- Email: [email protected]
Abattoir evidence on association between uterine and ovarian abnormalities in Ethiopian highland ewes
Animal Reproduction Science 111 (2009) 384–390
Short communication
Abattoir evidence on association between uterine and ovarian abnormalities in Ethiopian highland ewes F. Regassa a,∗ , D. Mengesha a , M. Dargie a , T. Tolosa b a
Addis Ababa University, Faculty of Veterinary Medicine, Debre Zeit, P.O. Box 34, Ethiopia b Jimma University, School of Veterinary Medicine, P.O. Box 745, Jimma, Ethiopia
Received 23 May 2007; received in revised form 21 February 2008; accepted 17 March 2008 Available online 1 April 2008
Abstract A study was conducted on 3275 non-pregnant Ethiopian highland ewes slaughtered at the Addis Ababa municipal abattoir to determine whether uterine and ovarian abnormalities were associated. Each reproductive tract was examined for the presence of ovarian cysts, ovarobursal adhesions and gross uterine abnormalities. The percentage of ewes with ovarian cysts, ovarobursal adhesions and combination of both on the same ovary was 4.3%, 7.6% and 1.7%, respectively. The percentage of uterine abnormalities in tracts with ovarian cysts, ovarobursal adhesions, combined ovarian cysts and ovarobursal adhesions and those with normal ovaries was 46.1%, 31.9%, 46.3% and 4.3%, respectively. The prevalence of uterine abnormalities including hydro/mucometra, endometritis and pyometra was significantly higher (P < 0.001) in ewes with abnormal ovarian conditions than in those with normal ovaries. Also, the prevalence of uterine abnormalities was higher (P < 0.01) in ewes with ovarian cysts than in those with ovarobursal adhesions alone while in those ewes with co-existing ovarian cysts and ovarobursal adhesions it did not differ (P > 0.05) from those with either of these ovarian conditions. Among uterine abnormalities hydro/mucometra was higher (P < 0.01) in ewes with abnormal ovaries. In both groups of ewes with and without ovarian abnormalities pyometra was the least prevalent uterine disorder. These results indicate a direct strong association between uterine and ovarian abnormalities in the Ethiopian highland ewes. © 2008 Elsevier B.V. All rights reserved. Keywords: Ewes; Ovarian cysts; Ovarobursal adhesions; Uterine abnormalities
∗
Corresponding author. Tel.: +251 1433 5657; fax: +251 1433 0077. E-mail address: [email protected] (F. Regassa).
0378-4320/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2008.03.020
F. Regassa et al. / Animal Reproduction Science 111 (2009) 384–390
385
1. Introduction Among acquired reproductive abnormalities cystic ovaries, ovarobursal adhesions and different uterine pathologies have been reported in ewes (Alosta et al., 1998; Winter and Dobson, 1992; Emady, 1976). Cystic ovaries arise as a result of anovulation whereby instead of regression follicles continue to increase in size and persist (Arthur et al., 1989). Follicular and luteinized ovarian cysts are the two pathologic forms in cows (Kesler and Garverick, 1982) and in ewes (Alosta et al., 1998). Previously, it has been suggested that cystic ovarian degeneration is a result of a neuroendocrine imbalance involving the hypothalamus-pituitary-gonadal axis (DeSilva and Reeves, 1988; Eyestone and Ax, 1984). Rubianes et al. (1997) reported that inadequate concentration of LH receptors in aged follicles could lead to the formation of ovarian cysts in the ewe. Although the significance of ovarian cysts in the ewe is not very well known it has been a common finding in different breeds of ewes (Alosta et al., 1998; Rubianes et al., 1997; Winter and Dobson, 1992). However, it is likely that ewes with cystic ovaries could have higher prevalence of uterine abnormalities than ewes with normal ovarian conditions since ovarian cysts in ewes have been associated with increased plasma progesterone concentrations (Rubianes et al., 1997) that can reduce uterine resistance to bacterial infection (Lewis, 2003; Seals et al., 2003). Therefore, the objective of this study was to determine whether cystic ovaries and/or ovarobursal adhesions were associated with uterine pathological changes such as hydro/mucometra, endometeritis and pyometra in Ethiopian highland ewes. 2. Materials and methods 2.1. Study animals This study was conducted at the Addis Ababa municipal abattoir for 3 years during October 2002–May 2005 on the flock of slaughter ewes. The data collection was carried out from October to May each year i.e. during dry season. The origins of the study animals were the Ethiopian highlands of Wello, Fiche, Arsi and Debrebrhan lying within 200 km radius surrounding Addis Ababa, the capital. The ewes were managed on natural pasture under smallholder settings. The rainfall pattern in the highlands is bimodal with heavy rains from mid June to September and small rains during March–April. In these areas there have been efforts to classify sheep into different broad types, but except in a few locations several types have interbred to produce the Ethiopian highland sheep (Mukassa Mugerwa and Tekley, 1988). The reproductive tracts from the whole flock were examined when the number of ewes was small and ewes were randomly selected when the slaughter flock was large. 