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European UrologyVolume 62, issue 5, pages e83-e94, November 2012
Occlusion of Seminal Vesicles Increases Sexual Activity in a Mouse Model
Accepted 10 April 2012, Published online 19 April 2012, pages 855 - 862
Little is known about the physiologic role of seminal vesicles beyond their fertility function. It has been suggested repeatedly that seminal vesicles have an impact on sexual activity. Although this has been investigated in various animal models, such a role has never been found.
To assess in a novel mouse model whether occlusion of seminal vesicles affects sexual activity.
Design, setting, and participants
Adult male CD1 mice (n = 77) were assigned randomly to the experimental groups: (1) seminal vesicle occlusion (SVO) (n = 24), (2) seminal vesicle resection (SVR) (n = 23), and (3) sham operation (SO) (n = 30). Adult females were brought into estrus by the Whitten effect. After recuperation, mouse pairs were observed during sessions of 3 h each. Sexual activity was analyzed separately by three observers blinded to the experimental conditions.
SVO, SVR, and SO.
Outcome measurements and statistical analysis
The primary end point was percentage of sessions with intromission; secondary end points were number of intromissions and latency until first intromission. A logistic regression model and the Kruskal-Wallis test were used.
Results and limitations
A total of 141 sessions for a total of 423 h were analyzed. Intromission was scored in 20 of 42 sessions (48%) with SVO mice, a significantly higher rate than the 8 of 39 sessions (21%) with SVR mice (p = 0.001) and 18 of 60 sessions (30%) with SO mice (p = 0.004). Secondary end points were comparable in all three groups (p = 0.303 and 0.450, respectively).
Males with SVO were significantly more often sexually active than males undergoing SVR or SO. This suggests that occluded, and thus engorged, seminal vesicles increase sex drive in male mice. Since the potential clinical benefit might be highly relevant, further studies should confirm these promising results and investigate the potential application in men.
Seminal vesicles were first described in 1561 by the Italian anatomist Gabriel Fallopius. In the late 19th. century, they became the focus of considerable interest because of their involvement in inflammatory diseases such as tuberculosis and gonorrhea . At that time, however, their physiologic role was still not entirely understood.
In one of the earliest observations, the physiologist Ivan R. Tarchanoff noticed in 1887 that the seminal vesicles of frogs were enlarged during mating season. He observed that their removal halted the coitus of mating frogs. Tarchanoff concluded that in frogs, and possibly, therefore, in mammals, the seminal vesicles were the starting point of sexual activity . In 1924, Floyd H. Allport, the father of experimental social psychology, made a similar postulation for humans: “The original stimulus for sex responses … in the male is the gradual distention of the seminal vesicles, a condition requiring a fairly periodic discharge of their contents”. Later in the 20th century, an increasing number of experiments were performed, which, despite occasional trends, were not able to prove an influence of internal genital organs on sexual activity and sex drive (Table 1) , , , , , , and .
|Pauker ||Beach and Wilson ||Lawson and Sorensen ||Larsson and Swedin ||Tisell and Larsson ||Chow et al. |
|Animal model||Golden hamster (Cricetus auratus)||Rat (Long-Evans)||Albino rat (Holtzman)||Rat (Wistar)||Rat (Wistar)||Golden hamster (Mesocricetus auratus)|
|Age of animals||11 wk||Adult||Not specified||5 mo||5 mo||8–10 wk|
|Male/female sexual experience||Not specified||Sexually experienced||Sexually experienced||High level of sexual activity||High level of sexual activity||Sexually experienced|
|Female priming||Hormonal injection (estradiol plus progesterone)||Hormonal injection (estradiol plus progesterone)||Not specified||Hormonal injection (estradiol plus progesterone)||Hormonal injection (estradiol plus progesterone)||Females considered as receptive by observation|
|Day/night cycle, illumination||Not specified||Not specified||Not specified||Reversed day/night cycle, observation in dark phase||Not specified||Red-light illumination; observation in dark phase|
|Recuperation time after surgery||3 d and 7 d, respectively||1 mo||28 d||Not specified||3–4 wk||3 wk|
|Time to male adaptation in apparatus||5 min||Not specified||Not specified||Not specified||5 min||None (home cage of male)|
|Observation duration||10–20 min||≥30 min||12 d (two estrus cycles)||Until ejaculation||≥30 min||15 min|
|Experimental groups||1. Resection of seminal vesicles and prostate (n = 6)
