Ovarian Cycle and Sympathoexcitation in Premenopausal Women
Open accessAbstract
The influence of the ovarian cycle on muscle sympathetic nerve activity (MSNA) remains controversial. Some studies report an increase of resting MSNA during the mid luteal (ML) phase of the ovarian cycle compared with the early follicular phase, whereas other studies do not. These inconsistent findings may be attributable, in part, to the variable surges in estradiol and progesterone. We tested the hypothesis that the degree of sympathoexcitation during the ML phase (ΔMSNA) is associated with changes in estradiol (ΔE(2)) and progesterone (ΔP). Multiple regression analysis of data from previous studies with complete recordings of mean arterial pressure, MSNA, E(2), and P during both early follicular and ML phases were available from 30 eumenorrheic women (age, 28 ± 1 years; body mass index, 23 ± 0 kg/m(2)). ML phase increased E(2) (37 ± 2 to 117 ± 9 pg/mL; P<0.001), P (1 ± 0 to 11 ± 1 ng/mL; P<0.001), and MSNA (12 ± 1 to 15 ± 1 bursts/min; P=0.02), but did not alter mean arterial pressure (83 ± 2 to 83 ± 2 mm Hg; P=0.91). ΔMSNA was correlated with ΔE(2) (r=-0.50, P=0.003) and ΔE(2)/ΔP (r=-0.52, P=0.002) but not ΔP (r=0.21, P=0.13). There was no association between Δmean arterial pressure and ΔE(2) (r=-0.13, P=0.49), ΔP (r=-0.04, P=0.83), or ΔE(2)/ΔP (r<0.01, P=0.98). In conclusion, sympathoexcitation during the ML phase of the ovarian cycle seems to be dependent, in part, on the degree of sex steroid surges. This dynamic interaction among E(2), P, and MSNA likely explains previously reported inconsistencies in the field; it remains possible that other sex steroids, such as testosterone, might explain further variance.
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3 of 6 cited sources checked · 3 supported · 0 flagged
- Findingown data
During the midluteal phase, estradiol increased compared with the early follicular phase in the 30 premenopausal women.
“ML phase increased E2 (37±2 to 117±9 pg/ml; p<.001)”
- Also stated in: § RESULTS · boosted
“Table 1 demonstrates that estradiol and progesterone were significantly elevated during the ML phase (p<0.001).”
Quote in the paperSubstantial claim - Also stated in: § RESULTS · boosted
- Findingown data
Changes in MSNA from EF to ML were not significantly correlated with changes in progesterone.
“ΔMSNA was correlated to ΔE2 (r=−.50, p=.003) and ΔE2/ΔP (r=−.52, p=.002), but not ΔP (r=.21, p=.13).”
- Also stated in: § RESULTS · hedged
“tended to be positively correlated to changes in progesterone (p=0.13)”
Quote in the paperSubstantial claim - Also stated in: § RESULTS · hedged
- Findingown data
The E2/P ratio explained only about 27% of the variance in ΔMSNA.
“even the E2/P ratio explained only ~27% of the variance in ∆MSNA.”
Quote in the paperSubstantial claim - Findingown data
Changes in MSNA from EF to ML were negatively correlated with changes in estradiol.
“ΔMSNA was correlated to ΔE2 (r=−.50, p=.003)”
- Also stated in: § RESULTS · plain
“changes in MSNA were negatively correlated to changes in estradiol (p≤0.005)”
- Also stated in: § DISCUSSION · plain
“increases in estradiol were significantly correlated with decreases in MSNA during the ML phase”
Quote in the paperSubstantial claim - Also stated in: § RESULTS · plain
- Findingown data
Among the sex steroid variables examined, the change in the E2/P ratio had the strongest association with change in MSNA.
“Our findings demonstrate that the strongest associations were between changes in MSNA and changes in the E2/P ratio.”
Quote in the paperSubstantial claim
- Findingown data
During the midluteal phase, progesterone increased compared with the early follicular phase in the 30 premenopausal women.
“P (1±0 to 11±1 ng/ml; p<.001)”
- Also stated in: § RESULTS · boosted
“Table 1 demonstrates that estradiol and progesterone were significantly elevated during the ML phase (p<0.001).”
Quote in the paperSubstantial claim - Also stated in: § RESULTS · boosted
- Findingown data
Changes in mean arterial pressure from EF to ML were not significantly correlated with changes in progesterone.
“Changes in MAP were not significantly correlated to changes in estradiol (r=−.132, p=.487), progesterone (r=−.042, p=.825), or the E2/P ratio (r=.004, p=.983).”
Quote in the paperNot a substantial claim - Findingown data
Changes in mean arterial pressure from EF to ML were not significantly correlated with changes in estradiol.
“There was no association between ΔMAP and ΔE2 (r=−.13, p=.49)”
- Also stated in: § RESULTS · plain
“Changes in MAP were not significantly correlated to changes in estradiol (r=−.132, p=.487)”
Quote in the paperNot a substantial claim - Also stated in: § RESULTS · plain
- Findingown data
Changes in MSNA from EF to ML were negatively correlated with the change in the estradiol-to-progesterone ratio.
“changes in MSNA were negatively correlated to changes in estradiol (p≤0.005) and the E2/P ratio (p=0.002)”
- Also stated in: § DISCUSSION · boosted
“the strongest association between the changes in sex steroids and MSNA were observed when changes in estradiol and progesterone were considered as a ratio (i.e., E2/P)”
Quote in the paperSubstantial claim - Also stated in: § DISCUSSION · boosted
- Findingown data
During the midluteal phase, resting MSNA increased compared with the early follicular phase in the 30 premenopausal women.
“MSNA (12±1 to 15±1 bursts/min; p=.02)”
- Also stated in: § RESULTS · plain
“The ML phase was associated with modest, yet significant, increases in resting MSNA expressed as either burst frequency (p=0.017) or burst incidence (p=0.013).”
Quote in the paperSubstantial claim - Also stated in: § RESULTS · plain
- Findingown data
Age and BMI did not significantly influence the relations between changes in sex steroids and changes in MSNA or MAP in the multiple regression analyses.
“The stepwise multiple regression excluded age and BMI in all analyses performed; thus age and BMI did not significantly influence reported relations.”
Quote in the paperNot a substantial claim - Findingown data
Changes in mean arterial pressure from EF to ML were not significantly correlated with changes in the E2/P ratio.
“There was no association between ΔMAP and ΔE2 (r=−.13, p=.49), ΔP (r=−.04, p=.83), or ΔE2/ΔP (r<.01, p=.98).”
- Also stated in: § RESULTS · plain
“Changes in MAP were not significantly correlated to changes in estradiol (r=−.132, p=.487), progesterone (r=−.042, p=.825), or the E2/P ratio (r=.004, p=.983).”
Quote in the paperNot a substantial claim - Also stated in: § RESULTS · plain
- Findingown data
Absolute MSNA values (burst frequency or incidence) were not correlated with absolute estradiol or progesterone levels during either the early follicular or midluteal phase.
“Absolute (i.e., raw) MSNA values expressed either as burst frequency or incidence were not correlated to absolute (i.e., raw) estradiol or progesterone levels during either the EF or ML phase.”
