Animal Reproduction Science 81 (2004) 115123

Ovarian cysts and their consequences on the reproductive performance of swine herds
Cezar Dobler Castagna a, , Carlos Henrique Peixoto a , Fernando Pandolfo Bortolozzo a , Ivo Wentz a , Guilherme Borchardt Neto b , Fabrcio Ruschel a
a

Setor de Sunos, Faculdade de Veterinria, Universidade Federal do Rio Grande do Sul, Av. Bento Gonalves, no. 9090, CEP 90540-000, Porto Alegre, RS, Brazil b Plo de Inovao Tecnolgica do Alto Jacu, Universidade de Cruz Alta, Av. Andrade Neves, no. 380, CEP 98.000-000, Cruz Alta, RS, Brazil

Received 6 March 2002; received in revised form 1 August 2003; accepted 19 August 2003

Abstract The aim of this work was to determine the incidence of ovarian cysts in the breeding herd and their consequences in the reproductive performance of the herd. Data from 1990 cyclic sows from two farms, with 012 parities, lactation length between 6 and 47 days and weaning-estrus interval between 0 and 32 days were evaluated by ultrasound examination for cyst incidence. As cyst was considered an anaechoic structure with smooth and thin walls with a diameter larger than 2 cm that remained visible for at least 5 days after estrus onset. Cyst incidence was found to be 2.4%. Sows with ovarian cysts have a greater return to estrus rate (34.0 7.7%, P < 0.01), and cysts were associated with around 10% of regular and irregular return to estrus patterns on both farms. The adjusted farrowing rate (52.2 90.0%, P < 0.01) and anestrual sows that were not pregnant (10.6 0.6%, P < 0.01) were also inuenced by the appearance of ovarian cysts, but they did not inuence litter size (P > 0.05). The incidence of cysts was not inuenced by parity (P > 0.05). Sows with shorter lactation had a greater incidence of cysts (P < 0.05). Sows with a weaning-estrus interval shorter than 3 days had a greater incidence of ovarian cysts (P < 0.05). The time of the year had no inuence on the incidence of ovarian cysts (P < 0.05). 2003 Elsevier B.V. All rights reserved.
Keywords: Swine; Ovarian cysts; Reproductive performance; Ovulation; Ovarian disorders

Corresponding author. Tel.: +55-51-3316-6132. E-mail address: ccastagna@hotmail.com (C.D. Castagna).

0378-4320/$ see front matter 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2003.08.004

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1. Introduction Occurrence of ovarian cysts in sow herds may affect overall reproductive performance. Some studies conrm the link between reproductive problems and the presence of ovarian cysts found at slaughter (Meredith, 1977; Miller, 1984; Gherpelli and Tarocco, 1996; Heinonen et al., 1998). Miller (1984) indicated that ovarian cysts are a cause of lesser conception rates, irregular estrous cycles and behavioral changes. By assessing the incidence of cysts in culled animals, it was observed that ovarian cysts are present in approximately 10% of sows that were culled for fertility problems (Miller, 1984). However, with surveys performed at slaughterhouses, little is known about the incidence of ovarian cysts in a herd because cysts may also occur without leading to culling for reproductive problems. According to Britt et al. (1999), it is difcult to diagnose cysts through serological methods because serum concentrations of progesterone, estradiol, luteinizing hormone and cortisol are similar to sows in diestrus. However, with the possibility of examining the ovary by ultrasound (Weitze et al., 1989), it is now possible to diagnose ovarian cysts preserving the integrity of the examined animals (Waberski et al., 1999; Lucy et al., 2001). The aim of the present work was to determine the incidence of ovarian cysts in gilts at the mating estrus and in sows after weaning, without hormonally induced estrus, and to evaluate their consequences on the reproductive performance of the herd. 2. Materials and methods The present study was performed at two Brazilian farms. Farm A (located in the State of Santa Catarina, close to parallel 27 South, with around 5000 sows) was evaluated from May to July 1999 and farm B (located in the State of Mato Grosso do Sul, close to parallel 21 South, with around 3500 sows) was evaluated from August to October in the same year. In farm A, 735 (gilts in mating estrus and sows in the rst estrus after weaning), and in farm B 1225 (gilts at the mating estrus and sows in the rst estrus after weaning) Cambourough 22 female swine were evaluated from onset of rst estrus after weaning onwards. The following sow characteristics were measured: parity, visual condition score (Patience and Thacker, 1989), back fat (Estienne et al., 2000), lactation length, weaning to estrus interval, farrowing rate and litter size. Information included in Table 1 describes the situation of both farms before the beginning of the experiments. Detection of estrus was performed twice daily using a sexually mature boar. Sows with positive back-pressure test were taken to the breeding pens where they were articially inseminated. The rst insemination was performed 12 h after estrus onset. The subsequent inseminations were performed in 1224 h intervals until estrus ended. Sows that presented a weaning-estrus interval shorter than 1 day and the nulliparous females received the rst insemination at the onset of estrus. Follicle dynamics were recorded from rst detection of estrus onward by transcutaneous ultrasound examination (Weitze et al., 1989), with a 5 MHz Aloka convex linear transducer. The ultrasound examination was repeated every 12 h. The size and the persistence of follicles were used as criteria to determine cysts. The structures were considered an ovarian cyst when an anaechoic structure with smooth and thin walls with a diameter larger than 2 cm that

