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Uterine Blood Flow and Perfusion in Mares with Uterine Cysts REPRODUCTIONRESEARCH Uterine blood flow and perfusion in mares with uterine cysts: effect of the size of the cystic area and age J C Ferreira1, E L Gastal2 and O J Ginther1,2 1Eutheria Foundation, Cross Plains, Wisconsin 53528, USA and 2Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin, 1656 Linden Drive, Madison, Wisconsin 53706, USA Correspondence should be addressed to E L Gastal; Email: [email protected] Abstract Transrectal color and power Doppler ultrasonography was used to study uterine blood flow and perfusion in mares with and without uterine cysts. Vascular perfusion of the uterus and blood flow velocities, vascular perfusion, diameter,circumference, and area of a cross section of the mesometrial attachment were evaluated. To study the effect of internal cysts, two matched groups (cystic and control, nZ21 mares/group) were used. Uterine vascular perfusion in mares with cysts was less (P!0.0001) in the cystic than the noncystic region and less (P!0.0009) than that for controls. Mares with cysts had lower (P!0.04) pulsatility index (PI) and greater end diastolic velocity (EDV; P!0.03) and time-averaged maximum velocity (TAMV; P!0.05) of the mesometrial vessels than the controls. To study the effect of the size of internal uterine cystic area, paired mares were arranged in four groups (nZ8–11/group): small uterine cystic area (%275 mm2) versus controls and large uterine cystic area (O410 mm2) versus controls. A small uterine cystic area did not affect uterine hemodynamics. Mares with large uterine cystic area had lower PI (P!0.05) and greater peak systolic velocity (P%0.05), EDV (P!0.009), and TAMV (P!0.005). To study the effect of age, old versus young mares without cysts were compared (nZ11/group). Old mares had greater EDV (P!0.02) and TAMV (P!0.01) than young mares. Results demonstrated, for the first time in any species, reduced uterine vascular perfusion in mares with uterine cysts and a positive association between size of the cystic area and disturbed uterine hemodynamics. Reproduction (2008) 135 541–550 Introduction periglandular fibrosis (Kenney & Ganjam 1975, Ricketts 1975, Kenney 1978). Glandular cysts range from a few Uterine cysts have been described in diverse species of millimeters to 1 cm in diameter and are frequently found in animals, including horses, cattle, ewes, pigs, cats, dogs, pregnant mares. Lymphatic cysts start as small microscopic elephants, and humans (Dow 1959, 1962, Adams 1975, structures that enlarge from several millimeters to several Ricketts 1975, Al-Dahash & David 1977, Dallenbach- centimeters (Kenney & Ganjam 1975, Kenney 1978)and Hellweg 1987, Lipetz et al.1987, Agnew et al. 2004). In have reported mean diameters ranging from 2 to 48 mm mares, uterine cysts are fluid-filled structures commonly (Tannus & Thun 1995). Cysts are usually located at or near found in the three uterine layers or attached to the exterior the base of both horns (Bracher et al.1992, Eilts et al. 1995, surface (Ginther & Pierson 1984) of a normal or chronically Tannus & Thun 1995) in the ventral-most portion of the inflamed uterus (Kenney & Ganjam 1975). The cysts arise suspended uterus (Ginther & Pierson 1984). The reported from the endometrium (Kenney & Ganjam 1975, Ricketts incidence in horses ranges from 13 to 55% (Wilson 1985, 1975, Kenney 1978)ormyometrium(reviewedbyStanton Adams et al. 1987, Kaspar et al. 1987, Leidl et al. 1987, et al. 2004). Although the etiopathogenesis of uterine cysts Bracher et al. 1992, Tannus & Thun 1995). Uterine cysts is uncertain, it is likely that abnormal uterine blood flow appear to have clinical importance (Adams et al. 1987, can contribute to cyst formation as a result of inadequate Leidl et al.1987, Tannus & Thun 1995,reviewedby drainage due to poor venous return and angiosis of Stanton et al.2004, Yang & Cho 2007). arterioles (Schoon et al. 1999). Two additional origins for A higher frequency of uterine cysts in older mares uterine cysts have been suggested: (1) lymphatic cysts from (Adams et al. 1987, Leidl et al.1987, Bracher et al.1992) obstruction of lymphatic channels (Kenney & Ganjam and a progressive incidence of cysts as age advances 1975) or from a gravitational effect in the enlarged, (Tannus & Thun 1995) have been described. Increased age gravid, or post partum uterus, resulting in an impediment in mares has also been accompanied by increased severity to fluid drainage and ventral collection of lymph of endometrial fibrosis, increased uterine vascular dys- (reviewed by Stanton et al.2004)and(2)glandularcysts function, and reduced fertility (Doig et al.1981, Oikawa from endometrial glandular distension resulting from et al.1993, Nambo et al. 1995, Gru¨ninger et al. 1998, q 2008 Society for Reproduction and Fertility DOI: 10.1530/REP-07-0447 ISSN 1470–1626 (paper) 1741–7899 (online) Online version via www.reproduction-online.org Downloaded from Bioscientifica.com at 09/30/2021 05:13:00AM via free access 542 J C Ferreira and others Schoon et al. 1999). Considering the reports of a