Ultrasonographic Measurement of Stallion Accessory Sex Glands and Excurrent Ducts during Seminal Emission and Ejaculation'

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BOLOGY OF REPRODUCTON 49 267-273 (1993) Ultrasonographic Measurement of Stallion Accessory Sex Glands and Excurrent Ducts during Seminal Emission and Ejaculation' JAMES A WEBER and GORDON L WOODS 2

1 BOLOGY OF REPRODUCTON (1993) Ultrasonographic Measurement of Stallion Accessory Sex Glands and Excurrent Ducts during Seminal Emission and Ejaculation' JAMES A WEBER and GORDON L WOODS 2 Northwest Equine Reproduction Laboratory Department of Animal and Veterinary Science University of daho Moscow daho ABSTRACT Accessory sex gland and excurrent duct activity of 1 stallions was visualized with transrectal ultrasonography during seminal emission and ejaculation First and last penile urethral contractions were defined as the start ( sec) and end of ejaculation respectively Duration of ejaculation (n = 63 ejaculations) averaged sec Penile urethral contractions occurred an average of times per ejaculation Right bulbourethral glands (n = 19 ejaculations) alternated repeatedly from ovoid to flattened irregular shapes during ejaculation Cross-sectional area of right bulbourethral glands did not change (p > 4) between 3 sec before ejaculation and the end of ejaculation Cross-sectional area of right prostatic lobes (n = 17 ejaculations) decreased (p < 1) between 3 sec before ejaculation and the end of ejaculation with decreases (p < 5) at 2 1 and sec before ejaculation and at the time of the second penile urethral contraction Excurrent ducts of ampullae (n = 17 ejaculations) first appeared to dilate with fluid at sec before ejaculation and subsequently dilated an average of 34 ± 3 times between 3 sec before ejaculation and the end of ejaculation Fifty-three of 58 (93%) ampullar duct dilations occurred prior to the start of ejaculation During each dilation of ampullar ducts fluid remained visible for 23 ± 4 sec Fluid was detected within the lumina of vesicular gland excurrent ducts during the 6 of 17 monitored ejaculations that produced detectable gel First and last dilations of vesicular gland ducts began at and sec respectively and a total of 43 7 dilations occurred between 3 sec before ejaculation and the end of ejaculation During each dilation of vesicular gland ducts fluid remained visible for 73 ± 21 sec NTRODUCTON Transport of semen from the accessory sex glands and the ductus deferens to the tip of the penis has been separated into two distinct processes: secretion of seminal fluid and spermatozoa from the accessory sex glands and the ductus deferens into the lumen of the pelvic urethra (emission) and expulsion of accumulated fluid through the penile urethra (ejaculation) [1] The accessory sex glands of stallions are the bulbourethral glands the prostate gland the ampullae and the vesicular glands [2] Stallion semen is ejaculated in 5-1 physically and chemically distinct seminal fractions during an 8-1-sec period [3 4] These fractions are propelled through the urethra by strong rhythmic contractions of the bulbospongiosus and ischiocavernosus muscles [5] nitial contractions are shorter in duration and propel larger seminal volumes than later jets [3 4] Approximately 8% of the spermatozoa and ampullar secretions in an ejaculate are ejaculated in the first three seminal fractions [3] The vesicular glands secrete a viscous gel [6] that is ejaculated in the last few seminal fractions The volume of vesicular gland fluid varies widely among stallions and ejaculates [7] The timing and extent of fluid movement from the prostate gland and bulbourethral gland during seminal emission and ejaculation have not been reported Transrectal ultrasonography has been utilized in stallions to produce accurate detailed images of accessory sex Accepted March Received August 'daho Agricultural Station series no 93A2 2 Correspondence FAX: (28) glands during sexual rest [8] and to measure changes in accessory sex gland fluid content after sexual preparation and ejaculation [9] Ultrasonography was proposed as a method for characterizing seminal fluid movement during seminal emission in stallions because of the relatively large fluid volumes and long duration of stallion ejaculates and the capacity of ultrasonography to distinguish between fluid and soft tissue within accessory sex glands The objective of the present study was to describe the sequence of ultrasonographically detectable accessory sex gland activity in stallions during seminal emission and ejaculation Stallions MATERALS AND METHODS The 1 stallions used in this study weighed 2-5 kg and were 3-12 yr old Stallions were housed together in a pen that was visually isolated from mares During May and June of 1988 the accessory sex glands or excurrent ducts of each stallion were examined twice weekly with transrectal ultrasonography Stallions were isolated from mares between the twice-weekly ejaculation attempts Technique for Transrectal Ultrasonography The technique used to obtain ultrasonographic images of stallion accessory sex glands during ejaculation has been described and the success rates achieved through use of this technique during the present study have been reported [1] A well-lubricated 75-MHz linear array ultrasound transducer (Corometrics Medical Supply Wallingford CT) 267 on 19 July 218

