Morphological and pathological aspects of the rete ovarii in sheep (Ovis aries)

Aspectos morfológicos e patológicos da rete ovarii em ovinos - Ovis aries

Morphological and pathological aspects of the rete ovarii in sheep (Ovis aries)

(Aspectos morfológicos e patológicos da rete ovarii em ovinos - Ovis aries)

G.D. Cassali¹, J.C. Nogueira¹, E.F. Nascimento², J.S. Cardoso¹, D.L. Ferreira¹

¹Instituto de Ciências Biológicas - ICB/UFMG

Caixa Postal 486

31270-901 - Belo Horizonte, MG

²Escola de Veterinária/UFMG

Recebido para publicação em 22 de julho de 1999.

E-mail: [e-mail]

ABSTRACT

Sixty-four ovaries of adult woolly sheep from the Centro de Pesquisa dos Campos Sul Brasileiros - Embrapa, Bagé-RS, Brazil, were analyzed histologically. The presence of the rete ovarii was detected in 55 of the 64 ovaries (85.9%), located in the periovarian tissue, in the hilus and in the medullary or cortical regions. As also observed in other mammals, the rete ovarii of sheep is morphologically divided into three portions: intraovarian rete, connecting rete and extraovarian rete. Continuity between the extraovarian rete and the uterine tube was observed in five ovaries (7.8%), suggesting a tuboretial connection, as reported for cows and does. Pathological examination of the rete showed the formation of cysts surrounding the connecting and/or extraovarian rete in seven cases (10.9%) and one case of hyperplasia of the extraovarian rete (1.6%).

Keywords: Sheep, ovary, rete ovarii

RESUMO

Foram analisados histologicamente 64 ovários de ovelhas lanadas adultas, procedentes do Centro de Pesquisa dos Campos Sul Brasileiros-Embrapa, Bagé-RS. Constatou-se, em 55 dos 64 ovários (85,9%), a presença da rete ovarii, localizada no tecido periovariano, no hilo, na medular ou na cortical. À semelhança do observado em outros mamíferos, a rete ovarii na ovelha é morfologicamente dividida em três porções: rete intra-ovárica, rete conectante e rete extra-ovárica. Em cinco ovários (7,8%) foi possível verificar uma continuidade entre a rete extra-ovárica e a tuba uterina, sugerindo uma conexão tubo-retial, de maneira similar à descrita para bovinos e para a corça. Quanto à patologia da rete, observaram-se a formação de cistos envolvendo a rete conectante e/ou extra-ovárica em sete casos (10,9%) e um caso de hiperplasia da rete extra-ovárica (1,6%).

Palavras-chave: Ovino, ovário, rete ovarii

INTRODUCTION

The rete ovarii is homologous to the rete testis and is classically considered to be the remnant of an embryonic structure in adult animals (Priedkalns, 1982; Fawcett, 1994). The rete ovarii develops from cells of mesonephric origin that migrate to the developing gonad and is characterized by a set of anastomosed tubules lined with columnar or cuboidal epithelium (Wenzel & Odend'hal, 1985). These tubules are usually located in the hilus of the ovary but may also extend through the ovarian medulla or be limited to the mesovarium adjacent to the hilus.

Three morphologically distinct portions of the rete ovarii have been described in newborn mice: extraovarian rete ovarii (ER), connecting rete ovarii (CR), and intraovarian rete ovarii (IR) (Byskov & Lintern-Moore, 1973). The ER consists of tortuous blind-bottomed tubules located in the periovarian tissue and lined with cuboidal, at times ciliated, epithelium. The IR is characterized by a system of cell cords that extend into the medullary and cortical layers and contain oocytes, with their cells being indistinguishable from granulosa cells. In contrast, the CR is located in the region of the ovarian hilus and is connected to the ER and IR by thick cell cords lined with stratified or pseudostratified columnar epithelium. This nomenclature has been used for the description of the rete ovarii of mice, rats, mink, ferrets, does, cats and cows (Wenzel et al., 1987).