2.2. Examination of the genital tracts During the routine course of slaughter each reproductive tract was removed immediately and examined within 4 h after slaughter. Each tract was incised along the long axis through cervix, uterine body into the horns and closely examined for the presence of conceptus. Those pregnant tracts were excluded and all non-pregnant uteri and ovaries were carefully examined for any gross abnormalities as described by Winter and Dobson (1992). The size of the largest follicle on the ovary was measured using vernier caliper as described by Restall (1964) and Alosta et al. (1998). Ovaries with follicles ≥10 mm in diameter were considered cystic (Alosta et al., 1998; Winter and Dobson, 1992; Rubianes et al., 1997). Based on the appearance the cysts were classified into
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F. Regassa et al. / Animal Reproduction Science 111 (2009) 384–390
follicular and luteinized cyst. Follicular cysts were more tense, thin-walled follicles distended with pale yellow fluid while luteinized cysts were presented as thick-walled follicles lined with connective tissue layer containing more amber or dark yellow fluid (Garcia, 1988). Cystic follicles with diameter of 10–12 mm were classified as small and those ≥12.5 mm as large (Rubianes et al., 1997). Then each tract was carefully examined for the presence of attachment between the ovaries and the oviducts. Those adhesions involving about half the area of the ovary were considered as moderate and over three-quarters ovary as complete ovarobursal adhesion. Those with minor adhesions at small areas were excluded because it was considered that ovulation could normally proceed in these cases. Finally, gross uterine abnormalities (hydro/mucometra, endometritis and pyometra) were determined separately for tracts with ovarian cysts, ovarobursal adhesions, and co-existing ovarian cysts entrapped in ovarobursal adhesions and those with normal ovaries. 2.3. Data analysis The data were presented as percentages and mean ± S.D. SAS (1998) was used for data analysis. Differences in proportions of gross uterine abnormalities between ewes with normal ovaries and those with ovarian cysts and/or ovarobursal adhesions and other frequency data were determined using x2 -testes. Comparison between the mean diameter of the follicular and luteinized cysts was performed using unpaired t-test. The level of significance was set at P < 0.05. 3. Results A total of 3275 non-pregnant reproductive tracts of ewes were examined and, of these, 727 (22.2%) had one or more genital abnormalities. The various types of reproductive tract disorders and percentage of ewes affected are summarized in Table 1. Ovarian cysts were observed in 4.3% of the ewes. The prevalence of follicular and luteinized cysts did not differ (P > 0.05) between the right and left ovaries. The occurrence of bilateral cysts was lower (P < 0.01) than that of unilateral cysts either on the right or left ovary. The prevalence of ovarobursal adhesions was 7.6%. The adhesives were fibrous strands with varying thickness. Among the ovarobursal adhesions recorded on the right and left ovaries 189 (76.2%) were moderate and 59 (23.8%) were presented as complete envelopment of the ovaries in a closely applied fibrous tissue. The location and proportion of ovarobursal adhesions are presented in Fig. 1. Co-existing ovarian cysts and ovarobursal adhesions on the same ovary were recorded in 1.6% of the ewes examined and 47 Table 1 Percentages of gross reproductive tract abnormalities in Ethiopian highland ewes Abnormalities abnormalitiesa
1 2 3 4 5 6 7 8
Uterine Ovarobursal adhesions Ovaries cysts Parovarian cysts Ovidnct lesion Co-existing ovarian cyst and ovarobursal adhesion Ovarian atrophy Cervical and vaginal lesions
Total a
Hydro/mucometra, endometritis and pyometra.
Number (%) 290 (8.9) 248 (7.6) 141 (4.3) 92 (2.8) 78 (2.4) 54 (1.7) 53 (1.6) 69 (2.1) 727 (22.2)
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Fig. 1. Distribution and location of ovarobursal adhesions. Table 2 Size and type of ovarian cysts in Ethiopian highland ewes Cyst
Follicular
Diameter (mm)
Number
Mean ± S.D.
Number
Mean ± S.D.
10–12 (small) ≥12.5 (large)
48 15
11.30 ± 0.60 12.69 ± 0.56
36 42
11.85 ± 0.49 13.31 ± 0.67
Overall*
63
11.78 ± 0.85
78
12.64 ± 0.89
*
Lutinized
P < 0.01, t-test.
