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Program in Neuroscience, Florida State University, Tallahassee, Florida 32306-1270
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Recent evidence suggests that lower urinary tract functions may be influenced by reproductive status, particularly under pathophysiological conditions. This study used repeated cystometrograms via a transurethral catheter to investigate the influence of estrous stage on micturition thresholds before and after turpentine-induced bladder inflammation in urethane-anesthetized female rats. Whereas there were no estrous influences on micturition threshold in the uninflamed bladder, micturition thresholds after bladder inflammation were significantly lower in rats in proestrus or estrus than in rats in metestrus or diestrus. Furthermore, the risk that the initial urethral catheterization and preinflammation cystometrogram would produce hematuria was significantly lower in estrus than in the other stages. These estrous influences are not readily explicable by levels of ovarian hormones at the time of testing and may relate instead to dynamic interactions between these hormones and other neuroactive molecules. In addition, the results here have relevance to interpretations of cystometrographic findings in the clinic and basic research.
lower urinary tract; interstitial cystitis; cystometrogram; reproductive status; visceral pain
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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NATURAL VARIATIONS in the reproductive status of females, such as those associated with the ovarian cycle, can influence functions of the lower urinary tract (25). For example, ~40% of premenopausal women with regular menstrual cycles report cyclical changes in their urinary symptoms (12). In addition, detrusor instability measured by cystometry increases with time after menstruation in a manner that reflects increasing progesterone levels (12). Furthermore, under inflammatory conditions of the bladder, such as interstitial cystitis, urinary urge and frequency symptoms are exacerbated perimenstrually (36).
Some studies related to this issue have been done using rodents. Spontaneous and nerve stimulation-induced muscular activity of the urinary bladder vary during the estrous cycle of the guinea pig (18), and the susceptibility of the bladder wall to cyclophosphamide-induced inflammation is greatest for rats in the estrous period after ovulation (3).
Cystometric studies in rats have shown that when a mild irritant such as turpentine is applied intravesicularly, the result is long-lasting bladder hyperreflexia (22). As the experimental bladder inflammation progresses over the course of several hours, so does the associated hyperreflexia, which is recognized by a decrease in micturition threshold (MT) and an increase in the number of contractions during a fixed amount of fluid infusion (7). None of the studies using cystometry, however, has examined the influence of reproductive status.
The female rat typically has a 4-day estrous cycle, divided into metestrus, diestrus, proestrus, and estrus. Estrogen and then progesterone levels surge during proestrus (in preparation for ovulation) and by midestrus (after ovulation) return to basal levels (31). The purpose of the present study was to assess the influence of estrous stage on the capacity of the uninflamed bladder as well as on the development of hyperreflexia after turpentine-induced inflammation.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals. Female Sprague-Dawley rats (200-250 g body wt) were individually housed in hanging cages and maintained on a 12:12-h light-dark schedule with free access to chow and water. Estrous stage was assessed by daily vaginal smears 2 h after lights on. Only rats that had at least two consecutive regular 4-day cycles before the day of the experiment were used, and assessments of bladder capacity were made 3-7 h after lights on.
Experimental and control groups. There were four experimental groups and two control groups: the bladders of experimental animals were infused with 50% turpentine in olive oil after the baseline cystometrograms (CMGs) had been run, and the bladders of the control animals were infused only with oil. Experimental groups consisted of rats in metestrus, diestrus, proestrus, or estrus. The two oil control groups, tested to assess the effects of repeated CMGs as opposed to chemically induced inflammation, consisted of rats in metestrus and estrus. Subsequently, an additional baseline study was added (see Additional study).
Experimental procedures.
The general experimental protocol was similar to that of Dmitrieva and
colleagues (7). Repeated CMGs were done in each rat to
compare MTs before and during a 3-h period after bladder inflammation
had been induced by intravesicular turpentine. Representative CMGs from
rats in each of the estrous stages are shown in Fig. 1. Experimenters were blind to the rat's
estrous stage until after the data had been analyzed.
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Surgery and CMGs. For each experiment, the rat was anesthetized with urethane (1.2 g/kg ip). Body temperature was maintained at ~37°C by a heating pad and warming lamp. The bladder was catheterized transurethrally with 1.1-mm-diameter polyethylene tubing, with the tip of the catheter placed ~2 mm within the bladder lumen so that it did not contact the bladder walls. A suture was tied around the skin where the catheter enters the urethra to secure the position of the catheter and prevent fluid leakage from around the catheter. This single catheter was used to fill the bladder and to measure bladder pressure. A 2- to 3-cm incision was made on the ventral midline to expose the bladder, so that it could be emptied completely before each CMG with gentle pressure using saline-moistened cotton-tipped applicators. The bladder was kept moist throughout the study with saline-dampened pads covering the incision.
