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Influence of oophorectomy on glycemia and lipidogram1 1 Research performed at Laboratory of Experimental Surgery, Universidade do Estado do Pará (UEPA), Belem-PA, Brazil.

Abstract

Purpose:

To verify the influence of oophorectomy on lipidogram and glycemia.

Methods:

Fifty six female rats were divided into the following 7 groups (n = 8): group 1 - sham group, group 2 - oophorectomy 30 days, group 3 - oophorectomy 35 days, group 4 - oophorectomy 40 days, group 5 - oophorectomy 45 days, group 6 - oophorectomy 70 days, group 7 - oophorectomy 55 days. Animals were following by number of days according the group. Was evaluated the serum levels of glucose and lipid profile.

Results:

The oophorectomized rats presented higher glycemia. Groups 3, 4, 6 and 7 had a higher glycemia and LDL levels (except for group 6) and groups 6 and 7 had lowest levels of HDL. Group 7 had highest level of VLDL than oophorectomy groups. There was no difference in triglycerides levels.

Conclusion:

Oophorectomy was related to dyslipidemia and insulin resistance, mainly after 50th days.

Key words:
Ovariectomy; Climacteric; Dyslipidemias; Rats.

Introduction

Low incidence of cardiovascular diseases has been reported in women due to protective hormone effect11 Castanho VS, Nakamura RT, Pinto-Neto AM, Faria EC. Postmenopausal therapy reduces catalase activity and attenuates cardiovascular risk. Arq Bras Cardiol. 2012 Nov;99(5):1008-14. PMID: 23108643.

2 Versiani CM, Freire AC, Dias GMM, Brito BD, Rocha JSB, Reis VMCP. Evaluation of cardiovascular risk in climacteric women aided by Family Health Program. Rev Bras Clin Med São Paulo. 2013;11(4):1-5.
-33 Schierbeck LL, Rejnmark L, Tofteng CL, Stilgren L, Eiken P, Mosekilde L, Køber L, Jensen JB. Effect of hormone replacement therapy on cardiovascular events in recently postmenopausal women: randomised trial. BMJ. 2012 Oct;345:e6409. doi: 10.1136/bmj.e6409.
https://doi.org/10.1136/bmj.e6409...
. These illnesses are rare in the premenopausal period, because high levels of estrogen acts improving lipid profile by reducing cholesterolemy. After menopause, hormones promote an increase in weight11 Castanho VS, Nakamura RT, Pinto-Neto AM, Faria EC. Postmenopausal therapy reduces catalase activity and attenuates cardiovascular risk. Arq Bras Cardiol. 2012 Nov;99(5):1008-14. PMID: 23108643.,22 Versiani CM, Freire AC, Dias GMM, Brito BD, Rocha JSB, Reis VMCP. Evaluation of cardiovascular risk in climacteric women aided by Family Health Program. Rev Bras Clin Med São Paulo. 2013;11(4):1-5.,44 AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
https://doi.org/10.1155/2015/787063...
, high insulin resistance22 Versiani CM, Freire AC, Dias GMM, Brito BD, Rocha JSB, Reis VMCP. Evaluation of cardiovascular risk in climacteric women aided by Family Health Program. Rev Bras Clin Med São Paulo. 2013;11(4):1-5.

3 Schierbeck LL, Rejnmark L, Tofteng CL, Stilgren L, Eiken P, Mosekilde L, Køber L, Jensen JB. Effect of hormone replacement therapy on cardiovascular events in recently postmenopausal women: randomised trial. BMJ. 2012 Oct;345:e6409. doi: 10.1136/bmj.e6409.
https://doi.org/10.1136/bmj.e6409...

4 AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
https://doi.org/10.1155/2015/787063...
-55 Wang L, Szklo M, Folsom AR, Cook NR, Gapstur SM, Ouyang P. Endogenous sex hormones, blood pressure change, and risk of hypertension in postmenopausal women: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis. 2012 Sep;224(1):228-34. doi: 10.1016/j.atherosclerosis.2012.07.005.
https://doi.org/10.1016/j.atherosclerosi...
and high blood pressure11 Castanho VS, Nakamura RT, Pinto-Neto AM, Faria EC. Postmenopausal therapy reduces catalase activity and attenuates cardiovascular risk. Arq Bras Cardiol. 2012 Nov;99(5):1008-14. PMID: 23108643.,33 Schierbeck LL, Rejnmark L, Tofteng CL, Stilgren L, Eiken P, Mosekilde L, Køber L, Jensen JB. Effect of hormone replacement therapy on cardiovascular events in recently postmenopausal women: randomised trial. BMJ. 2012 Oct;345:e6409. doi: 10.1136/bmj.e6409.
https://doi.org/10.1136/bmj.e6409...