Quote in the paperNot a substantial claim - Findingown data
During the midluteal phase, mean arterial pressure did not change compared with the early follicular phase in the 30 premenopausal women.
“but did not alter MAP (83±2 to 83±2 mmHg; p=.91)”
Quote in the paperSubstantial claim - Study design and conductcitation
The original inclusion and exclusion criteria were consistent across the laboratories.
“Original inclusion and exclusion criteria were consistent across laboratories (see original manuscripts)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites original manuscripts
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationown data
The results may not generalize to obese premenopausal women.
“Additionally, we acknowledge the present data set included relatively healthy, nonobese subjects, and that these individuals may not necessarily reflect the growing segment of obese, premenopausal women.”
Quote in the paperNot a substantial claim - Study design and conductreasoning
MSNA burst identification guidelines were followed consistently across the three laboratories.
“The MSNA burst identification guidelines (i.e., 3-to-1 noise ratio, a single identifier, etc.) were followed consistently across laboratories”
Quote in the paperSubstantial claim - Interpretationown data
The dynamic interaction between estradiol, progesterone, and MSNA likely explains previously reported inconsistencies in the field regarding the influence of the ovarian cycle on resting MSNA.
“This dynamic interaction between E2, P, and MSNA likely explains previously reported inconsistencies in the field”
- Also stated in: § DISCUSSION · hedged
“Collectively, our findings suggest that the variable surges in estradiol and progesterone likely explain previously reported inconsistencies in the field regarding the influence of the ovarian cycle on resting MSNA.”
- Also stated in: § Perspectives · hedged
“Our findings suggest a dynamic interaction between E2, P, and MSNA likely explains previously reported inconsistencies in the field regarding the influence of the ovarian cycle on resting MSNA.”
Quote in the paperSubstantial claim - Also stated in: § DISCUSSION · hedged
- Interpretationown data
Sympathoexcitation during the midluteal phase appears to be dependent, in part, on the degree of sex steroid surges.
“In conclusion, sympathoexcitation during the ML phase of the ovarian cycle appears to be dependent, in part, upon the degree of sex steroid surges.”
- Also stated in: § DISCUSSION · hedged
“Consistent with our hypothesis, sympathoexcitatory responses to the ML phase of the ovarian cycle appear to be related, in part, to the degree of sex steroid surge.”
- Also stated in: § Perspectives · hedged
“Our results demonstrate that the ML phase of the ovarian cycle is characterized by sympathoexcitation, but that the degree of sympathoexcitation appears to be partially dependent upon the degree of sex steroid surges.”
Quote in the paperSubstantial claim - Also stated in: § DISCUSSION · hedged
- Interpretationreasoning
Interindividual variability in sex steroid surges may be fundamentally important for autonomic control in women.
“In recent years, interindividual variability of MSNA has received much attention,21 and we posit that interindividual variability in sex steroid surges may also be fundamentally important when considering autonomic control in women.”
Quote in the paperSubstantial claim
- Classified as probably not a substantial claim. 6
- May combine two claims. 6
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductcitationThe order of testing was randomized or counterbalanced for each study.
“The order of testing was randomized5,8,12 or counterbalanced4,9 for each study.”
Quote in the paperNot a substantial claim3 of 5 sources checkedClassified as probably not a substantial claim. May combine two claims.
Study design and conductnone givenUrinary ovulation kits were used to confirm the LH surge, and midluteal testing was performed 8-10 days after detection.
“Each study used urinary ovulation kits to confirm the LH surge, and midluteal testing was consistently performed 8–10 days after this detection.”
Quote in the paperSubstantial claimMay combine two claims.
Study design and conductnone givenThe three laboratories had similar training and extensive experience with microneurography and used similar acquisition and analysis procedures.
“the three laboratories have similar training and extensive experience with the microneurographic technique, and utilize similar acquisition and analysis procedures.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductown dataBMI did not differ between phases in the 22 subjects measured during both phases, and BMI values were strongly correlated.
“BMI did not differ between phases in the 22 subjects measured during both phases (p=0.89), and the BMI values were strongly correlated (R2 = 0.94, p<0.001).”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataThe findings are consistent with the concept that estradiol is sympathoinhibitory and progesterone is sympathoexcitatory.
“Our findings are consistent with the prevailing concept that estradiol is sympathoinhibitory and progesterone is sympathoexcitatory.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim. May combine two claims.
Study design and conductnone givenVenous blood samples were collected to determine estradiol and progesterone levels and to confirm a surge of both during the ML phase.
“Venous blood samples were collected to determine estradiol and progesterone levels, and to confirm a surge of both estradiol and progesterone during the ML phase.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenAll original studies were approved by the corresponding institutional review boards.
“all studies were approved by the corresponding institutional review boards.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown dataNo outliers were detected in the multiple linear regressions (defined as 3 standard deviations from the mean).
“All multiple linear regressions were probed for outliers, and we did not detect any outliers as defined as 3 standard deviations from the mean.”
Quote in the paperNot a substantial claim
The authors state this as an assumption.
Lack of a progesterone surge during the midluteal phase indicates anovulation.
“After exclusion of assumed anovulation (i.e., lack of progesterone surge during ML)”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Muscle sympathetic nerve activity is higher during the luteal phase than during the follicular phase in women with natural menstrual cycles.
“This finding is analogous to the higher levels of MSNA seen during the luteal phase versus the follicular phase of women with natural menstrual cycles.7, 11, 12”
From Oral contraceptive use, muscle sympathetic nerve activity, and systemic hemodynamics in young women (2015) · cites this paper as [11]
Cites
Heart Disease and Stroke Statistics—2023 Update: A Report From the American Heart Association
Tsao, C. W., Aday, A. W., Almarzooq, Z. I., Anderson, C. A. M., Arora, P., Avery, C. L., Baker-Smith, C. M., Beaton, A. Z., Boehme, A. K., Buxton, A. E., et al. (2023) · Circulation · doi:10.1161/cir.0000000000001123 · Cited by 8,300 · see citing works
Heart Disease and Stroke Statistics—2012 Update: A Report From the American Heart Association
Writing Group Members, Roger, V. L., Go, A. S., Lloyd-Jones, D. M., Benjamin, E. J., Berry, J. D., Borden, W. B., Bravata, D. M., Dai, S., Ford, E. S., et al. (2012) · Circulation · doi:10.1161/cir.0b013e31823ac046 · Cited by 7,333 · see citing works
The vascular protective effects of estrogen
Farhat, M. Y., Lavigne, M. C., & Ramwell, P. W. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.5.8621060 · Cited by 648 · cited 1× · see citing works
“Estradiol is known to elicit endothelial vasodilation via a variety of mechanisms that include NO and prostaglandins or by directly altering membrane ionic permeability of the vascular smooth muscle.(32) It is possible that the increase of resting MSNA and subsequent α-adrenergic vasoconstriction during the ML phase i…”
BackgroundMinson, C. T., Halliwill, J. R., Young, T. M., & Joyner, M. J. (2000) · Circulation · doi:10.1161/01.cir.101.8.862 · Cited by 515 · cited 2× · see citing works
“Subjects Subjects were retrospectively analyzed from 5 previous studies.(4,5,8,9,12) Original inclusion and exclusion criteria were consistent across laboratories (see original articles), and all studies were approved by the corresponding institutional review boards.”