(87%) were unilateral and 7 (13%) were bilateral cases. The prevalence of co-existing ovarian cysts and ovarobursal adhesions on the right ovaries (61.1%) was higher (P < 0.05) than that on the left ovaries (38.9%). The overall mean diameter of luteinized cysts was higher (P < 0.01) than that of follicular cysts (Table 2). A total of 290 (8.9%) different gross uterine abnormalities including hydro/mucometra, endometritis and pyometra were recorded in ewes with abnormal ovarian conditions (ovarian cysts and/or ovarobursal adhesions) and those ewes with normal ovaries (Table 3). The prevalence of uterine abnormalities was significantly higher (P < 0.001) in ewes with abnormal ovarian conditions than in those with normal ovaries and the prevalence odd ratio was 6.46. The prevalence of different uterine pathology in ewes with and without ovarian pathology is presented in Table 4. The prevalence of uterine and ovarian abnormalities did not differ (P > 0.05) between the Table 3 Gross uterine disorders in ewe with and without ovarian abnormalities Ovarian condition
1 2 3 4
Normal Ovarobursal adhesions Ovarian cysts Co-existing ovarobursal adhesions and ovarian cysts
Uterine disorders Number observed
Number (%)
2832 248 141 54
121 (4.3)a 79 (31.9)b 65 (46.1)c 25 (46.3)bc
Figures in the same column with different superscripts are significantly different (P < 0.01).
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Table 4 Types of uterine abnormalities in ewes with and without abnormal ovarian conditions Uterine abnormalities
Ovarian conditions Normal (N = 2832)
Hydro/mucometra Endometritis Pyometra Total
39 (1.4)a 55 (1.9)a 27 (1.0)b 121 (4.3)
Abnormal (N = 443) 94 (21.2)a 44 (9.9)b 31 (7.0)c
x2 -test *** *** ***
169 (38.2)
Figures in the same column with different superscripts are significantly different (P < 0.05). *** P < 0.001.
years of study. Comparison between the dry and rainy season was not carried out because data collection took place during October–May and not during wet season (June–September). 4. Discussion The overall prevalence of reproductive tract abnormalities in the slaughter ewes in this study was 22.2%. Also, the present findings showed that the prevalence of ovarian cysts and ovarobursal adhesions were in agreement with previous studies in the Middle East ewes (Emady, 1976). The mean diameter of the follicular and luteinized cysts was similar to that reported by Rubianes et al. (1997), but lower than that reported by Alosta et al. (1998). This could be attributed to breed difference. However, these results indicated that ovarobursal adhesions were more frequently encountered on the right ovary and this was in agreement with the findings of Kessey and Noakes (1985). This could be associated with higher function of the right ovary in ewes (Casida et al., 1966). Ovarobursal adhesions may have resulted from ovulatory processes. Ovulation has been regarded as a physiological hazard that involves slight haemorrhage (Arthur et al., 1989) and inflammatory process (Epsey, 1994). In addition, ovarobursal adhesions may physically prevent ovulation and lead to development of cysts on the ovary (Herenda, 1987). In this study, the results showed a higher prevalence of uterine abnormalities in ewes with ovarian abnormalities than in ewes with no ovarian pathology. The odds of having uterine abnormalities with abnormal ovaries were about six times those with normal ovaries. In cows, disruption of ovarian function as result of uterine infection has been reported (Sheldon and Dobson, 2004; Sheldon et al., 2002). The effect of uterine infection on ovarian function could be due to the role of endotoxins, which are the components of the Gram-negative bacterial cell wall (Mateus et al., 2003). In cows (Peter et al., 1989) and ewes (Karsch et al., 2002) infusion of Escherichia coli endotoxin into uterine lumen prevents preovulatory LH surge and ovulation, causing persistent ovarian cysts. The effect of uterine infection and subsequent immune response may directly (Sheldon and Dobson, 2004) be exerted on the ovary or indirectly (Karsch et al., 2002) by suppression of LH secretion from pituitary. From these observations, it is likely that ovarian cysts in the present study resulted from uterine infection as indicated by endometritis and pyometra. Hydro/mucometra in this case may reflect earliest form of uterine infection or subclinical endometritis. In this study, ewes with ovarian cysts and clinically normal uteri were observed. This perhaps reflects the persistence of ovarian disorders even after clinical resolution of uterine damage (Sheldon and Dobson, 2004). Conversely, uterine resistance to bacterial infection is reduced when it is under the influence of progesterone and increases when progesterone concentrations are at basal levels (Lewis, 2003; Seals et al., 2003). Exogenous progesterone treatment and bacterial infusion into uterine lumen in