Each CMG provided a measurement of the pressure within the bladder while the bladder was slowly infused with saline via the single transurethral catheter. Before the beginning of each CMG, the bladder was emptied, and then saline was infused at a steady rate (0.05 ml/min) for 15 min (total volume 0.75 ml), during which time pressure was measured via a small-volume pressure transducer (Cobe) in-line with the catheter. The signal from the catheter was amplified and relayed to a videotape recorder and, after analog-to-digital conversion, to a computer that had been programmed locally for data collection. The urethral catheter was then disconnected from the transducer so the bladder could be emptied by natural drainage, gentle suction with absorbent cotton pledgets, and gentle pressure on the bladder with a moist cotton-tipped applicator. Two baseline CMGs were obtained before inflammation, with a 5-min interval between them. The second measure was used as the preinflammation baseline. If the fluid removed from the bladder before or after either of the baseline measures was bloody (i.e., obvious hematuria), the data were not used in the final analysis. Of a total of 106 rats, this elimination process created a final group of 72 (experimental groups: 14 in metestrus, 13 in diestrus, 12 in proestrus, and 12 in estrus; oil controls: 13 in metestrus and 8 in estrus). Next, 0.5 ml of 50% turpentine in olive oil (or 100% olive oil in oil control group) was infused into the bladder via the urethral catheter and allowed to remain for 1 h. The bladder was then emptied, and three more saline CMGs were done at hourly intervals for a total of three postinflammation CMGs.Data analysis. MT was measured for each CMG. MT was defined as the volume at which the first contraction began and provided an index of bladder capacity. If a contraction did not occur within the 15-min saline infusion period, MT was assigned the highest value, 0.75 ml.
Repeated-measures ANOVAs with least significant difference post hoc tests were performed between all groups to determine statistical significance across time and between groups. The prevalence of hematuria before inflammation was analyzed across groups using the
2 test. Statistical significance was accepted at P
< 0.05.
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RESULTS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Additional study.
Because the saline infusion volume had been limited to 
0.75 ml to
avoid overinflating the bladder (7), it was often the case
that the bladder did not contract, particularly during the preinflammation baseline CMGs. This situation affected interpretation of potential estrous influences on bladder capacity of the uninflamed bladder. In other words, if the "real" MTs were, in fact, >0.75 ml
in some groups and not others, estrous influences would not have been
observed. To test whether MTs were >0.75 ml, CMGs were done on another
group of 45 rats with uninflamed bladders (9 in metestrus, 16 in
diestrus, 8 in proestrus, and 11 in estrus). In these rats there was no
limit on saline infusion; instead, saline was infused until two
micturition contractions occurred. Although, as expected, the overall
means in the extra baseline group were slightly higher than those in
the experimental baseline group (the MT of the 4 estrous stages of the
additional baseline group averaged 0.74 ml while the MT of the 4 estrous stages of the original group averaged 0.62 ml), the MTs in the
two baseline groups did not differ significantly from each other when
the estrous stages were grouped together or analyzed separately
(P = 0.951, grouped together; P = 0.917 during metestrus; P = 0.220 during diestrus;
P = 0.336 during proestrus; P = 0.849 during estrus).
Baseline CMGs.
There were no significant differences in MTs across the estrous cycle
in either of the two baseline groups (Fig.
2; P = 0.43 for the group
in which maximum volume was limited to 0.75 ml; P = 0.44 for the extra group studied with unlimited maximum volumes).
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Influence of turpentine. Control rats in metestrus and estrus that received intravesicular treatment with the oil solvent, rather than turpentine, showed a small but significant decrease in MT relative to baseline across time (Fig. 2; P < 0.01 for both groups). Overall, this hyperreflexia was significantly less severe than that which developed in rats after intravesicular treatment with turpentine (P < 0.001). Significant hyperreflexia in all experimental groups developed as early as 1 h after turpentine infusion and persisted to 3 h (Fig. 2).
Influence of estrous stage. MTs of metestrus and estrus oil controls rats did not differ significantly from each other during the baseline or the postinfusion CMGs. The amount of hyperreflexia that developed over the 3 h after treatment with turpentine in experimental rats was significantly greater in proestrus and estrus than in metestrus and diestrus (Fig. 2). MTs during metestrus and diestrus in rats treated with turpentine never differed significantly from the thresholds in metestrus or estrus oil control rats, with the exception of metestrus differing from estrus oil controls at 3 h after infusion (P < 0.01). In contrast, by 1 h after turpentine treatment and continuing through 3 h after treatment, rats in proestrus and estrus had significantly lower MTs than metestrus and estrus oil controls (P < 0.05). As inflammation progressed, further differences appeared. By 1 h after inflammation, rats in proestrus and estrus had significantly lower MTs than rats in diestrus (P < 0.05). By 2 h after turpentine treatment, rats in estrus had significantly lower MTs than rats in metestrus and diestrus (P < 0.05). By 3 h after treatment, rats in metestrus, proestrus, and estrus had lower MTs than rats in diestrus (P < 0.05).
