Gender and chronic kidney disease_West China Medical Journal

Authors：

ZHANG Jue ¹ ,  LIU Fang ^1,2

1. Division of Nephrology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. Diabetic Nephropathy Laboratory, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

LIU Fang, Email: liufangfh@163.com

Keywords：

Chronic kidney disease; Diabetic kidney disease; Non-diabetic kindey disease; Gender; Sex hormones

DOI：

10.7507/1002-0179.202010118

Video：

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The incidence of chronic kidney disease is increasing worldwide, which greatly increases the risk of end-stage renal disease. It is particularly important to find out the risk factors for the development and progression of chronic kidney disease. Whether gender is a risk factor for the progression of kidney disease remains controversial with inconsistent results in human cohort studies with diabetic or non-diabetic kidney disease. In most of the studies, women seem to exhibit certain gender advantages. Sex hormones, renal hemodynamics and lifestyle differences may play an important role. The underlying mechanism of gender affecting the progression of kidney disease deserves further exploration. This article reviews the gender differences and possible mechanisms in diabetic and non-diabetic chronic kidney disease, in order to provide reference for future research.

Citation： ZHANG Jue, LIU Fang. Gender and chronic kidney disease. West China Medical Journal, 2021, 36(3): 396-400. doi: 10.7507/1002-0179.202010118 Copy

