For many years, feline reproduction has been neglected, but over the past decade, new data have been generated on the ovarian cycle and reproductive life in cats. Indeed, the cat is singular among mammals in many aspects of its reproductive physiology (induced ovulation, pregnancy regulation, etc.), and many parts of its reproductive life remained unknown or poorly studied. Like in dogs, reproduction in the cat can be defined by large individual or breed variations in the oestrous cycle, dependent on many parameters including genetic, diet, photoperiod, size of the colony, age, etc.

Puberty, Seasonality and Oestrous Cycle

The age of puberty in the domestic cat is variable. Cats usually start to show oestrus once they have reached 2.3-2.5 kg body weight, around 6-9 months of age, but some animals are observed to enter puberty as early as 3-4 months of age or as late as 18 months of age. There are breed and line variations demonstrating a certain degree of heredity in sexual maturity. However, the main factor responsible for both sexual maturity and cyclicity seems to be the amount and duration of sunlight received in relation to day length in outdoor cats or of artificial light in breeding colonies. The onset of puberty usually occurs when the amount of daylight increases at the end of the winter.

In the absence of pregnancy or pseudopregnancy, the cat will show repeated oestrous cycles every 2 or 3 weeks from spring to autumn. In breeding colonies with controlled light and in households with evening lighting, cats can become non-seasonal breeders and show oestrus during winter.

Behavioural Cycle

In terms of behaviour, the cycle of the queen can be divided into the heat and the non-heat period.

The heat period can be divided in pro-oestrus and oestrus. The behavioural pro-oestrous (1-4 days) and oestrous periods (2-19 days) last together on average between 3 and 10 days. Pro-oestrus per se is clinically difficult to detect and some cats express oestrous behaviour with acceptance of mating without this preliminary transition period. Follicular growth begins during pro-oestrus but plasma oestradiol concentration is still low and insufficient to allow full behavioural expression of heat.

Oestrus begins with the queen allowing the mating and ends with the first refusal. It is characterised by maximal synthesis and effects of the follicular oestrogens.

During heat, tomcats are attracted to the queen and when the queen is fully in heat she will show escapist tendencies and will allow mating to occur. Male thrusting movements cause the female to vocalise violently and this is followed immediately by the female, forcefully and sometimes aggressively, freeing herself from the male neck grip. The queen will then show a temporary uninterest in mating; however, this is soon followed by multiple copulations typically observed throughout oestrus. The interval between mating is a mean of 15-20 minutes.

Variation in the length of the different phases is important, with changes in the length of oestrus, season and number of cycles depending on light, genetics and localisation in the northern or southern hemisphere.

Queens as well as males can easily block and hide any reproductive behaviour in certain environmental or social circumstances. It is not rare to have queens showing no signs of oestrus when at home and as soon as they are far from the owner's eyes showing dramatic rolling and calling. Males may ignore or attack females if in a hostile or unknown environment. On the other hand, some really affectionate queens can present heat signs not really different from their usual behaviour, making heat detection difficult in the absence of a tomcat.

Interoestrus and Anoestrus

In the absence of mating and/or spontaneous ovulation, heat periods are observed at intervals of an average of 10-14 days (interval 0-20 days) during the whole reproductive season. This interval period without evidence of the oestrous cycle is called interoestrus. It corresponds to an apparent quiescence of the ovaries, which, however, are already preparing for the next follicular growth of the next oestrus. During the interoestrus, the oestrogen levels usually decline to basal values. In some cats however, sequential follicular growth waves may overlap, oestrogen concentrations may not decline and the queen may appear in constant oestrus. This phenomenon is often falsely called 'nymphomania' or prolonged oestrus.

True ovarian quiescence is only found during anoestrus, which, in contrast to interoestrus, is a long period without sexual activity. Anoestrus occurs under very short natural daylight (winter) or when the cats are submitted to short artificial lightening periods of 4-6 hours/day. Anoestrus could be absent in animals submitted to constant long days, particularly animals living indoors or animals living in breeding colonies with constant lighting.

Mating and Induced Ovulation

The cat was considered a reflex-mediated induced ovulator, i.e., a coital stimulus induces a neural firing reflex, stimulating the mediobasal hypothalamus to synthesise and liberate high levels of gonadotrophin-releasing hormone (GnRH) which allow, through the release of pituitary luteinising hormone (LH), ovulation to take place. Most queens will respond to mating with an LH release leading to ovulation, but the chance will be higher if mating occurs in mid to late oestrus while many early matings are not always associated with an LH surge or with ovulation.