MethodSelf-citationEffects of Estrogen Replacement Therapy on the Renin-Angiotensin System in Postmenopausal Women
Schunkert, H., Danser, A. H. J., Hense, H.-W., Derkx, F. H. M., Ku¨rzinger, S., & Riegger, G. A. J. (1997) · Circulation · doi:10.1161/01.cir.95.1.39 · Cited by 438 · cited 1× · see citing works
“However, other data suggest that only progesterone activates the RAAS, whereas estrogen might inhibit the activation of this system.(30,31) Szmuilowicz et al(27) reported that progesterone may directly contribute to increased luteal phase aldosterone production independent of the RAAS.”
BackgroundGender-Selective Interaction Between Aging, Blood Pressure, and Sympathetic Nerve Activity
Narkiewicz, K., Phillips, B. G., Kato, M., Hering, D., Bieniaszewski, L., & Somers, V. K. (2005) · Hypertension · doi:10.1161/01.hyp.0000160318.46725.46 · Cited by 398 · cited 1× · see citing works
“gested that lower sympathetic tone may contribute importantly to this premenopausal cardioprotection.(1) Conversely, cardio-”
BackgroundHart, E. C., Charkoudian, N., Wallin, B. G., Curry, T. B., Eisenach, J., & Joyner, M. J. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.212753 · Cited by 338 · see citing works
Self-citationSympathetic Nervous System and Blood Pressure in Humans
Joyner, M. J., Charkoudian, N., & Wallin, B. G. (2010) · Hypertension · doi:10.1161/hypertensionaha.109.140186 · Cited by 221 · see citing works
Self-citationIs polycystic ovary syndrome associated with high sympathetic nerve activity and size at birth?
Sverrisdóttir, Y. B., Mogren, T., Kataoka, J., Janson, P. O., & Stener-Victorin, E. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00725.2007 · Cited by 216 · see citing works
Transdermal Estrogen Replacement Therapy Decreases Sympathetic Activity in Postmenopausal Women
Vongpatanasin, W., Tuncel, M., Mansour, Y., Arbique, D., & Victor, R. G. (2001) · Circulation · doi:10.1161/01.cir.103.24.2903 · Cited by 203 · see citing works
Chapman, A. B., Zamudio, S., Woodmansee, W., Merouani, A., Osorio, F., Johnson, A., Moore, L. G., Dahms, T., Coffin, C., Abraham, W. T., et al. (1997) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.1997.273.5.f777 · Cited by 201 · see citing works
Estradiol With or Without Progesterone and Ambulatory Blood Pressure in Postmenopausal Women
Seely, E. W., Walsh, B. W., Gerhard, M. D., & Williams, G. H. (1999) · Hypertension · doi:10.1161/01.hyp.33.5.1190 · Cited by 176 · cited 1× · see citing works
“However, other data suggest that only progesterone activates the RAAS, whereas estrogen might inhibit the activation of this system.(30,31) Szmuilowicz et al(27) reported that progesterone may directly contribute to increased luteal phase aldosterone production independent of the RAAS.”
BackgroundHirshoren, N., Tzoran, I., Makrienko, I., Edoute, Y., Plawner, M. M., Itskovitz‐Eldor, J., & Jacob, G. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.4.8406 · Cited by 165 · see citing works
Variation in the Renin Angiotensin System throughout the Normal Menstrual Cycle
Chidambaram, M., Duncan, J. A., LAI, V. S., Cattran, D. C., Floras, J. S., Scholey, J. W., & Miller, J. (2002) · Journal of the American Society of Nephrology · doi:10.1681/asn.v132446 · Cited by 162 · see citing works
Sympathetic neural responses to 24-hour sleep deprivation in humans: sex differences
Carter, J. R., Durocher, J. J., Larson, R. A., DellaValla, J. P., & Yang, H. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01132.2011 · Cited by 153 · see citing works
Self-citationSympathetic activation during early pregnancy in humans
Jarvis, S. S., Shibata, S., Bivens, T. B., Okada, Y., Casey, B. M., Levine, B. D., & Fu, Q. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.228262 · Cited by 146 · cited 1× · see citing works
“A recent study showed that there was a significant positive relationship between the change in resting MSNA and the change in direct renin and aldosterone during early human pregnancy.(10) Thus, sympathoexcitatory responses to the ML phase may be attributable to the activation of the RAAS.”
BackgroundSelf-citationMenstrual cycle effects on sympathetic neural responses to upright tilt
Fu, Q., Okazaki, K., Shibata, S., Shook, R. P., VanGunday, T. B., Galbreath, M. M., Reelick, M. F., & Levine, B. D. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.168468 · Cited by 144 · cited 2× · see citing works
“Subjects Subjects were retrospectively analyzed from 5 previous studies.(4,5,8,9,12) Original inclusion and exclusion criteria were consistent across laboratories (see original articles), and all studies were approved by the corresponding institutional review boards.”
MethodSelf-citationSympathetic Activity and Baroreflex Sensitivity in Young Women Taking Oral Contraceptives
Minson, C. T., Halliwill, J. R., Young, T. M., & Joyner, M. J. (2000) · Circulation · doi:10.1161/01.cir.102.13.1473 · Cited by 139 · cited 2× · see citing works
“More specifically, estradiol has been suggested to be sympathoinhibitory,(13,14) whereas progesterone has been suggested to be sympathoexcitatory.(3,15) Thus,”
BackgroundResultSelf-citationEffects of the ovarian cycle on sympathetic neural outflow during static exercise
Ettinger, S. M., Silber, D. H., Gray, K. S., Smith, M. B., Yang, Q. X., Kunselman, A. R., & Sinoway, L. I. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.85.6.2075 · Cited by 125 · cited 1× · see citing works
“More specifically, estradiol has been suggested to be sympathoinhibitory,(13,14) whereas progesterone has been suggested to be sympathoexcitatory.(3,15) Thus,”
BackgroundHassager, C., Riis, B. J., Strøm, V, Guyene, T. T., & Christiansen, C. (1987) · Circulation · doi:10.1161/01.cir.76.4.753 · Cited by 124 · cited 3× · see citing works
“Studies using oral estrogen and progesterone in postmenopausal women have demonstrated that both hormones can activate the RAAS.28,29 However, other data suggest that only progesterone activates the RAAS, whereas estrogen might inhibit the activation of this system.30,31 Szmuilowicz et al27 reported that progesterone…”
BackgroundInfluentialSealey, J. E., Itskovitz-Eldor, J., Rubattu, S., James, G. D., August, P., Thaler, I., Levron, J., & Laragh, J. H. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.1.8027239 · Cited by 110 · see citing works
Relationship between Aldosterone and Progesterone in the Human Menstrual Cycle
Szmuilowicz, E. D., Adler, G. K., Williams, J. S., Green, D. E., Yao, T. M., Hopkins, P. N., & Seely, E. W. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1154 · Cited by 107 · see citing works
Postmenopausal Estrogen Administration Suppresses Muscle Sympathetic Nerve Activity<sup>1</sup>
Weitz, G., Elam, M., Born, J., Fehm, H. L., & Dodt, C. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.1.7138 · Cited by 97 · see citing works
Carter, J. R., Lawrence, J. E., & Klein, J. C. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00019.2009 · Cited by 87 · cited 2× · see citing works
“Subjects Subjects were retrospectively analyzed from 5 previous studies.(4,5,8,9,12) Original inclusion and exclusion criteria were consistent across laboratories (see original articles), and all studies were approved by the corresponding institutional review boards.”
