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Follicle-Stimulating Hormone Is Secreted More Irregularly Than Luteinizing Hormone in Both Humans and Sheep

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Follicle-Stimulating Hormone Is Secreted More Irregularly Than Luteinizing Hormone in Both Humans and Sheep Follicle-stimulating hormone is secreted more irregularly than luteinizing hormone in both humans and sheep. S M Pincus, … , J Randolph, A Rees Midgley J Clin Invest. 1998;101(6):1318-1324. https://doi.org/10.1172/JCI985. Research Article Recently introduced statistical tools capable of discerning differences between the pattern of luteinizing hormone (LH) secretion and that of follicle-stimulating hormone (FSH) could be valuable in understanding ovulation and menopause, and ultimately in making diagnostic decisions and treating infertility and polycystic ovary syndrome. We assessed the validity and scope of the hypothesis that FSH is secreted more irregularly than LH in ewes and fertile women. We compared secretory irregularity of LH to that of FSH in both ovariectomized ewes (n = 7) and women of proven fertility (n = 5) during the follicular and luteal phases of their reproductive cycles. In each sheep, time series from both hypophyseal portal blood (HPB) and peripheral blood were evaluated in 72 samples obtained every 5 min; in each human, both luteal and follicular periods were studied in 192 samples obtained every 7.5 min. To quantify serial irregularity, we used approximate entropy (ApEn), a scale- and model-independent statistic. FSH secretion was consistently more irregular than that of LH in each subject. For sheep HPB, ApEn(FSH) = 1.415+/-0.097 was larger than ApEn(LH) = 0. 822+/-0.213, P < 0.0001 (mean+/-SD, paired t test). This difference persisted peripherally: ApEn(FSHper) = 1.431+/-0.101 > ApEn(LHper) = 1.252+/-0.086, P = 0.024. In women, ApEn(FSH) = 1.467+/-0.217 > ApEn(LH) = 0.923+/- 0.305, P < 0.0001. ApEn(FSH) > ApEn(LH) in 100% of […] Find the latest version: https://jci.me/985/pdf Follicle-stimulating Hormone Is Secreted More Irregularly Than Luteinizing Hormone in Both Humans and Sheep Steven M. Pincus,* Vasantha Padmanabhan,‡ William Lemon,‡ John Randolph,‡ and A. Rees Midgley‡ *Guilford, Connecticut 06437; and ‡Reproductive Sciences Program, University of Michigan, Ann Arbor, Michigan 48109 Abstract Introduction Recently introduced statistical tools capable of discerning At least 15% of married couples in the USA (z 4.5 million) of differences between the pattern of luteinizing hormone (LH) reproductive age will experience some degree of infertility (1). secretion and that of follicle-stimulating hormone (FSH) Infertility difficulties are enhanced with increasing female age: could be valuable in understanding ovulation and meno- among healthy women without detectable reproductive disor- pause, and ultimately in making diagnostic decisions and ders, infertility in women ages 35–39 is estimated to be z 25%, treating infertility and polycystic ovary syndrome. We as- and in women 40 yr or older, z 27% (1). The properly regu- sessed the validity and scope of the hypothesis that FSH is lated release of hormones by both the hypothalamus and pitu- secreted more irregularly than LH in ewes and fertile itary gland is one essential requirement for monthly ovulation. women. We compared secretory irregularity of LH to that of If the hypothalamus functions abnormally, follicles will de- FSH in both ovariectomized ewes (n 5 7) and women of velop improperly, often resulting in anovulation. Thus, greater proven fertility (n 5 5) during the follicular and luteal understanding of gonadotropin-releasing hormone (GnRH),1 phases of their reproductive cycles. In each sheep, time se- luteinizing hormone (LH), and follicle-stimulating hormone ries from both hypophyseal portal blood (HPB) and periph- (FSH) secretion, and concomitant relationships among these eral blood were evaluated in 72 samples obtained every 5 hormones, is of vital importance scientifically, in understand- min; in each human, both luteal and follicular periods were ing the physiology of ovulation, and ultimately clinically in studied in 192 samples obtained every 7.5 min. To quantify treating disorders. serial irregularity, we used approximate entropy (ApEn), a Until recently, word models of pituitary secretion of LH scale- and model-independent statistic. FSH secretion was and FSH rendered their dynamics in a virtually identical fash- consistently more irregular than that of LH in each subject. ion since they are presumed to be driven commonly by GnRH For sheep HPB, ApEn(FSH) 5 1.41560.097 was larger than (2). Assuming common stimulation has led to tacit discounting ApEn(LH) 5 0.82260.213, P , 0.0001 (mean6SD, paired of differences in their secretory patterns or attribution of those t test). This difference persisted peripherally: ApEn(FSHper) 5 differences to changes or differences in clearance rates or iso- 1.43160.101 . ApEn(LHper) 5 1.25260.086, P 5 0.024. In forms (2, 3). Recently, detailed characterizations of circulating women, ApEn(FSH) 5 1.46760.217 . ApEn(LH) 5 0.9236 patterns of LH and FSH have uncovered