampfer, MJ, et al. (2008) Dietary glycemic index, dietary glycemic load, blood lipids, and C-reactive protein. Metabolism 57, 437443.
61. Dickinson, S, Hancock, DP, Petocz, P, et al. (2008) High-glycemic index carbohydrate increases nuclear factor-κB activation in mononuclear cells of young, lean healthy subjects. Am J Clin Nutr 87, 11881193.
62. Buyken, AE, Flood, V, Empson, M, et al. (2010) Carbohydrate nutrition and inflammatory disease mortality in older adults. Am J Clin Nutr 92, 634643.
63. Gaskins, AJ, Mumford, SL, Rovner, AJ, et al. (2010) Whole grains are associated with serum concentrations of high sensitivity C-reactive protein among premenopausal women. J Nutr 140, 16691676.
64. North, CJ, Venter, CS & Jerling, JC (2009) The effects of dietary fibre on C-reactive protein, an inflammation marker predicting cardiovascular disease. Eur J Clin Nutr 63, 921933.
65. Bo, S, Ciccone, G, Guidi, S, et al. (2008) Diet or exercise: what is more effective in preventing or reducing metabolic alterations? Eur J Endocrinol 159, 685691.
66. Qi, L & Hu, FB (2007) Dietary glycemic load, whole grains, and systemic inflammation in diabetes: the epidemiological evidence. Curr Opin Lipidol 18, 38.
67. Ma, Y, Hébert, JR, Li, W, et al. (2008) Association between dietary fiber and markers of systemic inflammation in the Women’s Health Initiative Observational Study. Nutrition 24, 941949.
68. Kallio, P, Kolehmainen, M, Laaksonen, DE, et al. (2007) Dietary carbohydrate modification induces alterations in gene expression in abdominal subcutaneous adipose tissue in persons with the metabolic syndrome: the FUNGENUT Study. Am J Clin Nutr 85, 14171427.
69. Jegatheesan, P & De Bandt, J (2017) Fructose and NAFLD: the multifaceted aspects of fructose metabolism. Nutrients 9, E230.
70. Barrea, L, Di Somma, C, Muscogiuri, G, et al. (2017) Nutrition, inflammation and liver–spleen axis. Crit Rev Food Sci Nutr 11, 118.
71. Sun, SZ & Empie, MW (2012) Fructose metabolism in humans – what isotopic tracer studies tell us. Nutr Metab (Lond) 9, 89.
72. Kennedy, A, Martinez, K, Chuang, CC, et al. (2009) Saturated fatty acid-mediated inflammation and insulin resistance in adipose tissue: mechanisms of action and implications. J Nutr 139, 14.
73. González, F (2015) Nutrient-induced inflammation in polycystic ovary syndrome: role in the development of metabolic aberration and ovarian dysfunction. Semin Reprod Med 33, 276286.
74. González, F, Sia, CL, Shepard, MK, et al. (2014) The altered mononuclear cell-derived cytokine response to glucose ingestion is not regulated by excess adiposity in polycystic ovary syndrome. J Clin Endocrinol Metab 99, E2244E2251.
75. Shorakae, S, Teede, H, de Courten, B, et al. (2015) The emerging role of chronic low-grade inflammation in the pathophysiology of polycystic ovary syndrome. Semin Reprod Med 33, 257269.
76. González, F (2012) Inflammation in polycystic ovary syndrome: underpinning of insulin resistance and ovarian dysfunction. Steroids 77, 300305.
77. Dunaif, A & Graf, M (1989) Insulin administration alters gonadal steroid metabolism independent of changes in gonadotropin secretion in insulin-resistant women with the polycystic ovary syndrome. J Clin Invest 83, 2329.
78. Macut, D, Bjekić-Macut, J, Rahelić, D, et al. (2017) Insulin and the polycystic ovary syndrome. Diabetes Res Clin Pract 130, 163170.
79. Wahrenberg, H, Ek, I, Reynisdottir, S, et al. (1999) Divergent effects of weight reduction and oral anticonception treatment on adrenergic lipolysis regulation in obese women with the polycystic ovary syndrome. J Clin Endocrinol Metab 84, 21822187.