4 AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
https://doi.org/10.1155/2015/787063...
-55 Wang L, Szklo M, Folsom AR, Cook NR, Gapstur SM, Ouyang P. Endogenous sex hormones, blood pressure change, and risk of hypertension in postmenopausal women: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis. 2012 Sep;224(1):228-34. doi: 10.1016/j.atherosclerosis.2012.07.005.
https://doi.org/10.1016/j.atherosclerosi...
. In addition to lipidogram changes, leading to an atherogenic lipoprotein profile.

Cholesterol and triglycerides levels are influenced by several factors44 AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
https://doi.org/10.1155/2015/787063...
,66 Widén E, Silventoinen K, Sovio U, Ripatti S, Cousminer DL, Hartikainen AL, Laitinen J, Pouta A, Kaprio J, Järvelin MR, Peltonen L, Palotie A. Pubertal timing and growth influences cardiometabolic risk factors in adult males and females. Diabetes Care. 2012 Apr;35(4):850-6. doi:10.2337/dc11-1365.
https://doi.org/10.2337/dc11-1365...
,77 Petroianu A, Veloso DF, Alberti LR, Vasconcellos LS. Plasma lipid alterations after total splenectomy, subtotal splenectomy and splenic auto-implants in rats. J Gastroenterol Hepatol. 2008 Jul;23(7 Pt 2):e221-4. doi: 10.1111/j.1440-1746.2007.05263.x.
https://doi.org/10.1111/j.1440-1746.2007...
, such as: diet, life style, age, sex, changes in spleen e hormonal changes. The women’s lipid profile has a high influence of this hormonal change, since physiological fluctuations in menstrual cycle change the lipidogram and glycemia88 Kleiblová P, Springer D, Haluzík M. The influence of hormonal changes during menstrual cycle on serum adiponectin concentrations in healthy women. Physiol Res. 2006;55(6):661-6. PMID: 17177633.. Showing the importance of these sexual hormones. However, mechanisms underlying the influence of hormone in metabolism are controversial yet.

Human studies are being poorly feasible, so, experimental animal model can be used in medical testing to resemble events occurring among the human being as their genetic, biological and behavior characteristics mimic those of human99 Chakraborty C, Hsu CH, Wen ZH, Lin CS, Agoramoorthy G. Zebrafish: a complete animal model for in vivo drug discovery and development. Curr Drug Metab. 2009;10:116-24. PMID: 19275547.. Rodents are excellent experimental model of dyslipidemia, because they pass through hormonal fluctuations occurring in middle age, similar to those in women. However, rodents enter an estropause rather than a true menopause. Rodents show irregular acyclicity at middle age, after which, they enter a state of persistent estrus, with complete stoppage of reproductive cycles1010 Maffucci JA, Gore AC. Age-related changes in hormones and their receptors in animal models of female reproductive senescence. In: Conn MP, editor. In Handbook of models for human aging. San Diego: Academic Press and Elsevier; 2006. pp. 533-52.,1111 Frick KM. Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here? Horm Behav. 2008;55:2-23. doi: 10.1016/j.yhbeh.2008.08.015.
https://doi.org/10.1016/j.yhbeh.2008.08....
. Due the importance of risk factors caused by oophorectomy and your relationship with lipid profile and insulin resistance, this paper aims to verify the influence of oophorectomy on lipidogram and glycemia.

Methods

This research followed the rules of the Brazilian Law for Animal Care (Law: 11.794/08) and was approved by the Animal Use and Care Committee, Universidade do Estado do Para (protocol Nº 22/11).