MethodSelf-citationHe, X.-R., Wang, W., Crofton, J. T., & Share, L. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.4.r1202 · Cited by 75 · see citing works
Effects of the menstrual cycle on sympathetic neural responses to mental stress in humans
Carter, J. R., & Lawrence, J. E. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.141051 · Cited by 71 · cited 2× · see citing works
“Subjects Subjects were retrospectively analyzed from 5 previous studies.(4,5,8,9,12) Original inclusion and exclusion criteria were consistent across laboratories (see original articles), and all studies were approved by the corresponding institutional review boards.”
MethodSelf-citationTorgrimson, B. N., Meendering, J. R., Kaplan, P., & Minson, C. T. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00762.2006 · Cited by 70 · see citing works
Self-citation(1967) · PubMed · Cited by 68 · see citing works
Miner, J. A., Martini, E. R., Smith, M. M., Brunt, V. E., Kaplan, P. F., Halliwill, J. R., & Minson, C. T. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00405.2011 · Cited by 66 · see citing works
Self-citationFu, Q., VanGundy, T. B., Shibata, S., Auchus, R. J., Williams, G. H., & Levine, B. D. (2010) · Hypertension · doi:10.1161/hypertensionaha.110.151787 · Cited by 62 · see citing works
Self-citationMiddlekauff, H. R., Park, J., & Gornbein, J. A. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00579.2011 · Cited by 44 · cited 1× · see citing works
“Although this study focused on defining resting MSNA during EF and ML phases in eumenorrheic women, 3 studies from independent laboratories have each confirmed that women taking oral contraceptives do not demonstrate altered resting MSNA during the low and high exogenous hormone phase.(6,15,34) However, the type, dosa…”
ResultCarter, J. R., Klein, J. C., & Schwartz, C. E. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00554.2009 · Cited by 40 · cited 1× · see citing works
“Although this study focused on defining resting MSNA during EF and ML phases in eumenorrheic women, 3 studies from independent laboratories have each confirmed that women taking oral contraceptives do not demonstrate altered resting MSNA during the low and high exogenous hormone phase.(6,15,34) However, the type, dosa…”
ResultSelf-citationJespersen, C. M., Arnung, K., Hagen, C., Hilden, T., Nielsen, F., Nielsen, M. D., & Giese, J. (1983) · Journal of Hypertension · doi:10.1097/00004872-198312000-00007 · Cited by 39 · see citing works
Meendering, J. R., Torgrimson, B. N., Miller, N. P., Kaplan, P., & Minson, C. T. (2010) · Contraception · doi:10.1016/j.contraception.2010.03.009 · Cited by 36 · see citing works
Self-citationAltered pattern of sympathetic activity with the ovarian cycle in female smokers
Park, J., & Middlekauff, H. R. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01197.2008 · Cited by 27 · see citing works
Vestibulosympathetic reflex during the early follicular and midluteal phases of the menstrual cycle
Lawrence, J. E., Ray, C. A., & Carter, J. R. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00056.2008 · Cited by 21 · cited 2× · see citing works
“Subjects Subjects were retrospectively analyzed from 5 previous studies.(4,5,8,9,12) Original inclusion and exclusion criteria were consistent across laboratories (see original articles), and all studies were approved by the corresponding institutional review boards.”
MethodSelf-citationMenstrual cycle elicits divergent forearm vascular responses to vestibular activation in humans
Lawrence, J. E., Klein, J. C., & Carter, J. R. (2010) · Autonomic Neuroscience · doi:10.1016/j.autneu.2009.11.002 · Cited by 20 · see citing works
Self-citation
Flagged first, then by citations
1 of the 39 references couldn’t be matched to a known paper.
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Sex differences and blood pressure regulation in humans
Joyner, M. J., Wallin, B. G., & Charkoudian, N. (2015) · Experimental Physiology · doi:10.1113/ep085146 · Cited by 237 · see citing works
“Experimental Physiology C© 2015 The Physiological Society DOI: 10.1113/EP085146 humans with epidemiological observations (Charkoudian et al. 2005, 2006; Hart et al. 2009a, 2011, 2012; Carter et al. 2013; Barnes et al. 2014).”
BackgroundInfluentialSelf-citationGender Differences in Hypertension: Myths and Reality
Doumas, M. N., Papademetriou, V., Faselis, C. J., & Kokkinos, P. F. (2013) · Current Hypertension Reports · doi:10.1007/s11906-013-0359-y · Cited by 185 · see citing works
The hypertension of Cushing's syndrome
Isidori, A. M., Graziadio, C., Paragliola, R. M., Cozzolino, A., Ambrogio, A. G., Colao, A., Corsello, S. M., & Pivonello, R. (2014) · Journal of Hypertension · doi:10.1097/hjh.0000000000000415 · Cited by 220 · see citing works
“This difference might be related to the specific vasoactive effects of adrenal sex steroids (androgens, estrogen and their metabolites), which are generally suppressed in cortisol-secreting adrenal tumors compared to pituitary tumors responsible for CD [93,94].”
BackgroundSympathetic Neural Regulation of Blood Pressure: Influences of Sex and Aging
Hart, E. C., & Charkoudian, N. (2014) · Physiology · doi:10.1152/physiol.00031.2013 · Cited by 146 · see citing works
“(3), although the dynamic interactions among estra-”
Influence of Sex and Age on Muscle Sympathetic Nerve Activity of Healthy Normotensive Adults
Keir, D. A., Badrov, M. B., TOMLINSON, G. A., Notarius, C. F., Kimmerly, D. S., Millar, P. J., Shoemaker, J. K., & Floras, J. S. (2020) · Hypertension · doi:10.1161/hypertensionaha.120.15208 · Cited by 127 · see citing works
“In premenopausal women, sympathetic activation coincident with the surge in endogenous estradiol during the mid-luteal phase of the menstrual cycle is not accompanied by parallel increases in mean arterial pressure, a finding consistent with the concept that, despite sex differences in receptor sensitivity and arteria…”
ResultNeural Control of the Circulation: How Sex and Age Differences Interact in Humans
Joyner, M. J., Barnes, J. N., Hart, E. C., Wallin, B. G., & Charkoudian, N. (2014) · Comprehensive physiology · doi:10.1002/cphy.c140005 · Cited by 143 · see citing works
Self-citationNeurovascular control of blood pressure is influenced by aging, sex, and sex hormones
Baker, S. E., Limberg, J. K., Ranadive, S. M., & Joyner, M. J. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00288.2016 · Cited by 96 · see citing works
“These changes are attributed to changes in circulating sex hormone levels (6).”
