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Biology of Reproduction 65, 9-13 (2001)
© 2001 Society for the Study of Reproduction, Inc.

Regular Article

Efficient In Vitro Production of Cat Embryos in Modified Synthetic Oviduct Fluid Medium: Effects of Season and Ovarian Status

Peter Freistedta, Miodrag Stojkovica, and Eckhard Wolf1,a

a Institute of Molecular Animal Breeding, Gene Center, Ludwig-Maximilian University, D-85764 Oberschleissheim, Germany

ABSTRACT

The effects of season (January–March = I; April–June = II; July–September = III; October–December = IV) and ovarian status (freshly ovulated, follicular, luteal, intermediate, or inactive) on the efficiency of the in vitro production of domestic cat embryos were evaluated. Ovaries and testes from cats with access to daylight were collected at local veterinary clinics. A total of 6843 cumulus-oocyte complexes (COCs) were recovered from 363 pairs of ovaries, matured in TCM 199 supplemented with BSA and gonadotropins (IVM), fertilized with epididymal sperm in a medium based on Tyrode albumin lactate pyruvate (IVF), and cultured in synthetic oviduct fluid (SOF) medium supplemented with 10% estrous cow serum (ECS) and essential and nonessential amino acids. The proportion of freshly ovulated, follicular, or luteal ovaries was higher (P < 0.05) in seasons II (64.4%) and III (60.5%) than in seasons I (42.0%) and IV (30.6%). The average number of COCs recovered per donor was not influenced by season. After IVM/IVF, cleavage rates (Day 2) were significantly higher (P < 0.05) in seasons II (mean ± SEM: 53.1% ± 1.9%) and III (54.6% ± 2.8%) than in seasons I (48.4% ± 1.4%) and IV (44.9% ± 3.0%). Blastocyst rates on Day 6 were similar in seasons I (25.3% ± 1.3%), II (28.2% ± 1.5%), and III (29.6% ± 2.3%) but were significantly lower (P < 0.01) in season IV (18.6% ± 2.4%). The corresponding blastocyst rates on Day 8 were 28.9% ± 1.3%, 33.7% ± 1.6%, 37.9% ± 2.3%, and 23.6% ± 2.6%. In addition, we found a significant effect (P < 0.05) of ovary type; luteal, follicular, and intermediate ovaries yielding a higher proportion of developmentally competent oocytes than did freshly ovulated and inactive ovaries. These data show that the culture system used in our study supports development of IVM/IVF cat oocytes to blastocysts at a higher rate than those obtained with other methods. Although embryos could be produced throughout the year, the efficiency was significantly affected by season and ovary type.

early development, embryo, in vitro fertilization, ovary, ovulatory cycle

INTRODUCTION

Under natural conditions the free-ranging domestic cat is seasonally polyestrous and can produce two or occasionally three litters per year, with one to five kittens in each litter [1]. Estrous cyclicity is initiated by increasing day length, and a period of anestrus occurs as day length decreases. Although cats breed throughout the year in equatorial zones, the breeding season decreases with increasing latitude from the equator to about 6 mo at the polar circles [2–6]. If cats are maintained under noncontrolled conditions in catteries, about half of them show cyclic activity throughout the year [7], and longhair cats show a more marked seasonal distribution of births than do shorthair cats [8].

During the last decade, much progress has been made in the field of assisted reproductive techniques in the domestic cat. The feasibility of oocyte recovery, in vitro maturation (IVM), in vitro fertilization (IVF), in vitro embryo culture (IVC), and transfer to recipients has been demonstrated [1]. A plethora of factors, including the storage of gonads [9–12], the quality of recovered cumulus-oocyte complexes (COCs) [13–16], and the protocols used for IVM, IVF, and IVC affect the efficiency of in vitro production (IVP) of cat embryos [14, 17–25]. The composition of the culture medium (complex vs. simple), the supplementation of hormones and gonadotropins, and the sources of proteins and macromolecules appear to be critical.

Little information is available concerning the number of high-quality oocytes that can be obtained from a pair of cat ovaries, the role of reproductive status of the ovaries at the time of oocyte recovery, the effect of the donor animal, and the influence of the season on the in vitro developmental competence up to the blastocyst stage of IVM/IVF oocytes [9, 12, 15, 17]. These questions were the focus of the present study and were investigated in a large field study using an efficient system for the IVP of cat embryos based on culture in synthetic oviduct fluid (SOF) medium supplemented with estrous cow serum (ECS) [26].