2. Castration 39 d after (n = 6, same males)
Comparison with castrated males (n = 4) used in a previous investigation
|Resection of seminal vesicles (n = 10)||Experiment 1 (n = 8)
1. Resection coagulating glands
2. Nonoperated males
Experiment 2 (n = 6)
Resection of coagulating glands
|Resection of coagulating glands
1. Only (n = 6)
2. Plus preganglion hypogastric denervation (n = 4)
3. Plus preganglion hypogastric denervation (n = 5) plus postganglion hypogastric denervation
4. Plus resection seminal vesicles (n = 4) plus resection ventral prostate lobe plus preganglion hypogastric denervation
|1. Resection seminal vesicles (n = 9) plus ventral/dorsolateral prostate plus coagulating glands
2. Sham operation (n = 9)
|1. Resection of ampullary glands (n = 7)
2. Resection of coagulating glands (n = 6)
3. Resection of dorsolateral prostate (n = 6)
4. Resection of seminal vesicles (n = 7)
5. Resection of ventral prostate (n = 8)
6. Resection of accessory sex glands (n = 7)
7. Sham operation (n = 7)
8. Nonoperated males (n = 6)
|Study design||Observations before and after resection of seminal vesicles and prostate, and after castration||Pre- and postoperative observations||Exp 1: Postoperative observations
Exp. 2: Pre- and postoperative observations
|Pre- and postoperative observations||Postoperative observations||Postoperative observations|
|End points||1. Mounting
2. Rear mounting
4. Latency time until first intromission
|1. Latency time until first mounting
2. Latency time until first intromission
3. Mounting/intromission series before ejaculation
4. Postejaculatory interval
|1. Litter size
2. Libido and mating activity
3. Evaluation of regeneration of coagulating glands
3. Latency time until first intromission
4. Latency time until first ejaculation
5. Postejaculatory interval
|1. Latency time until first mounting
2. Latency time until first intromission
3. Latency time until first ejaculation
4. Postejaculatory interval
5. Number of mountings
6. Number of intromissions
|1. Latency time until first intromission
2. Latency time until first ejaculation
3. Number of intromissions
4. Postejaculatory interval
5. Duration of ejaculations
6. Number of ejaculations
|Results||No difference between pre- and postoperative copulatory frequency and latency time||Unchanged postoperative copulatory frequency and latency time but fewer intromissions until ejaculation||Unchanged litter size, libido, and mating activity in operated and nonoperated males. No regeneration of coagulating glands||No difference of copulatory frequency and latency time between all four groups except for postoperative increase of mount frequency||No difference of copulatory frequency and latency time between experimental and sham-operated males||No difference in copulatory frequency and latency time between experimental and sham-operated males|
|Conclusion||Resection of accessory sex glands did not change sexual activity||Resection of seminal vesicles did not change sexual activity||Resection of coagulating glands did not change sexual activity or inhibit reproductive capacity||Resection of all accessory sex glands plus hypogastric nerve did not change sexual activity||Resection of seminal vesicles, prostate, and coagulating glands did not change sexual activity||Resection of any accessory sex glands did not change sexual activity|
* Modified from Schumacher .
Little also is known about the physiologic influence of seminal vesicles in humans beyond their fertility function. Driven by a persistent lack of evidence that distended seminal vesicles may increase sex drive, we sought to take a fresh approach to the issue by combining the experience of various previous experiments in the design of one novel animal model .
2. Materials and methods
Naive Crl:CD1(ICR) 10-wk-old male and female mice were purchased from Charles River Laboratories (L’Arbresle, France). The animals were housed in individually ventilated cages: males in groups of four in Makrolon II cages (23 × 17 × 14 cm) (Bayer MaterialScience LLC, Sheffield, MA, USA) and females in groups of eight in Makrolon III cages (39 × 23 × 15 cm). The day/night cycle was maintained with lights on at 06:00 and off at 18:00. The cages were equipped with sawdust, transparent red plastic nest boxes, and pieces of wood and paper. Food and water were available ad libitum. After arrival, the animals were allowed to acclimatize for at least 5 d. Male mice were randomly assigned to one of three experimental groups: (1) bilateral seminal vesicle occlusion (SVO), (2) bilateral seminal vesicle resection (SVR), and (3) sham operation (SO). The study was approved by the animal ethics committee of the canton of Bern, Switzerland.
