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Induction of precocious puberty in heifers I: Enhanced secretion of luteinizing hormone¹

Department of Animal Sciences, The Ohio State University, Columbus 43210

	Abstract

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In beef heifers weaned between 3 and 4 mo of age and fed a high-concentrate diet, approximately 50% reach puberty before 300 d of age (precocious puberty). The objectives of this experiment were 1) to determine whether precocious puberty could be induced experimentally by weaning heifers early and feeding a high-concentrate diet, and 2) to determine the dynamics of secretion of LH associated with precocious puberty. Crossbred Angus and Simmental heifer calves were weaned at 73 ± 3 d of age and 115 ± 3 kg of BW and fed a high-concentrate (60% corn; HI, n = 9) or control diet (30% corn; CONT, n = 9). Heifers were fed individually, and target BW gains were 1.50 and 0.75 kg/d for the HI and CONT treatments, respectively. Heifers were weighed every 2 wk. Blood samples were collected weekly and assayed for progesterone concentration to determine age at puberty. Serial blood samples were collected at 20-min intervals for 24 h at mean ages of 102, 130, 158, 172, 190, 203, 217, 231, and 259 d and assayed for LH concentration to evaluate the dynamics of secretion of LH. Heifers fed the HI diet exhibited greater BW gain (P < 0.01) than CONT heifers (1.27 ± 0.05 vs. 0.85 ± 0.05 kg/d, respectively). As a result, BW in the HI treatment was greater (P < 0.01) than in the CONT treatment by 188 d of age and remained different through the end of the experiment. Precocious puberty occurred in 8 of 9 heifers fed the HI diet and 0 of 9 heifers fed the CONT diet. Age at puberty was reduced in the HI (P < 0.01) compared with the CONT heifers (262 ± 10 vs. 368 ± 10 d of age, respectively). Body weight at puberty was also reduced in the HI (P < 0.05) compared with the CONT treatment (327 ± 17 vs. 403 ± 23 kg, respectively). Heifers attaining puberty during the experiment continued with subsequent luteal phases as evidenced by cyclic patterns of progesterone concentrations. Frequency of pulses of LH (pulses/24 h) increased with age (P < 0.01) for both treatments. Heifers in the HI treatment exhibited a greater number of pulses of LH (P < 0.01) than those in the CONT treatment by 190 d of age and in all subsequent collection periods (treatment x age, P < 0.05). Mean LH concentrations also increased with age (P < 0.01) for both treatments but did not differ between treatments. In conclusion, precocious puberty induced by early weaning and feeding of a high-concentrate diet is preceded by increasing frequency of pulses of LH.

Key Words: early weaning • heifer • luteinizing hormone • puberty

	INTRODUCTION

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To achieve optimal lifetime productivity, heifers should conceive early in their initial breeding season (Lesmeister et al., 1973), which occurs at 13 to 15 mo of age in most US systems. The likelihood of early conception in the initial breeding season is increased in heifers that have experienced multiple estrous cycles before onset of the breeding season (Byerly et al., 1987; Bagley, 1993). Unfortunately, failure to reach puberty at an appropriate time remains a major reason that heifers do not become pregnant during their first breeding season (Yelich et al., 1996).

Buskirk et al. (1995) reported the probability of heifers reaching puberty before the breeding season and conceiving to their first insemination increased as BW at weaning increased. Additionally, from other studies it seems apparent that heifer calves reached puberty at younger ages when they had greater BW at weaning or increased growth rates from birth to weaning, or both (Wiltbank et al., 1966; Arije and Wiltbank, 1971).

Wehrman et al. (1996) observed puberty before 300 d of age (precocious puberty) in 25 and 8% of heifers in 2 consecutive years and suggested the incidence of precocious puberty may have been related to increased growth rate around the time of weaning. Day and Anderson (1998) observed approximately 50% of heifers that were weaned at 3 to 4 mo of age and fed a high-concentrate diet through approximately 7 mo of age experienced spontaneous precocious puberty. With important aspects of reproductive development occurring during the first several months of age in heifers (for review see Day and Anderson, 1998), it is logical that environmental influences exerted during this time could accelerate sexual maturation. We hypothesized that precocious puberty could be induced in heifers weaned early and fed a high-concentrate diet and that earlier puberty would be associated with enhanced secretion of LH.