BackgroundSelf-citationSympathetic Nervous System Regulation in Human Normotensive and Hypertensive Pregnancies
Reyes, L. M., Usselman, C. W., Davenport, M. H., & Steinback, C. D. (2018) · Hypertension · doi:10.1161/hypertensionaha.117.10766 · Cited by 85 · see citing works
Oral contraceptive use, muscle sympathetic nerve activity, and systemic hemodynamics in young women
Harvey, R. E., Hart, E. C., Charkoudian, N., Curry, T. B., Carter, J. R., Fu, Q., Minson, C. T., Joyner, M. J., & Barnes, J. N. (2015) · HYPERTENSION · doi:10.1161/hypertensionaha.115.05179 · Cited by 76 · see citing works
“This finding is analogous to the higher levels of MSNA seen during the luteal phase versus the follicular phase of women with natural menstrual cycles.(7,11,12) In general, studies on this topic are limited because they do not compare women taking OCs with a control group of women with natural menstrual cycles who are…”
ResultSelf-citationVasomotor symptoms of menopause, autonomic dysfunction, and cardiovascular disease
Lee, E. J., Anselmo, M. F., Tahsin, C. T., Noven, M. V., Stokes, W., Carter, J. R., & Keller‐Ross, M. L. (2022) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00477.2022 · Cited by 91 · see citing works
Self-citationSex differences in baroreflex function in health and disease
Fu, Q., & Ogoh, S. (2019) · The Journal of Physiological Sciences · doi:10.1007/s12576-019-00727-z · Cited by 70 · see citing works
Self-citationMenstrual cycle and sex effects on sympathetic responses to acute chemoreflex stress
Usselman, C. W., Gimon, T. I., Nielson, C. A., Luchyshyn, T. A., Coverdale, N. S., Uum, S. H. M. V., & Shoemaker, J. K. (2014) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00345.2014 · Cited by 61 · see citing works
“While it should be noted that associations between menstrual cycle phase and baseline MSNA have not been observed universally (5, 6, 10, 17, 20), collectively the data indicate that the menstrual cycle, and specifically the changes in sex hormone levels that occur along the menstrual cycle (4), are associated with cha…”
BackgroundObesity-induced increases in sympathetic nerve activity: Sex matters
Brooks, V. L., Shi, Z., Holwerda, S. W., & Fadel, P. J. (2014) · Autonomic Neuroscience · doi:10.1016/j.autneu.2014.11.006 · Cited by 61 · see citing works
“(Carter et al., 2013) suggests that the increases in MSNA during the mid-luteal phase are due, in part, to the sympathoexcitatory actions”
Usselman, C. W., Wakefield, P. K., Skow, R. J., Stickland, M. K., Chari, R. S., Julian, C. G., Steinback, C. D., & Davenport, M. H. (2015) · Hypertension · doi:10.1161/hypertensionaha.115.05964 · Cited by 57 · see citing works
Sympathetic neural reactivity to mental stress in humans: test-retest reproducibility
Fonkoue, I. T., & Carter, J. R. (2015) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00344.2015 · Cited by 57 · see citing works
Self-citationShi, Z., & Brooks, V. L. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.284638 · Cited by 48 · see citing works
“It has been proposed that the inhibitory effects of oestrogen on SNA is opposed by excitatory effects of progesterone in women (Carter et al. 2013); these opposing actions may be balanced in the rat on the late afternoon of pro-oestrus, when our experiments were conducted.”
BackgroundResultMicroneurography and sympathetic nerve activity: a decade-by-decade journey across 50 years
Carter, J. R. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00570.2018 · Cited by 46 · see citing works
“…studies that seemed inconsistent with these initial findings; however, a multilaboratory effort to combine data sets led to a study that reported levels of sympathoexcitatory response during the midluteal phase might relate to the relative surges of estradiol and progesterone (Carter et al. 2013).”
ResultSelf-citationInfluence of Age and Estradiol on Sympathetic Nerve Activity Responses to Exercise in Women
Wenner, M. M., GREANEY, J. L., MATTHEWS, E. L., McGinty, S. J., KAUR, J., Vongpatanasin, W., & Fadel, P. J. (2021) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002823 · Cited by 45 · see citing works
Prasad, B., Morgan, B. J., Gupta, A., et al. (2020) · The Journal of Physiology · doi:10.1113/jp280515 · Cited by 44 · see citing works
“2012), MSNA (Minson et al. 2000; Carter et al. 2013) and ventilatory and sympathetic chemoreflex responsiveness (Schoene et al.”
BackgroundChallenges and methodology for testing young healthy women in physiological studies
Stachenfeld, N. S., & Taylor, H. S. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00038.2014 · Cited by 41 · see citing works
“Using menstrual cycle phase to keep hormone levels consistent within an investigation has the advantage of examining women during natural endogenous hormonal changes (5).”
BackgroundSex-Related Differences in Hypertension
Denton, K. M., Hilliard, L. M., & Tare, M. (2013) · Hypertension · doi:10.1161/hypertensionaha.113.00922 · Cited by 40 · see citing works
“Recent evidence also suggests that sympathetic activation is linked to the menstrual cycle, estrogen being sympathoinhibitory and progesterone being sympathoexcitatory.(50) Indeed, estrogen receptors, specifically estrogen receptor β, in the paraventricular nucleus and rostroventrolateral medulla have been recently sh…”
BackgroundSladek, C. D., Michelini, L. C., Stachenfeld, N. S., Stern, J. E., & Urban, J. H. (2015) · Comprehensive physiology · doi:10.1002/cphy.c140028 · Cited by 49 · see citing works
Abidi, S., Nili, M., Serna, S., Kim, S., Hazlett, C., & Edgell, H. (2017) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00035.2017 · Cited by 39 · see citing works
“Indeed, women in the HH phase have been shown to have greater sympathetic activity at rest and during orthostasis than women in the LH phase (8, 19).”
BackgroundEffects of menstrual cycle and menopause on internal carotid artery shear-mediated dilation in women
Iwamoto, E., Sakamoto, R., Tsuchida, W., Yamazaki, K., Kamoda, T., Neki, T., Katayose, M., & Casey, D. P. (2020) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00810.2020 · Cited by 38 · see citing works
Blood pressure and muscle sympathetic nerve activity are associated with trait anxiety in humans
Bigalke, J. A., Durocher, J. J., Greenlund, I. M., Keller‐Ross, M. L., & Carter, J. R. (2023) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00026.2023 · Cited by 38 · see citing works
Self-citationShi, Z., Wong, J., & Brooks, V. L. (2020) · Biology of Sex Differences · doi:10.1186/s13293-020-00286-8 · Cited by 37 · see citing works
Adaptations in autonomic nervous system regulation in normal and hypertensive pregnancy
Brooks, V. L., Fu, Q., Shi, Z., & Heesch, C. M. (2020) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64239-4.00003-5 · Cited by 37 · see citing works
Self-citationTranslational studies of estradiol and progesterone in fear and PTSD
Seligowski, A. V., Hurly, J. A., Mellen, E., Ressler, K. J., & Ramikie, T. S. (2020) · European Journal of Psychotraumatology · doi:10.1080/20008198.2020.1723857 · Cited by 35 · see citing works
“control), suggesting that sympathetic activity is more pronounced when estradiol is low, and progesterone is high (Carter et al., 2013) (this study appeared to calculate its P/E ratio as estradiol divided by progesterone, which likely explains this finding).”
BackgroundResultInfluentialOkada, Y., Best, S. A., Jarvis, S. S., Shibata, S., Parker, R. S., Casey, B. M., Levine, B. D., & Fu, Q. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.282277 · Cited by 34 · see citing works
“Conversely, oestrogen also acts on the brain to reduce central sympathetic outflow (He et al. 1998, 1999; Ma et al. 2008; Carter et al. 2013).”