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postpartum ewes lead to establishment of uterine infection (Lewis, 2003). In addition, early ovulation postpartum and establishment of progesterone phase before complete bacterial clearance leads to uterine infection (Olson et al., 1984) and a risk of prolonged luteal cycle (Opsomer et al., 2000). Ovarian cysts in ewes are associated with high plasma progesterone concentrations (Alosta et al., 1998; Rubianes et al., 1997). The emergence of ovarian cysts in cows following long-term exogenous progesterone treatment has also been reported (Noble et al., 2000). This could be either due to down regulation of uterine immunity and subsequent uterine infection (Lewis, 2003) or endocrine disturbance leading to ovulatory defect (Rubianes et al., 1997). Thus, it is possible that higher progesterone concentrations in cystic ovarian cases predisposed the ewes in this study to uterine infection. The duration of cystic conditions may lead to changes in uterine immunity and environment that result in accumulation of fluids, which eventually become infected with bacteria. Also, compared to tracts with normal ovaries those with ovarobursal adhesions without ovarian cysts had higher prevalence of uterine abnormalities. In this case obstruction of the oviduct might have led to accumulation of fluids that became secondarily infected with bacteria (Arthur et al., 1989). These results indicated that uterine and ovarian abnormalities were directly strongly associated and that ovarian cysts, ovarobursal adhesions and associated uterine abnormalities may have contributed to poor reproductive performance of the Ethiopian highland ewes. Acknowledgements We wish to express sincere thanks to the administration and technical staff of Addis Ababa municipal abattoir for their unreserved cooperation. References Alosta, R.A., Vaugnan, L., Collins, J.D., 1998. An abattoir survey of ovine reproductive tracts in Ireland. Theriogenology 50, 457–464. Arthur, G.H., Noakes, D.E., Pearson, H., 1989. Veterinary Reproduction and Obstetrics, sixth ed. Bailliere Tindall, London, pp. 59–89. Casida, L.E., Woody, C.O., Pope, A.L., 1966. Inequality in function of the right and left ovaries and uterine hrns of the ewe. Anim. Sci. 25, 1169–1171. DeSilva, M., Reeves, J.J., 1988. Hypothalamic-pituitary function in chronically cystic and regularly cycling dairy cows. Biol. Reprod. 38, 264–269. Emady, M., 1976. Reproduction of the ewe and female goat in the province of Fars, Iran. Vet. Rec. 99, 208–209. Epsey, L.L., 1994. Current status of the hypothesis that mammalian ovulation is comparable to inflammatory reaction. Biol. Reprod. 38, 264–269. Eyestone, W.H., Ax, R.L., 1984. A review of ovarian follicular cyst in cows, with comparison to the condition in woman, rats and rabbits. Theriogenology 22, 109–125. Garcia, M., 1988. A gross morphological abattoir survey of genital organs from female Zebu cattle. Acta Vet. Scand. 83, 34–45. Herenda, D., 1987. An abattoir survey of reproductive organ abnormalities in beef heifers. Can. Vet. J. 28, 33–36. Karsch, F.J., Battaglia, D.F., Breen, K.M., Debus, N., Harris, T.G., 2002. Mechanism for ovarian cycle disruption by immune inflammatory stress. Stress 5, 101–112. Kesler, D.J., Garverick, H.A., 1982. Ovarian cysts in dairy cattle: a review. Anim. Sci. 55, 1147–1158. Kessey, B.M., Noakes, D.E., 1985. Uterine tube abnormalities as a cause of bovine infertility. Vet. Rec. 117, 122–124. Lewis, G.S., 2003. Steroid regulation of uterine resistance to bacterial infection in livestock: a review. Reprod. Biol. Endocrinol. 1, 117. Mateus, L., Lopes da Costa, L., Diniz, P., Ziecik, A., 2003. Relationship between endotoxin and prostaglandin (PGE2 and PGFM) concentrations and ovarian function in dairy cows with puerperal endometritis. Anim. Reprod. Sci. 76, 143–154.