2.1. Anesthesia and analgesia
For surgery, mice were anesthetized with a subcutaneous injection of fentanyl 0.05 mg/kg body weight (Fentanyl; University of Bern, Switzerland), medetomidine 0.5 mg/kg (Dorbene; E. Gräub AG, Bern, Switzerland), and climazolanum 5 mg/kg (Climasol; E. Gräub AG, Bern, Switzerland). Anesthesia was finished by subcutaneously injecting a mixture of atipamezole 1.25 mg/kg (Alzane; E. Gräub AG, Bern, Switzerland), sarmazelinum 0.5 mg/kg (Sarmasol; E. Gräub AG, Bern, Switzerland), and buprenorphine 0.075 mg/kg (Temgesic; University of Bern, Switzerland). Analgesia with buprenorphine was administrated subcutaneously on postoperative days 1 and 2.
Surgery was performed under sterile conditions using a binocular microscope (Carl Zeiss AG, Feldbach, Switzerland). In the SVO group, the seminal vesicle outlets were occluded by titanium clips (Fig. 1A–1C); in the SVR group, both seminal vesicles were resected (Fig. 1D–1F); and in the SO group, both seminal vesicles were simply exposed (Fig. 1G–1I).
2.3. Whitten effect
At 10–14 d after male surgery, the cages of males and females were placed close to each other, allowing females to be exposed to male-originating pheromones for 3 d. Known as the Whitten effect, it induces and synchronizes estrus in females .
2.4. Evaluation of sexual activity
Tests of sexual activity were conducted during the dark phase of the nonreversed day/night cycle and begun at least 1 h after lights off. The floor of the rectangular glass apparatus (60 × 40 × 36 cm) housing the mice was covered with cardboard and sawdust. A clay bowl (10.5 × 5 × 3 cm) contained food and water ad libitum. The apparatus was placed in a box made of double-fluted corrugated cardboard (77 × 56.5 × 57 cm, 0.7-cm thick) allowing complete darkness and reduced noise. An infrared camera (1/4 Sharp CCD 450TVL; Sharp Electronics Corp., Osaka, Japan) was fixed 55 cm above the floor of the apparatus (Fig. 2). Twelve identical settings were used. Before each session, the apparatus was cleaned thoroughly and completely reinstalled. Males were allowed to adapt to the environment for 15 min before a female was introduced into the apparatus.
The experiment was conducted in two rounds of identical design, except for the number of sessions per mouse. In the first round, each naive male was observed with a naive female during a single session of 3 h. In the second round, each male was observed during three sessions of 3 h each on three consecutive days (Fig. 3). At the first session, the males were naive, at the second and third session they were considered non-naive. Naive females were used in the first session, and either naive or non-naive females in the second and third sessions. A female was considered non-naive when used for another session earlier the same day. After termination of the experiment, all mice were euthanized with carbon dioxide and a regional necropsy was performed to assess the status of seminal vesicles.
2.5. Copulatory behavior
The mouse copulatory behavior pattern consists of three basic steps: mounting, intromission, and ejaculation. Mounting is the action in which the male puts his forepaws on the back of the female and makes rapid, shallow pelvic movements without vaginal penetration. Intromission occurs when the male gains a successful vaginal penetration and slows down pelvic motions. Ejaculation is intromission with sperm transfer , , and .
2.6. Data acquisition
Evaluation of the recorded male sexual activity was done independently by three equally trained observers who were blinded to the type of surgery performed on each of the male mice.
2.7. Statistical analysis
The primary end point was the percentage of sessions with intromission. Secondary end points were the number of intromissions and the latency time from introduction of a female to first intromission per session.
To account for differences in male and female experience (naive or not) and order of the sessions, a logistic regression model containing both fixed and random effects was used for analysis of the primary end point . The specific identification (ID) number of each mouse was used as a clustering variable (random effect) to account for the possible correlation of sessions within the same mouse. The SVR and SO groups were each compared with the SVO group; the second and third sessions were each compared with the first session. A treatment by session-rank interaction was tested, as was female experience (naive or not). Male experience was not tested because it was directly related to session rank. For the analysis of secondary end points, the nonparametric Kruskal-Wallis test was used to compare average number of intromissions per mouse and average latency time to first intromission per mouse for mice with at least one intromission . The p values <0.05 were considered statistically significant. For the statistical analyses, Stata v.12.0 (StataCorp, College Station, TX, USA) was used.
