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a Departments of Urology and Cell Biology,
b University of Virginia Health Science Center, Charlottesville, Virginia 22908
ABSTRACT
Testicular microvascular blood flow is known to exhibit vasomotion, which has been shown to be significantly altered in the short term following the repair of testicular torsion. This loss of vasomotion may ultimately be responsible for the loss of spermatogenesis observed after testicular torsion in rats. In the present study, testicular vasomotion and interstitial oxygen tensions were simultaneously measured prior to, during, and at various time points after repair of testicular torsion in the rat. Testicular torsion was induced by a 720° rotation of the testis for 1 h. Laser-Doppler flowmetry and an oxygen electrode were used to simultaneously measure vasomotion and interstitial oxygen tensions (PO2), respectively. Pretorsion control testes had a mean blood flow of 16.3 ± 1.3 perfusion units (PU) and displayed vasomotion with a cycle frequency of 12 ± 0.2 cycles per minute and a mean amplitude of 4.2 ± 0.3 PU. Mean testicular interstitial PO2 was 12.5 ± 2.6 mm Hg, which displayed a cyclical variation of 11.9 ± 0.4 cycles per minute with a mean amplitude of 2.8 ± 0.8 mm Hg. During the torsion period, both mean blood flow and interstitial PO2 decreased to approximately zero. Upon detorsion, mean microvascular blood flow and mean interstitial PO2 values returned to values that were not significantly different from pretorsion values within 30 min; however, vasomotion and PO2 cycling did not return, even after 24 h. It was 7 days after the repair of torsion before a regular pattern of vasomotion and PO2 cycling returned. These results demonstrate for the first time a correlation between testicular vasomotion and interstitial PO2 cycling, and this correlation persists after the repair of testicular torsion.
spermatogenesis, testes
INTRODUCTION
Testicular torsion refers to a clinical condition involving rotation of the testis and a twisting of the spermatic cord. Twisting of the cord, in turn, obstructs blood flow to the affected testis. This lesion occurs most commonly in adolescent males, although it can occur in much younger and older males as well [1]. Most often, surgical intervention is necessary to repair the torsion, but testicular atrophy can result even after restoration of blood flow, depending on the degree of rotation and duration of torsion. Studies of testicular torsion in the rat model have shown that a 720° rotation of the testis for 1 h results in loss of spermatogenesis despite normally functioning Leydig cells [2] and Sertoli cells [3]. Aspermatogenesis after testicular torsion has been attributed to germ cell-specific apoptosis [4] arising from an increase in the proapoptotic molecules, Bax and Fas ligand [5]. It has been hypothesized that an increase in germ cell apoptosis is due to an increase in intratesticular reactive oxygen [4]. It has also been demonstrated, however, that microvascular blood flow in the testis does not return to normal after repair of torsion, at least in the short term [6], and this could also play a role in the continued impairment of spermatogenesis.
Testicular blood flow exhibits vasomotion [7–9]. Vasomotion is the rhythmic dilation and constriction of precapillary sphincters, which in turn results in cyclical variations in blood flow through capillaries [10]. Vasomotion modulates local vascular resistance and is believed to be involved in regulating the exchange of nutrients, O2, CO2, and fluids between the vasculature and interstitial space [10]. The mechanisms controlling vasomotion are complex and incompletely resolved, but in the rat testis, it is known that vasomotion is testosterone-dependent, is not seen prior to puberty, and is responsive to catecholamines whether peripherally infused [7, 11] or microperfused around restricted fields of the testicular microvasculature [9].
It has been previously demonstrated that experimental testicular torsion essentially eliminates testicular blood flow during the period of torsion, that mean blood flow returns to pretorsion values within minutes of the repair of torsion, but that vasomotion does not return by 1 h after torsion repair [6]. Whether or not vasomotion ever returns to pretorsion values after repair of torsion has not been established. Also, the relationship between vasomotion and interstitial oxygen tension (PO2) in the testis has not been established under either physiological or pathological conditions. It is conceivable that alterations in vasomotion could lead to significant changes in interstitial oxygen, and this value, which is permanently altered, could have lasting effects on spermatogenesis. Thus, the present study was undertaken with two aims. First, to determine the relationship between testicular vasomotion and testicular interstitial oxygen concentrations in real time, and second, to determine if testicular vasomotion and interstitial PO2 are permanently affected after repair of torsion.
