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anxiety, depression, metabolic syndrome, comorbidity, outpatients.
Background and aim of the work: To explore gender differences in patients suffering from anxious-depressive symptoms, Metabolic Syndrome (MetS) and Colorectal Adenomas (CRAs) in a sample of outpatients undergoing colonoscopy for screening purposes.
Methods: Cross-sectional study. 126 consecutive outpatients of both sexes undergoing colonoscopy for non-specific abdominal symptoms between January 2015 and June 2021 at the Modena Policlinico General Hospital (Modena, Northern Italy) were enrolled. MetS was diagnosed according to ATPIII and IDF criteria. Anxiety and depression were assessed with the Hospital Anxiety and Depression Scale (HADS), while the Temperament and Character Inventory (TCI) was used to study personality. The SF-36 was also included as a measure of quality of life perception.
Results: Among 126 outpatients (51.60% male) undergoing colonoscopy, 51 (44%) had CRAs, 54 (47%) MetS, 41 (41.40%) anxiety symptoms, 22 (22.20%) depressive symptoms and 13 (13.10%) combined anxious-depressive symptoms. HADS-Anxiety (t=2.68, p=0.01) and TCI Reward Dependence (TCI-RD) (t=3.01, p=0.00) mean scores were significantly higher in women; conversely, SF-36 Mental Component Summary scores were higher in men. CRAs were significantly prevalent in men (χ2=9.32, p=0.00) and were statistically significantly associated with male sex at the univariate logistic regression analysis (OR=3.27; p<0.01). At the multivariate logistic regression, diastolic hypertension (p<0.01) was positively associated with male sex, while TCI-RD (p=0.04) and HDL hypocholesterolemia (p=0.02) were inversely associated with male sex.
Conclusions: Several significant gender differences in anxious-depressive symptoms, MetS and CRAs were found. These preliminary data suggest the need to consider gender specificities while implementing therapeutic, diagnostic, and preventive strategies.
2. World Health Organization. Depression. Available at: https://www.who.int/news-room/fact-sheets/detail/depression. Last access: October 11, 2021.
3. Solomon MB, Herman JP. Sex differences in psychopathology: of gonads, adrenals and mental illness. Physiol Behav 2009;97(2):250-8.
4. Nolen-Hoeksema S, Larson J, Grayson C. Explaining the gender difference in depressive symptoms. J Pers Soc Psychol 1999;77(5):1061-72.
5. Altemus M, Sarvaiya N, Neill Epperson C. Sex differences in anxiety and depression clinical perspectives. Front Neuroendocrinol 2014;35(3):320-30.
6. Marques AA, Bevilaqua MC, da Fonseca AM, Nardi AE, Thuret S, Dias GP. Gender Differences in the Neurobiology of Anxiety: Focus on Adult Hippocampal Neurogenesis. Neural Plast 2016:5026713.
7. Kim J, Gorman J. The psychobiology of anxiety. Clinical Neuroscience Research 2005;4(5-6):335–347.
8. Kaczkurkin AN, Raznahan A, Satterthwaite TD. Sex differences in the developing brain: insights from multimodal neuroimaging. Neuropsychopharmacology 2019;44(1):71-85.
9. Lavretsky H, Kurbanyan K, Ballmaier M, et al. Sex differences in brain structure in geriatric depression. The American Journal of Geriatric Psychiatry: Official Journal of the American Association for Geriatric Psychiatry. 2004;12(6):653-657.
10. Ingalhalikar M, Smith A, Parker D, Satterthwaite TD, Elliott MA, Ruparel K, Hakonarson H, Gur RE, Gur RC, Verma R. Sex differences in the structural connectome of the human brain. Proc Natl Acad Sci USA 2014;111(2):823-8.
11. de Vries GJ, Södersten P. Sex differences in the brain: the relation between structure and function. Horm Behav. 2009;55(5):589-96.
12. Li SH, Graham BM. Why are women so vulnerable to anxiety, trauma-related and stress-related disorders? The potential role of sex hormones. Lancet Psychiatry 2017;4(1):73-82.