MATERIALS AND METHODS

Unless otherwise indicated, all chemicals were purchased from Sigma Chemical Co. (St. Louis, MO).

Collection, Storage, and Transport of Gonads

Gonads from female and male domestic cats were recovered at local veterinary clinics weekly for 16 mo (February 1999 to May 2000). The veterinary surgeons confirmed that each female cat weighed at least 2.5 kg and had access to natural light. Pairs of ovaries and testes were transferred immediately after excision into Dulbecco PBS (pH 7.4, containing 100 IU/ml penicillin and 100 IU/ml streptomycin sulfate; Biochrom KG, Berlin, Germany). Ovaries were stored at room temperature if oocytes were recovered within 8 h or at 4°C if stored overnight. The ovaries from 363 female cats were classified as follicular (at least one visible mature follicle >2 mm in diameter on at least one ovary), luteal (one or more corpora lutea on at least one ovary), freshly ovulated (one or more corpora hemorrhagica on at least one ovary), intermediate (1- to 2-mm follicles on at least one ovary), or inactive. Throughout the experiment, the oocytes of each pair of ovaries from a single cat were treated and evaluated separately.

Oocyte Recovery and IVM

Ovaries were placed into a 60-mm Petri dish containing TCM 199 (Gibco BRL, Paisley, Scotland) supplemented with 3 mg/ml BSA, 0.6 mg/ml potassium lactate, 3 mg/ml NaHCO3, 1.4 mg/ml Hepes, 0.25 mg/ml sodium pyruvate, 0.1 mg/ml cysteine, and 0.055 mg/ml gentamicin (mTCM199). The COCs from antral follicles were released by slicing the ovarian cortex with a scalpel blade. Only COCs with a uniformly dark, finely granulated or slightly less dark pigmented ooplasm and completely surrounded by at least two layers of compact cumulus cells were selected and washed three times in the same medium. Overall, 6843 COCs were cultured in groups of 4–60 in 400 µl of mTCM199 supplemented with 0.02 IU/ml bovine FSH and 0.01 IU/ml bovine LH (Sioux Biochemicals, Sioux Center, IA) for 24–28 h at 39°C in an atmosphere of 5% CO2 in air at maximum humidity.

Epididymal Sperm Recovery and IVF

Within 8 h after recovery of testis (storage at room temperature), the cauda epididymis and the first 1 cm of the ductus deferens were dissected from the testis and placed in a 35-mm Petri dish containing 800 µl of Hepes-Tyrode albumin lactate pyruvate (TALP) medium. Epididymal spermatozoa were released by mincing with a scalpel blade. Tissue debris was removed by forceps, and the remaining sperm suspension was diluted 1:2 with a commercial sperm extender based on Tris buffer and egg yolk (Biladyl A; Minitüb, Tiefenbach, Germany). Spermatozoa were used for insemination on the same day or were cooled at 4°C for up to 5 days. Before use, a modified swim-up treatment was done by gently layering 100 µl of sperm suspension under 200 µl of Hepes-TALP medium [27]. After 1 h of incubation at 39°C, the clear supernatant was aspirated, sperm motility was estimated, and sperm concentration was determined using a hemocytometer. IVF (Day 0) was performed by adding 105 motile spermatozoa to IVM oocytes in 400 µl of IVF medium (TALP solution containing 6 mg/ml BSA and 10 µg/ml heparin) and incubating for 20–22 h at 39°C in an atmosphere of 5% CO2 in air. The proportion of parthenogenetic development was evaluated by using pools of oocytes from 12 cats. Treatment of oocytes was identical as for IVF except for the coincubation with spermatozoa. The proportion of parthenogenetic cleavage was <3%.

IVC and Assessment of Development

Presumptive zygotes were washed three times and cultured in 400 µl of SOF medium [28] supplemented with 2% Eagle basal medium amino acids, 1% minimal essential medium (MEM) nonessential amino acids (both Gibco BRL), and 10% (v/v) ECS (SOF/ECS). At 36 h after insemination, putative zygotes were washed three times in culture medium to remove cumulus cells and were examined for cleavage. Embryos were transferred into 400 µl of fresh SOF/ECS medium under equilibrated paraffin oil and were cultured at 39°C in a humidified atmosphere of 5% CO2, 5% O2, and 90% N2. The development of embryos to the blastocyst stage was determined on Days 6 and 8 after insemination.

