Response of the Internal Reproductive Organs to Clitoral Stimulation: the Clitorouterine Reflex

Home , Cervical canal, Cervix, Endometrium, Uterus

Response of the internal reproductive organs to clitoral stimulation: The clitorouterine reflex

A Shafik1*, O El-Sibai2, R Mostafa3, AA Shafik1 and I Ahmed1

1Department of Surgery and Experimental Research, Faculty of Medicine, Cairo University, Cairo, Egypt; 2Department of Surgery, Faculty of Medicine, Menoufia University, Shebin-el-Kom, Egypt; and 3Department of Physiology, Faculty of Medicine, Zagazig University, Benha, Egypt

We investigated hypothesis that uterine erection, elevation and enlargement during sexual response are reflex and result from penis buffeting the glans clitoris (GC). In 23 healthy women, two recording electrodes were applied to the uterine mucosa and one to cervix uteri (CU). GC was stimulated electrically and mechanically by pencil electrode. The uterine and CU pressures were measured. Tests were repeated after anesthetization of the uterus or GC. Uterine electrodes recorded slow waves, followed by random bursts of action potentials (APs). No waves registered from CU. Electrical or mechanical GC stimulation eliminated uterine electric waves, but anesthetized GC did not, nor did GC stimulation while the uterus anesthetized. Uterine pressure declined on electrical or mechanical stimulation. Results suggest presence of reproducible reflex relationship between GC and the uterus, we call ‘clitorouterine reflex’. GC buffeting seems to evoke reflex and initiate uterine responses. Reflex may prove of diagnostic significance in sexual disorders. International Journal of Impotence Research (2005) 17, 121–126. doi:10.1038/sj.ijir.3901278 Published online 28 October 2004

Keywords: cervix uteri; uterus; clitoris; slow waves; action potentials; sexual disorders

Introduction elongation of the vagina. The uterus rises in the pelvis from its anteverted and anteflexed position and the cervix moves away from the posterior The reactions of the female reproductive organs vaginal wall. The uterus enlarges by as much as during the sexual response cycle have been studied 1–6 50%. The cause of uterine erection and elevation by many investigators. Sexual stimulation causes is not exactly known;2 some theories have tried changes in the external and internal reproductive 2,3,7,8 to explain these changes during sexual stimula- organs of the woman. The labia majora straddle tion proposing that they could be due to vasocon- apart exposing the vaginal introitus. With continued gestion in the true pelvis or to neuronally produced excitation, the labia majora and minora become contraction of the smooth musculature in the thickened due to venous congestion. Glans clitoris ligaments that support the uterus.2 (GC) also swells and increases in both length and We hypothesized that the uterine changes hap- thickness. These changes in the external reproduc- pening during sexual stimulation are reflex in tive organs are suggested to be either brought about 2,9–12 nature and occur as a result of penile buffeting of reflexly or to represent a psychogenic response. the GC. This hypothesis was investigated in the Likewise, the internal reproductive organs of the current communication. woman undergo changes during the sexual response cycle.2–4 These changes comprise vaginal transduc- tion of a mucoid fluid as well as expansion and Materials and methods

*Correspondence: A Shafik, Department of Surgery and Experimental Research, Cairo University, 2 Talaat Harb Subject Street, Cairo 11121, Egypt. E-mail: [email protected] Received 27 January 2004; revised 16 June 2004; accepted The study comprised 23 healthy female volunteers 19 August 2004 with a mean age of 36.776.3 standard deviation Clitorouterine reflex A Shafik et al 122 (s.d.) y (range 28–44). The women were recruited GC stimulation. GC was stimulated both electri- during the proliferative phase of the menstrual cally and mechanically. Electric stimulation was cycle. They were sexually active, had normal performed with a surface electrode (Vickers Medi- menses and no gynecologic complaint in the past cal, Medelec, Woking, UK) applied to the GC and or at the time of enrolment. A total of 10 were fixed by electrode gel. Mechanical stimulation was nulliparous and 13 multiparous with normal vaginal carried out with a pencil electrode consisting of a deliveries. Physical examination including gyneco- solid steel rod, 15 cm long and 5 mm in diameter. To logic and neurologic assessment had normal find- avoid injury to the GC, the distal end of the ings. Sonograms showed normal genitourinary electrode was covered for about 2 cm by a polyvinyl organs. Women with vaginal discharge, cervical sponge which was fashioned like a cone to simulate erosions or sonographic lesions were excluded from the shape of the glans penis. The response of uterus the study. The subjects were fully informed about and CU to gentle stroking of the GC by the pencil the nature of the study, the tests to be performed and electrode was recorded. The GC stroking by the their role in the study. The study was approved by pencil electrode intended to simulate GC buffeting the Review Board of the Cairo University Faculty of by the erect penis during coitus. It was performed by Medicine and its Ethics Committee. one investigator in all of the examined women. In all, 20 gentle GC strokes were made for each subject. The test was repeated at least twice in the individual subject. Methods