	MATERIALS AND METHODS

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Animals and Treatments
All animals were handled in accordance with procedures approved by The Ohio State University Agricultural Animal Care and Use Committee. Eighteen crossbred Angus and Simmental heifers were weaned at 73 ± 3 d of age and 115 ± 3 kg of BW and fed a receiving diet for 26 d after weaning. After the receiving period, heifers were blocked by age and BW and assigned randomly to receive a high-concentrate diet (n = 9; HI) or a control diet (n = 9; CONT). All diets consisted of whole shelled corn, alfalfa pellets, pelleted soybean hulls, and a supplement that contained ground corn, soybean meal, urea, vitamins, minerals, Rumensin, and fat (Table 1). The diets for the HI and CONT treatments were initiated at 99 ± 3 d of age.

Blood Sample Collection
Blood samples were collected weekly, beginning at a mean age of 130 d, via jugular venipuncture, centrifuged at 2,785 x g for 20 min immediately after collection, and plasma was frozen at –20°C until analyzed for progesterone concentration. Age at puberty was defined as 7 d before the date of collection of the first plasma sample that contained >2 ng of progesterone/mL or 7 d before the collection date of the first of 2 consecutive blood samples with >1 ng of progesterone/mL. Heifers that reached puberty before 300 d of age were considered to have experienced precocious puberty.

Serial blood samples were collected at 20-min intervals for 24 h when the mean age of the heifers was 102, 130, 158, 172, 190, 203, 217, and 231 d. Samples were collected via indwelling jugular catheters, blood was allowed to clot for 24 to 48 h at 4°C, samples were centrifuged at 7,735 x g for 20 min, and serum was harvested and frozen at –20°C until analyzed for LH concentration. Based on previous experience from our laboratory with serial blood sampling for detection of frequency of pulses of LH in ovary-intact heifers (Day et al., 1984, 1986, 1987), in which the frequency of pulses of LH consistently remained below 1 pulse/h through attainment of puberty, it was determined that a sampling interval of 20 min would be adequate to successfully detect the increase and decrease of LH concentrations associated with pulses of LH. Individual heifers were removed from serial blood sampling procedures after attainment of puberty was confirmed.

Hormone Analyses
Concentrations of LH were determined in duplicate for all serial blood serum samples with a double-antibody RIA previously validated in our laboratory (Anderson et al., 1996). Average intraassay CV was 3.4%, and average interassay CV for standard sera of 1.6 and 4.5 ng/mL were 13.2 and 13.2%, respectively. Average sensitivity of the assay was 0.1 ng/mL. Frequency of pulses of LH, amplitude of pulses of LH, and mean LH concentrations were determined as described by Goodman and Karsch (1980).

Concentrations of progesterone were determined using a commercially available RIA kit (Coat-a-Count, Diagnostic Products Corporation, Los Angeles, CA) as described previously for our laboratory (Burke et al., 2003). All weekly samples were included in a single assay. The intraassay CV was 1.6%, and the assay sensitivity was 0.02 ng/mL.

Statistical Analyses
The effects of treatment, age, and the interaction of treatment and age on BW, LH pulse frequency, mean LH pulse amplitude, and mean LH concentration were analyzed by ANOVA using the Mixed procedure of SAS (SAS Inst. Inc., Cary, NC), with repeated measures analysis included in the model. The repeated measures model was

where Y_ijk = observation of the j th heifer in the i th treatment on the k th day, µ = overall mean, T_i = i th treatment, h_j:i = random effect of the j th heifer within the i th treatment (h_j:i N[0,_h²]), D_k = k th day, (TD)_ik = treatment x day interaction, and e_ijk = random residual effect (e_ijk N [0, ]), where is the variance-covariance structure of the residual errors, with a first-order autoregressive (BW) or compound symmetry (LH variables) structure for repeated measurements within heifers.

The effect of treatment on ADG, age at puberty, and BW at puberty was analyzed by ANOVA using the MIXED procedure of SAS (model: Y_ij = µ + T_i + e_ij, with notations as defined previously).

	RESULTS

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The ADG during the time that heifers were fed the separate diets (mean age 99 to 286 d) differed (P < 0.01) at 1.27 ± 0.05 and 0.85 ± 0.05 kg/d for the HI and CONT treatments, respectively. Body weight of heifers in the HI treatment was greater (P < 0.01) than in the CONT treatment by mean age of 188 d, and heifers in this treatment remained heavier through the end of the experiment (treatment x age; P < 0.01; Figure 1). Subsequent to transition of heifers in the CONT treatment to the HI treatment diet at mean age of 286 d, ADG was less for HI than CONT treatment (1.10 ± 0.06 and 1.55 ± 0.06 kg/d, respectively).

