Aldosterone-progesterone relationship in sexually intact Chihuahua bitches.
Aldosterone
Dog
MMVD
Progesterone
RAAS
Sex
Journal
BMC veterinary research
ISSN: 1746-6148
Titre abrégé: BMC Vet Res
Pays: England
ID NLM: 101249759
Informations de publication
Date de publication:
05 Sep 2023
05 Sep 2023
Historique:
received:
18
11
2022
accepted:
24
08
2023
medline:
7
9
2023
pubmed:
6
9
2023
entrez:
5
9
2023
Statut:
epublish
Résumé
Aldosterone represents an important target of heart failure therapy and may be a valuable indicator of the renin-angiotensin-aldosterone system activity. However, its assessment might be challenging because of the effect of individual factors. In a recent study, intact female dogs showed the highest value of urinary aldosterone-to-creatinine ratio (UAldo:C) compared to other sex categories. In humans and rodents, an influence of progesterone has been reported by several studies. To our knowledge, the relationship between aldosterone and progesterone has not yet been investigated in dogs. The aim of this prospective study was to investigate this relationship in sexually intact Chihuahua females, measuring both hormones twice in the same bitch, that is in anoestrus when progesterone concentrations are baseline and in dioestrus when they are high. The study population consisted of 14 sexually intact Chihuahua bitches. Serum progesterone (34.06 (21.17-44.90) vs. 0.19 [0.13-0.38] ng/ml; P < 0.001) and urinary aldosterone (9886.98 ± 5735.22 vs. 5005.72 ± 2127.73 pg/ml; P = 0.01) were significantly higher in dioestrus compared to anoestrous. Urinary aldosterone-to-creatinine ratio was higher in dioestrus compared to anoestrus (4.16 [3.17-6.80] vs. 3.39 ± 1.64 µg/g), but it did not reach the statistical significance (P = 0.056). Serum progesterone showed a moderate positive correlation with urinary aldosterone (ρ = 0.638, P < 0.001) and UAldo:C (ρ = 0.516, P = 0.005). The results of the present study suggest the existence of a progesterone-aldosterone relationship in canine species, indicating that sex and phase of reproductive cycle should be taken into account when interpreting aldosterone concentrations. Further studies are needed to confirm these results on a larger canine population and to identify the underlying mechanisms in this species.
Sections du résumé
BACKGROUND
BACKGROUND
Aldosterone represents an important target of heart failure therapy and may be a valuable indicator of the renin-angiotensin-aldosterone system activity. However, its assessment might be challenging because of the effect of individual factors. In a recent study, intact female dogs showed the highest value of urinary aldosterone-to-creatinine ratio (UAldo:C) compared to other sex categories. In humans and rodents, an influence of progesterone has been reported by several studies. To our knowledge, the relationship between aldosterone and progesterone has not yet been investigated in dogs. The aim of this prospective study was to investigate this relationship in sexually intact Chihuahua females, measuring both hormones twice in the same bitch, that is in anoestrus when progesterone concentrations are baseline and in dioestrus when they are high.
RESULTS
RESULTS
The study population consisted of 14 sexually intact Chihuahua bitches. Serum progesterone (34.06 (21.17-44.90) vs. 0.19 [0.13-0.38] ng/ml; P < 0.001) and urinary aldosterone (9886.98 ± 5735.22 vs. 5005.72 ± 2127.73 pg/ml; P = 0.01) were significantly higher in dioestrus compared to anoestrous. Urinary aldosterone-to-creatinine ratio was higher in dioestrus compared to anoestrus (4.16 [3.17-6.80] vs. 3.39 ± 1.64 µg/g), but it did not reach the statistical significance (P = 0.056). Serum progesterone showed a moderate positive correlation with urinary aldosterone (ρ = 0.638, P < 0.001) and UAldo:C (ρ = 0.516, P = 0.005).
CONCLUSIONS
CONCLUSIONS
The results of the present study suggest the existence of a progesterone-aldosterone relationship in canine species, indicating that sex and phase of reproductive cycle should be taken into account when interpreting aldosterone concentrations. Further studies are needed to confirm these results on a larger canine population and to identify the underlying mechanisms in this species.
Identifiants
pubmed: 37670293
doi: 10.1186/s12917-023-03704-2
pii: 10.1186/s12917-023-03704-2
pmc: PMC10478304
doi:
Substances chimiques
Aldosterone
4964P6T9RB
Progesterone
4G7DS2Q64Y
Creatinine
AYI8EX34EU
Diuretics
0
Anti-Arrhythmia Agents
0
Cardiotonic Agents
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
144Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Ames MK, Atkins CE, Pitt B. The renin-angiotensin-aldosterone system and its suppression. J Vet Intern Med. 2019;1–20.