high uterine artery (Bollwein et al.1998) and its branches, incidence of cysts and degenerative changes in the uterine the mesometrial attachment and vessels located in the artery walls in older mares, there may be a relationship endometrium and myometrium can be evaluated for among the presence of uterine cysts, decreased uterine the study of uterine hemodynamics (Silva et al. 2005, vascular perfusion, and pregnancy loss. However, no study Silva & Ginther 2006). Doppler ultrasonography is a has been reported on the direct effect of age on vascular potential technique for the study of the pathogenesis and perfusion of the uterine layers in mares. effects of treatment or preventive approaches for uterine Uterine cysts are readily imaged by ultrasound, and cysts. However, no report was found in any species on the transrectal ultrasonography has been an important advance- use of color Doppler ultrasonography to investigate the ment in the study of uterine cysts, providing detailed relationships between uterine blood flow and uterine cysts. research and clinical information (Ginther & Pierson 1984). The purposes of the present study using B-mode and Ultrasonically, internal cysts are characterized by an color Doppler ultrasonography (Fig. 1) in mares were to anechoic area (fluid) with an irregular echoic wall involving study the incidence of internal and external uterine cysts uterine tissue or a prominent bulge in the uterine lumen. and the relationship with blood flow. Specific goals were Individual, compartmentalized, or multilobulated sacs, to (1) examine in detail the prevalence of uterine cysts in pedunculated or not, can be imaged. External cysts usually young and old mares and determine the number, size, project outward from the outer surface of the endometrium and longitudinal and cross-sectional uterine locations (Ginther & Pierson 1984, Ginther 1995a). In mares, uterine of individual cysts (Part 1); (2) test the hypothesis that cysts also have been studied by necropsy, histology, uterine regions with cysts have low uterine vascular transrectal palpation, hysteroscopy, and fiber-optic tech- perfusion and determine the effects of cysts on spectral niques (Kenney & Ganjam 1975, Wilson 1985, Kaspar et al. blood flow velocity in the vessels of the mesometrial 1987, Leidl et al. 1987). attachment (Part 2); (3) test the hypothesis that a larger Color and power Doppler ultrasonography is a non- uterine cystic area is associated with changes in uterine invasive pulse wave technique that has been used recently vascular perfusion and uterine hemodynamics of the for transrectal study of blood flow in the reproductive tract mesometrium than a smaller cystic area (Part 3); and of large domestic animals (Ginther 2007). In addition to the (4) test the hypothesis that older nulliparous mares Figure 1 Diagram of an equine cystic uterus divided into nine segments and three portions with representative ultrasonograms. The uterus is divided into three portions: extremities (dark pink), central segments (intermediate pink), and cornual-body junction (light pink). The black dots within the uterine diagram symbolize internal uterine cysts. A cystic uterine region and an adjacent uterine region without cysts are represented by black and blue dashed oval circles respectively, in the left horn. (A) Cross- sectional images in B-mode, (B) power flow Doppler of a noncystic region, and (C) power flow Doppler of a cystic region are shown. (D) The mesometrial attachment of each horn was identified in B-mode and (E) delineated for measurements of the mesometrial diameter, circumference, and area (F) and vascular perfusion. (B and C) Uterine and (F) mesome- trial vascular perfusion were estimated accor- ding to the number and intensity of color spots in the vessels of the tissue. (G) The sample gate was placed in a vessel of the mesometrium to generate the Doppler frequency spectral graph that represents the changing velocities over time and depicts the arterial pulses generated during cardiac cycles; the width of the gate (1.5 mm) is exaggerated in the drawing. Reproduction (2008) 135 541–550 www.reproduction-online.org Downloaded from Bioscientifica.com at 09/30/2021 05:13:00AM via free access Effect of cysts on uterine blood flow 543 without cysts have lower uterine vascular perfusion than middle and uterine body middle (LM, RM and BM) and younger mares and determine the effects of age on cornual-body junction left, right horn posterior and spectral blood flow velocity in the vessels of the uterine body anterior (LP, RP and BA). The number of mesometrial attachment (Part 4). cysts did not differ between the internal and external cysts in the extremities and central segments, and internal cysts were more (P!0.005) predominant than external cysts in Results the cornual-body junction. There were more (P!0.0001) ! Part 1: prevalence and distribution of uterine cysts cysts (total) comprising a larger area (P 0.0001) in the central segments and cornual-body junction than in The prevalence of ultrasonographically detected uterine the extremities.
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