differences in regula- 0.305, P , 0.0001. ApEn(FSH) . ApEn(LH) in 100% of tion of these two hormones, giving credence to efforts to mea- women (peripheral) and sheep HPB. Secretion during the sure and understand differences in patterns of secretion (4–6). follicular phase was more irregular than during the luteal Visually, it appears that the secretory pattern of FSH in sheep phase for both FSH and LH (P , 0.01). LH mean level se- is more complicated than that of LH, with many more minor cretion showed a wake/sleep difference in women, P , episodes or subordinate activity when measured from hypo- 0.005, with higher values awake. The consistency and statis- physeal portal blood (HPB), and somewhat less so when mea- tical significance of these findings suggest that this LH/FSH sured in peripheral blood (Fig. 1) (7). Motivated by this obser- difference may be broadly based within higher mammals. vation, we attempted to quantify the observed differences Ranges of normative and abnormal regularity values of LH, using approximate entropy (ApEn) (8, 9) (described below), FSH, and their difference can be used in a number of set- determine the breadth of the apparent finding across species tings, both (currently) research and (potentially ultimately) by analyses of both ovariectomized ewes and humans, and esti- clinical milieus. (J. Clin. Invest. 1998. 101:1318–1324.) Key mate the consistency of the finding. words: gonadotropin • irregularity • pulsatility • menopause • infertility Methods Sheep study. The experimental design and description of assays of Portions of this work were presented at the 24th annual meeting of LH and FSH in peripheral (jugular) and HPB of ovariectomized the Society of Neuroscience in Miami, FL, 13–18 November 1994 and sheep used in this study, herein statistically analyzed by ApEn, have at the 10th International Congress of Endocrinology in San Fran- been described previously (7, 10, 11). This method for monitoring LH cisco, CA, 12–15 June 1996. and FSH in portal blood reveals the dynamics of pituitary hormone Address correspondence to Steven M. Pincus, 990 Moose Hill secretion without deconvolution (11). In brief, the procedure in- Road, Guilford, CT 06437. Phone: 203-458-3455; FAX: 203-458-9063. volved surgically fitting ovariectomized Suffolk ewes with an appara- Received for publication 20 June 1997 and accepted in revised tus for collection of HPB (12, 13). 1 wk later, the sheep were heparin- form 30 December 1997. J. Clin. Invest. © The American Society for Clinical Investigation, Inc. 1. Abbreviations used in this paper: ApEn, approximate entropy; 0021-9738/98/03/1318/07 $2.00 FSH, follicle-stimulating hormone; GH, growth hormone; GnRH, go- Volume 101, Number 6, March 1998, 1318–1324 nadotropin-releasing hormone; HPB, hypophyseal portal blood; LH, http://www.jci.org luteinizing hormone. 1318 Pincus et al. mane to this analysis. Additionally, ApEn provides a direct barome- ter of feedback system change in many coupled systems (24, 25). In endocrine pathophysiology, ApEn has shown vivid distinctions (P , 10210) between normal and tumor-bearing subjects for growth hor- mone (GH) (26), ACTH and cortisol (27), and aldosterone (28), a pronounced and consistent gender difference in GH irregularity in both humans and rats (29), and a positive correlation between greater irregularity (larger ApEn) of GH and advancing age (30). ApEn assigns a nonnegative number to a time series, with larger values corresponding to greater apparent process randomness (serial irregularity), and smaller values corresponding to more instances of recognizable features or patterns in the data. Two input parameters, m and r, must be specified to compute ApEn. ApEn measures the logarithmic likelihood that runs of patterns that are close (within r) for m contiguous observations remain close (within the same toler- ance width r) on next incremental comparisons (8). For this study, we calculated ApEn values for all data sets, m 5 1 and r 5 20% of the standard deviation (SD) of the individual subject Figure 1. LH and FSH concentrations (ng/ml) measured at 5-min in- time series. Normalizing r to each time series SD gives ApEn a trans- tervals for 6 h from an ovariectomized ewe, with respective ApEn lation- and scale-invariance to absolute serum concentration levels (1, 20% SD) values. (A) Secreted (HPB) LH, ApEn 5 0.625; (B) se- (19). ApEn is a relative measure of process regularity, and can show creted (HPB) FSH, ApEn 5 1.256; (C) peripheral LH, ApEn 5 significant variation in its absolute numerical value with changing 1.161; and (D) peripheral FSH, ApEn 5 1.486. background noise characteristics. Since ApEn generally increases with increasing process noise (and increasing intraassay variation), it is appropriate to compare data sets with similar assay CVs, as we do here. Also, most importantly, despite algorithmic similarities, ized, the anterior face of the pituitary was lesioned, catheters from ApEn(m, r) is not intended (8, 9, 31) as an approximate value of the apparatus and jugular vein were run to fraction collectors in an the Kolmogorov-Sinai (K-S) entropy.
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