Chronic pelvic pain in congestion pelvic syndrome: clinical impact and electromyography pelvic floor activity prior and after endovascular treatment

doi:10.21203/rs.3.rs-3809569/v1

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Chronic pelvic pain in congestion pelvic syndrome: clinical impact and electromyography pelvic floor activity prior and after endovascular treatment

https://doi.org/10.21203/rs.3.rs-3809569/v1

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Background

To characterize clinical impact of endovascular treatment in Chronic Pelvic Pain (CPP) patients due to Pelvic Congestion Syndrome (PCS) and to assess the diagnostic value of surface electromyography (sEMG) study of pelvic floor musculature (PFM) in PCS patients pre- and post-endovascular treatment. Between January 2019 and July 2023, we studied consecutive patients who were referred for interventional radiology assessment and treatment to a tertiary trauma care Hospital, had evidence of non-obstructive PCS by Magnetic Resonance Imaging (MRI), had performed a sEMG of PFM and underwent endovascular treatment. The primary outcome was clinical, defined as change in symptoms severity after endovascular treatment. The secondary outcome was a difference in the sEMG values pre- and after endovascular therapy.

Results

We included 32 women (mean age 38 years). CPP was the leading symptom in 100% patients, followed by dysmenorrhea (75%) and post-coital pain (68.7%). Endovascular therapy included ovarian vein embolization in 28 patients (87.5%) and internal iliac vein embolization in only 2 patients (6.2%). After a median of 8 (range 6–10) months from endovascular treatment, 29 (90%) of patients reported improvement of the main symptoms, and 15 (46%) were symptom-free. The sEMG values didn’t show a statistical difference pre- and after PCS endovascular treatment.

Conclusions

Endovascular treatment appeared to be highly effective in CPP due to PCS and was associated with a low rate of complication. sEMG study could be useful in revealing alteration of PFM electrophysiology, but a difference pre and after embolization in PCS patient wasn’t demonstrated.

Sclero-embolization

Chronic pelvic pain

Congestion pelvic syndrome

Electromyography

Pelvic floor activity

Chronic pelvic pain (CPP) is a complex and disabling clinical condition among women of childbearing age; about one-quarter of women in reproductive age complain this clinical condition of greater one year in duration. The clinical symptoms are generally vague and inconsistent reflecting the multiple factors that have a role in its pathogenesis. The American College of Obstetricians and Gynaecologist define CPP as “pain of the pelvic region, sensed from the pelvic organs themselves that typically last more than 6 months”. Musculoskeletal, neurological and psychological conditions have been implicated in presentations of pelvic pain, but no diagnosis is made in over 60% of cases [1].

In 1948 Taylor firstly proposed a connection between the presence of pelvic varicosities and CPP [2]; this condition was classified as clinical entity, known as pelvic congestion syndrome (PCS), only after Beard et al. work of the 1980s, in which more than 90% of women with CPP presented in association pelvic varicosities [3]. However, more recent report described a prevalence of 39% of women with CPP and about 30% of these patients have a pelvic venous insufficiency related to PCS [4–5].

PCS is one of the main causes of CPP, accounting about 30% of these patients have a pelvic venous insufficiency. The pathophysiology of PCS pain includes the array of visceral, somatic and neurological pain generator [6]. In chronic lower extremities venous insufficiency, the pain state is related to abnormal vessel function [7]; Kaupilla 73 et al., about 4 decades ago, in a group of PCS patients affected by CPP demonstrated a higher rate of histological vascular anomalies (such as fibrosis, muscular hypertrophy and widened ovarian diameter) [8]. However, more recent views of pain states emphasize both peripheral and central contributors to nociception. Indeed, in some male affected by chronic pelvic pain, the presence of periprostatic pelvic varices have been described, suggesting a relationship between autonomic nervous system dysregulation of venous tone and some pelvic pain states [9]; similarly, the cerebral vasodilation seen in migraine headaches is thought to reflect neurological changes of the trigeminal system [10].

A correlation between CPP and dysfunction of the pelvic floor musculature (PFM) has been demonstrated; surface electromyography (sEMG) seems to be a useful tool to evaluate this kind of dysfunctions.