Sisson DD. Neuroendocrine evaluation of cardiac disease. Vet Clin Small Anim. 2004;34:1105–26.
doi: 10.1016/j.cvsm.2004.05.005
Struthers AD, MacDonald TM. Review of aldosterone- and angiotensin II-induced target organ damage and prevention. Cardiovasc Res. 2004;61:663–70.
pubmed: 14985063
doi: 10.1016/j.cardiores.2003.11.037
Leopold JA. Aldosterone, mineralocorticoid receptor activation, and cardiovascular remodeling. Circulation. 2011;124:e466–8.
pubmed: 22042931
pmcid: 3684970
doi: 10.1161/CIRCULATIONAHA.111.067918
Hezzell MJ, Boswood A, Chang YM, et al. Associations among serum N-terminal procollagen type III concentration, urinary aldosterone-to-creatinine ratio, and ventricular remodeling in dogs with myxomatous mitral valve disease. Am J Vet Res. 2012;73:1765–74.
pubmed: 23106462
doi: 10.2460/ajvr.73.11.1765
Bernay F, Bland JM, Häggström J, et al. Efficacy of spironolactone on survival in dogs with naturally occurring mitral regurgitation caused by myxomatous mitral valve disease. J Vet Intern Med. 2010;24:331–41.
pubmed: 20102506
doi: 10.1111/j.1939-1676.2009.0467.x
Ames MK, Atkins CE, Eriksson A, et al. Aldosterone breakthrough in dogs with naturally occurring myxomatous mitral valve disease. J Vet Cardiol. 2017;19:218–27.
pubmed: 28576479
doi: 10.1016/j.jvc.2017.03.001
Adin D, Atkins C, Domenig O, et al. Renin-angiotensin aldosterone profile before and after angiotensin-converting enzyme-inhibitor administration in dogs with angiotensin-converting enzyme gene polymorphism. J Vet Intern Med. 2020;34:600–6.
pubmed: 32112596
pmcid: 7097578
doi: 10.1111/jvim.15746
Galizzi A, Bagardi M, Stranieri A, et al. Factors affecting the urinary aldosterone-to-creatinine ratio in healthy dogs and dogs with naturally occurring myxomatous mitral valve disease. BMC Vet Res. 2021;17(1):15.
pubmed: 33413406
pmcid: 7792040
doi: 10.1186/s12917-020-02716-6
Meurs KM, Stern JA, Atkins CE, et al. Angiotensin-converting enzyme activity and inhibition in dogs with cardiac disease and an angiotensin-converting enzyme polymorphism. J Renin Angiotensin Aldosterone Syst. 2017;18:1470320317737184.
pubmed: 29069972
pmcid: 5843865
doi: 10.1177/1470320317737184
Szmuilowicz ED, Adler GK, Williams JS, et al. Relationship between aldosterone and progesterone in the human menstrual cycle. J Clin Endocrinol Metab. 2006;91:3981–7.
pubmed: 16868049
doi: 10.1210/jc.2006-1154
Hirshoren N, Tzoran I, Makrienko I, et al. Menstrual cycle effects on the neurohumoral and autonomic nervous systems regulating the cardiovascular system. J Clin Endocrinol Metab. 2002;87:1569–75.
pubmed: 11932284
doi: 10.1210/jcem.87.4.8406
Baker ME, Katsu Y, Progesterone. An enigmatic ligand for the mineralocorticoid receptor. Biochem Pharmacol. 2020;177:113976.
pubmed: 32305433
doi: 10.1016/j.bcp.2020.113976
Braley LM, Menachery AI, Yao T, et al. Effect of progesterone on aldosterone secretion in rats. Endocrinology. 1996;137:4773–8.
pubmed: 8895346
doi: 10.1210/endo.137.11.8895346
Robb CA, Davis JO, Johnson JA, et al. Mechanisms regulating the renal excretion of sodium during pregnancy. J Clin Invest. 1970;49(5):871–80.
pubmed: 5441541
pmcid: 535759
doi: 10.1172/JCI106306
Milani C, Rota A, Olsson U, et al. Serum concentration of mineralocorticoids, glucocorticoids, and sex steroids in peripartum bitches. Domest Anim Endocrinol. 2021;74:106558.