Statistical Analysis

The effect of semen treatment on early cleavage and blastocyst rates was analyzed by ANOVA. The effects of ovary type (freshly ovulated, follicular, luteal, intermediate, or inactive) and season (January–March = I; April–June = II; July–September = III; October–December = IV) on numbers of COCs recovered and on cleavage and blastocyst rates were evaluated by ANOVA followed by least significant difference post hoc tests only when a significant (P < 0.05) F-value was found. Differences in the proportions of ovary types between seasons were evaluated by chi-square tests.

RESULTS

Effect of Sperm Treatment

The ANOVA revealed no significant effect (P > 0.05) of cooled vs. freshly prepared spermatozoa on the early cleavage (F = 2.1) and blastocyst rates on Day 6 (F = 0.8) and Day 8 (F = 1.8).

Effect of Season on Ovarian Status

The proportion of freshly ovulated, follicular, or luteal ovaries was significantly higher (P < 0.05) in seasons II and III than in seasons I and IV, with the highest incidence of luteal ovaries observed in season III. Accordingly, the proportions of inactive or intermediate ovaries were significantly higher (P < 0.05) in seasons I and IV than in seasons II and III (Fig. 1).



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  		FIG. 1. Distribution (%) of feline ovary types during seasons

Effect of Season on the Efficiency of IVP of Cat Embryos

A total of 6843 COCs were recovered from 363 pairs of domestic cat ovaries (Table 1). The average number of COCs recovered per donor ranged from 17.9 in season I to 20.1 in season III, with no significant differences (P > 0.05) between seasons. In contrast, a clear seasonal effect was seen on the developmental potential of oocytes after IVM and IVF. The cleavage rate was significantly higher (P < 0.05) in seasons II and III than in seasons I and IV. The proportions of blastocysts observed on Day 6 were similar in seasons I, II, and III but significantly higher (P < 0.01) than in season IV. On Day 8 after IVF, the highest proportion of blastocysts was found in season III, followed by seasons II, I (P < 0.05), and IV (P < 0.01 vs. seasons II and III; P < 0.05 vs. season I) .


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  		TABLE 1. Effect of season on the efficiency of IVP of cat embryos.*

Effect of Ovary Type on the Efficiency of IVP of Cat Embryos

The average number of COCs recovered per donor was highest for intermediate (20.9) and inactive (20.8) ovaries followed by luteal (18.3; P < 0.05), freshly ovulated (15.1; P < 0.01), and follicular (14.8; P < 0.01) ovaries (Table 2). The developmental potential of oocytes recovered from the different types of ovaries was reflected by the cleavage rate after IVF. Cleavage rate was highest for oocytes from luteal ovaries (57.4%) and slightly lower for those recovered from follicular ovaries (53.4%). Oocytes from intermediate ovaries cleaved at a significantly lower rate (P < 0.01) than did those from luteal ovaries, whereas the developmental potential of oocytes from freshly ovulated or inactive ovaries was markedly reduced as compared with all other types of ovaries. These differences were largely reflected by the proportions of development to blastocysts (Fig. 2) on Day 6 and Day 8, when they were calculated relative to the number of COCs. However, when calculated as a proportion of embryos, blastocyst rates were similar in all groups (Table 2).


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  		TABLE 2. Effect of ovary type on the efficiency of IVP of cat embryos.*



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  		FIG. 2. IVP domestic cat blastocysts on Day 8 after fertilization. x100

DISCUSSION

Domestic cat embryos were successfully produced after IVM/IVF/IVC throughout the year using gonads from animals that had access to daylight but were otherwise maintained under noncontrolled conditions. Under natural daylight conditions, the reproductive behavior of the domestic cat is related to day length. At tropical latitudes, there is no seasonal effect on the distribution of litters throughout the year, but a shortening of this period occurs as latitude increases [3]. In the Northern Hemisphere, anestrus occurs in late fall and early winter, with resumption of estrous behavior beginning as early as January or February [2, 4–6, 29, 30].