C.D. Castagna et al. / Animal Reproduction Science 81 (2004) 115123 Table 1 Characterization of herds (means S.E.) evaluated at weaning, before the beginning of the experiment Farm A Means SE Parity Visual score condition Backfat thickness (mm) Weaning to estrus interval (day) Lactation length (day) Total litter size Farrowing rate (%) 4.0 1.8 3.0 0.5 16.5 4.4 4.2 0.8 19.6 1.7 11.9 2.6 87 Range 18 15 737 16 1426 720 Farm B Means SE 3.5 3.0 2.9 0.6 15.1 4.3 5.2 3.8 17.5 2.3 10.8 3.0 91

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Range 012 15 534 032 647 119

remained visible at the ultrasound examination for at least 5 days after estrus onset was present. The sows that did not show any cysts were followed by ultrasound examination until the time of ovulation. Ovulation was considered to have occurred at the time which preovulatory follicles (usually between 0.8 and 1.2 cm) were no longer present. In farm A, ovarian cysts were followed until the seventh day after estrus onset and in farm B until the 15th day after estrus onset. Reproductive performance was analyzed based on the return to estrus rate, adjusted farrowing rate and litter size. The calculation of adjusted farrowing rate was done by removing those sows that did not farrow for non-reproductive reasons such as death and culling due to locomotor problems (Dial et al., 1992). The number of piglets produced in 100 bred sows was calculated by multiplying the adjusted farrowing rate times the average total born. For the return to estrus rate and adjusted farrowing rate the comparison of means was performed with the aid of 2 -test. For litter size and the number of piglets produced in a 100 bred sows an analysis of variance was performed by the GLM procedure (SAS, 1998). The model used was Y = + cyst + e, where Y is the dependent variable (i.e., litter size or number of piglets produced in 100 bred sows), the overall means, cyst the presence or absence of cysts and e the error. The effect of farm, parity, visual condition score, back fat, lactation length, weaning to estrus interval, season, and interaction between farm with lactation length, farm with weaning to estrus interval were also tested, but was later removed from the model for not having been signicant (P > 0.05). Adjusted means were compared by Students t-test. Logistic regression was used to examine factors associated with the formation of ovarian cysts. The model included lactation length, parity and weaning-estrus interval. In order to do so, lactation length was broken down into four categories: (1) shorter than 14 days, (2) from 14 to 16 days, (3) from 17 to 19 days and (4) longer than 19 days. The 1719 days category was used as the standard, because this is the category representing the average lactation length in both farms. Parity categories used were: gilts, primiparous and multiparous. Multiparous females were considered as the standard because they were the most representative group of females. The weaning-estrus interval was divided into three categories: (1) shorter than 3 days, (2) from 3 to 6 days and (3) longer than 6 days. The second category was considered the standard duration because it represents the average weaning to estrus interval. The odds ratios were obtained from this analysis. As gilts did not have a

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previous lactation and weaning to estrus interval, they were excluded from lactation length and weaning to estrus interval analysis.