80. Thorp, AA & Schlaich, MP (2015) Relevance of sympathetic nervous system activation in obesity and metabolic syndrome. J Diabetes Res 2015, 341583.
81. Mancia, G, Bousquet, P, Elghozi, JL, et al. (2007) The sympathetic nervous system and the metabolic syndrome. J Hypertens 25, 909920.
82. Lara, HE, Dissen, GA, Leyton, V, et al. (2000) An increased intraovarian synthesis of nerve growth factor and its low affinity receptor is a principal component of steroid-induced polycystic ovary in the rat. Endocrinology 141, 10591072.
83. Lansdown, A & Rees, DA (2012) The sympathetic nervous system in polycystic ovary syndrome: a novel therapeutic target? Clin Endocrinol (Oxf) 77, 791801.
84. Shen, SH, Shen, SY, Liou, TH, et al. (2015) Obesity and inflammatory biomarkers in women with polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol 192, 6671.
85. Ouchi, N, Kihara, S, Funahashi, T, et al. (2003) Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation 107, 671674.
86. Nigro, E, Scudiero, O, Monaco, ML, et al. (2014) New insight into adiponectin role in obesity and obesity-related diseases. Biomed Res Int 2014, 658913.
87. Wickham, EP 3rd, Cheang, KI, Clore, JN, et al. (2011) Total and high-molecular weight adiponectin in women with the polycystic ovary syndrome. Metabolism 60, 366372.
88. Bastard, JP, Maachi, M, Lagathu, C, et al. (2006) Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17, 412.
89. Gonzalez, F (2017) Treating inflammation in polycystic ovary syndrome to ameliorate ovarian dysfunction (TIN-PCOS-AOD). https://clinicaltrials.gov/ct2/show/NCT03229408 (accessed June 2018).
90. Carmina, E, Legro, RS, Stamets, K, et al. (2003) Difference in body weight between American and Italian women with polycystic ovary syndrome: influence of the diet. Hum Reprod 18, 22892293.
91. Turner-McGrievy, G, Davidson, CR & Billings, DL (2015) Dietary intake, eating behaviors, and quality of life in women with polycystic ovary syndrome who are trying to conceive. Hum Fertil (Camb) 18, 1621.
92. Brzechffa, PR, Jakimiuk, AJ, Agarwal, SK, et al. (1996) Serum immunoreactive leptin concentrations in women with polycystic ovary syndrome. J Clin Endocrinol Metab 81, 41664169.
93. Marsh, K & Brand-Miller, J (2005) The optimal diet for women with polycystic ovary syndrome? Br J Nutr 94, 154165.
94. Moran, LJ, Noakes, M, Clifton, PM, et al. (2004) Ghrelin and measures of satiety are altered in polycystic ovary syndrome but not differentially affected by diet composition. J Clin Endocrinol Metab 89, 33373344.
95. Moran, LJ, Pasquali, R, Teede, HJ, et al. (2009) Treatment of obesity in polycystic ovary syndrome: a position statement of the Androgen Excess and Polycystic Ovary Syndrome Society. Fertil Steril 92, 19661982.
96. Escobar-Morreale, HF, Botella-Carretero, JI, Alvarez-Blasco, F, et al. (2005) The polycystic ovary syndrome associated with morbid obesity may resolve after weight loss induced by bariatric surgery. J Clin Endocrinol Metab 90, 63646469.
97. Anonymous (2000) Case problem: dietary recommendations to combat obesity, insulin resistance, and other concerns related to polycystic ovary syndrome. J Am Diet Assoc 100, 955957.
98. McKeown, NM, Meigs, JB, Liu, S, et al. (2004) Carbohydrate nutrition, insulin resistance, and the prevalence of the metabolic syndrome in the Framingham Offspring Cohort. Diabetes Care 27, 538546.
99. Juntunen, KS, Niskanen, LK, Liukkonen, KH, et al. (2002) Postprandial glucose, insulin, and incretin responses to grain products in healthy subjects. Am J Clin Nutr 75, 254262.