Hematuria.
Whereas before inflammation 27.5-37.5% of rats in
metestrus, diestrus, and proestrus developed severe hematuria, only
11.1% of rats in estrus developed severe hematuria, demonstrating a significantly greater risk for hematuria in metestrus, diestrus, and
proestrus than in estrus (2, P = 0.025).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Whereas MTs in the uninflamed bladder were not influenced by estrous stage, there were significant estrous differences in the vulnerability of the bladder to become hyperreflexic after turpentine-induced inflammation. Specifically, rats in proestrus and estrus developed more severe hyperreflexia than did rats in metestrus and diestrus. In addition, the risk that the preinflammation CMG would produce hematuria was lower in estrus than in the other estrous stages.
Estrous influences on inflammation-induced hyperreflexia. The estrous variations in hyperreflexia induced by intravesicular turpentine observed here are not easily predicted by estrous variations in ovarian hormone levels. The amount of hyperreflexia was similar in proestrus and estrus, yet estrogen levels are high in proestrus but very low in regularly cycling rats in estrus (31). Similarly, the amount of hyperreflexia in diestrus and metestrus was low, yet there are moderately low estrogen levels in diestrus but moderately low levels of estrogen and progesterone levels in metestrus (31). This situation indicates that the mechanisms underlying estrous differences in hyperreflexia vulnerability are not a direct result of current ovarian hormone levels. Instead, the mechanisms may relate to differences in how ovarian hormones and neuroactive molecules interact over time throughout the ovarian cycle.
Nerve growth factor. One possible mechanism that could underlie inflammation-induced hyperreflexia during proestrus is hormonal modulation of the actions of nerve growth factor (NGF) on afferent fibers supplying the bladder or on the bladder smooth muscle itself. The NGF receptor trkA is expressed by 75-90% of sensory afferents innervating the urinary bladder (2), as well as by bladder mast cells; bladder mast cells invade the inflamed bladder, and their degranulation by NGF causes further inflammation (13). Furthermore, instillation of NGF into the bladder results in bladder hyperreflexia that is similar to the hyperreflexia produced by turpentine inflammation (7), although this effect may not occur in all rodent species (4). Furthermore, turpentine-induced hyperreflexia, as well as the referred hyperalgesia it produces, is reversed by systemic pretreatment with trkA-IgG fusion proteins that interfere with NGF's action (16, 23).
Recent evidence suggests that NGF, trkA, and p75 levels are hormonally regulated. Studies on dorsal root ganglion cells show that estrogen receptors (ERs) colocalize with trkA and p75 receptors and that trkA and p75 mRNA is increased during proestrus relative to other estrous stages (32), decreased after ovariectomy, and increased after estrogen replacement (24). Finally, increased numbers of ER-positive mast cells, which have the capability of releasing NGF in multiple systems (6, 9, 38), as well as elevated NGF levels are two characteristics of the disease interstitial cystitis, an inflammatory disease of the bladder that affects mainly women and has symptoms that fluctuate with the menstrual cycle (36).Choline acetyltransferase.
One possible mechanism that could underlie the inflammation-induced
hyperreflexia of estrus is the influence of estrogen on choline
acetyltransferase (ChAT) in central neural pathways that control
micturition. The ChAT gene contains an estrogen response element that
binds ER-
and ER-
(14). In some areas of the basal
forebrain, ChAT mRNA levels fluctuate across the estrous cycle, are
downregulated by ovariectomy, and are upregulated by exogenous estrogen
treatment (10, 11, 24), suggesting that estrogen and
acetylcholine increase and decrease together. A recent study showed
that acetic acid-induced bladder inflammation results in increased
bladder reflexes, which are inhibited by the muscarinic agonist
oxotremorine, and that this inhibition is reduced by the central
muscarinic antagonist atropine but not by the peripheral muscarinic
antagonist scopolamine methylbromide (34). These authors
further showed that the central cholinesterase inhibitor physostigmine
inhibited bladder reflex activity, but the peripheral cholinesterase
inhibitor neostigmine did not. Together, these data suggest that
inflammation-induced bladder reflexes could be inhibited centrally via
the muscarinic acetylcholine system. Because estrogen and, therefore,
acetylcholine are at low circulating levels during estrus, the ability
of this system to counter the hyperreflexic effects of bladder
irritation is limited, and the result would be hyperreflexia in estrus.