13. Moieni M, Tan KM, Inagaki TK, Muscatell KA, Dutcher JM, Jevtic I, Breen EC, Irwin MR, Eisenberger NI. Sex Differences in the Relationship Between Inflammation and Reward Sensitivity: A Randomized Controlled Trial of Endotoxin. Biol Psychiatry Cogn Neurosci Neuroimaging. 2019;4(7):619-626.
14. Thompson AE, Voyer D. Sex differences in the ability to recognise non-verbal displays of emotion: a meta-analysis. Cogn Emot 2014;28(7):1164-95.
15. Bardeen JR & Stevens EN. Sex differences in the indirect effects of cognitive processes on anxiety through emotion regulation difficulties. Personality and Individual Differences 2015; 81: 180-187.
16. Hammen C. Interpersonal stress and depression in women. J Affect Disord. 2003;74(1):49-57.
17. Cyranowski JM, Frank E, Young E, Shear MK. Adolescent onset of the gender difference in lifetime rates of major depression: a theoretical model. Arch Gen Psychiatry 2000;57(1):21-7.
18. Derdikman-Eiron R, Indredavik MS, Bakken IJ, Bratberg GH, Hjemdal O, Colton M. Gender differences in psychosocial functioning of adolescents with symptoms of anxiety and depression: longitudinal findings from the Nord-Trøndelag Health Study. Soc Psychiatry Psychiatr Epidemiol 2012;47(11):1855-63.
19. Patel V, Araya R, de Lima M, Ludermir A, Todd C. Women, poverty and common mental disorders in four restructuring societies. Soc Sci Med 1999;49(11):1461-71.
20. Patel V, Kirkwood BR, Pednekar S, Pereira B, Barros P et al. Gender disadvantage and reproductive health risk factors for common mental disorders in women: a community survey in India. Arch Gen Psychiatry 2006;63(4):404-13.
21. Afifi M. Gender differences in mental health. Singapore Med J 2007;48(5):385-91.
22. Chen H, Zheng X, Zong X, Li Z, Li N, Hur J et al. Metabolic syndrome, metabolic comorbid conditions and risk of early-onset colorectal cancer. Gut 2021;70(6):1147-1154.
23. Lee J, Lee KS, Kim H, Jeong H, Choi MJ, Yoo HW et al. The relationship between metabolic syndrome and the incidence of colorectal cancer. Environ Health Prev Med. 2020;25(1):6.
24. Shen X, Wang Y, Zhao R, Wan Q, Wu Y, Zhao L, Wu X. Metabolic syndrome and the risk of colorectal cancer: a systematic review and meta-analysis. Int J Colorectal Dis 2021;36(10):2215-2225.
25. Wu H, Zhang J, Zhou B. Metabolic syndrome and colorectal adenoma risk: A systematic review and meta analysis. Clin Res Hepatol Gastroenterol. 2021;45(5):101749.
26. Ku MS, Chiu SY, Chien KL, Lee YC, Chen SL, Chen CD. Gender difference in metabolic syndrome and incident colorectal adenoma: A prospective observational study (KCIS No.42). Medicine (Baltimore) 2021;100(22):e26121.
27. Mancini S, Alboni S, Mattei G, Rioli G, Sena P, Marchi M et al. Preliminary results of a multidisciplinary Italian study adopting a Psycho-Neuro-Endocrine-Immunological (PNEI) approach to the study of colorectal adenomas. Acta Biomed 2020;92(1):e2021014.
28. Kim BC, Shin A, Hong CW, Sohn DK, Han KS, Ryu KH et al. Association of colorectal adenoma with components of metabolic syndrome. Cancer Causes Control 2012;23(5):727-35.
29. Regitz-Zagrosek V, Lehmkuhl E, Weickert MO. Gender differences in the metabolic syndrome and their role for cardiovascular disease. Clin Res Cardiol. 2006;95(3):136-47.