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Mukassa Mugerwa, E., Tekley, B., 1988. The reproductive performance of Ethiopia high land ewes. Anim. Reprod. Sci. 17, 95–102. Noble, K.M., Tebble, J.E., Harvey, D., Dobson, H., 2000. Ultrasonography and hormonal profiles of persistent ovarian follicles (cysts) induced with low doses of progesterone in cattle. J. Reprod. Fertil. 120, 361–366. Olson, J.D., Ball, L., Mortimer, R.G., Farin, P.W., Adney, W.S., Huffman, E.M., 1984. Aspect of bacteriology and endocrinology of cows with pyometra and retained foetal membranes. Am. J. Vet. Res. 45, 2251–2255. Opsomer, G., Grohn, Y.T., Hertl, J., Coryn, M., Deluyker, H., de Kruff, A., 2000. Risk factors for post partum ovarian dysfunction in high producing dairy cows in Belgium: a field study. Theriogenology 53, 841–857. Peter, A.R., Bosu, W.T.K., DeDecker, R.J., 1989. Suppression of preovulatory luteinizing hormone surgesin heifers after intrauterine infusion of Escherichia coli endotoxin. Am. J. Vet. Res. 50, 368–373. Restall, B.J., 1964. The growth and regression of the corpusluteum in the ewe. Aust. J. Exp. Agric. Anim. Husb. 4, 274–276. Rubianes, E., De Castro, T., Ungerfled, R., Meikle, A., Rivero, A., 1997. Ovarian response after a GnRH challenge in seasonally anoestrous ewes. Can. J. Anim. Sci. 77, 727–730. SAS, 1998. SAS institute Inc, Cary, NC, USA. Seals, R.C., Wulster-Radcliffe, M.C., Lewis, G.S., 2003. Uterine response to infectious bacteria in estrous cyclic ewes. Am. J. Reprod. Immunol. 49, 269–278. Sheldon, I.M., Dobson, H., 2004. Postpartum uterine health in cattle. Anim. Reprod. Sci. 82, 295–306. Sheldon, I.M., Noakes, D.E., Rycroft, A.N., Pfeiffer, D.U., Dobson, H., 2002. Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction 123, 837–845. Winter, A.C., Dobson, H., 1992. Observation on the genital tract of cull ewes. Vet. Rec. 30, 68–70.
Short communication
Abattoir evidence on association between uterine and ovarian abnormalities in Ethiopian highland ewes F. Regassa a,∗ , D. Mengesha a , M. Dargie a , T. Tolosa b a
Addis Ababa University, Faculty of Veterinary Medicine, Debre Zeit, P.O. Box 34, Ethiopia b Jimma University, School of Veterinary Medicine, P.O. Box 745, Jimma, Ethiopia
Received 23 May 2007; received in revised form 21 February 2008; accepted 17 March 2008 Available online 1 April 2008
Abstract A study was conducted on 3275 non-pregnant Ethiopian highland ewes slaughtered at the Addis Ababa municipal abattoir to determine whether uterine and ovarian abnormalities were associated. Each reproductive tract was examined for the presence of ovarian cysts, ovarobursal adhesions and gross uterine abnormalities. The percentage of ewes with ovarian cysts, ovarobursal adhesions and combination of both on the same ovary was 4.3%, 7.6% and 1.7%, respectively. The percentage of uterine abnormalities in tracts with ovarian cysts, ovarobursal adhesions, combined ovarian cysts and ovarobursal adhesions and those with normal ovaries was 46.1%, 31.9%, 46.3% and 4.3%, respectively. The prevalence of uterine abnormalities including hydro/mucometra, endometritis and pyometra was significantly higher (P < 0.001) in ewes with abnormal ovarian conditions than in those with normal ovaries. Also, the prevalence of uterine abnormalities was higher (P < 0.01) in ewes with ovarian cysts than in those with ovarobursal adhesions alone while in those ewes with co-existing ovarian cysts and ovarobursal adhesions it did not differ (P > 0.05) from those with either of these ovarian conditions. Among uterine abnormalities hydro/mucometra was higher (P < 0.01) in ewes with abnormal ovaries. In both groups of ewes with and without ovarian abnormalities pyometra was the least prevalent uterine disorder. These results indicate a direct strong association between uterine and ovarian abnormalities in the Ethiopian highland ewes. © 2008 Elsevier B.V. All rights reserved. Keywords: Ewes; Ovarian cysts; Ovarobursal adhesions; Uterine abnormalities
∗
Corresponding author. Tel.: +251 1433 5657; fax: +251 1433 0077. E-mail address: [email protected] (F. Regassa).