3. Results and discussion In the present study, ovarian cysts were found in 47 sows (2.36%), out of which 17 were from farm A (2.31%) and 30 from farm B (2.39%). The described incidence is based on the examination of 1990 sows evaluated either at rst breeding estrus (gilts) or in the rst estrus after weaning (multiparous sows), therefore, in animals without any previous record of individual reproductive problems. Despite these differences in weaning to estrus interval, parity and lactation length found in farms A and B, cyst incidence was similar in both. Due to the highly acceptable reproductive performance at both farms, the incidence of ovarian cysts was not great, maybe in farms with a lesser reproductive performance the incidence of ovarian cysts would have been greater. Evaluating sows with reproductive problems, Meredith (1977) found six cases of cysts in 46 animals (13%) by rectal palpation. Likewise, Heinonen et al. (1998) by evaluating tissues obtained from the slaughterhouse found that 6.2% of sows with reproductive failure had ovarian cysts. In non-pregnant sows, Gherpelli and Tarocco (1996) found 3.3% of cases associated with the presence of ovarian cysts. The described cyst incidences are based on the examination of a population where some previous reproductive problems had been found which led to reproductive failure and culling of sows. With the use of ultrasonography to evaluate the pre-weaning pattern of ovarian follicular development, Lucy et al. (1999) describes that a small percentage of sows have a pre-weaning cystic ovary and do not show signs of estrus after weaning. However, in the present study, all animals examined had shown estrus and did not have any record of previous reproductive failures, which may explain the low cyst incidence that was detected. Ovarian cyst incidence evaluations are usually performed on sows culled for reproductive problems. Based on the observations made in slaughterhouses, results are transferred to the herd. In these assessments, the incidence of cysts would be expected to be greater as compared with females that remain in breeding herds and that are not sent to the slaughterhouse. The sampling of tissues obtained from slaughterhouses is directed at low reproductive performance animals, therefore, not being a reliable reection of what is happening in the herd. This situation should be taken into account when comparisons with data gathered after slaughters are made. The incidence of ovarian cysts varied depending on the week the herd was examined. In two weeks no cysts were found, while in other weeks, up to eight new cases were found. This condition compromises the results obtained after slaughter and evaluation in the slaughterhouse due to the variability in cysts found over time. The variation between weeks could be explained by the observation of Gherpelli and Tarocco (1996) where the presence of zearalenone could be related to the incidence of cysts. However, the presence of mycotoxins was not evaluated in the present trial, although there is excellent quality control of feed production on both farms. Another that indicates the absence of zearalenone contamination is the very desirable reproductive performance of the herds in which evaluations occurred.