The present study revealed a significant seasonal influence on the developmental potential of recovered COCs. Although there were clear differences in ovarian function between seasons (Fig. 1), the seasonal variation in the quality of COCs was not simply a consequence of different proportions of ovary types; the effect persisted when ovaries yielding poor quality oocytes (freshly ovulated and inactive ovaries) were excluded (data not shown). It remains unclear which factors cause the impaired developmental competence of COCs recovered in season IV. In the domestic cat, a daylight exposure of <8 h results in a cessation of ovarian activity and an increase in melatonin synthesis [6, 29, 31]. Administration of melatonin suppresses ovarian activity [32] and decreases estrogen synthesis in follicular ovaries and decreases LH response after copulation [6]. There are many unanswered questions concerning the seasonality of the hypothalamic-pituitary-ovarian axis. Specific examples concern the secretion of GnRH and FSH, the peripheral sensitivity to gonadotropins, and the role of follicular atresia.

Spindler and Wildt [15] also found an extremely pronounced effect of season on the maturation, fertilization, and developmental potential of domestic cat oocytes in vitro. These authors reported a low rate of polar body extrusion (<20%) from July to November and a very low rate of development (<10%) to the four-cell stage in July and August, which decreased to 0% in September and October. Consequently, virtually no blastocysts were produced from July to November. The results of Spindler and Wildt [15] are quite different from the present results, in which cleavage and development to blastocysts occurred during every week throughout the year. There was an increase of cleavage and blastocyst rates up to the third quarter and a decrease in the fourth quarter of the year. The major differences between the results of Spindler and Wildt [15] and our results could be due to different latitude, different selection criteria for COCs, different in vitro systems, or a different genetic background of donor cats. Thus, it is difficult to compare the two studies. The average number of COCs per donor was only 3.8 in the study by Spindler and Wildt [15] but was 18.8 in our experiments, indicating marked differences in selection criteria, experimental conditions, and procedures. Specific differences between the present study and that of Spindler and Wildt [15], respectively, include the use of TCM-199-based medium vs. MEM-based medium, 0.02 IU/ml FSH vs. 1.64 IU/ml FSH for IVM, and cooled epididymal spermatozoa extended in TALP medium vs. cryopreserved spermatozoa obtained by electroejaculation and extended in Ham F10 medium with 5% fetal calf serum for IVF. Furthermore, our IVC system, which included the use of SOF supplemented with amino acids and ECS, was more efficient than culture in Ham F10 containing fetal calf serum, as used by Spindler and Wildt [15]. Other factors contributing to the improved efficiency of our culture system may have been the use of a gas atmosphere of 5% CO2, 5% O2, and 90% N2 rather than 5% CO2 in air and addition of cysteine to the IVM medium, as has been previously shown [25].

There was a clear effect of ovary type on the number of COCs recovered, frequency of cleavage and blastocyst development, and number of blastocysts produced per set of ovaries. Little information has been available concerning the effect of reproductive status of the ovaries on the IVP of cat embryos. Johnston et al. [17] observed a significantly lower maturation rate for oocytes recovered from ovaries of pregnant cats or those in the luteal phase as compared with oocytes from inactive or follicular phase ovaries. In contrast, we found that developmental potential of oocytes recovered from ovaries in the luteal phase was fairly good, whereas oocytes obtained from inactive or freshly ovulated ovaries had reduced cleavage rates after IVF. The tremendous changes of the endocrine and/or paracrine environment within the ovaries during and shortly after ovulation might be responsible for the low developmental potential of oocytes from the latter group of ovaries. Roth et al. [33] demonstrated that in vivo matured oocytes obtained from hormonally stimulated ovaries in the presence of corpora hemorrhagica at the time of oocyte aspiration showed reduced fertilization and cleavage rates.

In spite of the clear differences in cleavage rates of oocytes after IVF, the potential of embryos to reach the blastocyst stage was similar for all types of ovaries. These results indicate that the selection of developmentally competent oocytes occurs early at fertilization or first cleavage.

We have established an efficient system for the IVP of domestic cat embryos using gonads/gametes from cats maintained under noncontrolled conditions. Although embryos could be produced throughout the year, there were significant effects of season and ovary type on the number of developmentally competent oocytes.

ACKNOWLEDGMENTS

We thank the veterinary clinics in the Munich area for providing cat reproductive tissue, especially the Gynaecological and Ambulatory Veterinary Clinic, LMU Munich.

FOOTNOTES

First decision: 5 January 2001.

1 Correspondence: Eckhard Wolf, Institute of Molecular Animal Breeding, Hackerstrasse 27, D-85764 Oberschleissheim, Germany. FAX: 49 89 2180 6849; ewolf{at}lmb.uni-muenchen.de Back

Accepted: March 6, 2001.

Received: November 30, 2000.

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