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Endocrine control of ovarian function in dogs and other carnivores

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Concannon et al. Ovarian <strong>function</strong> <strong>in</strong> <strong>dogs</strong> <strong>and</strong> <strong>other</strong> <strong>carnivores</strong>.<br />

species (lions, tigers, jaguars, leopards). The importance <strong>of</strong><br />

the dog as a model species is evidenced by the support <strong>and</strong><br />

success <strong>of</strong> the can<strong>in</strong>e genome project f<strong>in</strong>ancially supported<br />

by the National Institutes <strong>of</strong> Health; furthermore, there are<br />

36 species <strong>in</strong> the family Canidae <strong>of</strong> which n<strong>in</strong>e are<br />

formally listed as threatened or endangered by ext<strong>in</strong>ction<br />

(see Songasassen <strong>and</strong> Wildt, 2002)<br />

Can<strong>in</strong>e <strong>ovarian</strong> cycle <strong>and</strong> pregnancy<br />

The <strong>ovarian</strong> cycle <strong>and</strong> pregnancy <strong>of</strong> the<br />

domestic dog (C. lupus familiaris) are not only<br />

prototypical <strong>of</strong> those <strong>of</strong> <strong>other</strong> canids <strong>and</strong> most<br />

<strong>carnivores</strong> but also likely exemplify to a large extent the<br />

<strong>ovarian</strong> activity <strong>and</strong> pregnancies <strong>in</strong>volved <strong>in</strong> the very<br />

early evolution <strong>of</strong> placental mammals. Domestic <strong>dogs</strong><br />

are monestrous, non-seasonal spontaneous ovulators<br />

with spontaneous luteal <strong>function</strong> <strong>and</strong> pronounced<br />

progesterone secretion that lasts from 55 to 75 days,<br />

average 65 days, <strong>and</strong> approximately the 2-month<br />

duration <strong>of</strong> pregnancy (Fig. 1 <strong>and</strong> 2). Thus the CL <strong>of</strong> the<br />

cycle are <strong>in</strong> most <strong>in</strong>stances sufficient to support a term<br />

pregnancy absent support or supplementation by any<br />

pregnancy specific mechanisms – a phenomenon critical<br />

<strong>in</strong> a species that has no placental progesterone<br />

production or placental gonadotroph<strong>in</strong>, <strong>and</strong> a scenario<br />

likely present early <strong>in</strong> mammalian evolution. This<br />

physiological pseudo-pregnancy follow<strong>in</strong>g ovulation is<br />

seen <strong>in</strong> all <strong>carnivores</strong> studied, either follow<strong>in</strong>g<br />

spontaneous ovulation, or follow<strong>in</strong>g <strong>in</strong>fertile mat<strong>in</strong>g <strong>in</strong><br />

<strong>in</strong>duced ovulators. It is also comparable to the<br />

prolonged luteal phases <strong>of</strong> hysterectomized <strong>in</strong>dividuals<br />

<strong>in</strong> species that have an acute uter<strong>in</strong>e luteolytic<br />

mechanism (Fig 3). Although <strong>dogs</strong> evolved from a<br />

photoperiod-entra<strong>in</strong>ed seasonal breeder, the primitive<br />

wolf, their non-seasonal breed<strong>in</strong>g pattern is potentially<br />

similar to the pattern <strong>of</strong> the progenitor to the orig<strong>in</strong>al<br />

<strong>carnivores</strong>. Inter-estrus <strong>in</strong>tervals <strong>in</strong> <strong>dogs</strong> range from 5 to<br />

13 months, average about 7 months <strong>in</strong> most breeds, <strong>and</strong><br />

potentially parallel an endogenous circannual cycle. The<br />

pre-ovulatory LH surge <strong>and</strong> ovulation 2 days later occur<br />

after a 1-3 week (average 9 day) period <strong>of</strong> proestrus.<br />

Proestrus is characterized by progressive <strong>and</strong> eventual<br />

full cornification <strong>of</strong> the vag<strong>in</strong>al epithelium,<br />

serosangu<strong>in</strong>ous discharge <strong>of</strong> fluid <strong>and</strong> erythrocytes<br />

orig<strong>in</strong>at<strong>in</strong>g by diapedesis through the uter<strong>in</strong>e capillaries,<br />

pheromonal secretion caus<strong>in</strong>g <strong>in</strong>creased attraction <strong>of</strong><br />

males, <strong>and</strong> progressive <strong>and</strong> anatomically visible edema<br />

<strong>and</strong> turgor <strong>of</strong> the vulva <strong>and</strong> vag<strong>in</strong>al stroma. All are<br />

effects <strong>of</strong> ris<strong>in</strong>g estradiol concentrations. Estrus is<br />

concomitant with subsequently decl<strong>in</strong><strong>in</strong>g phase <strong>of</strong> estradiol<br />

concentrations. Estrus beg<strong>in</strong>s typically 0-1 days after the<br />

LH surge <strong>and</strong> behaviorally lasts an average <strong>of</strong> 7 days.<br />

Cl<strong>in</strong>ical or morphological "estrus" is <strong>of</strong>ten def<strong>in</strong>ed as<br />

end<strong>in</strong>g when the vag<strong>in</strong>al smears previously characteristic<br />

<strong>of</strong> estrus are no longer predom<strong>in</strong>antly cornified (range days<br />

6-11, average 7.5), with the rem<strong>in</strong>der <strong>of</strong> the luteal be<strong>in</strong>g<br />

historically termed metestrus <strong>and</strong> more recently diestrus.<br />

Corroboration is also obta<strong>in</strong>ed cl<strong>in</strong>ically based on the<br />

day that the wr<strong>in</strong>kl<strong>in</strong>g <strong>and</strong> sacculation <strong>of</strong> previously<br />

smooth edematous <strong>and</strong> cornified vag<strong>in</strong>al mucosal folds<br />

produced dur<strong>in</strong>g proestrus ends with folds become<br />

visibly less pronounced <strong>and</strong> appear<strong>in</strong>g more flat <strong>and</strong><br />

obviously less white (less cornified) with submucosal<br />

capillaries aga<strong>in</strong> visible as they were prior to the vag<strong>in</strong>al<br />

growth <strong>of</strong> proestrus - end<strong>in</strong>g typically at 7-9 days after the<br />

LH surge.<br />

Days fom LH surge<br />

Figure 1. Schematic diagram <strong>of</strong> changes <strong>in</strong> circulat<strong>in</strong>g estradiol, LH, progesterone <strong>and</strong> prolact<strong>in</strong> concentrations<br />

dur<strong>in</strong>g pregnancy <strong>in</strong> <strong>dogs</strong>. More recent studies have demonstrated an even more pronounced pregnancy specific rise<br />

<strong>in</strong> prolact<strong>in</strong> beg<strong>in</strong>n<strong>in</strong>g at day 25-30 <strong>of</strong> pregnancy.<br />

Anim. Reprod., v.6, n.1, p.172-193, Jan./Mar. 2009 173

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