MATERIALS AND METHODS
Animals
This work was performed in accordance with the Guiding Principles of the Care and Use of Research Animals promulgated by the Society for the Study of Reproduction. Adult Sprague-Dawley rats (500–550 g) were obtained from the University of Virginia's vivarium sources and maintained on a cycle of 12L:12D with food and water ad libitum.
Rats were anesthetized with an i.p. injection of Inactin (0.1 g/kg body weight; RBI, Natick, MA) and placed on an autoregulating thermal heating pad to maintain body temperature at 37°C. Blood pressure was monitored via a heparinized saline-filled cannula installed in the right carotid and attached to a pressure transducer (DTX+, Ohmeda Medical Device Division, Inc., Madison, WI) and monitor (Model 78833B, Hewlett Packard, Wilmington, DE).
Measurement of Testicular Blood Flow
A laser-Doppler flowmeter and flow probe (ALF-21, Transonic Systems Inc., Ithaca, NY) attached to a micromanipulator were used to monitor testicular microvascular flow in real time. The flow probe (1 mm diameter) is capable of monitoring microvascular perfusion in a tissue volume of approximately 1 mm3. The principles of laser-Doppler flowmetry have been described elsewhere [6, 12]. Briefly, the fiber-optic flow probe directs monochromatic light to a microvascular bed. The light is subjected to a Doppler shift by moving red cells. Reflected light travels back down the fiber-optic cable to a photo detector in the flowmeter and the output signal is processed by the ALF-21 to report blood flow as relative perfusion units.
The laser-Doppler flow probe was carefully positioned at the testicular surface to avoid local pressure effects and to monitor flow over microvascular fields only. Three 30-sec measurements of blood flow were recorded and averaged. A computer interface and FlowTrace software (Transonic Systems, Inc.) were used to analyze the flowmeter output. Background noise was determined in each experiment by positioning the probe over the testis 10 min after the rats were killed with an intracardiac injection of saturated potassium chloride. This value was subtracted from all blood flow data before any subsequent calculation. Vasomotion frequency and amplitude were determined using GraphPad Prism software (GraphPad Software Inc., San Diego, CA).
Measurement of Testicular Interstitial Oxygen Tension
An isolated dissolved-oxygen meter and oxygen electrode (OXEL-1, World Precision Instruments, Inc., Sarasota, FL) attached to a micromanipulator were used to monitor interstitial testicular oxygen concentrations. A gas-selective polymer membrane covering the electrode tip (2-mm diameter) allowed diffusion of oxygen from the contact fluid and oxygen reduction at the platinum cathode. The magnitude of the resulting current is proportional to PO2 outside the membrane [13]. The instrument was calibrated in nitrogen-purged distilled water and air-saturated distilled water before each experiment. Continuous PO2 readings were monitored from a digital display and from output sent to a chart recorder (BD-40, Pharmacia, Uppsala, Sweden). Data collected as percent oxygen saturation were converted to mm Hg.
A 2-mm incision was made in the tunica albuginea, carefully avoiding trauma to underlying tissue. The oxygen probe was placed in the testicular interstitium avoiding major blood vessels. Three 1-min recordings were obtained over a 5-min period, and the data were averaged. Cycling characteristics of PO2 were determined by 15 peak and nadir values over a 3-min period. During ischemia periods, the electrometer occasionally recorded values at or below baseline. Negative values were recorded as zero for statistical analysis.
System Qualifications
To determine laser-Doppler flowmetry responsivity to graded vascular stimulation Rats were anesthetized with an i.p. injection of sodium pentobarbital (50 mg/kg body weight). The testis was exteriorized and delivered to a 35°C testicle receptacle, surrounded in 3% agar, and covered with mineral oil. Testicular microvascular blood flow was recorded for 3 min. A 10-µl saline solution containing 0.5, 5, 50, 500, or 1000 µM epinephrine was then administered subtunically over a 10-sec period using a 50-µm-tip micropipette. The laser-Doppler flow probe was placed within 3 mm of the microinjection site. Measurements were taken beginning 1 min after the 10-sec injection and continued for 3 min thereafter. Doses were administered in ascending order and each subsequent dose was administered only after blood flow returned to preinjection values.