30. Rochlani Y, Andries G, Yandrapalli S, Pothineni NV, Mehta JL. Gender Differences in Metabolic Syndrome. In: Mehta J., McSweeney J. (eds) Gender Differences in the Pathogenesis and Management of Heart Disease. 2018. Springer, Cham. https://doi.org/10.1007/978-3-319-71135-5_2
31. Vishram JKK, Borglykke A, Andreasen AH, Jeppesen J, Ibsen H, et al. Impact of Age and Gender on the Prevalence and Prognostic Importance of the Metabolic Syndrome and Its Components in Europeans. The MORGAM Prospective Cohort Project. PLOS ONE 2015; 10(5): e0128848.
32. Ferlitsch M, Reinhart K, Pramhas S, Wiener C, Gal O, Bannert C, Hassler M, Kozbial K, Dunkler D, Trauner M, Weiss W. Sex-specific prevalence of adenomas, advanced adenomas, and colorectal cancer in individuals undergoing screening colonoscopy. JAMA 2011;306(12):1352-8.
33. Lai MM, Li CI, Kardia SL, et al. Sex difference in the association of metabolic syndrome with high sensitivity C-reactive protein in a Taiwanese population. BMC Public Health 2010;10:429.
34. Poret JM, Gaudet DA, Braymer HD, Primeaux SD. Sex differences in markers of metabolic syndrome and adipose tissue inflammation in obesity-prone, Osborne-Mendel and obesity-resistant, S5B/Pl rats. Life Sci 2021;273:119290.
35. Oxenkrug GF. Metabolic syndrome, age-associated neuroendocrine disorders, and dysregulation of tryptophan-kynurenine metabolism. Ann N Y Acad Sci. 2010;1199:1-14.
36. Sun XZ, Zhao DY, Zhou YC, Wang QQ, Qin G, Yao SK. Alteration of fecal tryptophan metabolism correlates with shifted microbiota and may be involved in pathogenesis of colorectal cancer. World J Gastroenterol 2020;26(45):7173-7190.
37. Liu CY, Huang TT, Chen JL, Chu PY, Lee CH, Lee HC et al. Significance of Kynurenine 3-Monooxygenase Expression in Colorectal Cancer. Front Oncol 2021;11:620361.
38. Khera A, McGuire DK, Murphy SA, Stanek HG, Das SR, Vongpatanasin W et al. Race and gender differences in C-reactive protein levels. J Am Coll Cardiol 2005;46(3):464-9.
39. Badawy AA, Dougherty DM. Assessment of the Human Kynurenine Pathway: Comparisons and Clinical Implications of Ethnic and Gender Differences in Plasma Tryptophan, Kynurenine Metabolites, and Enzyme Expressions at Baseline and After Acute Tryptophan Loading and Depletion. Int J Tryptophan Res. 2016;9:31-49.
40. Marchi M, Mattei G, Mancini S, Roncucci L, Galeazzi GM, Ferrari S. Personality traits and physical activity may be involved in colorectal carcinogenesis: preliminary data from a cross-sectional study on patients undergoing colonoscopy. Minerva Psichiatrica;60(2):100-1.
41. Zigmond AS & Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand 1983;67(6),361-70.
42. Costantini M, Musso M, Viterbori P, Bonci F, Del Mastro L, Garrone O et al. Detecting psychological distress in cancer patients: validity of the Italian version of the Hospital Anxiety and Depression Scale. Support Care Cancer 1999;7(3),121-7.
43. Bjelland I, Dahl AA, Tangen Haug T, Neckelmann D. The validity of the Hospital Anxiety and Depression Scale: An updated literature review. J of psychosomatic Research 2002;52(2), 69-77.
44. Cloninger CR (1994) The temperament and character inventory (TCI): A guide to its development and use. Center for Psychobiology of Personality. St Louis, MO: Washington University.
45. Fossati A, Cloninger CR, Villa D, Borroni S, Grazioli F, Giarolli L et al. Reliability and validity of the Italian version of the Temperament and Character Inventory–Revised in an outpatient sample. Compr Psychiatry 2007; 48:380–3.
46. Apolone G, Mosconi P. The Italian SF-36 Health Survey: Translation, validation and norming. J Clin Epidemiol 1998; 51:1025–1036.
