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The Journal of Clinical Endocrinology & Metabolism Vol. 83, No. 1 76-80
Copyright © 1998 by The Endocrine Society

Original Studies

Effects of Fasting on Neuroendocrine Function and Follicle Development in Lean Women1

Ruben Alvero, Lorene Kimzey, Nancy Sebring, James Reynolds, Marion Loughran, Lynnette Nieman and Beatriz R. Olson

William Beaumont Army Medical Center (R.A.), El Paso, Texas 79922; Warren G. Magnuson Clinical Center, Departments of Nursing (L.K., M.L.), Diet and Nutrition (N.S.), and Nuclear Medicine (J.R.), Developmental Endocrinology Branch, National Institutes of Child Health and Human Development (L.N.), National Institutes of Health, Bethesda, Maryland 29892; and Waterbury Hospital (B.R.O.), Waterbury, Connecticut 06702

Address all correspondence and requests for reprints to: Dr. Ruben Alvero, Department of Obstetrics and Gynecology, William Beaumont Army Medical Center, 5005 North Piedras, El Paso, Texas 79922-5000.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
A 72-h fast in normal weight women during the follicular phase results in transient alterations in neuroendocrine function, but follicle development and follicular phase length remain unaltered. In this study we evaluated neuroendocrine and ovulatory function in lean women (body fat, <=20%) undergoing a similar 72-h fast.

Compared to fed controls, fasted lean women experienced significant weight loss, blunting of the diurnal variation of cortisol, suppression of the nocturnal TSH rise, and a decrease in T3 levels after a 72-h fast. In contrast to similarly fasted, normal weight women, lean women have significantly higher evening cortisol levels and do not exhibit a normal nocturnal TSH rise after the fast. Lean fasted women exhibited a 19% decrease in the number of LH pulses over 24 h compared to fed women (12.9 ± 1.3 vs. 16.0 ± 1.9; P < 0.05). Fasting did not result in significant differences in mean LH, LH amplitude, LH area under the curve, and mean FSH levels in these lean women. Of the seven fasted cycles, two were anovulatory. In the five women studied in fed and fasted cycles, one had interrupted lead follicle development with anovulation, and four had significant lengthening of the follicular phase compared to those during their fed cycles (14.4 ± 1.2 vs. 13.2 ± 1.0 days; P = 0.01).

The clinical observations made in this small sample of lean women showing more profound changes in neuroendocrine function, anovulation, and lengthened follicular phase after fasting suggest that lean women may be more vulnerable to fasting stress than normal weight women.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
WE AND OTHERS have shown that a 72-h fast in normal weight women decreases LH pulse frequency by 15–20% (1, 2) without significantly affecting follicle development (1). In our previous study, lead follicle growth was disrupted only in the leanest subject. It is well known that prolonged food deprivation or energy deprivation through vigorous exercise results in hypothalamic amenorrhea and menstrual dysfunction (3, 4, 5, 6, 7, 8, 9, 10). Men and monkeys, who have in common low body fat, have profound suppression of the hypothalamic-pituitary-gonadal axis within 24 h of fasting (11, 12, 13). Based on these data, we hypothesized that baseline energy expenditure or body fat stores may regulate the susceptibility of the hypothalamic-pituitary-gonadal axis to energy withdrawal. Therefore, the present study was designed to investigate whether lean women have clinically relevant alterations in reproductive function after a 72-h fast in the midfollicular phase, which is an important time in dominant follicle development. To do this, we recruited eight lean (body fat, <=20%), menstruant women. Subjects were initially randomized to either fast or eat for 72 h on cycle days 7–9 of the follicular phase, using our previous study design for normal weight women (body fat, 26–27%) (1). Follicular development was assessed using transvaginal ultrasonography.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

Eight healthy menstruant women participated in the study after giving informed consent for a protocol approved by the investigational review board of the NICHHD. Five of the 8 subjects served as their own controls, participating in fed and fasted study cycles. Thus, a total of 13 menstrual cycles were studied. Subjects were recruited by newspaper advertisement searching for lean, menstruating women. Eating disorders were excluded by a score of 5 points or less on the Eating Aptitudes Test (EAT) questionnaire (14). Inclusion criteria required normal medical and psychiatric histories, normal physical examination, no medication use, a body mass index of 20 or less, menstrual cycle lengths of 26–31 days during the previous 6 months, and willingness to use barrier methods of contraception during the study. No woman exercised more than 1.5 h at a time or more than 5 times/week during the study period. The reported physical activities included walking, weight lifting, aerobic dancing, and bicycling.