To determine oxygen probe responsivity to graded dissolved oxygen tension The oxygen electrode was calibrated in nitrogen-purged distilled water (0% or 0 mm Hg O2), ambient oxygen-saturated distilled water (100% or 150.5 mm Hg), and mixtures of the two to obtain solutions at 12.5% 25%, 50%, and 75% oxygen saturation.
To simultaneously determine microvascular blood flow and interstitial oxygen tension in the testis and monitor responses to an acute period of ischemia Rats were anesthetized and prepared as described earlier. The left testis was delivered into a glass testicle receptacle maintained at 35°C. The testis was immersed in 3% agar and occasionally covered with saline to prevent dehydration. A 2-mm incision was made in the tunica albuginea and the oxygen probe was inserted. The laser-Doppler flow probe was placed over microvascular beds approximately 1 mm away from the oxygen probe. After a 30-min system-stabilization period, testicular microvascular flow and PO2 were recorded simultaneously. Blood flow and PO2 patterns were monitored for 5 min. A microvessel clamp was then applied to the spermatic artery for approximately 2 min. The clamp was released, and the blood flow and interstitial PO2 patterns were monitored for 5 min.
Acute Effect of Torsion on Microvascular Blood Flow and Interstitial Oxygen Tension
Rats were prepared as described earlier. Bilateral scrotal incisions were made to allow a window to the testis while it was still in the scrotum. Testicular blood flow was monitored intrascrotally. The left testis was then exteriorized and placed in the 35°C testicle receptacle. Blood flow and oxygen recordings began 30 min later. The testis was then placed back into the scrotum and the incision was closed. These readings served as pretorsion control readings.
The right testis was then exteriorized and testicular torsion was induced as described previously [4, 6], except that the testis was reached through a scrotal incision rather than a mid-ventral laparotomy. This was performed because of the acute nature of the experiment and the need to place the testis in the 35°C testicle receptacle after torsion repair. Briefly, the testis was freed from the gubernaculum and the epididymo-testicular membrane and rotated 720° along the testicular axis. The twisted testis was returned to the scrotum and the incision was closed for 50 min. At that time, the testis was delivered to the testicle receptacle and microvascular blood flow was determined immediately prior to torsion repair. Determinations of PO2 require incising the testis; therefore, blood flow alone was determined during torsion in testicles going into the study of immediate post-torsion effects. In order to simultaneously determine blood flow and PO2 during torsion, another group of five testes were examined during torsion, but these testes were not further studied.
Using the right testis that had been twisted and subjected to only blood flow determinations, 1 h after induction of torsion, torsion repair was performed by a 720° counter-rotation of the testis, and the testis was immediately established in the 35°C testicle receptacle as described previously. Testicular microvascular blood flow and interstitial PO2 were simultaneously recorded at 30, 45, 60, and 90 min after torsion repair.
Chronic Effect of Torsion on Testicular Blood Flow and Interstitial Oxygen Tension
Rats were anesthetized and subjected to 1 h, 720° torsion via a laparotomy incision as previously described [4, 6]. After repair of torsion, the testis was reinserted into the scrotum via the inguinal canal. In these experiments, in which blood flow was not actually measured during and immediately after torsion, a subjective scoring system (1–4) was used to evaluate the consistency of the torsion effect on ischemia and of torsion repair on relief of ischemia. One or 7 days after torsion repair, rats were anesthetized and prepared as described previously for simultaneous determination of ipsilateral testicular microvascular blood and interstitial PO2. Both values were recorded 30 min after establishment of the testis in the testicle receptacle as described previously.
Statistical Analysis
All within-group data were subjected to Chauvenet's criterion for homogeneity [14]. All multiple comparisons were performed with analysis of variance followed by Tukey's range test (P < 0.05).