BackgroundSelf-citationOkamoto, T., Kobayashi, R., & Sakamaki‐Sunaga, M. (2017) · International Journal of Sports Medicine · doi:10.1055/s-0043-101377 · Cited by 33 · see citing works
Morning sympathetic activity after evening binge alcohol consumption
Greenlund, I. M., Cunningham, H. A., Tikkanen, A. L., Bigalke, J. A., Smoot, C. A., Durocher, J. J., & Carter, J. R. (2020) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00743.2020 · Cited by 33 · see citing works
“, early follicular versus mid luteal) (36).”
MethodSelf-citationNeural Control of the Circulation: How Sex and Age Differences Interact in Humans
Joyner, M. J., Barnes, J. N., Hart, E. C., Wallin, B. G., & Charkoudian, N. (2015) · Comprehensive physiology · doi:10.1002/j.2040-4603.2015.tb00598.x · Cited by 32 · see citing works
“However, recent evidence points to elevated MSNA when sex hormone levels are high (13).”
Self-citationSex differences in forearm vasoconstrictor response to voluntary apnea
Patel, H. M., Heffernan, M. J., Ross, A. J., & Muller, M. D. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00746.2013 · Cited by 31 · see citing works
Usselman, C. W., Luchyshyn, T. A., Gimon, T. I., Nielson, C. A., Van Uum, S. H. M., & Shoemaker, J. K. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00681.2013 · Cited by 30 · see citing works
“A recent study by Carter and colleagues (2) retrospectively correlated circulating concentrations of estradiol and progesterone to resting MSNA in 30 young premenopausal women who were not taking any exogenous hormones.”
BackgroundResultInfluentialD’Souza, A. W., Takeda, R., Manabe, K., et al. (2023) · The Journal of Physiology · doi:10.1113/jp284517 · Cited by 29 · see citing works
“, 2009) and is inversely related to resting sympathetic outflow in young females (Carter et al., 2013).”
BackgroundSelf-citationBrown, R., & Macefield, V. G. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00111 · Cited by 29 · see citing works
“We are grateful to the assistance provided by Elie Hammam and Azharuddin Fazalbhoy in some of the experiments.”
DeLorey, D. S. (2021) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2021-0399 · Cited by 28 · see citing works
“…in muscle mass, fibre types and distribution, and sensitivity of the metabo- and mechano- reflexes between men and women (Ettinger et al. 1996), as well cyclical changes in reproductive hormones throughout the menstrual cycle in women (Carter et al. 2013, Ettinger et al. 1998, Minson et al. 2000).”
BackgroundPulse transit time in pregnancy: a new way to diagnose and classify sleep disordered breathing?
Link, B. N., Eid, C., Bublitz, M. H., Pengo, M. F., Salameh, M., Ludwig, K. S., Millman, R. P., Dworkin, L. D., & Bourjeily, G. R. (2019) · SLEEP · doi:10.1093/sleep/zsz022 · Cited by 28 · see citing works
“There are sex differences in sympathetic activation, with women being more “sympathetic” in response to sleep disturbances [33], and potential differences being found to be related to sex hormones such as estrogens and progesterone in premenopausal women [34].”
BackgroundBrunt, V. E., Miner, J. A., Kaplan, P., Halliwill, J. R., Strycker, L. A., & Minson, C. T. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00194.2013 · Cited by 26 · see citing works
“Unloading of the carotid baroreceptors with neck pressure results in a robust increase in heart rate (HR) and muscle sympathetic nerve activity (MSNA) rapidly following the onset of external pressure (37).”
InfluentialSelf-citationSympathetic arousal increases a negative memory bias in young women with low sex hormone levels
Nielsen, S. E., Barber, S. J., Chai, A. L., Clewett, D., & Mather, M. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.08.001 · Cited by 26 · see citing works
Sympathetic neural reactivity to mental stress differs in black and non-Hispanic white adults
Fonkoue, I. T., Schwartz, C. E., Wang, M., & Carter, J. R. (2017) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00134.2017 · Cited by 24 · see citing works
“This is both a limitation (limited generalizability) and a strength (confounding effects of reproductive hormones are substantially reduced) (13).”
BackgroundSelf-citationUsselman, C. W., Adler, T. E., Coovadia, Y., Leone, C. A., Paidas, M. J., & Stachenfeld, N. S. (2020) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00578.2019 · Cited by 23 · see citing works
Cerebral autoregulation across the menstrual cycle in eumenorrheic women
Korad, S., Mündel, T., Fan, J., & Perry, B. G. (2022) · Physiological Reports · doi:10.14814/phy2.15287 · Cited by 22 · see citing works
“There is also some evidence to indicate that muscle sympathetic nerve activity is affected by the menstrual cycle at rest (Carter et al., 2013) and during orthostatic challenges (Carter et al.”
BackgroundSouza, G. M. P. R., Amorim, M. R., Moraes, D. J. A., & Machado, B. H. (2017) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2017.09.003 · Cited by 21 · see citing works
Venclovienė, J., Babarskienė, R. M., Dobožinskas, P., Šakalytė, G., Lopatienė, K., & Mikelionis, N. (2015) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph120302622 · Cited by 21 · see citing works
“Recent evidence also suggests that sympathetic activation is linked to the menstrual cycle, estrogen being sympathoinhibitory and progesterone being sympathoexcitatory [37].”
Usselman, C. W., Nielson, C. A., Luchyshyn, T. A., Gimon, T. I., Coverdale, N. S., Uum, S. H. M. V., & Shoemaker, J. K. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00190.2016 · Cited by 20 · see citing works
“, high estrogen and progesterone) phase of the menstrual cycle relative to the early follicular phase (EF; lower estrogen and progesterone) (3, 32, 33, 38, 47), although not all studies agree (4, 6, 14, 23).”
Oral contraceptives and menstrual cycle influence autonomic reflex function
Assadpour, E., Ivry, I., Wasef, S., Adeyinka, B. O., Murray, K. R., & Edgell, H. (2020) · Physiological Reports · doi:10.14814/phy2.14550 · Cited by 20 · see citing works
Giersch, G. E. W., Charkoudian, N., Pereira, T., Edgell, H., Freeberg, K. A., Craighead, D. H., Neill, M. G., Allison, E. Y., Zapcic, A. K., Smith, K. J., et al. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00809.2020 · Cited by 19 · see citing works
Self-citationStickford, A. S. L., VanGundy, T. B., Levine, B. D., & Fu, Q. (2015) · The Journal of Physiology · doi:10.1113/jp270088 · Cited by 19 · see citing works
“Specifically, sympathetic neural activity, measured via microneurography as muscle sympathetic nerve activity (MSNA), is increased in healthy women when the ratio of oestradiol to progesterone is lower (i.e. generally during the ML phase) (Carter et al. 2013).”