268 WEBER AND WOODS Cranial TABLE 1 Timing (mean + SD) of penile urethral contractions during ejaculation Contraction no (no of ejaculates) 1 (63) 2 (63) 3 (63) 4 (61) 5 (51) 6 (37) 7 (25) 8 (15) 9

2 268 WEBER AND WOODS Cranial TABLE 1 Timing (mean + SD) of penile urethral contractions during ejaculation Contraction no (no of ejaculates) 1 (63) 2 (63) 3 (63) 4 (61) 5 (51) 6 (37) 7 (25) 8 (15) 9 (9) 1 (5) Time (sec) ± ± ± 21 f Caudal Left ( Gland ) Right FG 1 Orientations of ultrasound transducer (solid bars) used to obtain images of right bulbourethral glands right prostatic lobes and pelvic urethrae was placed against the ventral wall of the rectum prior to ejaculation and was oriented to produce ultrasonographic images of either 1) the midline of the right bulbourethral gland in longitudinal section 2) the greatest mediolateral extent of the right prostatic lobe or 3) the portion of the pelvic urethra containing the seminal colliculus and the excurrent ducts of the ampullae and vesicular glands in transverse section (four ejaculation attempts per orientation per stallion; Fig 1) Stallions ejaculated into a Missouri-type artificial vagina (NASCO Modesto CA) while the ultrasound operator maintained the initial transducer orientation Stallions ejaculated during 117 of 12 (98%) ejaculation attempts Acceptable recordings (ultrasonographic images of the selected pelvic structure that were visible throughout ejaculation) were produced during 63 of 117 (54%) ejaculations Nineteen of 38 (5%) recordings of the bulbourethral gland 27 of 4 (68%) recordings of the prostate gland and 17 of 39 (44%) recordings of the pelvic urethra were of acceptable quality and these were subsequently analyzed Ultrasonographic images were recorded onto the video track of a 3/4" videotape prior to and during each ejaculation while the occurrences of palpable muscular contractions on the ventrum of the penis (penile urethral contractions) were simultaneously reported by an observer onto ral the audio track of the same videotape Total and gel volumes of all ejaculates were measured The occurrence of the first penile urethral contraction was designated the start of ejaculation ( sec) and each ultrasonographic image was assigned a time based on the interval from the start of ejaculation The occurrence of the last penile urethral contraction was designated the end of ejaculation All videotapes were analyzed from 3 sec preceding the start of ejaculation until the detection of the last penile urethral contraction Cross-sectional areas of the right bulbourethral gland and right prostatic lobe were calculated by computerized image analysis of ultrasonographic images (Universal maging Corporation Media PA) and were measured at 3 sec before ejaculation 2 sec before ejaculation 1 sec before ejaculation and coincident with each penile contraction Cross-sectional areas of the excurrent ducts of the left and right ampullae and vesicular glands were calculated as height (dorsoventral diameter) multiplied by width (mediolateral diameter) and were measured at 1/3-sec intervals from 3 sec preceding ejaculation until the occurrence of the last penile urethral contraction Statistical Analysis Data are expressed as mean + standard deviation The effect of time on prostatic lobe and bulbourethral gland cross-sectional area during ejaculation was determined by analysis of variance and the Student-Neuman-Keuls Multiple Comparison Test (SAS nstitute Cary NC) A p value less than 5 was considered significant RESULTS The total ejaculate volume (n = 63) averaged ml Twenty-three ejaculates contained detectable gel ( ml gel-free volume and ml gel volume) and 4 ejaculates did not contain detectable gel ( ml gel-free volume) Total ejaculate volume was significantly higher (p < 5) in ejaculates that contained gel than in gel-free ejaculates No significant differences were detected between ejaculates with and without gel in duration of ejaculation number of penile urethral contractions on 19 July 218