RESULTS
System Qualifications
Independent determinations of the laser-Doppler flowmeter responsiveness to graded microvascular stimulation and oxygen electrode responsiveness to graded dissolved oxygen concentrations Laser-Doppler flowmetry has been previously employed in this laboratory [6, 9]; however, it was further qualified in the present experiments. Epinephrine, a potent vasoconstrictor, microinjected under the tunica albuginea, caused a concentration-dependent decrease in microvascular blood flow (Fig. 1A). Control testicular microvascular blood flow exhibits vasomotion, which is eliminated after even the smallest concentration of epinephrine (Fig. 1A). Equivalent volume of saline alone had no effect (not shown). The oxygen electrode appropriately measured dissolved oxygen at various concentrations. It is important to note that oxygen probe sensitivity remained linear within the PO2 range of 0–30 mm Hg (Fig. 1B).
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Simultaneous determinations of testicular microvascular blood flow and interstitial fluid oxygen tension during a period of acute ischemia Pilot experiments were performed to establish the simultaneous use of the laser-Doppler flow probe and the oxygen electrode to determine microvascular blood flow and interstitial PO2 before, during, and after a period of acute ischemia in vivo. Testicular microvascular blood flow prior to ischemia displayed characteristic vasomotion (Fig. 2). Vasomotion and microvascular blood flow were eliminated by clamping the spermatic artery. Vasomotion and mean microvascular blood flow returned to preischemia values within approximately 90 sec after a 2-min occlusion period (Fig. 2). Simultaneous measurement of interstitial PO2 revealed a cycling pattern of tensions of 10–15 mm Hg (Fig. 2). Interstitial PO2 was reduced to 0 mm Hg within 10 sec of eliminating blood flow and, similar to microvascular blood flow, returned to preischemia values within 90 sec of reperfusion (Fig. 2). Thus, it is possible to simultaneously measure both parameters in this model system, and both blood flow and PO2 respond coherently to acute vascular occlusion.
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Effects of Testicular Torsion on Microvascular Blood Flow and Oxygen Tension
Mean carotid artery blood pressure in pretorsion animals was 114 ± 2.3 mm Hg, and this value was not significantly altered in any group. Testicular microvascular blood flow in control testes displayed vasomotion (Fig. 3A) with a mean flow value of 16.3 ± 1.3 perfusion units (PU; mean ± SEM). The mean amplitude of each vasomotion cycle was 4.2 ± 0.3 PU, or approximately 29% of the mean flow value, and the cycle frequency was 12.0 ± 0.2 cycles per min (Table 1). The mean testicular interstitial oxygen tension was 12.5 ± 2.6 mm Hg, and these values also displayed cyclical variation (Fig. 3A). The amplitude of the PO2 cycle was 2.8 ± 0.8 mm Hg, or approximately 16% of the mean value, and the cycle was 11.9 ± 0.4 cycles per minute (Table 2); thus, PO2 and blood flow cycle frequency were statistically identical, but the PO2 cycle had an amplitude approximately half that of the blood flow cycle.
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Mean testicular blood flow dropped to 0.1 ± 0.1 PU by the end of the 1-h torsion period (Fig. 4A) and oxygen tension had declined to zero (Fig. 4B). Both of these values were significantly different from pretorsion values. Blood flow and PO2 cycles were also eliminated during torsion (Tables 1 and 2). Upon detorsion, intraoperative appearance of the testis gave the qualitative impression of reperfusion within a few minutes of testicular counter-rotation. Analysis of quantitative data demonstrated that mean microvascular blood flow returned to values not significantly different from pretorsion values within 30 min of torsion repair, and remained not significantly different thereafter (Fig. 4A). Mean interstitial PO2 also returned to pretorsion values within 30 min of torsion repair and were maintained thereafter (Fig. 4B).
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Whereas mean blood flow and interstitial PO2 data were no longer significantly different from pretorsion values within 30 min of torsion repair, blood flow and PO2 cycling data remained significantly altered. Neither testicular vasomotion nor interstitial PO2 cycling returned within the 90 min of the acute experiments (Fig. 3B, Tables 1 and 2). By 24 h after torsion repair, however, there was evidence of vasomotor activity returning to the testicular microvasculature (Fig. 3C, Table 1). The activity was sporadic and irregular in waveform. Variations in oxygen tension also occurred within 24 h of torsion repair (Fig. 3C), but they were irregular and did not constitute a cycle with measurable amplitude and frequency (Table 2).