1.	Inker LA, Astor BC, Fox CH, et al. KDOQI US commentary on the 2012 KDIGO clinical practice guideline for the evaluation and management of CKD. Am J Kidney Dis, 2014, 63(5): 713-735.
2.	Mazure CM, Jones DP. Twenty years and still counting: including women as participants and studying sex and gender in biomedical research. BMC Womens Health, 2015, 15: 94.
3.	Floege J, Barbour SJ, Cattran DC, et al. Management and treatment of glomerular diseases (part 1): conclusions from a kidney disease: improving global outcomes (KDIGO) controversies conference. Kidney Int, 2019, 95(2): 268-280.
4.	Neugarten J, Acharya A, Silbiger SR. Effect of gender on the progression of nondiabetic renal disease: a meta-analysis. J Am Soc Nephrol, 2000, 11(2): 319-329.
5.	Molina JF, Drenkard C, Molina J, et al. Systemic lupus erythematosus in males. A study of 107 Latin American patients. Medicine (Baltimore), 1996, 75(3): 124-130.
6.	Cattran DC, Reich HN, Beanlands HJ, et al. The impact of sex in primary glomerulonephritis. Nephrol Dial Transplant, 2008, 23(7): 2247-2253.
7.	Gretz N, Zeier M, Geberth S, et al. Is gender a determinant for evolution of renal failure? A study in autosomal dominant polycystic kidney disease. Am J Kidney Dis, 1989, 14(3): 178-183.
8.	Ricardo AC, Yang W, Sha D, et al. Sex-related disparities in CKD progression. J Am Soc Nephrol, 2019, 30(1): 137-146.
9.	Jafar TH, Schmid CH, Stark PC, et al. The rate of progression of renal disease may not be slower in women compared with men: a patient-level meta-analysis. Nephrol Dial Transplant, 2003, 18(10): 2047-2053.
10.	Khan RMM, Chua ZJY, Tan JC, et al. From pre-diabetes to diabetes: diagnosis, treatments and translational research. Medicina (Kaunas), 2019, 55(9): 546.
11.	Saran R, Li Y, Robinson B, et al. US renal data system 2015 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis, 2016, 67(3 Suppl 1): Svii, S1-S305.
12.	Levin A, Tonelli M, Bonventre J, et al. Global kidney health 2017 and beyond: a roadmap for closing gaps in care, research, and policy. Lancet, 2017, 390(10105): 1888-1917.
13.	Ene-Iordache B, Perico N, Bikbov B, et al. Chronic kidney disease and cardiovascular risk in six regions of the world (ISN-KDDC): a cross-sectional study. Lancet Glob Health, 2016, 4(5): e307-e319.
14.	Raile K, Galler A, Hofer S, et al. Diabetic nephropathy in 27, 805 children, adolescents, and adults with type 1 diabetes: effect of diabetes duration, A1C, hypertension, dyslipidemia, diabetes onset, and sex. Diabetes Care, 2007, 30(10): 2523-2528.
15.	Orchard TJ, Dorman JS, Maser RE, et al. Prevalence of complications in IDDM by sex and duration. Pittsburgh epidemiology of diabetes complications studyⅡ. Diabetes, 1990, 39(9): 1116-1124.
16.	Hovind P, Tarnow L, Rossing P, et al. Predictors for the development of microalbuminuria and macroalbuminuria in patients with type 1 diabetes: inception cohort study. BMJ, 2004, 328(7448): 1105.
17.	Sibley SD, Thomas W, de Boer I, et al. Gender and elevated albumin excretion in the diabetes control and complications trial/epidemiology of diabetes interventions and complications (DCCT/EDIC) cohort: role of central obesity. Am J Kidney Dis, 2006, 47(2): 223-232.
18.	Mangili R, Deferrari G, Di Mario U, et al. Arterial hypertension and microalbuminuria in IDDM: the Italian microalbuminuria study. Diabetologia, 1994, 37(10): 1015-1024.
19.	Harjutsalo V, Maric C, Forsblom C, et al. Sex-related differences in the long-term risk of microvascular complications by age at onset of type 1 diabetes. Diabetologia, 2011, 54(8): 1992-1999.
20.	Holl RW, Grabert M, Thon A, et al. Urinary excretion of albumin in adolescents with type 1 diabetes: persistent versus intermittent microalbuminuria and relationship to duration of diabetes, sex, and metabolic control. Diabetes Care, 1999, 22(9): 1555-1560.
21.	Schultz CJ, Konopelska-Bahu T, Dalton RN, et al. Microalbuminuria prevalence varies with age, sex, and puberty in children with type 1 diabetes followed from diagnosis in a longitudinal study. Oxford Regional Prospective Study Group. Diabetes Care, 1999, 22(3): 495-502.
22.	Rossing P, Hougaard P, Parving HH. Risk factors for development of incipient and overt diabetic nephropathy in type 1 diabetic patients: a 10-year prospective observational study. Diabetes Care, 2002, 25(5): 859-864.
23.	de Hauteclocque A, Ragot S, Slaoui Y, et al. The influence of sex on renal function decline in people with type 2 diabetes. Diabet Med, 2014, 31(9): 1121-1128.
24.	Crook ED, Patel SR. Diabetic nephropathy in African-American patients. Curr Diab Rep, 2004, 4(6): 455-461.
25.	Looker HC, Krakoff J, Funahashi T, et al. Adiponectin concentrations are influenced by renal function and diabetes duration in Pima Indians with type 2 diabetes. J Clin Endocrinol Metab, 2004, 89(8): 4010-4017.
26.	Young BA, Maynard C, Boyko EJ. Racial differences in diabetic nephropathy, cardiovascular disease, and mortality in a national population of veterans. Diabetes Care, 2003, 26(8): 2392-2399.
27.	Meyer TW, Bennett PH, Nelson RG. Podocyte number predicts long-term urinary albumin excretion in Pima Indians with typeⅡdiabetes and microalbuminuria. Diabetologia, 1999, 42(11): 1341-1344.