However, there is now plenty of evidence that cats may ovulate spontaneously without mating. In the absence of spontaneous ovulation, it has been demonstrated that the ovulation rate seems to be directly related to the amplitude of the LH surge, which may be correlated to the number, interval and quality of the mating. Cats that have been in oestrus for several days ovulate sooner after mating than cats that have just entered oestrus. After ovulation, signs of heat disappear within 24-48 hours. An increase in plasma progesterone concentration typically follows ovulation.

If ovulation does not occur, the follicles become atretic and the oestrogen concentration declines. Luteinisation does not occur and newly recruited follicles may start to grow after a few days of interoestrus.

Events After Ovulation

In the queen, unlike the bitch, events after ovulation will depend on whether or not the mating was fertile. Indeed, two situations can be observed.

Ovulation Without Fertilisation

When oocytes are not fertilised after ovulation, corpora lutea develop and produce progesterone for a period of about 25-45 days. This luteal phase is shorter than the one associated with pregnancy and is therefore often called pseudopregnancy. In the cat, pseudopregnancy is not, as in dogs, associated with behavioural changes or lactation. At the end of this short luteal phase of pseudopregnancy, a brief period of interoestrus will precede the next return of oestrus, provided it is still the breeding season, otherwise anoestrus will occur.

Ovulation and Fertilisation

If the queen is mated with a fertile male or successfully inseminated, mature ovulated secondary oocytes are fertilised in the oviducts where the embryos develop for 4-5 days. Embryos then migrate into the uterine horns where implantation occurs around day 12-16 post-mating.

In controlled conditions, gestation length is 63-68 days but can range from 62-72 days when mating is allowed for several days and the exact day of ovulation is not determined.

Spontaneous abortion or resorption is nowadays well documented and occurs in 5-30% of pregnancies, affecting anything from one kitten to the whole litter. The litter size is always smaller in primiparous queens.

Parturition is always associated with a decline in plasma progesterone, but this decline can be observed as early as 5-10 days before whelping or as late as until after parturition. Queens can remain pregnant sometimes for days without any significant plasma progesterone concentration.

Parturition, and its different phases, are similar to that observed in dogs, with a few peculiarities: the placenta is red/brown instead of dark green, queening can be as short as 1 hour but sometimes as long as 1-2 days. Delayed parturition is often observed when environmental stress is present or can be characteristic of some animals. An interruption of 12-48 hours can be observed without any significant effects on the litter except when placental disruption is present.

At the end of the lactation period, if it is still the breeding season, a brief period of interoestrus will follow until the next oestrus; otherwise anoestrus will occur. In lactating queens, this oestrus period usually occurs about 10-15 days after weaning. However, in some cases, oestrus may be observed in nursing females 10-15 days after littering. In this case, if she is not mated or if ovulation does not occur, the queen will return to oestrus normally every 10-20 days. The first mating after kittening is often not fertile due to incomplete uterine involution but mating during the next oestrus may be fertile and it is not rare to see a nursing queen, that is pregnant again before weaning.

Infertility

Infertility in queens has so far been poorly studied. The causes might be similar to the ones observed in bitches but some specific disorders are also described. Knowledge about infertility can only be enhanced by careful and methodical reproductive examinations and good record keeping. Careful observation of the animal will help in the diagnosis process: if the queen returns to oestrus within 4-8 weeks after mating either she did not ovulate or ovulation was not followed by fertilisation. A progesterone assay performed within 2-3 weeks after mating would allow differentiation between the two conditions. There are non-infectious and infectious causes of infertility.

Non-Infectious Causes

 Abnormal mating behaviour. This can be observed in timid queens, low in social status in a colony or having experienced unpleasant sexual relations previously. Successful breeding management supposes correct intromission and ejaculation. Indeed, stimulation without intromission could be associated with spontaneous ovulation without fertilisation and pseudopregnancy, leading to a false diagnosis of infertility.