ACCESSORY SEX GLAND ACTVTY N EJACULATNG STALLONS 269 FG 2 Ultrasonographic appearance of a right bulbourethral gland (A) prior to a glandular contraction (B) during a glandular contraction and (C)

3 ACCESSORY SEX GLAND ACTVTY N EJACULATNG STALLONS 269 FG 2 Ultrasonographic appearance of a right bulbourethral gland (A) prior to a glandular contraction (B) during a glandular contraction and (C) mmediately after a glandular contraction Arrows outline the ventral border of the gland a C * O 3 a E ) _ Co o O A 1U (19) 119) * 16) 1 a (1) rwj ql ~l Eql~l & ~ J[ '"' '"- (17) 1 Start of ejaculation '1[- '1r' ql ' 1 2 S 4 P -_4 l (12) (9) (i4) 1 Ti'~~(1! N ' ! FG 3 Cross-sectional area (mean + SD) of right bulbourethral glands during emission and ejaculation Numbers in parentheses are the number of ejaculations that contributed to each mean on 19 July 218

27 WEBER AND WOODS FG 4 Ultrasonographic appearance of the right lobe of a prostate gland (A) prior to (B) during and (C) after ejaculation Arrows outline the ventral border of the prostatic lobe E c

4 27 WEBER AND WOODS FG 4 Ultrasonographic appearance of the right lobe of a prostate gland (A) prior to (B) during and (C) after ejaculation Arrows outline the ventral border of the prostatic lobe E c C * _ Ċ c o A (: a l b b : (26) (26) T c c ) - am (26) 2(1)) (8) () (4) % o 2- Stuart of6 ejaculation V V 11 i FG 5 Cross-sectional area (mean - SD) of right prostatic lobes during emission and ejaculation Means without a common superscript letter are significantly different (p < 5) Numbers in parentheses are the number of ejaculations that contributed to each mean on 19 July 218

ACCESSORY SEX GLAND ACTVTY N EJACULATNG STALLONS 271 FG 6 Ultrasonographic appearance of a pelvic urethra in transverse section (A) prior to dilation of ampullar or vesicular gland excurrent ducts