pubmed: 32980594
doi: 10.1016/j.domaniend.2020.106558
Concannon PW. Reproductive cycles of the domestic bitch. Anim Reprod Sci. 2011;124(3–4):200–10.
pubmed: 21055888
doi: 10.1016/j.anireprosci.2010.08.028
Ahmed AH, Gordon RD, Ward G, et al. Should aldosterone suppression tests be conducted during a particular phase of the menstrual cycle, and, if so, which phase? Results of a preliminary study. Clin Endocrinol (Oxf). 2015;83(3):303–7.
pubmed: 25523596
doi: 10.1111/cen.12705
Sundsfjord JA, Aakvaag A. Plasma renin activity, plasma renin substrate and urinary aldosterone excretion in the menstrual cycle in relation to the concentration of progesterone and oestrogens in the plasma. Acta Endocrinol (Copenh). 1972;71(3):519–29.
pubmed: 4343780
Michelakis AM, Yoshida H, Dormois JC. Plasma renin activity and plasma aldosterone during the normal menstrual cycle. Am J Obstet Gynecol. 1975;123(7):724–6.
pubmed: 1200065
doi: 10.1016/0002-9378(75)90495-0
Wambach G, Higgins JR. Antimineralocorticoid action of progesterone in the rat: correlation of the effect on electrolyte excretion and interaction with renal mineralocorticoid receptors. Endocrinology. 1978;102(6):1686–93.
pubmed: 217633
doi: 10.1210/endo-102-6-1686
Landau RL, Lugibihl K. Inhibition of the sodium-retaining influence of aldosterone by progesterone. J Clin Endocrinol Metab. 1958;18(11):1237–45.
pubmed: 13587641
doi: 10.1210/jcem-18-11-1237
Myles K, Funder JW. Progesterone binding to mineralocorticoid receptors: in vitro and in vivo studies. Am J Physiol. 1996;270(4 Pt 1):E601–607.
pubmed: 8928765
Oelkers WK. Effects of estrogens and progestogens on the renin-aldosterone system and blood pressure. Steroids. 1996;61(4):166–71.
pubmed: 8732994
doi: 10.1016/0039-128X(96)00007-4
Katz FH, Romfh P. Plasma aldosterone and renin activity during the menstrual cycle. J Clin Endocrinol Metab. 1972;34(5):819–21.
pubmed: 5012493
doi: 10.1210/jcem-34-5-819
De Cramer KGM, Nöthling JO. The precision of predicting the time of onset of parturition in the bitch using the level of progesterone in plasma during the preparturient period. Theriogenology. 2018;107:211–18.
pubmed: 29175732
doi: 10.1016/j.theriogenology.2017.11.018
Nicolini G, Balzan S, Morelli L, et al. LH, progesterone, and TSH can stimulate aldosterone in vitro: a study on normal adrenal cortex and aldosterone producing adenoma. Horm Metab Res. 2014;46(5):318–21.
pubmed: 24297486
Uotinen N, Puustinen R, Pasanen S, et al. Distribution of progesterone receptor in female mouse tissues. Gen Comp Endocrinol. 1999;115(3):429–41.
pubmed: 10480995
doi: 10.1006/gcen.1999.7333
Burwell LR, Davis WW, Bartter FC. Studies on the loci of action of stimuli to the biogenesis of aldosterone. Proc R Soc Med. 1969;62(12):1254–7.
pubmed: 4312098
pmcid: 1815457
Herrera AY, Nielsen SE, Mather M. Stress-induced increases in progesterone and cortisol in naturally cycling women. Neurobiol Stress. 2016;3:96–104.
pubmed: 27981182
pmcid: 5146195
doi: 10.1016/j.ynstr.2016.02.006
Vecchiola A, Lagos CF, Fuentes CA, et al. Different effects of progesterone and estradiol on chimeric and wild type aldosterone synthase in vitro. Reprod Biol Endocrinol. 2013;11:76.
pubmed: 23938178
pmcid: 3848474
doi: 10.1186/1477-7827-11-76
Funder JW. Aldosterone and Mineralocorticoid Receptors—Physiology and pathophysiology. Int J Mol Sci. 2017;18(5):1032.
pubmed: 28492512
pmcid: 5454944
doi: 10.3390/ijms18051032
Katsu Y, Oka K, Baker ME. Evolution of human, chicken, alligator, frog, and zebrafish mineralocorticoid receptors: allosteric influence on steroid specificity. Sci Signal. 2018;11(537):eaao1520.