 Pseudopregnancy and spontaneous ovulation. In the past, spontaneous ovulation was considered exceptional in queens and generally associated with non-fertile matings. However, the characterisation of cats as being primarily copulation-induced ovulators requires reconsideration. There is nowadays clear evidence that spontaneous ovulation is a frequent phenomenon observed both in the presence or the absence of a male during heat. In colonies, the spontaneous ovulation rate has been described to reach 30-60% of animals and this percentage appears to be higher when a male is present in the same room even if mating is not allowed. The sexual behaviour of the queens during heat, which includes rolling, neck rubbing, meowing, licking of its own, or another cat's, external genitalia, female-female mounting and neck biting could induce the nervous feedback allowing GnRH and LH release and leading to ovulation. A pheromone effect is probably also present, favouring or inducing spontaneous ovulation. Indeed, 67% of females have been shown to ovulate during the 20 days following the introduction (but without direct contact) of a male into the room. This suggests that this may have been a response to some visual or airborne olfactory cues from the male. Every time a queen is suspected of infertility, progesterone levels have to be checked to insure that pseudopregnancy has not been spontaneously induced.

 Prolonged heat behaviour. Frequent regular follicular waves may overlap, leading to apparent prolonged oestrous behaviour and prolonged period of receptivity. This is often observed in Siamese queens housed alone without access to males. This prolonged oestrous behaviour is sometimes called pseudonymphomania. It has to be clearly differentiated from nymphomania, which is related to the presence of follicular cysts, or centrally mediated nymphomania observed in ovariectomised animals. Follicular cysts are associated with persistent oestrous behaviour. Mating does not induce ovulation because the follicles are abnormal, the hypothalamo-pituitary axis is not responding, or the animal presents autoantibodies against its own GnRH, follicle-stimulating hormone (FSH) or LH. The condition frequently reoccurs in subsequent cycles and is associated with general clinical signs: weight loss, sparse, roughened hair coat. Treatment with GnRH or human chorionic gonadotrophin (HCG) can be successful in some cases but sterilisation is certainly the treatment of choice.

 Persistence of oestrus behaviour in castrated animals may or may not be related to remnant ovaries (cf. infra). The role of the adrenal cortex cannot be underestimated: the high levels of testosterone spontaneously produced and metabolised to oestrogens by the hypothalamus may be responsible for the centrally mediated persistence of oestrous behaviour, but the idiopathic production of oestrogens by the adrenal cortex could also explain the persistent reproductive behaviour. In the case of idiopathic adrenal stimulation, Shille and Tatcher have described effective adrenal suppression by the administration of a short-acting glucocorticoid, resulting in the disappearance of the oestrous signs. In the case of centrally mediated persistent oestrus, the use of long-acting progestin blocking the receptors has been successful in the author's clinical experience.

 Spontaneous and iatrogenic prolonged anoestrus. Prolonged anoestrus may be related to photoperiod, as variations in daylight exposition have clearly been demonstrated to control the oestrous cycle. It can easily be corrected by modifying the duration and intensity of lighting. Prolonged anoestrus can also be socially related as a stressful interrelation and hierarchy can induce suppression of the oestrous behaviour and apparition of the so-called 'silent heat'. Long-acting progestin injections or irreversible centrally mediated blockade of the tonic-clonic hypothalamic centres by previous repeated progestin treatments can also be associated with prolonged anoestrus or chemically induced contraception. When progestins are no longer present, oestrus induction can be obtained using gonadotrophins.

 Mucometra (also called hydrometra). This may be the consequence of cystic endometrial hyperplasia but the exact cause of this pathological process is not clearly defined and can be observed in animals without evidence of cystic endometrial hyperplasia. It has been suggested to be due to prolonged progestin treatment; however, the author has often observed this condition in young animals (2-3 years old), without any evidence of previous progestin treatment. Endogenous progesterone associated with spontaneous ovulation may be responsible for the occurrence of this often asymptomatic disease.

However, this has not yet been demonstrated. Although possible, a relationship between the occurrence of mucometra and pyometra has not been directly observed.

Acknowledgement

BSAVA thanks John Verstegen DVM MSc PhD DipECAR for his assistance with these notes.

References

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3.  Schille VM, Sojka NJ. Feline reproduction. In: Ettinger, SJ; Feldman, EC. eds. Textbook of Veterinary Internal Medicine. Philadelphia: WB Saunders, 1995; 1690.

4.  Verstegen JP, Russel HA. (eds.) Fertility and infertility in dogs cats and other carnivores. Journal of Reproduction and Fertility 1993, suppl 47.

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