28.	Ritz E, Schwenger V. Lifestyle modification and progressive renal failure. Nephrology (Carlton), 2005, 10(4): 387-392.
29.	Kos M, Denger S, Reid G, et al. Upstream open reading frames regulate the translation of the multiple mRNA variants of the estrogen receptor alpha. J Biol Chem, 2002, 277(40): 37131-37138.
30.	Kumar A, Bean LA, Rani A, et al. Contribution of estrogen receptor subtypes, ERα, ERβ, and GPER1 in rapid estradiol-mediated enhancement of hippocampal synaptic transmission in mice. Hippocampus, 2015, 25(12): 1556-1566.
31.	Reckelhoff JF, Zhang H, Srivastava K. Gender differences in development of hypertension in spontaneously hypertensive rats: role of the renin-angiotensin system. Hypertension, 2000, 35(1 Pt 2): 480-483.
32.	Doublier S, Lupia E, Catanuto P, et al. Testosterone and 17β-estradiol have opposite effects on podocyte apoptosis that precedes glomerulosclerosis in female estrogen receptor knockout mice. Kidney Int, 2011, 79(4): 404-413.
33.	Steffes MW, Schmidt D, McCrery R, et al. Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int, 2001, 59(6): 2104-2113.
34.	Lemley KV, Blouch K, Abdullah I, et al. Glomerular permselectivity at the onset of nephropathy in type 2 diabetes mellitus. J Am Soc Nephrol, 2000, 11(11): 2095-2105.
35.	Lemley KV, Lafayette RA, Safai M, et al. Podocytopenia and disease severity in IgA nephropathy. Kidney Int, 2002, 61(4): 1475-1485.
36.	Sharma PK, Thakur MK. Estrogen receptor alpha expression in mice kidney shows sex differences during aging. Biogerontology, 2004, 5(6): 375-381.
37.	Potier M, Karl M, Zheng F, et al. Estrogen-related abnormalities in glomerulosclerosis-prone mice: reduced mesangial cell estrogen receptor expression and prosclerotic response to estrogens. Am J Pathol, 2002, 160(5): 1877-1885.
38.	Berg UB. Differences in decline in GFR with age between males and females. Reference data on clearances of inulin and PAH in potential kidney donors. Nephrol Dial Transplant, 2006, 21(9): 2577-2582.
39.	Erdely A, Freshour G, Tain YL, et al. DOCA/NaCl-induced chronic kidney disease: a comparison of renal nitric oxide production in resistant and susceptible rat strains. Am J Physiol Renal Physiol, 2007, 292(1): F192-F196.
40.	Erdely A, Greenfeld Z, Wagner L, et al. Sexual dimorphism in the aging kidney: effects on injury and nitric oxide system. Kidney Int, 2003, 63(3): 1021-1026.
41.	Holden DP, Cartwright JE, Nussey SS, et al. Estrogen stimulates dimethylarginine dimethylaminohydrolase activity and the metabolism of asymmetric dimethylarginine. Circulation, 2003, 108(13): 1575-1580.
42.	Singh R, Pervin S, Shryne J, et al. Castration increases and androgens decrease nitric oxide synthase activity in the brain: physiologic implications. Proc Natl Acad Sci USA, 2000, 97(7): 3672-3677.
43.	Reckelhoff JF, Granger JP. Role of androgens in mediating hypertension and renal injury. Clin Exp Pharmacol Physiol, 1999, 26(2): 127-131.
44.	Chen YF, Naftilan AJ, Oparil S. Androgen-dependent angiotensinogen and renin messenger RNA expression in hypertensive rats. Hypertension, 1992, 19(5): 456-463.
45.	Khoury S, Yarows SA, O’Brien TK, et al. Ambulatory blood pressure monitoring in a nonacademic setting. Effects of age and sex. Am J Hypertens, 1992, 5(9): 616-623.
46.	Benjamin EJ, Blaha MJ, Chiuve SE, et al. Heart disease and stroke statistics-2017 Update: a report from the American Heart Association. Circulation, 2017, 135(10): e146-e603.
47.	Filler G, Ramsaroop A, Stein R, et al. Is testosterone detrimental to renal function?. Kidney Int Rep, 2016, 1(4): 306-310.
48.	Orth SR, Stöckmann A, Conradt C, et al. Smoking as a risk factor for end-stage renal failure in men with primary renal disease. Kidney Int, 1998, 54(3): 926-931.
49.	Christiansen JS. Cigarette smoking and prevalence of microangiopathy in juvenile-onset insulin-dependent diabetes mellitus. Diabetes Care, 1978, 1(3): 146-149.
50.	Chuahirun T, Wesson DE. Cigarette smoking predicts faster progression of type 2 established diabetic nephropathy despite ACE inhibition. Am J Kidney Dis, 2002, 39(2): 376-382.
51.	Han Qq, Wang Ss, Zhang Jl, et al. The association between cigarette smoking and diabetic nephropathy in Chinese male patients. Acta Diabetol, 2018, 55(11): 1131-1141.
52.	Ramirez SPB, McClellan W, Port FK, et al. Risk factors for proteinuria in a large, multiracial, southeast Asian population. J Am Soc Nephrol, 2002, 13(7): 1907-1917.
53.	Bonnet F, Deprele C, Sassolas A, et al. Excessive body weight as a new independent risk factor for clinical and pathological progression in primary IgA nephritis. Am J Kidney Dis, 2001, 37(4): 720-727.
54.	Krzyżowska S, Matejko B, Kieć-Wilk B, et al. Assessment of selected food intake frequency in patients with type 1 diabetes treated with personal insulin pumps. Rocz Panstw Zakl Hig, 2019, 70(3): 259-265.
55.	Pérez-Torres I, Roque P, El Hafidi M, et al. Association of renal damage and oxidative stress in a rat model of metabolic syndrome. Influence of gender. Free Radic Res, 2009, 43(8): 761-771.