0378-4320/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2008.03.020
F. Regassa et al. / Animal Reproduction Science 111 (2009) 384–390
385
1. Introduction Among acquired reproductive abnormalities cystic ovaries, ovarobursal adhesions and different uterine pathologies have been reported in ewes (Alosta et al., 1998; Winter and Dobson, 1992; Emady, 1976). Cystic ovaries arise as a result of anovulation whereby instead of regression follicles continue to increase in size and persist (Arthur et al., 1989). Follicular and luteinized ovarian cysts are the two pathologic forms in cows (Kesler and Garverick, 1982) and in ewes (Alosta et al., 1998). Previously, it has been suggested that cystic ovarian degeneration is a result of a neuroendocrine imbalance involving the hypothalamus-pituitary-gonadal axis (DeSilva and Reeves, 1988; Eyestone and Ax, 1984). Rubianes et al. (1997) reported that inadequate concentration of LH receptors in aged follicles could lead to the formation of ovarian cysts in the ewe. Although the significance of ovarian cysts in the ewe is not very well known it has been a common finding in different breeds of ewes (Alosta et al., 1998; Rubianes et al., 1997; Winter and Dobson, 1992). However, it is likely that ewes with cystic ovaries could have higher prevalence of uterine abnormalities than ewes with normal ovarian conditions since ovarian cysts in ewes have been associated with increased plasma progesterone concentrations (Rubianes et al., 1997) that can reduce uterine resistance to bacterial infection (Lewis, 2003; Seals et al., 2003). Therefore, the objective of this study was to determine whether cystic ovaries and/or ovarobursal adhesions were associated with uterine pathological changes such as hydro/mucometra, endometeritis and pyometra in Ethiopian highland ewes. 2. Materials and methods 2.1. Study animals This study was conducted at the Addis Ababa municipal abattoir for 3 years during October 2002–May 2005 on the flock of slaughter ewes. The data collection was carried out from October to May each year i.e. during dry season. The origins of the study animals were the Ethiopian highlands of Wello, Fiche, Arsi and Debrebrhan lying within 200 km radius surrounding Addis Ababa, the capital. The ewes were managed on natural pasture under smallholder settings. The rainfall pattern in the highlands is bimodal with heavy rains from mid June to September and small rains during March–April. In these areas there have been efforts to classify sheep into different broad types, but except in a few locations several types have interbred to produce the Ethiopian highland sheep (Mukassa Mugerwa and Tekley, 1988). The reproductive tracts from the whole flock were examined when the number of ewes was small and ewes were randomly selected when the slaughter flock was large. 2.2. Examination of the genital tracts During the routine course of slaughter each reproductive tract was removed immediately and examined within 4 h after slaughter. Each tract was incised along the long axis through cervix, uterine body into the horns and closely examined for the presence of conceptus. Those pregnant tracts were excluded and all non-pregnant uteri and ovaries were carefully examined for any gross abnormalities as described by Winter and Dobson (1992). The size of the largest follicle on the ovary was measured using vernier caliper as described by Restall (1964) and Alosta et al. (1998). Ovaries with follicles ≥10 mm in diameter were considered cystic (Alosta et al., 1998; Winter and Dobson, 1992; Rubianes et al., 1997). Based on the appearance the cysts were classified into
386
F. Regassa et al. / Animal Reproduction Science 111 (2009) 384–390
follicular and luteinized cyst. Follicular cysts were more tense, thin-walled follicles distended with pale yellow fluid while luteinized cysts were presented as thick-walled follicles lined with connective tissue layer containing more amber or dark yellow fluid (Garcia, 1988). Cystic follicles with diameter of 10–12 mm were classified as small and those ≥12.5 mm as large (Rubianes et al., 1997). Then each tract was carefully examined for the presence of attachment between the ovaries and the oviducts. Those adhesions involving about half the area of the ovary were considered as moderate and over three-quarters ovary as complete ovarobursal adhesion. Those with minor adhesions at small areas were excluded because it was considered that ovulation could normally proceed in these cases. Finally, gross uterine abnormalities (hydro/mucometra, endometritis and pyometra) were determined separately for tracts with ovarian cysts, ovarobursal adhesions, and co-existing ovarian cysts entrapped in ovarobursal adhesions and those with normal ovaries. 2.3. Data analysis The data were presented as percentages and mean ± S.D. SAS (1998) was used for data analysis. Differences in proportions of gross uterine abnormalities between ewes with normal ovaries and those with ovarian cysts and/or ovarobursal adhesions and other frequency data were determined using x2 -testes. Comparison between the mean diameter of the follicular and luteinized cysts was performed using unpaired t-test. The level of significance was set at P < 0.05. 3. Results A total of 3275 non-pregnant reproductive tracts of ewes were examined and, of these, 727 (22.2%) had one or more genital abnormalities. The various types of reproductive tract disorders and percentage of ewes affected are summarized in Table 1. Ovarian cysts were observed in 4.3% of the ewes. The prevalence of follicular and luteinized cysts did not differ (P > 0.05) between the right and left ovaries. The occurrence of bilateral cysts was lower (P < 0.01) than that of unilateral cysts either on the right or left ovary. The prevalence of ovarobursal adhesions was 7.6%. The adhesives were fibrous strands with varying thickness. Among the ovarobursal adhesions recorded on the right and left ovaries 189 (76.2%) were moderate and 59 (23.8%) were presented as complete envelopment of the ovaries in a closely applied fibrous tissue. The location and proportion of ovarobursal adhesions are presented in Fig. 1. Co-existing ovarian cysts and ovarobursal adhesions on the same ovary were recorded in 1.6% of the ewes examined and 47 Table 1 Percentages of gross reproductive tract abnormalities in Ethiopian highland ewes Abnormalities abnormalitiesa
1 2 3 4 5 6 7 8
Uterine Ovarobursal adhesions Ovaries cysts Parovarian cysts Ovidnct lesion Co-existing ovarian cyst and ovarobursal adhesion Ovarian atrophy Cervical and vaginal lesions
Total a
Hydro/mucometra, endometritis and pyometra.