Fifty-six Wistar female rats (Rattus norvegicus) were kept in a controlled environment, with food and water ad libitum. All animals had the same birth date, 90 days old at baseline and were randomly divided into the following seven groups (n = 8):

  • Group 1 - Sham - identification and manipulation of the ovaries without removing them.

  • Group 2 - Bilateral oophorectomy and followed during 30 days after surgery.

  • Group 3 - Bilateral oophorectomy and followed during 35 days after surgery.

  • Group 4 - Bilateral oophorectomy and followed during 40 days after surgery.

  • Group 5 - Bilateral oophorectomy and followed during 45 days after surgery.

  • Group 6 - Bilateral oophorectomy and followed during 50 days after surgery.

  • Group 7 - Bilateral oophorectomy and followed during 55 days after surgery.

All surgical procedures were performed in anesthesia (ketamine and xylazine 70 and 10 mg/kg, respectively, IP). The bilateral oophorectomy was performed similar to described by Brito et al.1212 Brito NMB, Carvalho RKV, Matos LTMB, Lobato RC, Brito RB. The oophorectomy effect on Walker 256 tumor inoculated into the vagina and uterine cervix of female rats. Acta Cir. Bras. 2009;24(1):26-9. PMID: 19169538.. At the end of the following period, 5ml of blood was collected from vena cava for glucose, cholesterol fractions and triglyceride studies, using colorimetric assay, using kits from Labtest®. The animals were killed under deep anesthesia by intravenous injection of KCl.

The software BioEstat© 5.4 was used. All data were expressed as means ±standard deviation. The serum levels of glucose and lipid profile were comparing by analysis of variance (ANOVA), followed by Tukey post hoc test correction when necessary. Statistical significance was assumed at p< 0.05.

Results

All animals survived during the study period. Table 1 presents the mean and standard error of mean glycemia and lipidograms of the 7 groups. Regarding the measurement of serum glucose, the groups 3, 4, 6 and 7 had a higher level than group 1 (p<0.01). With respect to total cholesterol, only the groups 2, 3 and 4 had a significant increase than group 1 (p<0.01).

Table 1
Mean levels of serum glucose, total cholesterol and fractions and triglycerides according groups.

By analyzing the cholesterol fractions, the groups 2 and 3 had increased and groups 6 and 7 had a reduction of HDL levels, comparing to group 1; already in relation to LDL, the group 7 show higher levels than group 1 (p=0.02). The group 7 had the highest levels of VLDL than other oophorectomy groups (p<0.01), however, its had similar levels than groups 1. There was no statistically significant difference in the analysis of serum triglycerides.

Discussion

The mechanism by which ovarian hormones affect the women’s physiology still not fully understood. However, the lack of these, due to ovarian failure (menopause) or surgical removal (oophorectomy) is associated with development of adverse conditions, such as: obesity44 AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
https://doi.org/10.1155/2015/787063...
,1313 Vasconcellos LS, Leite JM, Sabino KR, Petroianu A. Influence of oophorectomy on the weight variance in young and adult female rats. Arq Bras Endocrinol Metab. 2004;48(2):299-304. doi: /S0004-27302004000200014., diabetes44 AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
https://doi.org/10.1155/2015/787063...
,55 Wang L, Szklo M, Folsom AR, Cook NR, Gapstur SM, Ouyang P. Endogenous sex hormones, blood pressure change, and risk of hypertension in postmenopausal women: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis. 2012 Sep;224(1):228-34. doi: 10.1016/j.atherosclerosis.2012.07.005.
https://doi.org/10.1016/j.atherosclerosi...
and dyslipidemia44 AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
https://doi.org/10.1155/2015/787063...
,55 Wang L, Szklo M, Folsom AR, Cook NR, Gapstur SM, Ouyang P. Endogenous sex hormones, blood pressure change, and risk of hypertension in postmenopausal women: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis. 2012 Sep;224(1):228-34. doi: 10.1016/j.atherosclerosis.2012.07.005.
https://doi.org/10.1016/j.atherosclerosi...
. Possibly these changes are linked to estrogen action, once the replacement of only estrogen in menopause rats and humans decrease the plasma cholesterol levels and glycemia1414 Lundeen SG, Carver JM, McKean ML, Winneker RC. Characterization of the ovariectomized rat model for the evaluation of estrogen effects on plasma cholesterol levels. Endocrinology. 1997 Apr;138(4):1552-8. doi: 10.1210/endo.138.4.5083.
https://doi.org/10.1210/endo.138.4.5083...
,1515 Faulds MH, Zhao C, Dahlman-Wright K, Gustafsson JÅ. The diversity of sex steroid action: regulation of metabolism by estrogen signaling. J Endocrinol. 2012 Jan;212(1):3-12. doi: 10.1530/JOE-11-0044.
https://doi.org/10.1530/JOE-11-0044...
.