100. Barrea, L, Annunziata, G, Muscogiuri, G, et al. (2017) Could hop-derived bitter compounds improve glucose homeostasis by stimulating the secretion of GLP-1? Crit Rev Food Sci Nutr 14, 18.
101. Galgani, JE, Moro, C & Ravussin, E (2008) Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab 295, E1009E1017.
102. Bonadonna, RC, Groop, LC, Zych, K, et al. (1990) Dose-dependent effect of insulin on plasma free fatty acid turnover and oxidation in humans. Am J Physiol 259, E736E750.
103. Corpeleijn, E, Saris, WH & Blaak, EE (2009) Metabolic flexibility in the development of insulin resistance and type 2 diabetes: effects of lifestyle. Obes Rev 10, 178193.
104. Mehran, AE, Templeman, NM, Brigidi, GS, et al. (2012) Hyperinsulinemia drives diet-induced obesity independently of brain insulin production. Cell Metab 16, 723737.
105. Kopp, HP, Kopp, CW, Festa, A, et al. (2003) Impact of weight loss on inflammatory proteins and their association with the insulin resistance syndrome in morbidly obese patients. Arterioscler Thromb Vasc Biol 23, 10421047.
106. Chavarro, JE, Rich-Edwards, JW, Rosner, BA, et al. (2009) A prospective study of dietary carbohydrate quantity and quality in relation to risk of ovulatory infertility. Eur J Clin Nutr 63, 7886.
107. Stamets, K, Taylor, DS, Kunselman, A, et al. (2004) A randomized trial of the effects of two types of short-term hypocaloric diets on weight loss in women with polycystic ovary syndrome. Fertil Steril 81, 630637.
108. Moran, L & Norman, RJ (2004) Understanding and managing disturbances in insulin metabolism and body weight in women with polycystic ovary syndrome. Best Pract Res Clin Obstet Gynaecol 18, 1936.
109. Douglas, CC, Gower, BA, Darnell, BE, et al. (2006) Role of diet in the treatment of polycystic ovary syndrome. Fertil Steril 85, 679688.
110. Marsh, KA, Steinbeck, KS, Atkinson, FS, et al. (2010) Effect of a low glycemic index compared with a conventional healthy diet on polycystic ovary syndrome. Am J Clin Nutr 92, 8392.
111. Mehrabani, HH, Salehpour, S, Amiri, Z, et al. (2012) Beneficial effects of a high-protein, low-glycemic-load hypocaloric diet in overweight and obese women with polycystic ovary syndrome: a randomized controlled intervention study. J Am Coll Nutr 31, 117125.
112. Gower, BA & Goss, AM (2015) A lower-carbohydrate, higher-fat diet reduces abdominal and intermuscular fat and increases insulin sensitivity in adults at risk of type 2 diabetes. J Nutr 145, 177S183S.
113. Pohlmeier, AM, Phy, JL, Watkins, P, et al. (2014) Effect of a low-starch/low-dairy diet on fat oxidation in overweight and obese women with polycystic ovary syndrome. Appl Physiol Nutr Metab 39, 12371244.
114. Eslamian, G, Baghestani, AR, Eghtesad, S, et al. (2017) Dietary carbohydrate composition is associated with polycystic ovary syndrome: a case–control study. J Hum Nutr Diet 30, 9097.
115. Johnson, LK, Holven, KB, Nordstrand, N, et al. (2015) Fructose content of low calorie diets: effect on cardiometabolic risk factors in obese women with polycystic ovarian syndrome: a randomized controlled trial. Endocr Connect 4, 144154.
116. Mavropoulos, JC, Yancy, WS, Hepburn, J, et al. (2005) The effects of a low-carbohydrate, ketogenic diet on the polycystic ovary syndrome: a pilot study. Nutr Metab (Lond) 2, 35.
117. Galletly, C, Moran, L, Noakes, M, et al. (2007) Psychological benefits of a high-protein, low-carbohydrate diet in obese women with polycystic ovary syndrome – a pilot study. Appetite 49, 590593.
118. McGrice, M & Porter, J (2017) The effect of low carbohydrate diets on fertility hormones and outcomes in overweight and obese women: a systematic review. Nutrients 9, E204.