Number (%) 290 (8.9) 248 (7.6) 141 (4.3) 92 (2.8) 78 (2.4) 54 (1.7) 53 (1.6) 69 (2.1) 727 (22.2)
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Fig. 1. Distribution and location of ovarobursal adhesions. Table 2 Size and type of ovarian cysts in Ethiopian highland ewes Cyst
Follicular
Diameter (mm)
Number
Mean ± S.D.
Number
Mean ± S.D.
10–12 (small) ≥12.5 (large)
48 15
11.30 ± 0.60 12.69 ± 0.56
36 42
11.85 ± 0.49 13.31 ± 0.67
Overall*
63
11.78 ± 0.85
78
12.64 ± 0.89
*
Lutinized
P < 0.01, t-test.
(87%) were unilateral and 7 (13%) were bilateral cases. The prevalence of co-existing ovarian cysts and ovarobursal adhesions on the right ovaries (61.1%) was higher (P < 0.05) than that on the left ovaries (38.9%). The overall mean diameter of luteinized cysts was higher (P < 0.01) than that of follicular cysts (Table 2). A total of 290 (8.9%) different gross uterine abnormalities including hydro/mucometra, endometritis and pyometra were recorded in ewes with abnormal ovarian conditions (ovarian cysts and/or ovarobursal adhesions) and those ewes with normal ovaries (Table 3). The prevalence of uterine abnormalities was significantly higher (P < 0.001) in ewes with abnormal ovarian conditions than in those with normal ovaries and the prevalence odd ratio was 6.46. The prevalence of different uterine pathology in ewes with and without ovarian pathology is presented in Table 4. The prevalence of uterine and ovarian abnormalities did not differ (P > 0.05) between the Table 3 Gross uterine disorders in ewe with and without ovarian abnormalities Ovarian condition
1 2 3 4
Normal Ovarobursal adhesions Ovarian cysts Co-existing ovarobursal adhesions and ovarian cysts
Uterine disorders Number observed
Number (%)
2832 248 141 54
121 (4.3)a 79 (31.9)b 65 (46.1)c 25 (46.3)bc
Figures in the same column with different superscripts are significantly different (P < 0.01).
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Table 4 Types of uterine abnormalities in ewes with and without abnormal ovarian conditions Uterine abnormalities
Ovarian conditions Normal (N = 2832)
Hydro/mucometra Endometritis Pyometra Total
39 (1.4)a 55 (1.9)a 27 (1.0)b 121 (4.3)
Abnormal (N = 443) 94 (21.2)a 44 (9.9)b 31 (7.0)c
x2 -test *** *** ***
169 (38.2)
Figures in the same column with different superscripts are significantly different (P < 0.05). *** P < 0.001.
years of study. Comparison between the dry and rainy season was not carried out because data collection took place during October–May and not during wet season (June–September). 4. Discussion The overall prevalence of reproductive tract abnormalities in the slaughter ewes in this study was 22.2%. Also, the present findings showed that the prevalence of ovarian cysts and ovarobursal adhesions were in agreement with previous studies in the Middle East ewes (Emady, 1976). The mean diameter of the follicular and luteinized cysts was similar to that reported by Rubianes et al. (1997), but lower than that reported by Alosta et al. (1998). This could be attributed to breed difference. However, these results indicated that ovarobursal adhesions were more frequently encountered on the right ovary and this was in agreement with the findings of Kessey and Noakes (1985). This could be associated with higher function of the right ovary in ewes (Casida et al., 1966). Ovarobursal adhesions may have resulted from ovulatory processes. Ovulation has been regarded as a physiological hazard that involves slight haemorrhage (Arthur et al., 1989) and inflammatory process (Epsey, 1994). In addition, ovarobursal adhesions may physically prevent ovulation and lead to development of cysts on the ovary (Herenda, 1987). In this study, the results showed a higher prevalence of uterine abnormalities in ewes with ovarian abnormalities than in ewes with no ovarian pathology. The odds of having uterine abnormalities with abnormal ovaries were about six times those with normal ovaries. In cows, disruption of ovarian function as result of uterine infection has been reported (Sheldon and Dobson, 2004; Sheldon et al., 2002). The effect of uterine infection on ovarian function could be due to the role of endotoxins, which are the components of the Gram-negative bacterial cell wall (Mateus et al., 2003). In cows (Peter et al., 1989) and ewes (Karsch et al., 2002) infusion of Escherichia coli endotoxin into uterine lumen prevents preovulatory LH surge and ovulation, causing persistent ovarian cysts. The effect of uterine infection and subsequent immune response may directly (Sheldon and Dobson, 2004) be exerted on the ovary or indirectly (Karsch et al., 2002) by suppression of LH secretion from pituitary. From