BackgroundResultInfluentialSelf-citationEffects of losartan and allopurinol on cardiorespiratory regulation in obstructive sleep apnoea
Morgan, B. J., Teodorescu, M., Pegelow, D. F., Jackson, E. R., Schneider, D. L., Plante, D. T., Gapinski, J. P., Hetzel, S., & Dopp, J. M. (2018) · Experimental Physiology · doi:10.1113/ep087006 · Cited by 15 · see citing works
Shorakae, S., Lambert, É., Jona, E., Sari, C. I., de Courten, B. V., Dixon, J. B., Lambert, G. W., & Teede, H. J. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01486 · Cited by 15 · see citing works
“, 2002) and phase of the ovarian cycle (Carter et al., 2013).”
BackgroundLong-term effects of earthquake experience of young persons on cardiovascular disease risk factors
Li, N., Wang, Y., Yu, L., Song, M., Wang, L., Ji, C., Wang, X., & Wu, S. (2017) · Archives of Medical Science · doi:10.5114/aoms.2017.64716 · Cited by 14 · see citing works
“Sympathetic activation is related to the menstrual cycle, and estrogen inhibits such activation according to a recent report [23].”
BackgroundStickford, A. S. L., Okada, Y., Best, S. A., Parker, R. S., Levine, B. D., & Fu, Q. (2016) · Clinical Autonomic Research · doi:10.1007/s10286-016-0372-8 · Cited by 13 · see citing works
“concentrations of E2/P are associated with augmented levels of MSNA [5].”
BackgroundSelf-citationMenopause and its effects on autonomic regulation of blood pressure: Insights and perspectives
Lee, E., & Keller‐Ross, M. L. (2025) · Autonomic Neuroscience · doi:10.1016/j.autneu.2025.103295 · Cited by 12 · see citing works
Sympathetic and blood pressure reactivity in young adults with major depressive disorder
Darling, A. M., Young, B. E., Skow, R. J., Dominguez, C. M., Saunders, E. F. H., Fadel, P. J., & Greaney, J. L. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.06.053 · Cited by 12 · see citing works
Kagitani, H., Hoshide, S., & Kario, K. (2014) · American Journal of Hypertension · doi:10.1093/ajh/hpu210 · Cited by 12 · see citing works
Cardiovascular Disease in Women Across the Lifespan: The Importance of Sleep
Daugherty, S. L., Carter, J. R., & Bourjeily, G. R. (2020) · Journal of Women s Health · doi:10.1089/jwh.2020.8331 · Cited by 12 · see citing works
Self-citationA possible important regulatory role of estrogen in obstructive sleep apnea hypoventilation syndrome
Zhou, P., Li, H., Li, H., Chen, Y., & Lv, Y. (2025) · Frontiers in Medicine · doi:10.3389/fmed.2025.1369393 · Cited by 11 · see citing works
Sladek, C. D., Michelini, L. C., Stachenfeld, N. S., Stern, J. E., & Urban, J. H. (2015) · Comprehensive physiology · doi:10.1002/j.2040-4603.2015.tb00634.x · Cited by 12 · see citing works
“To describe the relationship of the menstrual cycle and sympathoexitation, a recent report combined data from several studies that had examined MSNA in the early follicular and mid-luteal phases of the menstrual cycle (48).”
Takeda, R., Stickford, A. S. L., Best, S. A., Yoo, J., & Fu, Q. (2020) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00197.2020 · Cited by 11 · see citing works
“It is possible that high estrogen may affect BP regulation during LS and HS via modulation of sympathetic activity (7) and vascular function through nitric oxide (NO) production (11).”
BackgroundSelf-citationHissen, S. L., Takeda, R., Badrov, M. B., Arias-Franklin, S., Patel, S. A., Nelson, D. B., Babb, T. G., & Fu, Q. (2023) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00098.2023 · Cited by 11 · see citing works
Self-citationPinkham, M. I., & Barrett, C. J. (2015) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12392 · Cited by 11 · see citing works
“There is very limited evidence regarding the effects of progesterone on sympathetic control [22].”
BackgroundBlood Pressure: Return of the Sympathetics?
Joyner, M. J., & Limberg, J. K. (2016) · Current Hypertension Reports · doi:10.1007/s11906-015-0616-3 · Cited by 10 · see citing works
Self-citationBaker, S. E., Limberg, J. K., Scruggs, Z. M., Curry, T. B., Nicholson, W. T., Barnes, J. N., & Joyner, M. J. (2020) · Hypertension · doi:10.1161/hypertensionaha.119.14042 · Cited by 9 · see citing works
“MSNA, however, fluctuates across the menstrual cycle where it is greatest in the low-hormone early follicular phase and highest in the high-hormone midluteal phase of the menstrual cycle.(35,36) These changes are thought to be related to changes in circulating hormone levels, particularly estrogen.”
BackgroundSelf-citationD’Souza, A. W., Hissen, S. L., Okada, Y., Jarvis, S. S., Washio, T., Akins, J. D., Nelson, D. B., & Fu, Q. (2022) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00239.2022 · Cited by 9 · see citing works
Self-citationGreenlund, I. M., Bigalke, J. A., Tikkanen, A. L., Durocher, J. J., Smoot, C. A., & Carter, J. R. (2021) · SLEEP · doi:10.1093/sleep/zsab130 · Cited by 11 · see citing works
Self-citationCardiovascular Autonomic Profile in Women With Premenstrual Syndrome
Koifman, R., Dayan, L., Ablin, J. N., & Jacob, G. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01384 · Cited by 9 · see citing works
Bigalke, J. A., Greenlund, I. M., Solis-Montenegro, T. X., Durocher, J. J., Joyner, M. J., & Carter, J. R. (2024) · Hypertension · doi:10.1161/hypertensionaha.124.23416 · Cited by 10 · see citing works
Self-citationCoovadia, Y., Shoemaker, J. K., & Usselman, C. W. (2023) · Autonomic Neuroscience · doi:10.1016/j.autneu.2023.103093 · Cited by 7 · see citing works
Shiozawa, K., Saito, M., Lee, J. B., Kashima, H., Endo, M. Y., Ishida, K., Millar, P. J., & Katayama, K. (2023) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00472.2023 · Cited by 7 · see citing works
Miranda, K. T., Schwende, B. K., Duval, A., Streed, C. G., Delage, S. I., Chokly, K., Hodgins, V., & Usselman, C. W. (2025) · Autonomic Neuroscience · doi:10.1016/j.autneu.2025.103283 · Cited by 6 · see citing works
Sex differences in blood pressure responsiveness to spontaneous K-complexes during stage II sleep
Greenlund, I. M., Smoot, C. A., & Carter, J. R. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00825.2020 · Cited by 6 · see citing works
Self-citationSex differences in autonomic function
Fu, Q. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-85492-4.00056-9 · Cited by 5 · see citing works
Self-citationThe influence of sleep on autonomic nervous system regulation in women across the lifespan
Bigalke, J. A., & Carter, J. R. (2025) · Autonomic Neuroscience · doi:10.1016/j.autneu.2025.103275 · Cited by 5 · see citing works
Self-citationHwang, C., Okazaki, K., Shibata, S., et al. (2021) · Clinical Autonomic Research · doi:10.1007/s10286-021-00832-3 · Cited by 5 · see citing works
“In women, MSNA and its response are influenced by the fluctuation in ovarian hormones throughout the menstrual cycle [2].”