Odend'hal et al. (1986) detected a communication between the ER and the infundibulum of the uterine tube in the rete ovarii of does, which was denoted tuboretial connection (TRC). The epithelium of the TRC shows a gentle transition to the epithelium of the infundibulum. Secretion similar to that in the lumen of the IR can be seen on the surface of the infundibular fimbria and the muscles around the rete ovarii are thought to expel this secreted material. Thus, secretions produced in the rete ovarii may theoretically be expelled through the TRC. While the function of the rete ovarii in the reproductive processes of adult animals continues to be speculative, the presence of a connection between the rete ovarii and the uterine tube, at least in some individuals, opens new perspectives. Other implications also arise with respect to the embryology of the tubular genitals derived from the paramesonephric system and the remaining portion of the mesonephric system.

Adenomatous changes have been observed in the rete ovarii of a small percentage of cows (Kanagawa, 1963; Abdo, 1987) and in dogs, goats and sheep (Marchevsky, 1981; Moreira, 1986; Cassali, 1989). Metaplastic alterations of the retial epithelium have also been reported in two cows with nymphomania due to follicular cysts (Donaldson & Hansel, 1968).

In a study of the ovaries of 225 sheep, Cassali (1989) observed the rete ovarii in 85.8% of the samples, with 34.7% of cases having the classical form (anastomosed tubules) and 51.1% having the form of separate cords or tubules. The author also detected 11 cases (4.9%) of adenomatous hyperplasia of the rete ovarii in sheep.

Cysts of the rete ovarii occur in all domestic animal species and are more frequent in dogs and cats (McEntee, 1990). According to Odend'hal et al. (1986), a likely explanation for the development of these cysts would be obstruction of the TRC.

The description of more accurate criteria for the study of the rete ovarii in mammals introduced by Odend'hal et al. (1986) led us to reevaluate the rete ovarii of sheep according to this methodology.

MATERIAL AND METHODS

Ovaries of 32 adult woolly sheep (Ovis aries) slaughtered at the Centro de Pesquisa dos Campos Sul Brasileiros-EMBRAPA, Bagé-RS, Brazil, were collected. The ovaries, together with the mesovaria and infundibula of the uterine tube, were fixed in 10% buffered neutral formalin for 24 to 48 hours. After fixation the ovaries were measured for length, width and thickness and only their central portion was removed together with the mesovarium and the infundibulum. The material thus obtained was routinely processed for paraffin embedding. The blocks were cut into semiserial 7µm thick sections and each 12th section was preserved. The sections were stained with hematoxylin-eosin, Gomori trichrome, PAS (Lillie & Fullmer, 1976), Alcian Blue, pH 2.5 (Mowry, 1956) and Alcian Blue, pH 1.0 (Lev & Spicer, 1964), and ninhydrin-Schiff (Yasuma & Ichikawa, 1953).

RESULTS AND DISCUSSION

The mean length, width and thickness of the ovaries were 1.4 ± 0.2, 1.1 ± 0.2 and 0.9 ± 0.2cm, respectively. These values are similar to those obtained in a previous study for material from adult sheep from the same region (Cassali, 1989).

The rete ovarii was present in 55 of the 64 ovaries examined (85.9%) and was located in the periovarian tissue, in the hilus, and in the medullary or cortical layer, as also observed in mice by Byskov & Lintern-Moore (1973). These observations support the findings reported by Hadek (1958) and Cassali (1989) but disagree with those reported by Shehata (1964) who found no medullary cords in the ovaries of 10 adult sheep. All three portions were detected in 23 (43.7%) of the 64 ovaries examined. On the basis of the results obtained, the rete ovarii of the sheep consists of three portions: intraovarian rete, connecting rete and extraovarian rete (Fig 1), according to the nomenclature used for mice, rats, minks, ferrets, cats, cows, and does (Wenzel et al., 1987).

The classical shape of the rete ovarii, i.e., in the form of anastomosed tubules lined with simple cuboidal epithelium and with a distinct lumen, was observed in the region of the ovarian hilus and mesovarium, thus corresponding to the CR and ER (Figs. 2A,B). The ER was characterized at times by anastomosed tubules and at others by sinuous tubular structures with a thin wall and lined with cuboidal or cylindrical epithelium. They were often contiguous to other tubular structures with a regular lumen surrounded by a fine smooth muscle layer (mesonephric tubules) (Fig. 2B). This connection of the rete with mesonephric tubules and the presence of cystic formations surrounding these tubules and the ER have been previously described by Saraumo (1954), Clement (1989) and McEntee (1990). In contrast, the intraovarian rete was located in regions of corticomedullary transition and in the cortical layer, with the aspect of small separate or multiple tubules lined with cuboidal epithelium with a rounded or oval nucleus, with scarce cytoplasm and with the lumen not always visible, contrary to what was observed in the CR and ER (Figs. 2C,D). Thus, the morphological features of the rete ovarii of sheep observed in the present study are similar, in general, to those described by Wenzel & Odend'hal (1985) and Odend'hal et al. (1986).