View larger version (11K): [in this window] [in a new window]   Figure 1. Body weight of heifers from early weaning at 73 ± 3 d of age through a mean age of 362 d. All heifers were fed a receiving diet for 26 d after weaning, after which they were transitioned to a high-concentrate (HI) or control (CONT) diet. Body weight of heifers fed the HI diet was greater (P < 0.01) than CONT heifers from a mean age of 188 d through the end of the experimental period (treatment x age, P < 0.05). The arrow indicates the time at which transition of heifers in the CONT treatment to the diet fed in the HI treatment was initiated.

View larger version (11K): [in this window] [in a new window]   Figure 2. Cumulative percentage of heifers that were pubertal after early weaning and feeding either a high-concentrate (HI) or control (CONT) diet.

View larger version (15K): [in this window] [in a new window]   Figure 3. Age (d) and BW (kg) at puberty in heifers that were weaned early and fed a high-concentrate (HI) or control (CONT) diet. Heifers fed the HI diet were younger and lighter at puberty (*P < 0.05; **P < 0.01).

View larger version (10K): [in this window] [in a new window]   Figure 4. Concentration of LH during 3 serial blood collections at mean ages of 102, 190, and 217 d, for 1 heifer from each treatment, in heifers that were weaned early and fed a high-concentrate (HI) or control (CONT) diet. Serial blood samples were collected every 20 min for 24 h at each serial blood collection. The number of days relative to puberty are shown following the treatment label for each heifer at each serial blood collection.

View larger version (11K): [in this window] [in a new window]   Figure 5. Number of LH pulses/24 h in heifers that were weaned early and fed a high-concentrate (HI) or control (CONT) diet. Serial blood samples were collected every 20 min for 24 h at each serial blood collection. Frequency of pulses of LH was greater in heifers fed the HI diet than CONT heifers from a mean age of 190 d through all subsequent serial blood collections (treatment x age, P < 0.05; **Indicates that means differ within age, P < 0.01).

	DISCUSSION

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The factors responsible for induction of precocious puberty and acceleration of the peripubertal increase in secretion of LH when heifers are weaned early and fed a high-concentrate diet are unknown at present. Physiological responses to separation from their dam, accelerated growth rate as a result of increased energy density of the diet, qualitative aspects of the diet, or some interaction of these aspects are all potential factors responsible for precocious puberty. Variation may also exist among breeds and in their response to management systems and effectiveness of induction of precocious puberty with the model used in this experiment.

Precocious puberty was not induced in heifers in the control treatment even though they were weaned early, suggesting that this is not a primary factor responsible for precocious puberty. It is important to note, however, that the diet in the control treatment was not limiting; BW at the typical weaning age was comparable with that of heifers that remained with their dams in other years for heifers from this herd. For example, in a previous year (Day and Anderson, 1998) heifers weaned at 111 ± 4.3 d of age and fed a diet similar to the CONT diet in the current experiment were not different from contemporary heifers weaned at 202 ± 2.8 d of age for BW at 204 d of age (221 ± 7.6 and 228 ± 5.0 kg, respectively). Likewise, BW was 279 ± 12 kg and 276 ± 7 kg at 208 ± 3 d of age for early weaned heifers fed the CONT diet and heifers that remained with their dams in a subsequent year (Gasser et al., 2006).

Feeding the high-concentrate diet increased BW gain over that of heifers fed the control diet. Whereas heifers fed the high-concentrate diet were heavier through a large portion of the feeding period, puberty occurred at a lesser BW than in heifers from the control treatment. This finding is in contrast to results from other reports in which nutritionally induced advancement of puberty was associated with either similar or increased BW at puberty (Marston et al., 1995; Yelich et al., 1995, 1996). An important difference between these reports and the current study is that dietary treatments were initiated between 9 and 12 mo of age, whereas in the present experiment, diets were fed beginning at 99 d of age. That increased growth rate during the period before approximately 7 mo of age can alter age at puberty is not without precedent (Wiltbank et al., 1966; Arije and Wiltbank, 1971), but the extent of the reduction in age at puberty was much greater with the approach taken in the current study.