A baseline dietary history and body mass composition determination were obtained for all women. Body composition determination by bioelectrical impedance (BIA) was performed as previously described (1). Only subjects with a body fat composition of 20% or less on the bioelectrical impedance determination could participate. These eight women also had whole body fat composition determination by dual x-ray densitometry to determine site-specific fat distribution. An ovulatory cycle was documented before study cycles using a LH surge detection kit.

Protocol

Subjects were admitted to the NICHHD Clinical Research Unit on the evening of cycle day 5 and remained on the ward without exercising. Weight and urinary ketone measurements were obtained daily. Subjects maintained their usual sleep patterns while hospitalized. In the first study cycle, women were randomized either to fast on cycle days 7–9 or to continue a weight maintenance diet. As in our previous study, on cycle day 6 all subjects ate a 35 cal/kg/day weight maintenance diet divided into four feedings (three meals and one snack). This diet (50% carbohydrate, 20% protein, and 30% fat) consisted of the same food every day for those assigned to the weight maintenance diet (1). Saline (NaCl; 0.15 mol/L at a rate of 75 mL/h by vein) was administered to all women (fed and fasted) on cycle days 7–9. Five women repeated the study after a 1-month rest period and received the alternate diet protocol. Women kept a menstrual calendar throughout the protocol.

Hormone measurements

Urine was collected from all subjects at the same time each afternoon from cycle day 9 for detection of the LH surge using the OvuQuick 9 day kit (Monoclonal Antibodies, Sunnyvale, CA). Except for progesterone and out-patient estradiol determinations, all blood samples for hormonal evaluation were obtained through indwelling venous catheters. Samples for measurement of GH and T3 and cortisol were obtained on cycle days 6 and 9. Samples for estradiol determinations were obtained each morning during hospitalization and then every other day until the LH surge or cycle day 15. Evaluation of the diurnal secretory patterns of TSH and cortisol was performed as previously described (1). Briefly, samples were obtained hourly from 1700–1900 h and from 2300–0100 h for TSH measurments and at 0600 and 0000 h for cortisol determinations. The TSH values for each 3-h period were averaged to obtain mean afternoon and nighttime values. Blood samples were obtained every 10 min for 24 h beginning at 0001 h on cycle day 9 for the measurement of LH by RIA. Serum from the 24-h sampling was used to measure FSH by RIA at 30-min intervals.

Transvaginal ultrasonography

Transvaginal ultrasonography was performed by a single examiner at approximately the same time each day from cycle day 6 until the dominant follicle collapsed, using the General Electric RT 3600 transvaginal 5 MHz Ultrasound Unit (Rancho Cordova, CA). Two perpendicular diameters were recorded for the longitudinal and transverse views of the largest follicle each day. The mean of these four measurements was considered the follicle diameter for that day. Although the dominant follicle usually was evident by cycle day 7, other follicles in each ovary were monitored to assure consistent location and identification of the growing dominant follicle.

Hormone assays

Serum from blood samples was stored at -70 C until assayed. Hormones and peptides were measured by RIA using commercially available kits at Hazelton Laboratory (Vienna, VA). Samples for each hormone were run in the same assay to avoid interassay variability. Serum LH RIA assay sensitivity was 0.3 IU/L (a 10-fold increase in sensitivity from that of the assay used in our previous study (1), and the intraassay coefficient of variation was 3.4%. For all other assays, the inter- and intraassay coefficients of variation were as previously described (1).