Metestrus and diestrus. The lack of hyperreflexia that was seen during metestrus and proestrus suggests that a mechanism exists to protect the bladder during these stages. Unlike the periovulatory time of proestrus and estrus, when estrogen, progesterone, luteinizing hormone, and follicle-stimulating hormone first surge to stimulate ovulation and then rapidly drop to basal levels, there are no large and rapid hormonal fluctuations during metestrus and diestrus. Instead, hormone levels of estrogen and progesterone (metestrus) or estrogen (diestrus) are slowly rising during these periods. It is therefore possible that gradual increases in estrogen or estrogen and progesterone protect the bladder during metestrus and diestrus while rapid hormonal fluctuations associated with proestrus and estrus contribute to the hyperreflexia. Consistent with this possibility is that long-term, but not short-term, estrogen replacement after ovariectomy decreases trkA mRNA levels in dorsal root ganglion neurons (19, 20). Similarly, in women with urinary symptoms of frequency or urgency, abnormal CMG findings are least likely to be observed during the luteal phase of their cycle (30), i.e., when estrogen and progesterone levels are slowing rising.
Lack of estrous influence on MTs in the uninflamed bladder. The finding here that bladder capacity of the uninflamed bladder does not vary with estrous stage indicates that, in the absence of an inflammatory challenge, the rapid changes in hormone levels associated with the ovarian cycle are not sufficient to influence the central or peripheral mechanisms that control bladder reflexes.
Risk of hematuria during CMGs. The risk of hematuria in the uninflamed bladder sometime during the initial catheterization and baseline CMG procedure was lower in estrus than in metestrus, diestrus, or proestrus. The latter three stages are characterized by higher circulating estrogen levels than in estrus (31). One possible explanation for the lower risk of hematuria in estrus could be estrogen's ability to promote vascularization (17). ERs have been found in the lower urinary tract of female rats, rabbits, and humans, specifically in the areas of the urethra and trigone, the entry point of the catheter (15, 28, 29). Furthermore, it has been shown in rats that estrogen administration after ovariectomy provokes metaplasia and hyperplasia as well as increased vascularization throughout most of the urinary tract, including the proximal urethra (8, 33). It is therefore possible that the urethra and trigone are less vascularized during estrus than during the other stages and that this lowered vascularization made the tissue less vulnerable to damage by the catheter.
Influence of anesthesia. The relevance of the estrous effects observed here to the conscious animal is uncertain. A wide range of drugs have been reported to affect micturition reflexes in rats (39, 26), whereas others do not (26). With respect to urethane, some studies have shown that it reduces bladder hyperreflexia induced by occlusion of the middle cerebral artery (40, 41). However, other studies using chronically implanted bladder catheters [rats (27)] or transurethral catheters [guinea pigs (21)] have shown that urethane has little effect on CMG parameters. In the present study, all groups were anesthetized similarly. Therefore, any influence of urethane would apply equally to all of them, thus eliminating urethane as a confounding variable, unless of course urethane's pharmacokinetics or pharmacodynamics are influenced by reproductive status, a question that remains to be addressed for many drugs (37).
Perspectives
Cystometry is one of the main clinical assessments carried out during urodynamic studies to aid diagnosis and treatment of symptoms of bladder dysfunction, such as urinary urgency and frequency. However, CMG findings can be inconsistent and do not always correlate with symptoms, as when MT or bladder capacity is found to be normal, despite the woman's report of severe urgency and frequency (1, 5). The findings here that the urethane-anesthetized female rat's vulnerability to inflammation-induced bladder hyperreflexia varies with estrous stage encourage further studies on how a woman's reproductive status at the time of cystometry might contribute to this discrepancy and to clinical variability (12, 25, 30, 35). Similarly, for basic research on animals, these findings indicate the importance of assessing the reproductive status of the experimental subjects when MTs are used to assess various aspects of lower urinary tract function after inflammation. Finally, the surprising finding that rats were protected from inflammation-induced bladder hyperreflexia during half of their estrous cycle warrants future studies on the mechanisms of this protection.| |
FOOTNOTES |
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Address for reprint requests and other correspondence: K. J. Berkley, Program in Neuroscience/Psychology, Florida State University, Tallahassee, FL 32306-1270 (E-mail: kberkley{at}psy.fsu.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 20 July 2001; accepted in final form 12 September 2001.
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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