Seventy-seven males completed 141 sessions for a total observation time of 423 h. Due to higher perioperative mortality, the number of mice in the SVO (n = 24) and SVR (n = 23) groups were smaller than in the SO group (n = 30) (Table 2). Naive males were used in 77 sessions (55%) and non-naive males in 64 sessions (45%). Naive females were used in 97 sessions (69%), non-naive females in 44 (31%).
|Total duration of sessions, h||126||117||180||423|
|Median mouse weight at surgery, g (range)||39 (34–46)||39 (35–48)||39 (35–46)||39 (34–48)|
|Primary end point|
|Sessions with observed intromission, no. (%)||20 (48)||8 (21)||18 (30)||46 (33)|
|Secondary end points|
|Median intromissions per session, no. (range)||15 (1–96)||11 (4–115)||29 (1–290)||20 (1–290)|
|Median latency time until first intromission per session, min (range)||26 (3–172)||28 (13–112)||14 (5–142)||24 (3–172)|
A logistic regression model sequentially showed that treatment by session-rank interaction, female experience, and the constant term were not statistically significant. These parameters were dropped from the model at each step. The SVO males had 20 of 42 sessions (48%) with intromission, which was significantly higher than both the 8 of 39 (21%) achieved by SVR males (p = 0.001) and the 18 of 60 (30%) achieved by SO males (p = 0.004) (Fig. 5). In the second round, with three consecutive sessions for each male, the percentage of sessions with intromission was lower in the first sessions than in the second (p = 0.038), but there was no statistically significant difference between the first and third sessions (p = 0.813). This model, with resection group and session order, was statistically significant compared with a null model with only a constant term (p = 0.0017). It also showed that the difference between this model and an ordinary logistic regression model, which did not take into account the clustering (mouse ID) as a random effect, was not significant (p = 0.2379); that is, it did not provide a better fit than an ordinary logistic regression model.
The two secondary end points (number of intromissions and the latency time until the first intromission per session) did not differ statistically among the three groups (p = 0.303 and 0.450, respectively) (Table 2).
Regional necropsies confirmed enlarged seminal vesicles (2.5- to 3.0-cm long) in all SVO, absent seminal vesicles in all SVR, and normal-sized seminal vesicles (1.5-cm long) in all SO mice (Fig. 4).
Over decades, many vain attempts have been made to elucidate the influence of various genital organs on sexual activity in animal models. We think our present mouse experiment finally reveals a novel aspect of the physiologic understanding of the seminal vesicles. Showing that males with occluded, and thus engorged, seminal vesicles were significantly more often sexually active than males with SVR or who underwent SO suggests that seminal vesicles affect sex drive.
Unlike previous animal experiments on the role of seminal vesicles on sexual activity, ours uses a mouse model, which is now recognized, together with the rat and some other small animal models, as one of the most important mammalian models for the study of male and female sexual function , , , and . We attribute our ability, in contrast to others (Table 1), to show significant differences in sexual activity depending on seminal vesicle status to three major factors. First, the experimental design was based on maintaining a natural environment and keeping animal stress as low as possible by, for example, preserving the natural day/night cycle, use of noise-reducing boxes, and allowing sufficient time for males to habituate to the apparatus. We also applied the Whitten effect, which allows for natural and reliable female priming by male pheromones with up to 80% females reaching estrus . In mice, unlike in rats, the Whitten effect is possibly even more effective than hormone priming  and . Second, to optimize assessment of natural mouse sexual activity, each observation was extended to 3 h, since short observation times (eg, 15 min) often do not capture later components of sexual activity, such as intromission and ejaculation, and therefore might underestimate sexual activity . Third, the study design focused on a single genital organ, namely seminal vesicles.
The persistent lack of standardized tests for assessing sexual activity in animals (ie, mice) has led to heterogeneous experimental designs and inconclusive results  and . The number of intromissions and latency times until first intromission were often used as end points; however, the number of intromissions is considered to be mainly an indicator of sexual endurance . Moreover, intromission ending in ejaculation usually terminates male sexual interest and thus sexual activity for several hours. This affects reliability . The latency time until first intromission is influenced by the receptiveness of the female and so may inaccurately reflect male sexual activity  and . Therefore, we chose to assess male sexual activity by distinguishing between sessions with and without intromission.
Sexual experience and natural variance within the same male can also influence sexual activity  and . The female is also a relevant confounding factor when assessing male sexual activity  and . To render the outcome of the experiment as independent of sexual experience as possible, both naive and non-naive males and females were used. By adding these data into a logistic regression model, sexual experience was excluded as a confounding factor for both males and females.