Seven days after torsion repair, a regular vasomotion pattern had returned to the testicular microvasculature (Fig. 3D). Cycle frequency was not significantly different from pretorsion values but cycle amplitude, both as unadjusted PU and as a percent of mean flow, was significantly elevated (Table 1). A regular interstitial PO2 cycle also returned 7 days after torsion repair (Fig. 3D), and average amplitude and frequency characteristics returned to values that were not significantly different from those of the pretorsion testis (Table 2).
DISCUSSION
Vasomotion has been observed in several different tissues, including renal cortex [15], skin [16], and testis [7, 9, 17]. Previous studies of vasomotion in rat testis employing laser-Doppler flowmetry have reported vasomotion frequencies that were similar to the results described in the present study. Damber et al. [7] reported that testicular microvascular blood flow oscillated with a periodicity of approximately nine cycles per minute. Subsequently, the same laboratory reported vasomotion frequencies of 7–10 cycles per minute, which were abrogated in rats in which Leydig cells had been eliminated by ethane dimethyl sulfonate [18]. Testosterone supplementation replaced this vasomotion [19].
The rhythmic contraction of arteriolar smooth muscle cells is believed to be the cause of vasomotion; however, the underlying stimuli are not fully understood. Studies investigating the mechanism of vasomotion in rat testis have demonstrated that vasomotion is hormonally and developmentally controlled [19–21] and influenced by unspecified factors from the seminiferous tubules [8]. Recently, Bergh et al. [17] used two laser-Doppler probes to simultaneously examine vasomotion in two different sites of the same testis and found that vasomotion-induced variations in microvascular blood flow were generally not correlated between the two sites. This suggests that vasomotion is induced by local factors and is not due to a general effect such as pulsatile contraction of the testicular capsule [22].
There have been few studies examining interstitial oxygen tension in the testis. Free et al. [23] reported a PO2 of 15.2 ± 3.5 mm Hg in interstitial tissue of rat testis, which is in agreement with the 12.5 ± 2.6 mm Hg value reported in the present study as well as the 11.6 ± 1.6 mm Hg value previously reported for rabbit testis [24]. Testicular interstitial PO2 values within a similar range have also been described in sheep and dogs [24]. Klotz et al. [25] reported an interstitial PO2 value in rat testis of 21 ± 5 mm Hg, a value slightly elevated in comparison to most previous studies; nevertheless, Cross and Silver [24], Free et al. [23], and Klotz et al. [25] have all noted that the PO2 in the testicular interstitium is lower than in other tissues examined. For example, the testis PO2 value from Klotz et al. [25] (21 ± 5 mm Hg) is approximately half the value recorded for thigh muscle (41 ± 6 mm Hg) in that same study, and the value from Cross and Silver [24] for rabbit testis (11.6 ± 1.6 mm Hg) is approximately half the value these investigators reported for rabbit epididymis (21.8 ± 1.5 mm Hg). Setchell [26] speculated that the testis operates on the verge of hypoxia because testicular PO2 is relatively low, oxygen extraction is high due to the metabolic demands of spermatogenesis, and the testis has little capacity to increase total blood flow. This could have important consequences on spermatogenesis. Because PO2 is dependent on blood flow, disturbances in blood flow may easily alter the amount of oxygen available for critical metabolic processes in spermatogenesis. Oxygen availability within cells is ultimately an important factor in gene expression and in hierarchical processes such as spermatogenesis, whereas inappropriate gene expression in early cell types (e.g., spermatogonia) can have profound effects on the outcome of the entire process (e.g., spermatozoa). Alternatively, germ cell development in an environment in which oxygen tension is relatively low may be developmentally important. Preventing excessive oxygen tension could be important in limiting germ cell exposure to reactive oxygen species and subsequent damage to membrane lipids or germ-line DNA.
To our knowledge, this is the first report to simultaneously measure interstitial oxygen tension and microvascular blood flow in testes. Interstitial PO2 fluctuated at a statistically identical frequency (11.9 ± 0.4 cycles per minute; Table 2) to that observed for microvascular vasomotion (12.0 ± 0.2 cycles per minute; Table 1), which suggests a direct link between interstitial PO2 and microvascular vasomotion. A similar link between vasomotion and spontaneous oscillations of oxygen in rat brain has recently been reported [27], but underlying mechanisms were not discussed.