5 ACCESSORY SEX GLAND ACTVTY N EJACULATNG STALLONS 271 FG 6 Ultrasonographic appearance of a pelvic urethra in transverse section (A) prior to dilation of ampullar or vesicular gland excurrent ducts (B) during dilation of ampullar excurrent ducts (arrows) and (C) during dilation of vesicular gland excurrent ducts (arrows) per ejaculation or total number of sperm per ejaculate Sperm concentration averaged x 1 9 cells/ejaculate (range 81 x 18 to 147 x 1' cells/ejaculate) The average number of penile urethral contractions during ejaculation was 62 ± 22 (range 3-1 contractions; Table 1) Duration of ejaculation averaged sec Bulbourethral Glands Ultrasonographic images of the right bulbourethral gland were ovoid in cross section prior to ejaculation; they repeatedly alternated from an ovoid to a flattened irregular shape several times during ejaculation (Fig 2) The excurrent ducts of the right bulbourethral gland were not visible in ultrasonographic images The cross-sectional area of the right bulbourethral gland did not change (p > 1) be- TABLE 2 Starting time and duration (sec) of ampullar and vesicular gland excurrent duct dilations (mean - SD) during emission and ejaculation Times are referenced to the first penile urethral contractions ( sec) Dilation number Excurrent duct dilations (no of ejaculates) Start Duration Ampulla: 1 (17) (15) (12) (9) (5) Vesicular gland 1 (6) (5) (5) (5) (5) tween 3 sec before ejaculation and the end of ejaculation (Fig 3) Prostate Gland Elongated fluid-filled regions were visualized within the right prostatic lobe prior to ejaculation (Fig 4A) The width of these regions appeared to decrease during ejaculation (Fig 4 B and C) The cross-sectional area of the prostatic lobe decreased (p < 1) between 3 sec before ejaculation and the end of ejaculation with decreases (p < 5) at 2 1 and sec preceding ejaculation and at the time of the second penile urethral contraction (Fig 5) Pelvic Urethra Ultrasonographic images of ampullar and vesicular gland excurrent ducts were detectable during short distinct periods when their lumina were distended with glandular secretions (Fig 6 A-C) Ampullar excurrent ducts (n = 17 ejaculations) first dilated with fluid (Fig 6B) at sec before ejaculation (Table 2 Fig 7) and dilated an average of times between 3 sec before ejaculation and the end of ejaculation Fifty-three of 58 (93%) ampullar duct dilations occurred prior to the start of ejaculation During individual dilations ampullar excurrent ducts were visible for an average of sec each Fluid was detected within the lumina of the vesicular gland excurrent ducts during the six ejaculations that produced gel; fluid was not detected during the eleven ejaculations that did not produce gel First and last dilations of vesicular gland ducts began at and sec respectively (Table 2 Fig 8) and an average of dilations (range = 1-5) occurred between 3 sec before ejaculation and the on 19 July 218

6 272 WEBER AND WOODS 6 4 S S E 5 L E 4 ō Start of ejaculation --- -Ampulla Vesicular Gland C L o x w 2 1' i FG 7 Cross-sectional area of ampullar and vesicular gland excurrent ducts during one ejaculation that produced 85 ml gel-free volume 41 ml gel volume and 57 x 19 spermatozoa 1 C aa O r e oa x w C i A Prostate Gland Bulbourethral : Gland : *-*_i_i-? ---?-- Start of ejaculation Ampullsa u lb :! ) Vesicular Gland: q FG 8 Ultrasonographically detectable changes in stallion accessory sex glands during seminal emission and ejaculation Ampullar excurrent ducts dilated (black bars) and prostatic area decreased prior to the onset of ejaculation (first penile urethral contraction) Prostatic area continued to decrease during the initial penile urethral contractions Vesicular gland excurrent ducts dilated (black bars) after cessation of ampullar and prostatic activity Decreases in bulbourethral gland area were not detected end of ejaculation (Fig 6C) During individual dilations vesicular gland excurrent ducts were visible for an average of 73 ± 21 sec each Changes in the cross-sectional area of ampulla and vesicular gland excurrent ducts during a representative ejaculation are depicted in Figure 7 DSCUSSON The study reported here demonstrates that transrectal ultrasonography can be used to detect accessory sex gland activity during emission and ejaculation in stallions Because changes in glandular fluid content were not directly measured these results estimated the timing rather than the volume of each gland's contribution to the ejaculate Because it is likely that changes in glandular or excurrent duct area occurred coincident with glandular fluid flow the following pattern of glandular fluid release is proposed Ampullar and prostatic activity appeared to begin prior to the start of ejaculation with ampullar fluid passing through the excurrent ducts in distinct boluses During most ejaculations fluid movement from the ampulla to the pelvic urethra appeared to end before the start of ejaculation while fluid movement from the prostate gland to the pelvic urethra apparently continued during the initial penile urethral contractions Fluid passed through vesicular gland excurrent ducts only during ejaculations that produced measur- on 19 July 218