The response of the uterus to electrical and Manometric studies. The uterine and CU pressures mechanical stimulation of the GC was determined. were measured by a manometric tube of a 0.5 mm inner and a 1 mm outer diameter, with two side ports, perfused with normal saline at a rate of 1.6 ml/ min by a pneumohydraulic perfusion system (Arn- Electromyographic (EMG) studies. The procedure dorfer, Medical Specialities, Greendale, WI, USA), A was carried out without sedation on an outpatient vaginal speculum was inserted into the vagina to basis. However, some women, especially the nulli- expose the CU. One lubricated tube was introduced parous, were given intravenous diazepam (10 mg; 4–5 cm into the uterine cavity and another one into Hoffman La Roche, Basle, Switzerland) for sedation the CU. They were connected to a strain gauge during cervical dilatation. With the women in the pressure transducer (Statham 230B, Oxnard, CA, lithotomy position, a self-retaining speculum was USA). We started recording the uterine electric introduced into the vagina. Cervical dilation was activity and pressure 30 min after the electrodes performed with Hegar’s dilators in the sizes from 2/5 and the manometric tubes had been applied to the to 3/6 mm. The uterine electric activity was recorded uterus and CU. During this half-hour the uterus by means of a 4F catheter attached to the uterine would have adapted to these devices. At least two wall by suction to a negative pressure of 20 cmH O 2 recording sessions of 60 min each were performed that was maintained during the test. The myo- for every woman. electric activity was recorded by a monopolar silver–silver chloride electrode, 0.25 mm in diameter and situated 1 cm from the tip of the catheter (Smith Kline-Becham, Los Angeles, CA, USA). The Clitoral and uterine anesthetization. To study protruding part of the electrode lay in contact with whether the uterine response to clitoral stimulation the endometrium, thus acting as a surface electrode. was a direct or a reflex action, GC stimulation was Three electrodes were applied to the uterus: two performed after individual anesthetization of the to the uterine and one to the cervix uteri (CU) uterus and GC. GC was anesthetized by means of mucosa. The two uterine electrodes were introduced xylocaine gel (Astra, So¨derta¨lje, Sweden). At 20 min through the CU to be attached by suction to the following gel application, the response of the uterus mucosa of the uterine wall, one electrode above the to GC electrical and mechanical stimulation was other and 2 cm apart. The third electrode was recorded. After 3 h later when the anesthetic applied to the cervical mucosa at about the middle response had disappeared, the uterine response to of the cervical canal. The reference electrode was a GC stimulation was registered. The test was re- metal disk applied to the skin of the abdomen. The peated using bland gel instead of xylocaine gel. On signals detected by the electrodes were amplified another day, the uterus was anesthetized by instil- using an AC amplifier with a frequency response ling 10 ml of 2% xylocaine, added to 10 ml of normal within 73 dB from 0.016 Hz to 1 kHz and were saline, into the uterine cavity through the CU. The displayed on a recorder at a sensitivity of 1 mV/cm. uterine response to GC stimulation after 20 min and A strain gauge respiration transducer was attached after 3 h was recorded. The test was repeated using to the thoracic wall to exclude respiratory artifacts. normal saline instead of xylocaine.

International Journal of Impotence Research Clitorouterine reflex A Shafik et al 123 The results were analyzed statistically using the Student’s t-test. Values were given as the mean7s.d. Differences assumed significance at Po0.05.

Results

All the women finished the tests without complica- Figure 2 Electrohysterogram showing disappearance of the tions during or after the test performance and were uterine electric waves (U) on electrical stimulation of the glans evaluated. clitoris. m ¼ stimulation; C ¼ cervical waves. The suction electrodes were atraumatic to the uterine or cervical wall. They were easy to apply, were stable and not dislodged as long as the already mentioned suction pressure was maintained. Dis- lodgment of an electrode would have been recogniz- able from loosening of the catheter.