We initiated these studies to characterize the better time to evaluation the lipidogram and glycemia levels in oophorectomized rats, since this time is not well defined. Cholesterol total was maintained at similar levels in all groups (p>0.05), however, its fractions showed a decrease of HDL and increase of LDL and VLDL, mainly from the group 6 (50 days). Well-known that after oophorectomy, sex hormones circulate in the body at a high level for 21-30 days1111 Frick KM. Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here? Horm Behav. 2008;55:2-23. doi: 10.1016/j.yhbeh.2008.08.015.
https://doi.org/10.1016/j.yhbeh.2008.08....
,1212 Brito NMB, Carvalho RKV, Matos LTMB, Lobato RC, Brito RB. The oophorectomy effect on Walker 256 tumor inoculated into the vagina and uterine cervix of female rats. Acta Cir. Bras. 2009;24(1):26-9. PMID: 19169538.. Therefore, groups 2 to 5 were in adaptation to new condition of hormonal suppression, explaining fluctuations of serum levels identified in this period (30-45 days). Thus, studies evaluating these parameters at this time may be harmed.

In more than sixty days follow-up of oophorectomized rats1616 Hassan HA, Abdel-Wahhab MA. Effect of soybean oil on atherogenic metabolic risks associated with estrogen deficiency in ovariectomized rats: dietary soybean oil modulate atherogenic risks in overiectomized rats. J Physiol Biochem. 2012 Jun;68(2):247-53. doi: 10.1007/s13105-011-0137-8.
https://doi.org/10.1007/s13105-011-0137-...

17 Behr GA, Schnorr CE, Moreira JC. Increased blood oxidative stress in experimental menopause rat model: the effects of vitamin A low-dose supplementation upon antioxidant status in bilateral ovariectomized rats. Fundam Clin Pharmacol. 2012 Apr;26(2):235-49. doi: 10.1111/j.1472-8206.2010.00923.x.
https://doi.org/10.1111/j.1472-8206.2010...
-1818 Henriques HN, Câmara NR, de Carvalho AC, Pantaleão JA, Guzmán-Silva MA. Effect of high doses of tibolone in body weight and lipid profile of ovariectomized rats. Rev Bras Ginecol Obstet. 2010 Feb;32(2):88-93. PMID: 20305947., studies show similar levels of plasma cholesterol and glucose than groups 6 and 7. These findings strengthen the possibility that it is necessary at least fifty days for adaptation to hormonal suppression.

Triglycerides have a close relationship with diet and energy consumption, however is slightly influenced by sexual hormones. Vasconcellos et al.1313 Vasconcellos LS, Leite JM, Sabino KR, Petroianu A. Influence of oophorectomy on the weight variance in young and adult female rats. Arq Bras Endocrinol Metab. 2004;48(2):299-304. doi: /S0004-27302004000200014. reported that oophorectomy does not imply changes in dietary habits on female rats. Some studies that show increase of triglycerides have a bigger follow-up than this study and probably the obesity, associate to oophorectomy, influence the serum levels.