pubmed: 29970600
doi: 10.1126/scisignal.aao1520
Geller DS, Farhi A, Pinkerton N, et al. Activating mineralocorticoid receptor mutation in hypertension exacerbated by pregnancy. Science. 2000;289(5476):119–23.
pubmed: 10884226
doi: 10.1126/science.289.5476.119
Johnson JA, Davis JO, Baumber JS, et al. Effects of estrogens and progesterone on electrolyte balances in normal dogs. Am J Physiol. 1970;219(6):1691–7.
pubmed: 5485687
doi: 10.1152/ajplegacy.1970.219.6.1691
Adin DB, Atkins CE, Friedenberg SG, et al. Prevalence of an angiotensin-converting enzyme gene variant in dogs. Canine Med Genet. 2021;8(1):6.
pubmed: 34256860
pmcid: 8276509
doi: 10.1186/s40575-021-00105-2
Gardner SY, Atkins CE, Rausch WP, et al. Estimation of 24-h aldosterone secretion in the dog using the urine aldosterone:creatinine ratio. J Vet Cardiol. 2007;9(1):1–7.
pubmed: 17689463
doi: 10.1016/j.jvc.2006.11.001
Waikar SS, Sabbisetti VS, Bonventre JV. Normalization of urinary biomarkers to creatinine during changes in glomerular filtration rate. Kidney Int. 2010;78(5):486–94.
pubmed: 20555318
pmcid: 3025699
doi: 10.1038/ki.2010.165
Lee G, Kim S, Park H, et al. Variability of urinary creatinine, specific gravity, and osmolality over the course of pregnancy: implications in exposure assessment among pregnant women. Environ Res. 2021;198:110473.
pubmed: 33189745
doi: 10.1016/j.envres.2020.110473
Phipps WR, Duncan AM, Merz BE, et al. Effect of the menstrual cycle on creatinine clearance in normally cycling women. Obstet Gynecol. 1998;92(4 Pt 1):585–8.
pubmed: 9764633
Cheung KL, Lafayette RA. Renal physiology of pregnancy. Adv Chronic Kidney Dis. 2013;20(3):209–14.
pubmed: 23928384
pmcid: 4089195
doi: 10.1053/j.ackd.2013.01.012
Odutayo A, Hladunewich M. Obstetric nephrology: renal hemodynamic and metabolic physiology in normal pregnancy. Clin J Am Soc Nephrol. 2012;7(12):2073–80.
pubmed: 22879432
doi: 10.2215/CJN.00470112
Wolf J, Gerlach N, Weber K, et al. The diagnostic relevance of NT-proBNP and proANP 31–67 measurements in staging of myxomatous mitral valve disease in dogs. Vet Clin Pathol. 2013;42(2):196–206.
pubmed: 23614733
doi: 10.1111/vcp.12044
Misbach C, Chetboul V, Concordet D, et al. Basal plasma concentrations of N-terminal pro-B-type natriuretic peptide in clinically healthy adult small size dogs: effect of body weight, age, gender and breed, and reference intervals. Res Vet Sci. 2013;95(3):879–85.
pubmed: 23993661
doi: 10.1016/j.rvsc.2013.07.025
Chang AY, Abdullah SM, Jain T, et al. Associations among androgens, estrogens, and natriuretic peptides in young women: observations from the Dallas Heart Study. J Am Coll Cardiol. 2007;49(1):109–16.
pubmed: 17207730
doi: 10.1016/j.jacc.2006.10.040
Fragopoulu E, Panagiotakos DB, Pitsavos C, et al. N-terminal ProBNP distribution and correlations with biological characteristics in apparently healthy greek population: ATTICA study. Angiology. 2010;61(4):397–404.
doi: 10.1177/0003319709350134
Redfield MM, Rodeheffer RJ, Jacobsen SJ, et al. Plasma brain natriuretic peptide concentration: impact of age and gender. J Am Coll Cardiol. 2002;40(5):976–82.
pubmed: 12225726
doi: 10.1016/S0735-1097(02)02059-4
Loke I, Squire IB, Davies JE, et al. Reference ranges for natriuretic peptides for diagnostic use are dependenton age, gender and heart rate. Eur J Heart Fail. 2003;5(5):599–606.
pubmed: 14607197
doi: 10.1016/S1388-9842(03)00108-9
Sutton TM, Stewart RAH, Gerber IL, et al. Plasma natriuretic peptide levels increase with symptoms and severity of mitral regurgitation. J Am Coll Cardiol. 2003;41(12):2280–7.