Although hormone-induced morphological changes of the rete ovarii were not investigated in the present study, in other mammals these aspects have been correlated to the phases of the ovarian cycle or to pregnancy (Saraumo, 1954; Archbald et al., 1971; Kumar & Singh, 1984; Wenzel et al., 1987).

In five ovaries (7.8%) there was continuity between the rete ovarii and the uterine tube, suggesting the existence of tuboretial connections, as also reported for cows and does (Odend'hal et al., 1986). However, in contrast to the data reported by the above authors, the transition between the ER epithelium and the uterine tube was abrupt (Fig. 2E).

With respect to rete pathology, the formation of cysts surrounding the CR or the ER were observed in seven cases (10.9%). Cassali (1989), in a study of 450 sheep ovaries, observed cystic dilation of the rete in 0.44% of cases. However, it should be pointed out that, although the sample was significant, the method previously used by the author consisted simply of examination of a single ovarian section. Other investigators, using a similar method in the study of goats (Moreira, 1986) and cows (Costa, 1984; Abdo, 1987), reported frequencies of 0.24%, 2.1% and 0.58%, respectively, for these alterations.

Cystic dilation in the TRC was observed in one of the ovaries examined here (Fig. 3A), and connection between mesonephric tubule cysts and the rete was observed in two other cases, in one of which the rete was also cystic (Fig. 3B).

Positive reactions to PAS, Alcian Blue, pH 2.5 and 1.0, and ninhydrin-Schiff indicated that the secretions inside the lumen of the CR and ER and of mesonephric tubules contain neutral mucosubstances associated with carboxylated and sulfated acid mucosubstances. However, more accurate evaluations of the PAS-positive material in the rete ovarii of cattle during the estrous cycle have been previously reported by Archbald et al. (1971) and Wenzel et al. (1987).

According to Gelberg et al. (1987), the development of rete cysts is not surprising since the rete of adult cats ends in a blind bottom and their cells are secretory. However, based on the study by Odend'hal et al. (1986), the most probable hypothesis for the formation of these cysts is obstruction of the TRC.

Although melanin was observed in 70.2% of the uteri of sheep previously examined by Cassali (1989), in the present study melanin was detected in the ER of only one ovary (1.6%). The presence of melanin in the ovary was demonstrated using the techniques of Whartin-Starry and the melanin bleach method described by Johnson (1992). The functional significance of this pigment in the female genital apparatus remains unknown.

ER hyperplasia was observed in only one ovary (1.6%) and was characterized by proliferation of anastomosed tubular structures of cord-like or acinar appearance lined with cuboidal epithelium and with slightly eosinophilic cytoplasm.

In conclusion, the present histological study of the rete ovarii showed that only a systematic analysis based on serial or semiserial sections permits an accurate visualization of its different portions and alterations.

ACKNOWLEDGEMENTS

We are grateful to the FAPEMIG, EMBRAPA and CNPq, Brazil, for the financial support, and Dr. José Carlos Ferrugem Moraes for his help during collection of samples.

REFERENCES

ABDO, M.A.G.S. Alterações morfológicas em ovários e útero de vacas azebuadas não gestantes. Belo Horizonte: Escola de Veterinária da UFMG, 1987. 70p.(Dissertação, Mestrado).

ARCHBALD, L.F., SCHULTZ, R.H., FAHNING, M.L. et al. Rete ovarii in heifers: a preliminary study. J. Reprod. Fertil., v.26, p.413-414, 1971.

BYSKOV, AG., LINTERN-MOORE, S. Follicle formation in the immature mouse ovary: the role of the rete ovarii. J. Anat., v.116, p.207-217, 1973.

CASSALI, G.D. Achados anátomo-patológicos em ovários e útero de ovelhas lanadas provenientes de dois rebanhos do Rio Grande do Sul. Belo Horizonte: Escola de Veterinária da UFMG, 1989. 77p.(Dissertação, Mestrado).