Menopause is associated with an increased risk of development of diabetes1919 Hoogeveen EK, Kostense PJ, Beks PJ, Mackaay AJ, Jakobs C, Bouter LM, Heine RJ, Stehouwer CD. Hyperhomocysteinemia is associated with an increased risk of cardiovascular disease, especially in non-insulin-dependent diabetes mellitus: a population-based study. Arterioscler Thromb Vasc Biol. 1998 Jan;18(1):133-8. PMID: 9445267., related to increase of insulin resistance caused by estrogen depletion. The glycemia, as plasma cholesterol levels, shows fluctuations of serum levels (groups 2 to 5) before the fifty days of post-operation; strengthen the hypothesis of adaptation to hormonal suppression. This hormonal influence is important to be highlighted, because after menopause other risk factors involved in insulin resistance happen44 AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
https://doi.org/10.1155/2015/787063...
,55 Wang L, Szklo M, Folsom AR, Cook NR, Gapstur SM, Ouyang P. Endogenous sex hormones, blood pressure change, and risk of hypertension in postmenopausal women: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis. 2012 Sep;224(1):228-34. doi: 10.1016/j.atherosclerosis.2012.07.005.
https://doi.org/10.1016/j.atherosclerosi...
,1919 Hoogeveen EK, Kostense PJ, Beks PJ, Mackaay AJ, Jakobs C, Bouter LM, Heine RJ, Stehouwer CD. Hyperhomocysteinemia is associated with an increased risk of cardiovascular disease, especially in non-insulin-dependent diabetes mellitus: a population-based study. Arterioscler Thromb Vasc Biol. 1998 Jan;18(1):133-8. PMID: 9445267., such as obesity and muscle loss.

The data from this study favors the early use of hormone replacement in women, since the earlier they are used, the lower the metabolic changes suffered by women and the less the side effects they may present. However, more studies are needed to confirm these promising findings.

We limited to study the effects of oophorectomy on rats in lipidogram and glycemia in the first days of post-operative, to understand better the physiology. Meanwhile, it is necessary more studies evaluation the liver metabolism to confirm these findings and with a longer follow-up, correlated with weight of the animals.

Conclusion

Oophorectomy was related to dyslipidemia and insulin resistance, mainly after 50th days.