In our experiment, males with SVO had the highest sexual activity, with intromission occurring in 48% of sessions. Their sexual activity was significantly higher compared with that of SVR and SO males, with intromission in those mice occurring in 21% and 30% of sessions, respectively. The secondary end points did not differ statistically among the three experimental groups. We hypothesize, therefore, that occluded, and thus engorged, seminal vesicles act as an intrinsic stimulus for sexual activity, eventually resulting in greater sexual activity. Possibly reflecting a general physiologic preparedness of enough seminal fluid for a successful sperm transfer, the intrinsic stimulus is consequently highest in males with SVO and absent in males with SVR. The mechanism by which sexual activity is influenced when occluding the seminal vesicles’ outlet is unknown and was not the subject of this experiment. The identification of a possible mechanism, such as neural or humoral substrates, must be a subject of future experiments.
The results achieved in the present mouse model cannot necessarily be translated to other mouse strains, or other species, including humans, although some of them have numerous common components of sexual behavior that may reflect similar physiologic actions  and . That male sexual activity is also influenced to varying degrees by factors other than SVO (eg, by extrinsic stimuli emitted by the female) is best reflected by the fact that seminal vesicles are not present in all mammals. They are absent in marsupials, monotremes, and carnivores, and they are smaller in some insectivores, rodents, lagomorphs, bats, and primates , , and .
The extent to which the seminal vesicles play a role in sexual activity in humans is unknown. However, subjective observations in clinical practice suggest that men who have undergone seminal vesicle-sparing radical cystoprostatectomy tend to report a higher sex drive than men who have undergone radical cystoprostatovesiculectomy (ie, after seminal vesicle removal). Knowing from our mouse experiment that seminal vesicle sparing may positively influence sex drive should be an additional incentive to question the need for standard seminal vesicle removal during cystoprostatectomy, especially because several trials have shown seminal vesicle sparing to be oncologically safe in selected patients  and .
A potential limitation of our experiment is its design involving two different rounds, which was necessary because of limited housing and testing capabilities. The differences between the two rounds were taken into account in the logistic regression model. The criticism can also be made that after the Whitten effect, selection of females was not based on a positively detected fertility status. We think, however, that the inclusion of all females is also a strength of the experiment, as any selection by means of seemingly obvious criteria inherently bears the risk of a selection bias. Instead, we accounted for the female factor in the logistic regression model and eventually ruled it out as a confounding factor. Finally, our method for assessing sexual activity as such had not been previously standardized. We think, however, that our method straightforwardly reflects sexual activity by scoring each session as being with or without intromission, leading to even more conservative results compared with counting the absolute numbers of intromissions and the latency times until first intromission, which are more susceptible to biasing factors.
Male mice with SVO were significantly more often sexually active than males undergoing SVR or SO. These findings suggest that occluded, and thus engorged, seminal vesicles have a significant effect on sex drive in mice. The applications of these results in men, especially the potential benefits of seminal vesicle-sparing techniques in uro-oncologic surgery, warrant further investigation.
Author contributions: Urs E. Studer had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Studer, Birkhäuser.
Acquisition of data: Birkhäuser, Schumacher, Seiler, de Meuron, Wetterwald, Cecchini.
Analysis and interpretation of data: Birkhäuser, Studer, Schumacher, Seiler, de Meuron.
Drafting of the manuscript: Birkhäuser, Schumacher.
Critical revision of the manuscript for important intellectual content: Studer, Roth, Zehnder, Thalmann.
Statistical analysis: None.
Obtaining funding: Birkhäuser.
Administrative, technical, or material support: Zehnder, Thalmann, Roth.
Other (specify): None.
Financial disclosures: Urs E. Studer certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.
Funding/Support and role of the sponsor: Max und Hedwig Niedermaier foundation, Zurich, Switzerland, was involved in the design and conduct of this study.
Acknowledgment statement: The authors are grateful to Richard J. Sylvester, ScD, Department of Biostatistics, European Organisation for Research and Treatment of Cancer (EORTC), Brussels, Belgium, who performed all of the statistical analyses. They also thank Ursula Gerber for her excellent technical help and Hans Peter Käsermann, PhD, Institute of Laboratory Animal Science, University of Zurich, Switzerland, for his valuable advice.
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a Department of Urology, University of Bern, Switzerland
b Department of Clinical Research, University of Bern, Switzerland
© 2012 European Association of Urology, Published by Elsevier B.V.
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