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Out of the 30 sows in with ovarian cysts on farm B, only nine (30%) cysts disappeared when evaluated by ultrasound examination until the 15th day of evaluation. This was also described by Waberski et al. (1999), when they found that 75% of cysts remained visible in the ultrasound examination until the 15th day. However, Lucy et al. (1999) reported that cysts regressed approximately one week after formation and a new cohort of follicles was formed. Length of estrus could not be determined in all sows that had an ovarian cyst. The main problem that made it difcult to make this determination was the fact that most of these sows had intermittent periods of estrus, not responding to the back-pressure test in some shifts, and responding to it in some subsequent shifts. During the trial, four sows with ovarian cysts presented nymphomaniac behavior. According to Britt et al. (1999), small cysts produce estrogen and thus, sows may present irregular estrous cycles or nymphomania. The rate of return to estrus was greater in sows with ovarian cysts (P < 0.001). This factor indicates that cysts appear to be an important risk factor for returning to estrus. Out of the 47 sows with ovarian cysts, 16 (34.0%) returned to estrus in a regular or an irregular cycle, 2 (4.3%) had an abortion (days 34 and 42 of pregnancy), 24 (51.1%) farrowed and 5 (10.6%) were not in pregnant (i.e., when they were expected to farrow). These latter sows were not pregnant, with anestrus. Data for the results on reproductive performance comparing females with or without cysts are included in Table 2. During the time the trial was performed, the return to estrus rate was 9.7 and 7.6% in farms A and B, respectively. In the sows that had ovarian cysts, some of them had a reproductive performance similar to the other sows, a situation that had previously been described by Dorka and Plonait (1995). These previous authors suggested that sows with cystic ovaries could maintain normal ovarian cycles and conceive. Of all evaluated sows, 157 returned to estrus, out of which 16 had cystic ovarian structures that amounts to approximately 10% of returns on both farms being related to the presence of cysts. The return to estrus observed for sows with ovarian cysts was of an interval equal to or longer than 25 days. Possibly a large part of clinical diagnoses related to irregular returns to estrus is compromised due to the presence of ovarian cysts. According to Meredith (1995), one of the risk factors associated with return to estrus is the presence of irregular estrous cycles caused by ovarian cysts. The presence of abortion among sows with ovarian cysts was above the average found for sows considered normal, but as only two cases were recorded, few conclusions could be made. However, the hypothesis that abortions could have been induced by endocrine disorders associated with the presence of ovarian cysts should not be ruled out. Small cysts have increased concentrations of estrogens (Miller, 1984) that can cause abortion in swine (Jainudeen and Hafez, 1995). Another situation found was the presence of non-pregnant anestrous sows. Out of 1990 sows evaluated, 17 (0.8%) were not pregnant, out of which ve had ovarian cysts (i.e., almost one-third, 29.4%) of all cases in both farms were associated with cysts. Miller (1984) suggested that large cysts have luteinized tissue that can produce progesterone in an amount great enough to suppress onset of estrus, thus causing an increase in the non-pregnant anestrous sow rate. The average litter size in sows without cysts was 10.5, while in sows with ovarian cysts it was 9.8 (P > 0.05). Although there was no statistical difference between both groups

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Table 2 Reproductive performance in sows with or without ovarian cysts Rates Farm A Without cyst N Return to estrus rate (%) Not in pig sows (%) Adjusted farrowing rate (%) Litter size, means SE (range) Piglet production in 100 sows 718 8.3 0.6 88.9 11.44 0.12 (320) 999 With cyst 17 35.3 5.9 50.9 11.11 0.98 (714) 588 P-value 0.001 0.184 0.001 0.739 0.001 Farm B Without cyst 1225 7.2 0.6 91.7 9.89 0.09 (119) 869 With cyst 30 33.3 13.3 53.3 9.06 0.78 (515) 436 P-value 0.001 0.001 0.001 0.293 0.001 For both farms Without cyst 1943 7.7 0.6 90.0 10.46 0.07 (120) 940 With cyst 47 34.0 10.6 52.2 9.83 0.62 (515) 524 P-value 0.001 0.001 0.001 0.319 0.001