ACCESSORY SEX GLAND ACTVTY N EJACULATNG STALLONS 273 able gel During these ejaculations vesicular gland secretions were apparently released in several distinct boluses after cessation of prostatic

7 ACCESSORY SEX GLAND ACTVTY N EJACULATNG STALLONS 273 able gel During these ejaculations vesicular gland secretions were apparently released in several distinct boluses after cessation of prostatic activity A significant change in bulbourethral gland area was not detected although the bulbourethral glands changed shape rhythmically throughout ejaculation This suggests that the bulbourethral glands do not release fluid during emission or ejaculation The pattern of seminal emission described here is consistent with the sequence in which accessory sex gland secretions appear in stallion ejaculates [ ] with the highest spermatozoa concentration in the first seminal fraction and decreasing concentrations in successive fractions The detection of successively lower sperm concentrations in seminal fractions over time may be explained by rapid deposition of sperm into the urethra prior to ejaculation followed by continuous dilution of sperm by prostatic secretions and incomplete removal of urethral contents during each urethral contraction The appearance of vesicular gland secretions and low sperm concentrations during the last half of ejaculation is consistent with emission of vesicular gland fluid after removal of ampullar and prostatic secretions This is the first report to describe accessory sex gland and excurrent duct activity during emission and ejaculation in any mammalian species While this study describes the pattern of seminal emission in a small group of apparently normal stallions further work is needed to determine factors that initiate emission ncreased understanding of emission in normal stallions could potentially lead to improved diagnosis and treatment of pathological conditions that interfere with emission and ejaculation in abnormal stallions The model proposed for emission and ejaculation in stallions if interpreted cautiously may also provide insight into the pattern of emission in males of other species including humans ACKNOWLEDGMENTS This work was funded by Diane Kem Donald Jacldin Ty Scheumann Patricia Hewitt AL and Pat Hallowell and the daho Equine Education Bill The authors thank the Advisory Board of the Northwest Equine Reproduction Laboratory for their support and Rick Geary William Fullmer Jed McKinlay and David Silcock for technical assistance REFERENCES 1 Benson GS Male sexual function: erection emission and ejaculation n: Knobil E Neill JD (eds) The Physiology of Reproduction New York: Raven Press Ltd; 1988: Schummer A Nickel R Sack WO Urogenital System-Male Equine Genitalia n: The Viscera of the Domestic Mammals 2nd ed New York: Springer-Verlag; 1979: Tischner M Kosiniak K Bielanski W Analysis of the pattern of ejaculation in stallions J Reprod Fertil 1974; 41: Kosiniak K Characteristics of the successive jets of ejaculated semen of stallions J Reprod Fertil Suppl 1975; 23: Little TV Holyoak GR Reproductive anatomy and physiology of the stallion n: Turner AS Blanchard TL Varner DD (eds) The Veterinary Clinics of North America; Equine Practice-Stallion Management Philadelphia: WB Saunders Co; 1992: Pickett BW Voss JL The influence of season on seminal characteristics sexual behavior and testosterone levels in the stallion Thoroughbred Rec 1974; 2: Mann T Leone E Polge C The composition of the stallion's semen Endocrinology 1956; 13: Little TV Woods GL Ultrasonography of accessory sex glands in the stallion J Reprod Fertil Suppl 1987; 35: WeberJA Geary RT Woods GL Changes in accessory sex glands of stallions after sexual preparation and ejaculation J Am Vet Med Assoc 199; 196: Weber JA Woods GL A technique for transrectal ultrasonography of stallion accessory sex glands during ejaculation Theriogenology 1991; 36: Mann T Biochemistry of stallion semen J Reprod Fertil Suppl 1975; 23: Mann T Biochemistry of semen and secretions of male accessory organs n: Cole HH Cupps PT (eds) Reproduction in Domestic Animals vol 2 New York: Academic Press; 1959: 51-7 on 19 July 218

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