Qualitative differences in the diets, independent of effects on BW gain, cannot be overlooked as a possible causative factor for the responses observed in age at puberty and secretion of LH. The high-concentrate diet would be expected to increase the propionate:acetate ratio in the rumen. Sprott et al. (1988) has suggested that the increased propionate:acetate ratio in the rumen that is characteristic of ionophore feeding may be a cause of the decreased age at puberty seen in heifers that are fed ionophores. Conversely, Lalman et al. (1993) showed that supplementing heifer diets with propionic acid did not advance puberty when BW gain was held constant with that of control heifers. Comparison of age at puberty in animals receiving the HI treatment used in the current study with heifers (both weaned early and nonweaned) fed to gain at a similar rate on a diet that does not increase the propionate:acetate ratio in the rumen would permit the assessment of the effects of fatty acid fermentation patterns; independent of BW. Further research is necessary to determine the relative importance of increased BW gain, qualitative aspects of diets, and possible interactions with early weaning that may be responsible for the profound influence that manipulation of growth during early development has on sexual maturation.

It should not be surprising that manipulation during early development in heifers can alter sexual maturation because many important endocrine and morphological changes occur during this time (Day and Anderson, 1998; Honaramooz et al., 2004). Additionally, advancement of puberty in heifers has been achieved through administration of exogenous GnRH from 4 to 8 wk of age (Madgwick et al., 2005). The somatotropic axis is also of clear importance during early development in heifers; immunization against GHRH between 3 and 6 mo of age has been shown to delay puberty in heifers (Simpson et al., 1991; Cohick et al., 1996; Schoppee et al., 1996).

It seems logical that the mechanisms associated with peripubertal development that lead to puberty such as increasing secretion of LH, increasing follicular development, and decreasing estradiol negative feedback inhibition of secretion of LH (Day and Anderson, 1998) were shifted back to an earlier age through manipulation of weaning and diet in the present experiment. In this initial report of the endocrinology associated with this type of manipulation of weaning and diet, an increase in secretion of LH was detected, predominantly frequency of pulses of LH, which supports this hypothesis of a shifted peripubertal period. It has been demonstrated that frequency of pulses of LH in individual heifers approaches 16 to 18 pulses/24 h during the 10 d preceding puberty in heifers (Day et al., 1987), whereas the mean frequency was approximately 6 pulses/24 h during the last 2 sampling periods in the HI treatment in the present experiment. These mean values are expected to be somewhat decreased compared with LH values of individual heifers immediately before puberty for multiple reasons, including: individual heifers were removed from the analyses after attainment of puberty, data from 1 heifer that reached puberty at 327 d of age are included, and heifers at varying intervals before puberty are represented in each mean. Further research is needed to determine if changes in follicle development and estradiol negative feedback are influenced in a similar manner with this system. Also of interest is the impact of this model on lifetime reproductive performance and potential for breeding at a younger age.

Nutritional status has previously been shown to be an important regulator of the mechanisms that lead to puberty in heifers. Restriction of dietary energy intake that resulted in delayed puberty also delayed ovarian follicular development (Bergfeld et al., 1994) and the increase in secretion of LH that precedes puberty (Day et al., 1986, Yelich et al., 1996). Nutritionally stimulated advancement of puberty in heifers was associated with increased concentrations of IGF-I and decreased concentrations of GH (Granger et al., 1989; Yelich et al., 1995, 1996), which may be potential cues for the attainment of puberty in heifers.

In conclusion, the precocious attainment of puberty can be induced in heifers that are weaned early and fed a high-concentrate diet from weaning through puberty. In addition, this induced precocious puberty is preceded by increasing frequency of pulses of LH. This model is useful to examine the endocrine mechanisms that are associated with the precocious attainment of puberty in heifers.

	IMPLICATIONS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION IMPLICATIONS LITERATURE CITED

 
The combination of weaning calves early and increasing dietary energy intake through feeding a corn-based, high-concentrate diet is an effective method to accelerate reproductive development in beef heifers. These results are evidence that management of heifer diet and growth during early development can provide substantial control of puberty onset in heifers. With application of this method, the average age at puberty can be reduced to less than 10 months of age, allowing for multiple estrous cycles in heifers before the beginning of their first breeding season, potentially resulting in improved pregnancy rates.

	Footnotes

 
¹ Salaries and research support provided by USDA NRICGP Award 00-35203-9133 and state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University (Manuscript No. 7-06AS)

² Current address: Southern Utah University, 351 W. University Blvd., Cedar City 84720.

³ Corresponding author: day.5{at}osu.edu

Received for publication November 3, 2005. Accepted for publication March 8, 2006.

	LITERATURE CITED

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