1. Inker LA, Astor BC, Fox CH, et al. KDOQI US commentary on the 2012 KDIGO clinical practice guideline for the evaluation and management of CKD. Am J Kidney Dis, 2014, 63(5): 713-735.
2. Mazure CM, Jones DP. Twenty years and still counting: including women as participants and studying sex and gender in biomedical research. BMC Womens Health, 2015, 15: 94.
3. Floege J, Barbour SJ, Cattran DC, et al. Management and treatment of glomerular diseases (part 1): conclusions from a kidney disease: improving global outcomes (KDIGO) controversies conference. Kidney Int, 2019, 95(2): 268-280.
4. Neugarten J, Acharya A, Silbiger SR. Effect of gender on the progression of nondiabetic renal disease: a meta-analysis. J Am Soc Nephrol, 2000, 11(2): 319-329.
5. Molina JF, Drenkard C, Molina J, et al. Systemic lupus erythematosus in males. A study of 107 Latin American patients. Medicine (Baltimore), 1996, 75(3): 124-130.
6. Cattran DC, Reich HN, Beanlands HJ, et al. The impact of sex in primary glomerulonephritis. Nephrol Dial Transplant, 2008, 23(7): 2247-2253.
7. Gretz N, Zeier M, Geberth S, et al. Is gender a determinant for evolution of renal failure? A study in autosomal dominant polycystic kidney disease. Am J Kidney Dis, 1989, 14(3): 178-183.
8. Ricardo AC, Yang W, Sha D, et al. Sex-related disparities in CKD progression. J Am Soc Nephrol, 2019, 30(1): 137-146.
9. Jafar TH, Schmid CH, Stark PC, et al. The rate of progression of renal disease may not be slower in women compared with men: a patient-level meta-analysis. Nephrol Dial Transplant, 2003, 18(10): 2047-2053.
10. Khan RMM, Chua ZJY, Tan JC, et al. From pre-diabetes to diabetes: diagnosis, treatments and translational research. Medicina (Kaunas), 2019, 55(9): 546.
11. Saran R, Li Y, Robinson B, et al. US renal data system 2015 annual data report: epidemiology of kidney disease in the United States. Am J Kidney Dis, 2016, 67(3 Suppl 1): Svii, S1-S305.
12. Levin A, Tonelli M, Bonventre J, et al. Global kidney health 2017 and beyond: a roadmap for closing gaps in care, research, and policy. Lancet, 2017, 390(10105): 1888-1917.
13. Ene-Iordache B, Perico N, Bikbov B, et al. Chronic kidney disease and cardiovascular risk in six regions of the world (ISN-KDDC): a cross-sectional study. Lancet Glob Health, 2016, 4(5): e307-e319.
14. Raile K, Galler A, Hofer S, et al. Diabetic nephropathy in 27, 805 children, adolescents, and adults with type 1 diabetes: effect of diabetes duration, A1C, hypertension, dyslipidemia, diabetes onset, and sex. Diabetes Care, 2007, 30(10): 2523-2528.
15. Orchard TJ, Dorman JS, Maser RE, et al. Prevalence of complications in IDDM by sex and duration. Pittsburgh epidemiology of diabetes complications studyⅡ. Diabetes, 1990, 39(9): 1116-1124.
16. Hovind P, Tarnow L, Rossing P, et al. Predictors for the development of microalbuminuria and macroalbuminuria in patients with type 1 diabetes: inception cohort study. BMJ, 2004, 328(7448): 1105.
17. Sibley SD, Thomas W, de Boer I, et al. Gender and elevated albumin excretion in the diabetes control and complications trial/epidemiology of diabetes interventions and complications (DCCT/EDIC) cohort: role of central obesity. Am J Kidney Dis, 2006, 47(2): 223-232.
18. Mangili R, Deferrari G, Di Mario U, et al. Arterial hypertension and microalbuminuria in IDDM: the Italian microalbuminuria study. Diabetologia, 1994, 37(10): 1015-1024.