Oscillations in testicular interstitial PO2 alone were observed by Free et al. [23] who suggested that oxygen fluctuations were most likely the result of contractions of the testicular capsule. The present study demonstrates a direct link between interstitial PO2 and vasomotion, however, and it has previously been shown that vasomotion continues in the absence of an intact testicular capsule [11]. Thus, oscillations of oxygen tension within the testis are most likely the result of vasomotion and not contraction of the testicular capsule.
The pretorsion cycle amplitude of interstitial PO2 as a proportion of mean PO2 (16.4% ± 3.6%; Table 2) was approximately half the cycle amplitude of vasomotion when expressed as a proportion of mean blood flow (29.2% ± 2.1%; Table 1); thus, the relative fluctuations of PO2 were less than those for microvascular blood flow. The reasons for this are unclear, but influencing factors are likely to be metabolic demand, interstitial fluid flow, and extravascular space into which oxygen can diffuse relative to the intravascular space from which oxygen originates.
In the present study, acute and chronic testicular microvascular blood flow and interstitial oxygen tension were examined prior to, during, and after the repair of torsion. Testicular vasomotion and corresponding fluctuations in interstitial oxygen tension occurred under normal physiological conditions (Fig. 3A). These properties were eliminated during the torsion period (Fig. 3B) and did not return within 24 h of torsion repair (Fig. 3C). While the dynamics of microvascular blood flow were altered in the acute phase after torsion repair, mean values for both microvascular blood flow and interstitial PO2 returned to values that were not significantly different from pretorsion values within 90 min of torsion repair (Fig. 4).
Seven days after the repair of torsion, both testicular vasomotion and the oscillations of interstitial PO2 returned to frequency and amplitude patterns that were similar to pretorsion values (Fig. 3D, Tables 1 and 2). It is the case that vasomotion amplitude was significantly elevated (Table 1) 7 days after torsion repair, and this increase was not matched by the amplitude of PO2 oscillations. It is perhaps not surprising that congruence of the two cycles was not maintained 7 days after torsion repair because the effects of torsion on spermatogenesis are profound by that time [3]. Capillary permeability, interstitial fluid flow, and metabolic demands could all play roles in altering the characteristics of interstitial oxygen patterns from those observed for blood flow. It is important to note that previous studies have indicated a role for seminiferous tubule factors in regulating testicular vasomotion [8], and it is possible that such factors play roles in the increased amplitude of the vasomotion observed in an injured testis 7 days after torsion repair.
Previous studies from this laboratory have noted acute effects of torsion repair on microvascular blood flow [6], and testicular interstitial oxygen tensions during and after torsion have been independently assessed by Klotz et al. [25]. Klotz and colleagues reported slightly higher values for pretorsion and post-torsion intratesticular PO2 compared with the present study, perhaps because of different oximeter devices or the different anesthetics used, but the overall pattern of PO2 decline during the torsion period and return after torsion repair are similar. The advance of the present study is that microvascular blood flow and interstitial oxygen tensions were measured simultaneously rather than individually, and that the technique was applied to the understanding of the pathophysiology of a testicular lesion.
The present study demonstrates that vasomotion and interstitial oxygen characteristics return to normal patterns within 7 days of torsion repair; thus, permanent alteration of testicular blood flow after torsion repair is not the reason for the permanent loss of spermatogenesis [3, 4]. Alternatively, brief disruptions of vasomotion and intersititial PO2 induced by testicular torsion can have profound and long-term effects on cellular and tissue homeostasis. It has previously been demonstrated that germ cell apoptosis is stimulated as early as 4 h after torsion repair [4] and up-regulation of mRNA for proapoptotic molecules is also observed within this acute time frame [5]. The role of vascular events and tissue oxygenation in the pathological events immediately following testicular reperfusion are presently under examination in our laboratory.
FOOTNOTES
1 Supported by National Institutes of Health grant DK-53072. 
2 Correspondence: Jeffrey J. Lysiak, Department of Urology, Box 800422, University of Virginia Health System, Charlottesville, VA 22908. FAX: 804 924 8311; jl6n{at}virginia.edu
Accepted: June 8, 2000.
Received: April 27, 2000.
REFERENCES
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