BackgroundResultInfluentialSelf-citationThe sympathetic nervous system in normotensive and hypertensive pregnancies
Ayesha, S., Davenport, M. H., & Steinback, C. D. (2025) · Autonomic Neuroscience · doi:10.1016/j.autneu.2025.103293 · Cited by 4 · see citing works
“In non-pregnant populations there is a significant positive correlation between estrogen and MSNA (Charkoudian, 2001; Reyes et al., 2018a, Carter et al., 2013), and estrogen to progesterone ratio (Charkoudian, 2001).”
The Effect of Cardiovascular Responses after Aerobic Exercise in Menstrual Cycle
Park, J.-S., Kim, M.-S., Nho, H., et al. (2017) · Health · doi:10.4236/health.2017.93030 · Cited by 4 · see citing works
“After exercise, SV is reduced as suspended muscle contraction which helps to pump blood decreases venous return [22].”
BackgroundTsuda, K. (2013) · Hypertension · doi:10.1161/hypertensionaha.111.01075 · Cited by 3 · see citing works
Role of the ovarian cycle on neural cardiovascular control in sleep-deprived women
Yang, H., Durocher, J. J., Larson, R. A., & Carter, J. R. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00626.2014 · Cited by 2 · see citing works
“We hypothesized that resting MSNA would be augmented during the ML phase based on a recent study supporting the concept that the ML phases is sympathoexcitatory if certain surges of estradiol and progesterone are observed (7).”
BackgroundResultInfluentialSelf-citationSex and menstrual cycle effects on cerebrovascular responses to a single foot cold pressor test
Mei, Y., Allison, E. Y., Mizzi, V., et al. (2026) · Applied Physiology Nutrition and Metabolism · doi:10.1139/apnm-2024-0552 · Cited by 2 · see citing works
Resting metabolic rate fluctuations across the menstrual cycle: a systematic review
Hurtová, A., Gimunová, M., & Beníčková, M. (2026) · Frontiers in Physiology · doi:10.3389/fphys.2026.1778735 · Cited by 2 · see citing works
“This heightened sympathetic tone not only supports thermogenesis but may also stimulate metabolic processes that have been proposed to contribute to the elevated resting oxygen consumption observed in the luteal phase independently of temperature changes (Carter et al., 2013).”
Autonomic control during pregnancy
Brooks, V. L. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-85492-4.00084-3 · Cited by 2 · see citing works
Berbrier, D. E., Adler, T. E., Leone, C. A., Paidas, M. J., Stachenfeld, N. S., & Usselman, C. W. (2024) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00020.2024 · Cited by 2 · see citing works
The role of peripheral venous distension reflex in regulating hemodynamics: mini review
Hamaoka, T., Sinoway, L. I., & Cui, J. G. (2024) · Autonomic Neuroscience · doi:10.1016/j.autneu.2024.103217 · Cited by 2 · see citing works
Ghniem, S., Dawson, E. A., & Tryfonos, A. (2025) · Sports · doi:10.3390/sports13070210 · Cited by 2 · see citing works
Novel Advances in Our Understanding of Sex-Dependent Control of Blood Pressure
Muir, R. Q., Xu, J., Medcalf, A. D., & Pluznick, J. L. (2025) · Annual Review of Physiology · doi:10.1146/annurev-physiol-050724-022450 · Cited by 3 · see citing works
Sympathetic nervous system control across the menstrual cycle
Mei, Y., Allison, E. Y., Stone, J. C., & Al‐Khazraji, B. K. (2026) · Autonomic Neuroscience · doi:10.1016/j.autneu.2026.103438 · Cited by 1 · see citing works
Tabti, E., Benmekki, A., Bestaoui, M. H., Messaad, M., Ghembaza, A., & Lounici, A. (2018) · Annales de Cardiologie et d Angéiologie · doi:10.1016/j.ancard.2018.05.001 · Cited by 1 · see citing works
Short-Term Fasting and Autonomic Control
Gonzalez, J. E. (2021) · doi:10.37099/mtu.dc.etdr/1257 · Cited by 1 · see citing works
Uum, S. H. M. V., Kevin, J. C., Charlotte, S., Usselman, W., Luchyshyn, T. A., Gimon, T. I., Nielson, C. A., & Nicole, S. (2015)
Laffin, L. J., Jafar, M. S., & Bakris, G. L. (2017) · Journal of Clinical Hypertension · doi:10.1111/jch.13052
Just, T. P. (2018) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3jm23x23
Sex, Age, and Neurovascular Control
Joyner, M. J., Limberg, J. K., Ranadive, S. M., & Baker, S. E. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813197-8.00019-1
Self-citationWatso, J. C. (2024) · Library, Museums and Press - UDSpace (University of Delaware) · doi:10.58088/9f2f-3764
Voloshynska, K. O., Kovalchuk, S. М., Kovalchuk, M., & Peresunko, O. M. (2019) · ScienceRise Medical Science · doi:10.15587/2519-4798.2020.193270
Sympathetic Neural Responses to Acute Thermal Sensations
Cunningham, H. A. (2020) · doi:10.37099/mtu.dc.etdr/1042
Jacob, D. W. (2021) · doi:10.32469/10355/90966
“In other words, the greater the surge or increase in estrogen between phases from the low to high-hormone phase, the greater the change in resting, basal MSNA (10).”
BackgroundVenter, G., der Berg, C. L. V., Jacobs, T., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-16892-8
“At days 12–14, estrogen concentrations peak at ~ 160 pg/ml just prior to ovulation, after which the concentrations in the luteal phase decline to ~ 40–100 pg/ml 4,5 .”
Paterson, A. R., Loh, S.-Y., Gholami, S. K., et al. (2026) · Biology of Sex Differences · doi:10.1186/s13293-025-00818-0
“This strategy, however, presents potential issues with gene expression influences that arise from oestrus [69, 70], so this group was not assessed.”
- Authors
- Carter, J. R., Fu, Q., Minson, C. T., & Joyner, M. J.
- Affiliations
- Michigan Technological University (US)
- Venue
- Hypertension
- Published
- 2013-02
- Volume
- 61
- Issue
- 2
- Pages
- 395-399
- ISSN
- 0194-911X (ISSN-L)
- 1524-4563
- PMC
- PMC3548043
- OpenAlex
- W2140240484
- Cited by
- 105
- References
- 39
- Citations by year
- 2026: 9 · 2025: 8 · 2024: 5 · 2023: 7 · 2022: 3 · 2021: 6 · 2020: 15 · 2019: 5 · 2018: 6 · 2017: 7 · 2016: 5 · 2015: 12 · 2014: 11 · 2013: 6
- FWCI
- 5.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Hypertension (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Digital Commons - Michigan Tech (Michigan Technological University) (submittedVersion)
- Funders
- Michigan Technological University
- National Heart, Lung, and Blood Institute (HL 083947, R21HL098676, HL075283, HL088689, R15HL088689, K23HL075283, HL081671, R01HL081671, R01HL083947)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Menopause: Health Impacts and Treatments
- Keywords
- ovarian cycle, muscle sympathetic nerve activity, sympathoexcitation, mid-luteal phase, estradiol, progesterone, mean arterial pressure, premenopausal women, eumenorrheic women
- MeSH terms
- Adult, Blood Pressure, Estradiol, Female, Heart Rate, Humans, Menstrual Cycle, Progesterone, Retrospective Studies, Sympathetic Nervous System, Body Mass Index, Premenopause
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