Analysis of gonadotropin secretion

LH secretory characteristics (pulse frequency, amplitude, mean, and LH area under the curve) were analyzed by the Cluster 5.0 program (provided by Dr. Johannes Veldhuis, University of Virginia, Charlottesville, VA) (15, 16) using criteria previously described (1). Briefly, each data set for a 24-h sampling period contained 147 duplicate samples, a test cluster size of 2 x 1 (nadir and peak), and a t statistic (peak detection threshold) of 2 for the peak upstroke and downstroke, and the minimum absolute value required for the detection of a LH peak was set at 0.6 IU/L (twice the assay sensitivity) (15). The LH pulse frequency and peak amplitude, mean LH, and LH area under the curve were calculated by the program and used for comparison by cycle day between fed and fasted cycles. Only pulses detected by the Cluster program were used for analysis. A mean FSH value was obtained from the FSH values obtained for each woman on cycle day 9.

Statistical analyses

The follicular phase length was defined as beginning on the first day of vaginal bleeding and ending on the day of the LH surge, and the luteal phase length was defined as beginning on the day after the LH surge and ending on the day before the onset of the next menses. Data are presented as the mean ± SE in all tables and graphs. The Statistica program (Macintosh, Statsoft, Tulsa, OK) was used for statistical analyses. Comparison of parameters was performed between fed and fasted groups using ANOVA or repeated measures ANOVA and/or post-hoc paired or unpaired t tests. Paired comparisons were made in subjects completing both fed and fasted cycles. Unpaired t tests were made between six fed and seven fasted cycles. Data were considered significant at P <= 0.05.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Hypothalamic effects of the fast in lean women

The baseline demographics and cycle characteristics of the women studied are shown in Table 1Go. Despite the leanness detected by the BIA, there was a wide spectrum of site-specific percent body fat in these women, with the trunk having the lowest and the thighs the highest fat content. Fasting physiology was achieved in women fasted on cycle days 7–9. These subjects had ketonuria 24 h after entering the fast. Fasted women had significant weight loss by cycle day 9 (P = 0.038) compared to their baseline weights on cycle day 6. Body weight in fed women remained unchanged.


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  		Table 1. Baseline demographics and cycle characteristics of the eight women studied

 
Table 2Go shows the hormone levels on cycle days 6 and 9 in fed and fasted lean women and on cycle day 9 in similarly fasted normal weight women (1). GH levels were not significantly different between fed and fasted women at any time during the study. Mean nighttime TSH levels were significantly lower on cycle day 9 in fasted women (P < 0.05) than in fed women, and the nocturnal rise in TSH, which was present on cycle day 6 in all women, was lost on cycle day 9 in fasted lean women only (P < 0.05). T3 levels were significantly lower in fasted women on day 9 compared to baseline day 6 levels (P = 0.046). T3, TSH, and the nocturnal TSH rise did not change during the study in fed women.


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  		Table 2. Hormone values on cycle days 6 and 9 of lean (body fat, <=20%) women studied in fed in fed and fasted cycles

 
Evening cortisol levels on day 9 in fasted women were significantly higher than these women’s values on day 6 (P < 0.05) and those in fed women on cycle day 9 (P = 0.05). The evening elevation in cortisol levels and the loss of the normal nocturnal TSH rise after fasting occurred in the lean women, but not in similarly fasted normal weight women previously studied (1).

Effects of fasting on the hypothalamic-pituitary-ovarian axis of lean women

Figure 1Go shows the individual LH pulsatility data for the five women who participated in fed and fasted cycles. Note that four of five women had decreases in LH pulsatility, ranging between 13.1–42%. One subject had an increase in LH pulse number of 10%.



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  		Figure 1. LH pulsatility during 24 h on cycle day 9 in the five women that underwent both fasted (left panels) and fed (right panels) study cycles. Cycle day 9 in fasted cycles was the third day of the fast. The values on the y-axis vary to accommodate individual LH pulse amplitudes for each woman. The asterisks represent pulses identified using Cluster pulse analysis from which statistics are derived. The circles reflect visually apparent pulsatile events not detected by the program in each set of data.

 
Paired comparisons of mean LH pulses in fed and fasted women did not reach statistical significance (P = 0.06). Table 3Go shows the number of LH pulsatile events, LH area under the curve, mean LH, LH amplitude, and mean FSH obtained over 24 h on cycle day 9 of all fed and fasted cycles. Compared to fed cycles, fasted cycles as a group had a significantly lower number of LH pulses detected by the Cluster program (P < 0.05). This decrement is consistent with a 19% decrease in pulsatile events over 24 h. The area under the curve for LH, the mean LH, the mean LH amplitude, and the mean FSH values were not significantly different between fed or fasted women, although a trend for higher FSH levels was noted in fasted women.