19. Harjutsalo V, Maric C, Forsblom C, et al. Sex-related differences in the long-term risk of microvascular complications by age at onset of type 1 diabetes. Diabetologia, 2011, 54(8): 1992-1999.
20. Holl RW, Grabert M, Thon A, et al. Urinary excretion of albumin in adolescents with type 1 diabetes: persistent versus intermittent microalbuminuria and relationship to duration of diabetes, sex, and metabolic control. Diabetes Care, 1999, 22(9): 1555-1560.
21. Schultz CJ, Konopelska-Bahu T, Dalton RN, et al. Microalbuminuria prevalence varies with age, sex, and puberty in children with type 1 diabetes followed from diagnosis in a longitudinal study. Oxford Regional Prospective Study Group. Diabetes Care, 1999, 22(3): 495-502.
22. Rossing P, Hougaard P, Parving HH. Risk factors for development of incipient and overt diabetic nephropathy in type 1 diabetic patients: a 10-year prospective observational study. Diabetes Care, 2002, 25(5): 859-864.
23. de Hauteclocque A, Ragot S, Slaoui Y, et al. The influence of sex on renal function decline in people with type 2 diabetes. Diabet Med, 2014, 31(9): 1121-1128.
24. Crook ED, Patel SR. Diabetic nephropathy in African-American patients. Curr Diab Rep, 2004, 4(6): 455-461.
25. Looker HC, Krakoff J, Funahashi T, et al. Adiponectin concentrations are influenced by renal function and diabetes duration in Pima Indians with type 2 diabetes. J Clin Endocrinol Metab, 2004, 89(8): 4010-4017.
26. Young BA, Maynard C, Boyko EJ. Racial differences in diabetic nephropathy, cardiovascular disease, and mortality in a national population of veterans. Diabetes Care, 2003, 26(8): 2392-2399.
27. Meyer TW, Bennett PH, Nelson RG. Podocyte number predicts long-term urinary albumin excretion in Pima Indians with typeⅡdiabetes and microalbuminuria. Diabetologia, 1999, 42(11): 1341-1344.
28. Ritz E, Schwenger V. Lifestyle modification and progressive renal failure. Nephrology (Carlton), 2005, 10(4): 387-392.
29. Kos M, Denger S, Reid G, et al. Upstream open reading frames regulate the translation of the multiple mRNA variants of the estrogen receptor alpha. J Biol Chem, 2002, 277(40): 37131-37138.
30. Kumar A, Bean LA, Rani A, et al. Contribution of estrogen receptor subtypes, ERα, ERβ, and GPER1 in rapid estradiol-mediated enhancement of hippocampal synaptic transmission in mice. Hippocampus, 2015, 25(12): 1556-1566.
31. Reckelhoff JF, Zhang H, Srivastava K. Gender differences in development of hypertension in spontaneously hypertensive rats: role of the renin-angiotensin system. Hypertension, 2000, 35(1 Pt 2): 480-483.
32. Doublier S, Lupia E, Catanuto P, et al. Testosterone and 17β-estradiol have opposite effects on podocyte apoptosis that precedes glomerulosclerosis in female estrogen receptor knockout mice. Kidney Int, 2011, 79(4): 404-413.
33. Steffes MW, Schmidt D, McCrery R, et al. Glomerular cell number in normal subjects and in type 1 diabetic patients. Kidney Int, 2001, 59(6): 2104-2113.
34. Lemley KV, Blouch K, Abdullah I, et al. Glomerular permselectivity at the onset of nephropathy in type 2 diabetes mellitus. J Am Soc Nephrol, 2000, 11(11): 2095-2105.
35. Lemley KV, Lafayette RA, Safai M, et al. Podocytopenia and disease severity in IgA nephropathy. Kidney Int, 2002, 61(4): 1475-1485.
36. Sharma PK, Thakur MK. Estrogen receptor alpha expression in mice kidney shows sex differences during aging. Biogerontology, 2004, 5(6): 375-381.
37. Potier M, Karl M, Zheng F, et al. Estrogen-related abnormalities in glomerulosclerosis-prone mice: reduced mesangial cell estrogen receptor expression and prosclerotic response to estrogens. Am J Pathol, 2002, 160(5): 1877-1885.