47. Ware JE, Snow KK, Kosinski M, Gandek B (1993). SF-36 Health Survey: Manual and interpretation guide. Boston, MA: The Health Institute.
48. Van Reedt Dortland AKB, Peters LL, Boenink AD, Smit JH, Slaets JPJ, Hoogendoorn AW et al. Assessment of biopsychosocial complexity and health care needs: Measurement properties of the INTERMED Self-Assessment Version. Psychosom Med 2017; 79:485–492.
49. Borsini A, Alboni S, Horowitz MA, Tojo LM, Cannazza G, Su KP et al. Rescue of IL-1β-induced reduction of human neurogenesis by omega-3 fatty acids and antidepressants. Brain Behav Immun 2017;65:230-238.
50. International Diabetes Federation, IDF (2006). The IDF consensus worldwide definition of the Metabolic Syndrome. Brussels, Belgium: International Diabetes Federation. Available at: https://www.idf.org/e-library/consensus-statements/60- idfconsensus-worldwide-definitionof-the-metabolic-syndrome.
51. National Cholesterol Education Program (NCEP): Expert Panel on Detection and Treatment of High Blood Cholesterol in Adults. Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation 2002;106, 3143–3421.
52. de Girolamo, G., Polidori, G., Morosini, P., Scarpino, V., Reda, V., Serra, G., et al. Prevalence of common mental disorders in Italy. Social Psychiatry and Psychiatric Epidemiology 2006; 41, 853-861.
53. PASSI (Progressi delle Aziende Sanitarie per la Salute in Italia, Progress of Health Authorities in Italy). Sovrappeso e obesità in Emilia-Romagna: i dati del sistema di sorveglianza PASSI triennio 2007-09. Available at: https://www.epicentro.iss.it/passi/pdf2010/obesita_ER0709.pdf. Last accessed: October, 12th, 2021.
54. Luu HN, Tran MT, Nguyen MV, Tuong TT, Tran QH, Le LC et al. Association between body mass index and colorectal adenomas: Findings from a case-control study in Vietnam. Int J Cancer 2021;149(11):1898-1909.
55. Wong MCS, Huang J, Huang JLW, Pang TWY, Choi P, Wang J et al. Global Prevalence of Colorectal Neoplasia: A Systematic Review and Meta-Analysis. Clin Gastroenterol Hepatol 2020;18(3):553-561.e10.
56. Siren R, Eriksson JG, Vanhanen H. Waist circumference a good indicator of future risk for type 2 diabetes and cardiovascular disease. BMC Public Health 2012;12:631.
57. Despres JP, Lemieux I, Prud’homme D. Treatment of obesity: need to focus on high risk abdominally obese patients. BMJ 2001;322:716-720.
58. Luppino FS, van Reedt Dortland AK, Wardenaar KJ, Bouvy PF, Giltay EJ, Zitman FG et al. Symptom dimensions of depression and anxiety and the metabolic syndrome. Psychosom Med. 2011;73(3):257-64.
59. Zhao G, Ford ES, Li C, Tsai J, Dhingra S, Balluz LS. Waist circumference, abdominal obesity, and depression among overweight and obese U.S. adults: National Health and Nutrition Examination Survey 2005-2006. BMC Psychiatry. 2011;11:130.
60. Moreira RO, Marca KF, Appolinario JC, Coutinho WF. Increased waist circumference is associated with an increased prevalence of mood disorders and depressive symptoms in obese women. Eat Weight Disord. 2007;12(1):35-40.
61. Labad J, Price JF, Strachan MW, Fowkes FG, Ding J, Deary IJ et al. Edinburgh Type 2 Diabetes Study Investigators. Symptoms of depression but not anxiety are associated with central obesity and cardiovascular disease in people with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetologia 2010;53(3):467-71.
62. Gomes AP, Soares ALG, Menezes AMB, Assunção MC, Wehrmeister FC, Howe LD et al. Adiposity, depression and anxiety: interrelationship and possible mediators. Rev Saude Publica 2019;53:103.