119. Frary, JM, Bjerre, KP, Glintborg, D, et al. (2016) The effect of dietary carbohydrates in women with polycystic ovary syndrome: a systematic review. Minerva Endocrinol 41, 5769.
120. Moran, LJ, Ko, H, Misso, M, et al. (2013) Dietary composition in the treatment of polycystic ovary syndrome: a systematic review to inform evidence-based guidelines. J Acad Nutr Diet 113, 520545.
121. Sears, B (2009) Anti-inflammatory diets for obesity and diabetes. J Am Coll Nutr 28, Suppl., 482S491S.
122. Kalgaonkar, S, Almario, RU, Gurusinghe, D, et al. (2011) Differential effects of walnuts vs almonds on improving metabolic and endocrine parameters in PCOS. Eur J Clin Nutr 65, 386393.
123. Moran, LJ, Grieger, JA, Mishra, GD, et al. (2015) The association of a Mediterranean-style diet pattern with polycystic ovary syndrome status in a community cohort study. Nutrients 7, 85538564.
124. Muscogiuri, G, Palomba, S, Laganà, AS, et al. (2016) Current insights into inositol isoforms, Mediterranean and ketogenic diets for polycystic ovary syndrome: from bench to bedside. Curr Pharm Des 22, 55545557.
125. Salama, AA, Amine, EK, Salem, HA, et al. (2015) Anti-inflammatory dietary combo in overweight and obese women with polycystic ovary syndrome. N Am J Med Sci 7, 310316.
126. Azadbakht, L, Surkan, PJ, Esmaillzadeh, A, et al. (2011) The Dietary Approaches to Stop Hypertension eating plan affects C-reactive protein, coagulation abnormalities, and hepatic function tests among type 2 diabetic patients. J Nutr 141, 10831088.
127. Asemi, Z, Samimi, M, Tabassi, Z, et al. (2014) Effects of DASH diet on lipid profiles and biomarkers of oxidative stress in overweight and obese women with polycystic ovary syndrome: a randomized clinical trial. Nutrition 30, 12871293.
128. Foroozanfard, F, Rafiei, H, Samimi, M, et al. (2017) The effects of dietary approaches to stop hypertension diet on weight loss, anti-Müllerian hormone and metabolic profiles in women with polycystic ovary syndrome: a randomized clinical trial. Clin Endocrinol (Oxf) 87, 5158.
129. Azadi-Yazdi, M, Karimi-Zarchi, M, Salehi-Abargouei, A, et al. (2017) Effects of Dietary Approach to Stop Hypertension diet on androgens, antioxidant status and body composition in overweight and obese women with polycystic ovary syndrome: a randomised controlled trial. J Hum Nutr Diet 30, 275283.
130. Liepa, GU, Sengupta, A & Karsies, D (2008) Polycystic ovary syndrome (PCOS) and other androgen excess-related conditions: can changes in dietary intake make a difference? Nutr Clin Pract 23, 6371.
131. Thakker, D, Raval, A, Patel, I, et al. (2015) N-acetylcysteine for polycystic ovary syndrome: a systematic review and meta-analysis of randomized controlled clinical trials. Obstet Gynecol Int 2015, 817849.
132. Akbari, M, Ostadmohammadi, V, Lankarani, KB, et al. (2018) The effects of vitamin D supplementation on biomarkers of inflammation and oxidative stress among women with polycystic ovary syndrome: a systematic review and meta-analysis of randomized controlled trials. Horm Metab Res 50, 271279.
133. Maktabi, M, Jamilian, M & Asemi, Z (2018) Magnesium–zinc–calcium–vitamin D co-supplementation improves hormonal profiles, biomarkers of inflammation and oxidative stress in women with polycystic ovary syndrome: a randomized, double-blind, placebo-controlled trial. Biol Trace Elem Res 182, 2128.
134. Banaszewska, B, Wrotyńska-Barczyńska, J, Spaczynski, RZ, et al. (2016) Effects of resveratrol on polycystic ovary syndrome: a double-blind, randomized, placebo-controlled trial. J Clin Endocrinol Metab 101, 43224328.

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