38. Berg UB. Differences in decline in GFR with age between males and females. Reference data on clearances of inulin and PAH in potential kidney donors. Nephrol Dial Transplant, 2006, 21(9): 2577-2582.
39. Erdely A, Freshour G, Tain YL, et al. DOCA/NaCl-induced chronic kidney disease: a comparison of renal nitric oxide production in resistant and susceptible rat strains. Am J Physiol Renal Physiol, 2007, 292(1): F192-F196.
40. Erdely A, Greenfeld Z, Wagner L, et al. Sexual dimorphism in the aging kidney: effects on injury and nitric oxide system. Kidney Int, 2003, 63(3): 1021-1026.
41. Holden DP, Cartwright JE, Nussey SS, et al. Estrogen stimulates dimethylarginine dimethylaminohydrolase activity and the metabolism of asymmetric dimethylarginine. Circulation, 2003, 108(13): 1575-1580.
42. Singh R, Pervin S, Shryne J, et al. Castration increases and androgens decrease nitric oxide synthase activity in the brain: physiologic implications. Proc Natl Acad Sci USA, 2000, 97(7): 3672-3677.
43. Reckelhoff JF, Granger JP. Role of androgens in mediating hypertension and renal injury. Clin Exp Pharmacol Physiol, 1999, 26(2): 127-131.
44. Chen YF, Naftilan AJ, Oparil S. Androgen-dependent angiotensinogen and renin messenger RNA expression in hypertensive rats. Hypertension, 1992, 19(5): 456-463.
45. Khoury S, Yarows SA, O’Brien TK, et al. Ambulatory blood pressure monitoring in a nonacademic setting. Effects of age and sex. Am J Hypertens, 1992, 5(9): 616-623.
46. Benjamin EJ, Blaha MJ, Chiuve SE, et al. Heart disease and stroke statistics-2017 Update: a report from the American Heart Association. Circulation, 2017, 135(10): e146-e603.
47. Filler G, Ramsaroop A, Stein R, et al. Is testosterone detrimental to renal function?. Kidney Int Rep, 2016, 1(4): 306-310.
48. Orth SR, Stöckmann A, Conradt C, et al. Smoking as a risk factor for end-stage renal failure in men with primary renal disease. Kidney Int, 1998, 54(3): 926-931.
49. Christiansen JS. Cigarette smoking and prevalence of microangiopathy in juvenile-onset insulin-dependent diabetes mellitus. Diabetes Care, 1978, 1(3): 146-149.
50. Chuahirun T, Wesson DE. Cigarette smoking predicts faster progression of type 2 established diabetic nephropathy despite ACE inhibition. Am J Kidney Dis, 2002, 39(2): 376-382.
51. Han Qq, Wang Ss, Zhang Jl, et al. The association between cigarette smoking and diabetic nephropathy in Chinese male patients. Acta Diabetol, 2018, 55(11): 1131-1141.
52. Ramirez SPB, McClellan W, Port FK, et al. Risk factors for proteinuria in a large, multiracial, southeast Asian population. J Am Soc Nephrol, 2002, 13(7): 1907-1917.
53. Bonnet F, Deprele C, Sassolas A, et al. Excessive body weight as a new independent risk factor for clinical and pathological progression in primary IgA nephritis. Am J Kidney Dis, 2001, 37(4): 720-727.
54. Krzyżowska S, Matejko B, Kieć-Wilk B, et al. Assessment of selected food intake frequency in patients with type 1 diabetes treated with personal insulin pumps. Rocz Panstw Zakl Hig, 2019, 70(3): 259-265.
55. Pérez-Torres I, Roque P, El Hafidi M, et al. Association of renal damage and oxidative stress in a rat model of metabolic syndrome. Influence of gender. Free Radic Res, 2009, 43(8): 761-771.

West China Medical Journal

Gender and chronic kidney disease

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