Electromyographic recording

Slow waves (SWs) were recorded from the two Figure 3 Electrohysterogram showing appearance of occasional uterine slow waves (U) on electrical stimulation of the glans electrodes applied to the uterus. They were mono- clitoris. m ¼ stimulation; C ¼ cervical waves. phasic and negatively deflected (Figure 1). The waves had a regular rhythm and exhibited the same frequency, amplitude and velocity of conduction from the two electrodes of the individual women. The mean frequency was 3.270.9 cycle/min, (cpm, range 2–5), the amplitude 0.570.1 mV (range 0.3–0.8), and the conduction velocity 4.171.6 cm/s (range 3.2–5.6, Figure 1). The SWs variables were constant in the two electrodes when the test was repeated in the same woman. The SWs were followed, or superimposed, by Figure 4 Electrohysterogram showing disappearance of the bursts of fast activity spikes or action potentials uterine electric waves (U) on mechanical stimulation of the glans (APs), represented by negative deflections (Figure 1). clitoris. m ¼ stimulation; C ¼ cervical waves. They did not accompany each SW and their number varied from one test to the other. While the uterus exhibited resting electric waves, (mean 50.7710.9). At threshold, no electric waves the CU did not. No waves were registered from the were recorded from the three electrodes applied CU during the two recording sessions (Figure 1). to the uterus and CU (Figure 2). However, in some Electrical stimulation of the GC was induced by a women, we recorded occasional SWs from the train of five square pulses of 1 ms duration and 1 ms uterus which were not associated with APs apart, with the threshold varying from 35 to 75 mA (Figure 3). The uterus responded to GC stimulation as long as the stimulation was maintained. Upon cessation of electrical GC stimulation, the uterine SWs reappeared with variables similar to those before electrical GC stimulation. The latency which is the period from the stimulus to the start of the response recorded a mean of 19.472.1 ms (range 17–23). Mechanical stimulation of the GC with pencil electrode caused disappearance of the uterine resting electric waves (Figure 4). The response was momentary; it occurred synchronously with the Figure 1 Electrohysterogram at rest showing the electric activity stroking of the GC by the pencil electrode and then recorded by the two electrodes applied to the uterus (U) in the form of slow waves followed or superimposed by the action the electric waves reappeared. Repeated buffeting of potentials (arrow). No waves were recorded from the cervix uteri. the GC with the pencil electrode was coupled with C ¼ cervical EMG. dis- and reappearance of the electric waves. The

International Journal of Impotence Research Clitorouterine reflex A Shafik et al 124 latency recorded a mean of 20.672.2 ms (range Discussion 18–25). No electric waves were recorded from the CU on mechanical GC buffeting. We did not find a significant difference in the The external and internal reproductive organs 1–8 resting electric activity of the uterus or in the undergo changes during the sexual act. These response to GP stimulation between nulli- and changes reflect the functional adaptability of the multiparous women and between the young and reproductive organs to serve the sexual performance elderly women. and notably the process of reproductivity. The current study may shed some light on the mechanism of the uterocervical changes that occur during the sexual act. Response of the uterus to clitoral anesthetization Upon GC stimulation, the uterus seems to adapt to the reproductive process. The rise of the uterus in Electrical and mechanical stimulation of the GC the pelvis from its anteverted and anteflexed 20 min after its anesthetization effected no disap- position with a subsequent movement of the CU away from the posterior vaginal wall as reported by pearance of the uterine electric waves (Figure 5), 2–4 whereas the waves disappeared with stimulation investigators is a mechanism which is suggested following bland gel application to the GC. Further- to serve a twofold function: (a) it enables proper CU more, the anesthetized uterus did not respond to GC buffeting by the glans penis and (b) it brings the os of stimulation, while it did when normal saline was the CU in apposition with the glans penis to allow instilled into it. The response of the uterus to GC for direct passage of the deposited semen through stimulation returned when 3 h after anesthetic the cervical os to the uterine cavity. In a previous application its effect had disappeared. study, we have demonstrated that, during sexual intercourse, the levator ani muscle undergoes reflex contractions mediated through the vaginolevator reflex.13 Levator muscle contraction pulls up the Pressure measurements vaginal wall at the vaginal fornices (Figure 6) leading to their ballooning and formation of a receptacle for semen collection during the sexual The uterine and CU resting pressure recorded a 13,14 mean of 11.672.1 cmH O (range 9–14). Electrical act. It may also lead to elevation of the CU and 2 consequently of the uterus. stimulation of the GC using the aforementioned 15 variables led to a significant reduction of the uterine The current study as well as previous studies pressure to a mean of 2.770.7 cmH O (range 1.6– have shown that the uterus exhibits electric waves 2 which are presumably responsible for the motor 3.4; Po0.05). The pressure reduction was main- 16–21 tained on continued GC stimulation. Mechanical GC activity of the organ. Thus it seems that the stimulation also effected a significant uterine pres- uterine electric activity is responsible for inducing the uterine resting tone which is assumed to assist sure reduction to a mean of 3.270.8 cmH2O (range 2–4.2; Po0.05). The pressure reduction was inter- in keeping the uterus in its resting position and mittent and coupled with GC buffeting with the shape. The source of these electric waves is pencil electrode. It did not differ significantly from controversial. They could be discharged from the that induced by electrical stimulation. During the uterine smooth muscle fibers or the interstitial cells aforementioned pressure measurements we did not find significant changes in the CU pressure (P40.05). The current results were reproducible with no significant difference when we repeated the tests in the individual subject.