pubmed: 12821260
doi: 10.1016/S0735-1097(03)00486-8
Lam CSP, Cheng S, Choong K, et al. Influence of sex and hormone status on circulating natriuretic peptides. J Am Coll Cardiol. 2011;58(6):618–26.
pubmed: 21798425
pmcid: 3170816
doi: 10.1016/j.jacc.2011.03.042
Hong M, Yan Q, Tao B, et al. Estradiol, progesterone and testosterone exposures affect the atrial natriuretic peptide gene expression in vivo in rats. Biol Chem Hoppe Seyler. 1992;373(4):213–8.
pubmed: 1534483
doi: 10.1515/bchm3.1992.373.1.213
Maffei S, Del Ry S, Prontera C, et al. Increase in circulating levels of cardiac natriuretic peptides after hormone replacement therapy in postmenopausal women. Clin Sci (Lond). 2001;101(5):447–53.
pubmed: 11672449
doi: 10.1042/cs1010447
Deng Y, Kaufman S. The influence of reproductive hormones on ANF release by rat atria. Life Sci. 1993;53(9):689–96.
pubmed: 8355570
doi: 10.1016/0024-3205(93)90245-X
Maffei S, Clerico A, Iervasi G, et al. Circulating levels of cardiac natriuretic hormones measured in women during menstrual cycle. J Endocrinol Invest. 1999;22(1):1–5.
pubmed: 10090129
doi: 10.1007/BF03345470
Yeko TR, Rao PS, Parsons AK, et al. Atrial natriuretic peptide, oestradiol and progesterone in women undergoing spontaneous and gonadotrophin-stimulated ovulatory cycles. Hum Reprod. 1995;10(11):2872–4.
pubmed: 8747035
doi: 10.1093/oxfordjournals.humrep.a135810
Jensen LK, Svanegaard J, Husby H. Atrial natriuretic peptide during the menstrual cycle. Am J Obstet Gynecol. 1989;161(4):951–2.
pubmed: 2529771
doi: 10.1016/0002-9378(89)90760-6
Ames MK, Atkins CE, Lee S, et al. Effects of high doses of enalapril and benazepril on the pharmacologically activated renin-angiotensin-aldosterone system in clinically normal dogs. Am J Vet Res. 2015;76(12):1041–50.
pubmed: 26618728
doi: 10.2460/ajvr.76.12.1041
Sallsten G, Barregard L. Variability of urinary creatinine in healthy individuals. Int J Environ Res Public Health. 2021;18(6):3166.
pubmed: 33808539
pmcid: 8003281
doi: 10.3390/ijerph18063166
Mochel JP, Fink M, Peyrou M, et al. Chronobiology of the renin-angiotensin-aldosterone system in dogs: relation to blood pressure and renal physiology. Chronobiol Int. 2013;30(9):1144–59.
pubmed: 23931032
doi: 10.3109/07420528.2013.807275
Kenee BW, Atkins CE, Bonagura JD, et al. ACVIM consensus guidelines for the diagnosis and treatment of myxomatous mitral valve disease in dogs. J Vet Intern Med. 2019;33:1127–40.
doi: 10.1111/jvim.15488
Acierno MJ, Brown S, Coleman AE, et al. ACVIM consensus statement: guidelines for the identification, evaluation, and management of systemic hypertension in dogs and cats. J Vet Intern Med. 2018;32:1803–22.
pubmed: 30353952
pmcid: 6271319
doi: 10.1111/jvim.15331
Thomas WP, Gaber CE, Jacobs GJ, et al. Recommendations for standards in transthoracic two-dimensional echocardiography in the dog and cat. Echocardiography committee of the specialty of cardiology, american college of veterinary internal medicine. J Vet Intern Med. 1993;7:247–52.
pubmed: 8246215
doi: 10.1111/j.1939-1676.1993.tb01015.x
IRIS Canine GN Study Group Standard Therapy Subgroup, Brown S, Elliott J, Francey T, et al. Consensus recommendations for standard therapy of glomerular disease in dogs. J Vet Intern Med. 2013;27:27–S43.
doi: 10.1111/jvim.12230
Brugger N, Otzdorff C, Walter B, et al. Quantitative determination of progesterone (P4) in canine blood serum using an enzyme-linked fluorescence assay. Reprod Domest Anim. 2011;46(5):870–3.
pubmed: 21323757
doi: 10.1111/j.1439-0531.2011.01757.x