CLEMENT, P.B. Anatomy and histology of the ovary. In: KURMAN, R.J. Blaustein’s pathology of the female genital tract. 3.ed. New York: Springer Verlag. 1989. p.438-470.

COSTA, S.A Ocorrência de alterações em ovários de vacas azebuadas abatidas em matadouros dos Estados de Goiás e Minas Gerais. Belo Horizonte: Escola de Veterinária da UFMG, 1984. 131p.(Dissertação, Mestrado).

DONALDSON, L.E., HANSEL, W. Cystic corpora lutea and normal and cystic graafian follicles in the cow. Aust. Vet. J., v.44, p.304-308, 1968.

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HADEK, R. Morphological and histochemical study on the ovary of the sheep. Am. J. Vet. Res., v.19, p.873-881, 1958.

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KANAGAWA, H. Histopathological studies on the reproductive organs, pituitaries, thyroid, adrenals, and livers, from slaughtered cattle in Hokkaido. Jpn. Vet. Res., v.11, p.61-64, 1963.

KUMAR, N., SINGH, B. Histomorphological structures in ovaries of aged buffaloes. Indian J. Anim. Sci., v.54, p.628-635, 1984.

LEV, R., SPICER, S.S. Specific staining of sulphate groups with Alcian Blue at low pH. J. Histochem. Cytochem., v.12, p.309, 1964.

LILLIE, R. D., FULLMER, H.M. Histopathologic technique and pratical histochemistry. 4.ed. New York: Mc Graw-Hill, 1976. 942p.

MARCHEVSKY, R.S. Alterações morfológicas no ovário e corno uterino da cadela. Frequência e interações. Belo Horizonte: Escola de Veterinária da UFMG, 1981. 71p.(Dissertação, Mestrado).

McENTEE, K. Reproductive pathology of domestic mammals. San Diego: Academic Press. 1990. 401p.

MOREIRA, E.L.T. Alterações morfológicas em ovário e útero de Capra hircus L. Belo Horizonte: Escola de Veterinária da UFMG, 1986. 67p.(Dissertação, Mestrado).

MOWRY, R.W. Alcian blue, technique for the histochemical study of acidic carbohydrates. J. Histochem. Cytochem., v.4, p.407, 1956.

ODEND’HAL, S., WENZEL, J.G.W., PLAYER, E.C. The rete ovarii of cattle and deer communicates with the uterine tube. Anat. Rec., v.216, p.40-43, 1986.

PRIEDKALNS, J.S. Sistema reprodutor feminino. In: DELLMAN, H., BROWN, E.M Histologia veterinária. Rio de Janeiro: Guanabara Koogan, 1982. p.255-277.

SARAUMO, H. Development, occurrence, function and pathology of the rete ovarii. Acta Obstet. Gynec. Scand., v.33, p.29-46, 1954.

SHEHATA, R. Medullary tubes in the ovary of the camel and other mammals. Vet. Rec., v.76, p.750-753, 1964.

WENZEL, J.G.W., ODEND’HAL, S. The mammalian rete ovarii: a literature review. Cornell Vet., v.75, p.411-425, 1985.

WENZEL, J.G.W., ODEND’HAL, S., PLAYER, E.C. Histological and histochemical characterization of the bovine rete ovarii throught the estrous cycle and gestation. Anat. Histol. Embryol., v.16, p.124-135, 1987.

YASUMA, A, ICHIKAWA, T. Ninhydrin-Schiff and alloxan-Schiff staining. A new histochemical staining method for protein. J. Lab. Clin. Med., v.41, p.296-299, 1953.