References

  • 1
    Castanho VS, Nakamura RT, Pinto-Neto AM, Faria EC. Postmenopausal therapy reduces catalase activity and attenuates cardiovascular risk. Arq Bras Cardiol. 2012 Nov;99(5):1008-14. PMID: 23108643.
  • 2
    Versiani CM, Freire AC, Dias GMM, Brito BD, Rocha JSB, Reis VMCP. Evaluation of cardiovascular risk in climacteric women aided by Family Health Program. Rev Bras Clin Med São Paulo. 2013;11(4):1-5.
  • 3
    Schierbeck LL, Rejnmark L, Tofteng CL, Stilgren L, Eiken P, Mosekilde L, Køber L, Jensen JB. Effect of hormone replacement therapy on cardiovascular events in recently postmenopausal women: randomised trial. BMJ. 2012 Oct;345:e6409. doi: 10.1136/bmj.e6409.
    » https://doi.org/10.1136/bmj.e6409
  • 4
    AnikóP, RenátaS, Krisztinak, Csonka A, Szalai Z, Veszelka M, Török S, Daruka L, Varga C. Exercise training and calorie restriction influence the metabolic parameters in ovariectomized female rats. Oxid Med Cell Longev. 2015; 2015:787063. doi: 10.1155/2015/787063.
    » https://doi.org/10.1155/2015/787063
  • 5
    Wang L, Szklo M, Folsom AR, Cook NR, Gapstur SM, Ouyang P. Endogenous sex hormones, blood pressure change, and risk of hypertension in postmenopausal women: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis. 2012 Sep;224(1):228-34. doi: 10.1016/j.atherosclerosis.2012.07.005.
    » https://doi.org/10.1016/j.atherosclerosis.2012.07.005
  • 6
    Widén E, Silventoinen K, Sovio U, Ripatti S, Cousminer DL, Hartikainen AL, Laitinen J, Pouta A, Kaprio J, Järvelin MR, Peltonen L, Palotie A. Pubertal timing and growth influences cardiometabolic risk factors in adult males and females. Diabetes Care. 2012 Apr;35(4):850-6. doi:10.2337/dc11-1365.
    » https://doi.org/10.2337/dc11-1365
  • 7
    Petroianu A, Veloso DF, Alberti LR, Vasconcellos LS. Plasma lipid alterations after total splenectomy, subtotal splenectomy and splenic auto-implants in rats. J Gastroenterol Hepatol. 2008 Jul;23(7 Pt 2):e221-4. doi: 10.1111/j.1440-1746.2007.05263.x.
    » https://doi.org/10.1111/j.1440-1746.2007.05263.x
  • 8
    Kleiblová P, Springer D, Haluzík M. The influence of hormonal changes during menstrual cycle on serum adiponectin concentrations in healthy women. Physiol Res. 2006;55(6):661-6. PMID: 17177633.
  • 9
    Chakraborty C, Hsu CH, Wen ZH, Lin CS, Agoramoorthy G. Zebrafish: a complete animal model for in vivo drug discovery and development. Curr Drug Metab. 2009;10:116-24. PMID: 19275547.
  • 10
    Maffucci JA, Gore AC. Age-related changes in hormones and their receptors in animal models of female reproductive senescence. In: Conn MP, editor. In Handbook of models for human aging. San Diego: Academic Press and Elsevier; 2006. pp. 533-52.
  • 11
    Frick KM. Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here? Horm Behav. 2008;55:2-23. doi: 10.1016/j.yhbeh.2008.08.015.
    » https://doi.org/10.1016/j.yhbeh.2008.08.015
  • 12
    Brito NMB, Carvalho RKV, Matos LTMB, Lobato RC, Brito RB. The oophorectomy effect on Walker 256 tumor inoculated into the vagina and uterine cervix of female rats. Acta Cir. Bras. 2009;24(1):26-9. PMID: 19169538.
  • 13
    Vasconcellos LS, Leite JM, Sabino KR, Petroianu A. Influence of oophorectomy on the weight variance in young and adult female rats. Arq Bras Endocrinol Metab. 2004;48(2):299-304. doi: /S0004-27302004000200014.
  • 14
    Lundeen SG, Carver JM, McKean ML, Winneker RC. Characterization of the ovariectomized rat model for the evaluation of estrogen effects on plasma cholesterol levels. Endocrinology. 1997 Apr;138(4):1552-8. doi: 10.1210/endo.138.4.5083.
    » https://doi.org/10.1210/endo.138.4.5083
  • 15
    Faulds MH, Zhao C, Dahlman-Wright K, Gustafsson JÅ. The diversity of sex steroid action: regulation of metabolism by estrogen signaling. J Endocrinol. 2012 Jan;212(1):3-12. doi: 10.1530/JOE-11-0044.
    » https://doi.org/10.1530/JOE-11-0044
  • 16
    Hassan HA, Abdel-Wahhab MA. Effect of soybean oil on atherogenic metabolic risks associated with estrogen deficiency in ovariectomized rats: dietary soybean oil modulate atherogenic risks in overiectomized rats. J Physiol Biochem. 2012 Jun;68(2):247-53. doi: 10.1007/s13105-011-0137-8.
    » https://doi.org/10.1007/s13105-011-0137-8
  • 17
    Behr GA, Schnorr CE, Moreira JC. Increased blood oxidative stress in experimental menopause rat model: the effects of vitamin A low-dose supplementation upon antioxidant status in bilateral ovariectomized rats. Fundam Clin Pharmacol. 2012 Apr;26(2):235-49. doi: 10.1111/j.1472-8206.2010.00923.x.
    » https://doi.org/10.1111/j.1472-8206.2010.00923.x
  • 18
    Henriques HN, Câmara NR, de Carvalho AC, Pantaleão JA, Guzmán-Silva MA. Effect of high doses of tibolone in body weight and lipid profile of ovariectomized rats. Rev Bras Ginecol Obstet. 2010 Feb;32(2):88-93. PMID: 20305947.
  • 19
    Hoogeveen EK, Kostense PJ, Beks PJ, Mackaay AJ, Jakobs C, Bouter LM, Heine RJ, Stehouwer CD. Hyperhomocysteinemia is associated with an increased risk of cardiovascular disease, especially in non-insulin-dependent diabetes mellitus: a population-based study. Arterioscler Thromb Vasc Biol. 1998 Jan;18(1):133-8. PMID: 9445267.
  • Financial source:

    none
  • 1
    Research performed at Laboratory of Experimental Surgery, Universidade do Estado do Pará (UEPA), Belem-PA, Brazil.

Publication Dates

  • Publication in this collection
    May 2018

History

  • Received
    26 Jan 2018
  • Reviewed
    27 May 2018
  • Accepted
    25 Apr 2018
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