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of sows, we should not rule out the hypothesis that the potential litter size was affected due to the small number of sows with cysts that actually farrowed. According to Miller (1984) ovulation cannot occur from cystic follicles. Cysts present before conception may not interfere with ovulation from other follicles, but they can decrease the number of normal viable eggs. This situation would lead to a reduction in potential litter size. By analyzing the estimated litter size in 100 bred sows, the damage caused by the presence of ovarian cysts becomes evident. The estimated number of piglets produced by 100 inseminated sows that had ovarian cysts was 512, while the others produced 941 piglets. Some authors suggest that the presence of ovarian cysts is related to seasons of the year. Liptrap and Doble (1981) suggesting that there is a greater incidence of cysts in spring than in autumn. According to Gherpelli and Tarocco (1996), the incidence is greater in autumn and winter months. The present trial was performed from autumn to spring and no seasonal effect was found during this period. Another factor that should be taken into account is the difference in temperatures and photoperiod due to location and time of the year in the present trial. In spite of these facts, the presence of ovarian cysts in sows at both farms was similar, thus suggesting that these factors were not signicant in contributing to the formation of ovarian cysts. In Table 3, the data are presented according to parity, previous lactation length and weaning to estrus interval on the incidence of ovarian cysts. Although only 1% of sows had lactation length as long as 14 days, 26.7% of these sows had ovarian cysts. This indicates that cyst incidence is signicantly greater when lactation period is shorter than 14 days. According to Sesti and Britt (1993), lactation can be divided into the following phases according to its endocrine status: hypergonadotropic phase (from farrowing to the second to third day), hypogonadotropic or transition phase (from the 3rd to 14th) and normalization phase (after the 14th day). According to these authors, if pigs are weaned in the rst phase,

Table 3 Distribution and odds ratio of ovarian cysts in sows according to the following categories: lactation length, parity and weaning to estrus interval Categories Lactation length category <14 days From 14 to 16 days From 17 to 19 days >19 days Parity category Nulliparous Primiparous Multiparous n 15 400 836 593 146 299 1545 Cyst cases 4 13 16 10 4 3 40 18 22 3 Percent 26.7a 3.2b 1.9b 1.7b 2.7 1.0 2.6 19.3a 1.3b 3.2b Odds ratio 5.922a 1.626b 1.000b 0.861b 1.060 0.381 1.000 15.292a 1.000b 2.013b

Weaning to estrus interval category <3 days 93 From 3 to 6 days 1656 >6 days 95
a b

On the same column P < 0.05. On the same column P < 0.05.

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the follicles present at farrowing can continue to grow because LH and FSH secretion is not suppressed. However, as sows are unable to produce a preovulatory surge release of LH, these follicles tend to grow into cysts. If sows are weaning during the hypogonadotropic phase, LH and FSH will be suppressed. According to Estienne et al. (1997), there is a GnRH secretion inhibition induced by the production of endogenous opioids released by the suckling stimulus. The exact cause and pathogeny of ovarian cysts, although not fully determined, is associated with LH release defciencies (Close and Liptrap, 1975; Miller, 1984). Stress situations, such as the one found in early weaning, could induce the release of adrenocorticotropic hormone and according to Miller (1984) daily administration of adrenocorticotropic hormone in the follicular phase can produce ovarian cysts. It should be stressed that although parity has inuenced lactation length, it did not inuence cyst incidence. Gherpelli and Tarocco (1996) did not nd any correlation either between parity and cyst incidence, although some previous research indicates that cyst incidence increases with age (Maclachlan and Foley, 1996). The weaning to estrus category also inuenced the presence of cysts (Table 3). Sows that had a weaning to estrus interval shorter than 3 days had a greater probability of developing cysts. The greater incidence of cysts in categories with a weaning to estrus interval shorter than 3 days and in categories with lactation length shorter than 14 days indicate that these animals may need more time to restore the LH surge mechanism, as it has been observed in cattle (Echternkamp et al., 1982). Sows with short weaning to estrus intervals and short lactation length have a greater risk for ovarian cyst development because they would have a well developed pulse frequency system allowing follicles to grow to preovulatory size, producing enough estrogen to express estrus, but have an insufcient LH surge system so that follicles fail to ovulate and become cystic. 4. Conclusions Results obtained from the present trial enables us to conclude that ovarian cysts are associated with around 10% of cases of return to estrus in farms where one-third of sows that suffer from this ovarian disorder return to estrus. The presence of ovarian cysts is more detrimental to the farrowing rate than to the number of total pigs born alive. Sows with weaning to estrus intervals shorter than 3 days and a lactation length shorter than 14 days have a greater probability of developing ovarian cysts. Acknowledgements The authors are grateful to the nancial support of: CAPES, CNPq, Perdigo Agroindustrial and Grupo Hofg Jr. References
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