• ABDO, M.A.G.S. Alteraçőes morfológicas em ovários e útero de vacas azebuadas năo gestantes. Belo Horizonte: Escola de Veterinária da UFMG, 1987. 70p.(Dissertaçăo, Mestrado).
• ARCHBALD, L.F., SCHULTZ, R.H., FAHNING, M.L. et al. Rete ovarii in heifers: a preliminary study. J. Reprod. Fertil, v.26, p.413-414, 1971.
• BYSKOV, AG., LINTERN-MOORE, S. Follicle formation in the immature mouse ovary: the role of the rete ovarii J. Anat, v.116, p.207-217, 1973.
• CASSALI, G.D. Achados anátomo-patológicos em ovários e útero de ovelhas lanadas provenientes de dois rebanhos do Rio Grande do Sul. Belo Horizonte: Escola de Veterinária da UFMG, 1989. 77p.(Dissertaçăo, Mestrado).
• COSTA, S.A Ocorręncia de alteraçőes em ovários de vacas azebuadas abatidas em matadouros dos Estados de Goiás e Minas Gerais Belo Horizonte: Escola de Veterinária da UFMG, 1984. 131p.(Dissertaçăo, Mestrado).
• DONALDSON, L.E., HANSEL, W. Cystic corpora lutea and normal and cystic graafian follicles in the cow. Aust. Vet. J, v.44, p.304-308, 1968.
• FAWCETT, D.W. Bloom and Fawcett - A textbook of histology. New York: Chapman & Hall, 1994. 964p.
• GELBERG, H. B. , McENTEE, K., HEATH, E.H. Feline cystic rete ovarii Vet. Pathol, v.21, p.304-307, 1987. .
• HADEK, R. Morphological and histochemical study on the ovary of the sheep. Am. J. Vet Res, v.19, p.873-881, 1958.
• JOHNSON, F.B. Pigments and minerals. In: PROPHET, E.B., MILLS, B., ARRINGTON, J.B. et al. Laboratory methods in histotechnology Washington: American Registry of Pathology, 1992. p.183-202.
• KANAGAWA, H. Histopathological studies on the reproductive organs, pituitaries, thyroid, adrenals, and livers, from slaughtered cattle in Hokkaido. Jpn. Vet. Res., v.11, p.61-64, 1963.
• KUMAR, N., SINGH, B. Histomorphological structures in ovaries of aged buffaloes. Indian J. Anim. Sci., v.54, p.628-635, 1984.
• LEV, R., SPICER, S.S. Specific staining of sulphate groups with Alcian Blue at low pH. J. Histochem. Cytochem, v.12, p.309, 1964.
• LILLIE, R. D., FULLMER, H.M. Histopathologic technique and pratical histochemistry 4.ed. New York: Mc Graw-Hill, 1976. 942p.
• MARCHEVSKY, R.S. Alteraçőes morfológicas no ovário e corno uterino da cadela. Frequęncia e interaçőes. Belo Horizonte: Escola de Veterinária da UFMG, 1981. 71p.(Dissertaçăo, Mestrado).
• McENTEE, K. Reproductive pathology of domestic mammals San Diego: Academic Press. 1990. 401p.
• MOREIRA, E.L.T. Alteraçőes morfológicas em ovário e útero de Capra hircus L. Belo Horizonte: Escola de Veterinária da UFMG, 1986. 67p.(Dissertaçăo, Mestrado).
• MOWRY, R.W. Alcian blue, technique for the histochemical study of acidic carbohydrates. J. Histochem. Cytochem, v.4, p.407, 1956.
• ODENDHAL, S., WENZEL, J.G.W., PLAYER, E.C. The rete ovarii of cattle and deer communicates with the uterine tube. Anat. Rec., v.216, p.40-43, 1986.
• PRIEDKALNS, J.S. Sistema reprodutor feminino. In: DELLMAN, H., BROWN, E.M Histologia veterinária Rio de Janeiro: Guanabara Koogan, 1982. p.255-277.
• SARAUMO, H. Development, occurrence, function and pathology of the rete ovarii. Acta Obstet. Gynec. Scand., v.33, p.29-46, 1954.
• SHEHATA, R. Medullary tubes in the ovary of the camel and other mammals. Vet. Rec., v.76, p.750-753, 1964.
• WENZEL, J.G.W., ODENDHAL, S. The mammalian rete ovarii: a literature review. Cornell Vet, v.75, p.411-425, 1985.
• WENZEL, J.G.W., ODENDHAL, S., PLAYER, E.C. Histological and histochemical characterization of the bovine rete ovarii throught the estrous cycle and gestation. Anat. Histol. Embryol, v.16, p.124-135, 1987.
• YASUMA, A, ICHIKAWA, T. Ninhydrin-Schiff and alloxan-Schiff staining. A new histochemical staining method for protein. J. Lab. Clin. Med., v.41, p.296-299, 1953.

Publication Dates

• Publication in this collection
  14 Aug 2000
• Date of issue
  Feb 2000

History

• Received
  22 July 1999