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  		Table 3. LH pulse frequency, LH area under the curve (AUC), LH pulse amplitude, and mean LH in lean women undergoing fed and fasted cycles

 
Figure 2Go shows the daily dominant follicle development for individual women in all cycles studied. All women studied in fed cycles showed a normal progression of dominant follicle growth, attaining follicle diameters greater than 17 mm before ovulation. The period from detection of the dominant follicle to ovulation for the fed women ranged from 5–9 days. In contrast, women undergoing fasted cycles had evidence of abnormal follicle development. All five women studied in fed and fasted cycles had notable alterations in aspects of follicle development. We noted a 1- to 2-day prolongation of dominant follicle growth until ovulation (subjects A, B, C, and D), resulting in a significant lengthening of the follicular phase from 13.2 ± 1.0 days in fed cycles to 14.4 ± 1.2 days in fasted cycles (P = 0.01) and dysfunctional follicle development with failure to ovulate (subject E). Subject G, studied during fasting only, had abnormal dominant follicle growth and did not ovulate. Abnormal follicle growth in these latter two subjects was first detected 24 h after the end of the fast. In Table 1Go note that when comparisons of follicular lengths were made by unpaired analysis of six fed vs. seven fasted cycles, statistical significance was lost. In sum, of seven fasted cycles, two resulted in anovulation, and four were shown to have prolongation of the follicular phase.



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  		Figure 2. Dominant follicle development from cycle day 6 until ovulation in ovulatory cycles for the eight women studied. Subjects A–E were studied in both fed and fasted cycles. Note the failure of follicle development in two of the seven fasted cycles (subjects E and G). Note that peak follicle size before ovulation is larger and occurs 1–2 days later in fasted cycles than in fed cycles (subjects A–D).

 
Estradiol levels were significantly different between the fed and fasted cycles when paired comparisons of mean estradiol levels for cycle day were made (Fig. 3Go; P = 0.049). Specifically, fed and fasted groups differed on the morning of the first day of the fast (87.6 ± 9.7 vs. 44.7 ± 10.4 pg/mL; P = 0.01), estrogen values were similar during the fast and were again noted to be different transiently after the fasted period (mean estradiol values for days 11 and 12, 174.9 ± 56 and 72.4 ± 14.8 pg/mL; P = 0.043). As all fed women had ovulated by day 15, no estradiol levels were obtained thereafter. For all ovulatory cycles, progesterone levels 1 week after ovulation were similar (P = 0.271) in fed (16.6 ± 5.4 ng/ml) and fasted (8.3 ± 4.2 ng/ml) women.



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  		Figure 3. Serum estradiol levels (mean ± SEM) from cycle day 6 to cycle day 15 in fed (n = 6) and fasted (n = 7) women in all cycles studied. The asterisk denotes a significant difference (P < 0.05) between fed and fasted groups on that cycle day. Estradiol values on days 11–12 and days 13–14 are averaged because of the alternate day sampling schedule.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
In this small cohort of lean women fasted for 72 h in the midfollicular phase, we found that fasting resulted in a 19% reduction in the number of LH pulses per 24 h. This finding is consistent with data from previous studies demonstrating a 20% decrease in LH pulsatility in normal weight, fasted women (1, 2). The novel observations in this study are that decrements in LH pulse frequency are associated in some women with a range of alterations in the pattern of follicle development in that fasted cycle. Two of seven women had complete ablation of dominant follicle growth. Additionally, in all five women studied in fed and fasted cycles, we found perturbations in follicle development; one woman failed to ovulate, and the other four had significant lengthening of their follicular phases compared to those during fed cycles.