Figure 6 Diagram illustrating the effect of levator ani and puborectalis muscles contraction on the vagina and uterus. Antero-posterior view. (a) At rest (b) Upon levator contraction, the muscle becomes elevated and laterally retracted, with a Figure 5 Electrohysterogram 20 min after GC anesthetization. GC resulting elevation of the uterus as well as dilatation of the upper electric stimulation did not cause disappearance of the uterine vagina and vaginal fornices. Puborectalis muscle contraction electric waves (U). m ¼ stimulation; C ¼ cervical waves. compresses the lower vagina (from Shafik14).

International Journal of Impotence Research Clitorouterine reflex A Shafik et al 125 of Cajal (ICC).22–25 The ICC exist in the gut,23–25 yet we do not know if they also exist in the uterus. As previously demonstrated,15 the CU did not exhibit electric waves; this may be related to the fact that the CU contains but a few smooth muscle fibers. Presumably, the motor activity of the electric waves is produced by the APs.16–21 Earlier studies have revealed that the APs were coupled with a rise of the intrauterine pressure, while the SWs were not.15 As the APs followed or were superimposed on the SWs, we postulated that probably the SWs pace the APs 20 in terms of direction and amplitude. Figure 7 Respiratory artifacts recorded from a transducer On GC stimulation, electrical or mechanical, the attached to the chest wall. uterine electric waves disappeared. Disappearance of the APs seems to be associated with absence of are stimulated by penile buffeting of the GC. uterine motor activity. The uterine resting tone Afferent impulses appear to be transmitted to the apparently disappears on GC stimulation. We sacral segment by the pudendal nerve (S2, 3, 4), propose that disappearance of the uterine tone while the efferent limb probably passes via the during GC stimulation is accountable for uterine autonomic supply to the uterus. enlargement as well as for the rise of the uterus in Recordings of the electric waves of the uterus are the pelvis from its anteverted and anteflexed limited by artifacts. It may be argued that these position. Furthermore, the disappearance of the waves represent artifacts. However, the consistency uterine motor tone which results in uterine wall and reproducibility of the waves are against this relaxation, uterine cavity dilatation, and uterine argument. The uterine electric waves could be easily pressure reduction, appears to create a condition of differentiated from the electrocardiographic waves relatively negative uterine pressure and suction by the characteristic shape of the latter waves. The action that sucks the semen collected in the vaginal possibility of respiratory artifacts was excluded by fornices into the uterine cavity. recording the respiratory electric activity via a transducer attached to the chest wall (Figure 7).

The clitorouterine reflex Diagnostic role of the clitorouterine reflex The current findings postulate a hitherto unrecog- nized relationship between GC stimulation and the The investigative tools for the diagnosis of female uterine electric activity. The disappearance of the sexual disorders are few.27 Episodic vaginal blood uterine electric waves on GC stimulation hypothe- flow during sleep is measured in an attempt to sized the possible involvement of a reflex which assess the neurophysiological substrate of the sexual we term ‘clitorouterine reflex’. The constancy of this desire in women.28,29 The diagnostic significance of reflex relationship is evidenced by reproducibility vaginal responses to erotic stimuli in the waking and by its absence on individual anesthetization of state is not yet clear.30 the assumed two arms of the reflex arc, namely the The clitorouterine reflex may be considered as an GC and the uterus. Anesthetization with xylocaine investigative tool in the diagnosis of female sexual (lidocaine) blocks C and Aa- fibers which are disorders. Changes in the reflex latency or the wave responsible for pain and reflex activity.26 variables or the response to clitoral stimulation may We suggest that the clitorouterine reflex is evoked indicate a defect in the reflex pathway. However, during penile buffeting of the GC in the sexual act. further investigations need to be performed to The resulting disappearance of the uterine electric confirm the current results. activity and the possible consequent uterine muscle In conclusion, the findings of our study suggest relaxation and uterine dilatation appear to explain the presence of a reproducible reflex relationship the changes in the uterus and CU during coitus. between the GC and the uterus which we call the These changes, assumed to be preparatory for ‘clitorouterine reflex’. During the sexual act and receiving the semen deposited in the vaginal penile buffeting of the GC, the clitorouterine reflex fornices, comprise uterine enlargement as well as seems to be evoked and initiates the uterine the rising of the uterus in the pelvis from its response that comprises erection, elevation and anteverted and anteflexed position with a resulting enlargement of the uterus. Owing to paucity of the movement of the CU away from the posterior vaginal currently available investigative tools for the diag- wall.2,3 nosis of sexual disorders, the clitorouterine reflex The afferent limb of reflex arc seemingly com- may be incorporated, after further studies, as an prises the sensory nerve endings in the GC which investigative tool in the diagnosis of such disorders.

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