these observations, it is likely that ovarian cysts in the present study resulted from uterine infection as indicated by endometritis and pyometra. Hydro/mucometra in this case may reflect earliest form of uterine infection or subclinical endometritis. In this study, ewes with ovarian cysts and clinically normal uteri were observed. This perhaps reflects the persistence of ovarian disorders even after clinical resolution of uterine damage (Sheldon and Dobson, 2004). Conversely, uterine resistance to bacterial infection is reduced when it is under the influence of progesterone and increases when progesterone concentrations are at basal levels (Lewis, 2003; Seals et al., 2003). Exogenous progesterone treatment and bacterial infusion into uterine lumen in
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postpartum ewes lead to establishment of uterine infection (Lewis, 2003). In addition, early ovulation postpartum and establishment of progesterone phase before complete bacterial clearance leads to uterine infection (Olson et al., 1984) and a risk of prolonged luteal cycle (Opsomer et al., 2000). Ovarian cysts in ewes are associated with high plasma progesterone concentrations (Alosta et al., 1998; Rubianes et al., 1997). The emergence of ovarian cysts in cows following long-term exogenous progesterone treatment has also been reported (Noble et al., 2000). This could be either due to down regulation of uterine immunity and subsequent uterine infection (Lewis, 2003) or endocrine disturbance leading to ovulatory defect (Rubianes et al., 1997). Thus, it is possible that higher progesterone concentrations in cystic ovarian cases predisposed the ewes in this study to uterine infection. The duration of cystic conditions may lead to changes in uterine immunity and environment that result in accumulation of fluids, which eventually become infected with bacteria. Also, compared to tracts with normal ovaries those with ovarobursal adhesions without ovarian cysts had higher prevalence of uterine abnormalities. In this case obstruction of the oviduct might have led to accumulation of fluids that became secondarily infected with bacteria (Arthur et al., 1989). These results indicated that uterine and ovarian abnormalities were directly strongly associated and that ovarian cysts, ovarobursal adhesions and associated uterine abnormalities may have contributed to poor reproductive performance of the Ethiopian highland ewes. Acknowledgements We wish to express sincere thanks to the administration and technical staff of Addis Ababa municipal abattoir for their unreserved cooperation. References Alosta, R.A., Vaugnan, L., Collins, J.D., 1998. An abattoir survey of ovine reproductive tracts in Ireland. Theriogenology 50, 457–464. Arthur, G.H., Noakes, D.E., Pearson, H., 1989. Veterinary Reproduction and Obstetrics, sixth ed. Bailliere Tindall, London, pp. 59–89. Casida, L.E., Woody, C.O., Pope, A.L., 1966. Inequality in function of the right and left ovaries and uterine hrns of the ewe. Anim. Sci. 25, 1169–1171. DeSilva, M., Reeves, J.J., 1988. Hypothalamic-pituitary function in chronically cystic and regularly cycling dairy cows. Biol. Reprod. 38, 264–269. Emady, M., 1976. Reproduction of the ewe and female goat in the province of Fars, Iran. Vet. Rec. 99, 208–209. Epsey, L.L., 1994. Current status of the hypothesis that mammalian ovulation is comparable to inflammatory reaction. Biol. Reprod. 38, 264–269. Eyestone, W.H., Ax, R.L., 1984. A review of ovarian follicular cyst in cows, with comparison to the condition in woman, rats and rabbits. Theriogenology 22, 109–125. Garcia, M., 1988. A gross morphological abattoir survey of genital organs from female Zebu cattle. Acta Vet. Scand. 83, 34–45. Herenda, D., 1987. An abattoir survey of reproductive organ abnormalities in beef heifers. Can. Vet. J. 28, 33–36. Karsch, F.J., Battaglia, D.F., Breen, K.M., Debus, N., Harris, T.G., 2002. Mechanism for ovarian cycle disruption by immune inflammatory stress. Stress 5, 101–112. Kesler, D.J., Garverick, H.A., 1982. Ovarian cysts in dairy cattle: a review. Anim. Sci. 55, 1147–1158. Kessey, B.M., Noakes, D.E., 1985. Uterine tube abnormalities as a cause of bovine infertility. Vet. Rec. 117, 122–124. Lewis, G.S., 2003. Steroid regulation of uterine resistance to bacterial infection in livestock: a review. Reprod. Biol. Endocrinol. 1, 117. Mateus, L., Lopes da Costa, L., Diniz, P., Ziecik, A., 2003. Relationship between endotoxin and prostaglandin (PGE2 and PGFM) concentrations and ovarian function in dairy cows with puerperal endometritis. Anim. Reprod. Sci. 76, 143–154.
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