63. Guedes EP, Madeira E, Mafort TT, Madeira M, Moreira RO, Mendonça LM et al. Body composition and depressive/anxiety symptoms in overweight and obese individuals with metabolic syndrome. Diabetol Metab Syndr 2013;5(1):82.
64. Bocicor AE, Buicu G, Varga A, Tatar R, Sabau D, Tilea I et al. Association Between Increased Waist Circumference and Depression and Anxiety Trend. Acta Medica Marisiensis 2015;61(2):87-90. DOI: 10.1515/amma-2015-0028.
65. Räikkönen K, Matthews KA, Kuller LH. Anthropometric and psychosocial determinants of visceral obesity in healthy postmenopausal women. Int J Obes Relat Metab Disord 1999;23(8):775-82.
66. Bella JN, Palmieri V, Kitzman DW, Liu JE, Oberman A, Hunt SC et al. Gender difference in diastolic function in hypertension (the HyperGEN study). Am J Cardiol. 2002;89(9):1052-6.
67. Alhawari HH, Al-Shelleh S, Alhawari HH, Al-Saudi A, Aljbour Al-Majali D et al. Blood Pressure and Its Association with Gender, Body Mass Index, Smoking, and Family History among University Students. Int J Hypertens 2018;2018:4186496.
68. Gillis EE, Sullivan JC. Sex Differences in Hypertension: Recent Advances. Hypertension 2016;68(6):1322-1327.
69. Calderwood AH, Bacic J, Kazis LE, Cabral H. Association between self-reported depression and screening colonoscopy participation. J Ambul Care Manage 2013;36(4):345-55.
70. Abgrall-Barbry G, Lemogne C, Lamarque D, Leuret B, Bydlowski S, Jian R et al. Depressive mood and subsequent cancer diagnosis in patients undergoing a colonoscopy. Psychosomatics 2012;53(4):356-62.
71. Bangasser DA, Cuarenta A. Sex differences in anxiety and depression: circuits and mechanisms. Nat Rev Neurosci 2021. Epub ahead of print.
72. Calvet B, Péricaud M, Parneix M, Jouette A, Bricaud M, Clément JP. Age and Sex Differences in Temperament and Character Dimensions in a French Nonclinical Population. Journal of Individual Differences 2016; 37, 168-180.
73. Al-Halabí S, Herrero R, Sáiz PA, García Portilla MP, Errasti JM, Corcoran P, et al. A cross-cultural comparison between Spain and the USA: temperament and character distribution by sex and age. Psychiatry Research 2011; 186, 397-401.
74. Mendlowicz MV, Jean-Louis G, Gillin JC, Akiskal HS, Furlanetto LM, Rapaport MH et al. Sociodemographic predictors of temperament and character. Journal of Psychiatric Research 2000; 34:221-226.
75. Parker G, Cheah YC, Parker K. Properties of the temperament and character inventory in a Chinese sample. Acta Psychiatrica Scandinavica 2003;108: 367-373.
76. Miettunen J, Veijola J, Lauronen E, Kantojarvi L, Joukamaa M. Sex differences in Cloninger's temperament dimensions—a meta-analysis. Comprehensive Psychiatry 2007; 48:161-169.
77. Liu CC, Chang HT, Chiang SC, Chen HS, Lin MH, Chen TJ, Hwang SJ. Sex differences in relationships between metabolic syndrome components and factors associated with health-related quality of life in middle-aged adults living in the community: a cross-sectional study in Taiwan. Health Qual Life Outcomes 2018;16(1):76.
78. Cherepanonv D, Palta M, Fryback DG, Robert SA. Gender differences in health-related quality of life are partly explained by socio-demographic and socioeconomic variation between adult men and women in the US: Evidence from four US nationally representative data sets. Qual Life Res 2010;19:1115–24.
79. Meier TB, Drevets WC, Teague TK, Wurfel BE, Mueller SC, Bodurka J et al. Kynurenic acid is reduced in females and oral contraceptive users: Implications for depression. Brain Behav Immun 2018;67:59-64.