The pattern of gonadotropin suppression in our population primarily showing suppression of LH, but not FSH, is consistent with prior studies that suggest that there is preferential inhibition of LH compared to FSH when women are given GnRH antagonists (17, 18). Our data for follicle growth disruption are also consistent with the sensitivity of the emerging dominant follicle in the midfollicular phase to gonadotropin withdrawal in these studies. Consistent with our findings in normal weight women, we found relatively higher, although not statistically significant, FSH levels in fasted women, which may reflect the presence of lower estrogen levels after fasting.

A striking feature of the women studied was their leanness. It was very difficult to find this lean cohort of women with normal menstrual cycles and exercise habits similar to those of the normal weight women of our previous study (1). Although the overall body mass composition was less than 20%, as measured by the BIA, fractionating the fat distribution using dual energy x-ray absortiometry scan showed that the trunk was quite lean comapared to the periphery, but the pear-shaped body types did not vary between our two studies. The ability of some of these women to maintain normal cyclicity despite high lean/fat ratios may be related to this distribution. In this regard it is also interesting to note that despite the perturbations described in the lean fasted subjects, five of the seven women did go on to ovulate. In 1974, Frisch and McArthur theorized that the maintenance of normal menstrual function was related to a critical level of 22% body fat (19). We speculate that site-specific body composition may also be important in regulating reproductive function.

Consistent with prior observations of thyroid function in an acute fast (1, 2, 20, 21), TSH and T3 levels declined during this study in the fasted cycles. In contrast to prior observations in normal weight women (1, 22, 23), lean fasted women do not show a nocturnal TSH rise and have blunted diurnal variation in cortisol secretion after fasting. These changes in TSH and cortisol secretory dynamics suggest that fasting may be more stressful in individuals with lower energy stores.

The clinical observations made in this study are limited by the statistical power of our sample size. Therefore, our data suggest, but do not prove, that lean women may be at higher risk of developing neuroendocrine and follicular phase reproductive abnormalities when nutrition is acutely withdrawn. Nutrition, food intake habits, and percent body fat may be relevant factors that can be altered without significant financial cost when evaluating and treating lean women that present with anovulation and/or infertility.


   Footnotes
 
1 This work was conducted at the NIH with funding from the NICHHD while Dr. Alvero completed the research year of his Fellowship in Reproductive Endocrinology at the NIH (Bethesda, MD). Back

Received December 30, 1996.

Revised July 16, 1997.

Revised September 18, 1997.

Accepted September 18, 1997.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

  1. Olson BR, Cartledge T, Sebring N, Defensor R, Nieman L. 1995 Short-term fasting affects luteinizing hormone secretory dynamics but not reproductive function in normal-weight sedentary women. J Clin Endocrinol Metab. 80:1187–1193.[Abstract]
  2. Loucks AB, Heath EM, Law T, Verdun M, Watts JR. 1994 Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women. J Clin Endocrinol Metab. 78:910–915.[Abstract]
  3. Warren MP, Vande Wiele RL. 1973 Clinical and metabolic features of anorexia nervosa. Am J Obstet Gynecol. 117:435–449.[Medline]
  4. Vigersky RA, Andersen AE, Thompson RH, Loriaux DL. 1977 Hypothalamic dysfunction in secondary amenorrhea associated with simple weight loss. N Engl J Med. 297:1141–1145.[Abstract]
  5. Marshall JC, Kelch RP. 1979 Low dose pulsatile gonadotropin-releasing hormone in anorexia nervosa: a model for human pubertal development. J Clin Endocrinol Metab. 49:712–718.[Abstract]
  6. Boyar RM, Katz J, Finkelstein JW, et al. 1984 Anorexia nervosa: immaturity of the 24 hour luteinizing hormone secretory pattern. N Engl J Med. 291:861–865.
  7. Warren MP. 1980 The effects of exercise on pubertal progression and reproductive function in girls. J Clin Endocrinol Metab. 51:1150–1157.[Abstract]
  8. Frisch RE, Wyshak G, Vincent L. 1980 Delayed menarche and amenorrhea in ballet dancers. N Engl J Med. 303:17–19.[Medline]
  9. Bullen BA, Skrinar GC, Beitins IZ, von Mering G, Turnbull BA, McArthur JW. 1985 Induction of menstrual disorders by strenuous exercise in untrained women. N Engl J Med. 312:1349–1353.[Abstract]
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