CPP are closely associated with dysfunction of the PFM and the sEMG turned out to be a useful tool to assess this kind of patients. sEMG is the electric signal recorded by means of electrodes attached to the surface of the skin produced by the sum of the extracellular potentials from the active muscle fibers beneath the electrodes. A greater power of the PFM activity has been demonstrated in CPP patients than in healthy women, especially when compared with mature/parous subjects; this difference is related to an increased number of motor units recruited and the muscle fatigue caused by overactivation of the PFM [11–12].

The aim of our retrospective observational study is to analyze the clinical impact of endovascular treatment in CPP patients due to PCS and to assess the diagnostic value of sEMG study of PFM in PCS patients pre- and post-endovascular treatment.

Patients. Between January 2019 and July 2023, 32 consecutive patients (mean age, 38 years; 29–60) with clinical diagnosis of CPP due to type 1 Greiner’s classification PCS underwent endovascular treatment in a major hospital of an Italian metropolitan city [13]. An Excel database was prospectively recorded and retrospectively analyzed. Data was collected from medical report, discharge letters and endovascular procedure report, including demographic information, relevant comorbidities and symptoms. Moreover, a clinical score, derived from a previously manuscript, was used to diagnose PCS and to evaluate clinical improvement [14]. The main demographic and clinical characteristics of patients are shown in Table 1.

Table 1

Main demographic and clinical characteristics of patients
Patients	32
Age (years), mean ± SD	38.0 ± 5.4
BMI, mean ± SD	21.8 ± 2.8
Number of pregnancies, mean ± SD	1.6 ± 0.8
Comorbidities
Uterine myomas, n (%)	5 (15.6)
Endometriosis, n (%)	2 (6.25)
Varicosis vein, n (%)	18 (56.25)
Pelvic cysts, n (%)	4 (12.5)
Deep vein thrombosis, n (%)	2 (6.25)
Acquisite Arteriovenous Malformation, n (%)	1 (3.1)

26 (81.2%) of 32 patients had previous pregnancies (mean number of deliveries:2; 1–3) and only 2 had previous history of endometriosis treated with laparoscopic surgery in 1 case and with hormones in both cases. The most prevalent symptoms were CPP (100% of patients), dysmenorrhea (75%), post-coital pain (68.7%), dyspareunia (50%) and leg varicosities (48.8%) (Table 2). A pre-procedural Magnetic Resonance Imaging (MRI) imaging was performed in all patients to exclude the presence of a PCS related to a nutcracker syndrome, a May-Thurner one or other secondary causes.

Table 2

Symptoms and PCS score at baseline of the study population
Symptoms	Baseline
Chronic lower abdominal pain, n (%)	32 (100)
Dysmenorrhea, n (%)	24 (75)
Postcoital pain, n (%)	22 (68.75)
Leg varicosities, n (%)	15 (48.8)
Vulvar varicosities, n (%)	3 (9.3)
Orthostatic pain, n (%)	10 (31.25)
Dyspareunia, n (%)	16 (50)
Back pain, n (%)	8 (25)
Hemorrhoids, n (%)	4 (12.5)
Depression, n (%)	2 (6.25)
Dysuria, n (%)	2 (6.25)
PCS score (mean ± sd)	7.2 ± 1.9

This study was approved by the local ethic committee and was conducted according to the Declaration of Helsinki principles. The human ethics review board at our institution approved the study design. Informed consent for data collection was obtained from all conscious patients. To characterize PFM activity a sEMG was carried out at baseline prior endovascular treatment and 6 months after it. The latency of the P40 response (n.v. 37.68 ± 2.60 msec), the P1-N1 amplitude (n.v.119 3.64 ± 1.01µV) and the latency of the R1 early response (n.v.<45 msec) were evaluated in the paraclitoral site (Fig. 1). Contraindications to procedure include active pelvic infection, severe contrast medium allergy, coagulopathy and pregnancy.

Endovascular technique. The procedure was undertaken in inpatient condition with mild analgosedation. Bilateral ovarian and iliac diagnostic subtraction phlebography was performed from femoral access to delineate the anatomy and identify the main vessels and collateral pathway, obtained with and without provocation such as Valsalva maneuver. Ovarian catheterization was achieved with a 5 Fr HET or another shaped tip catheter (COOK Medical, Bloomington, IN, USA) with a 0.038” lumen due to type of the coils utilized. In case where 0.018” micro-coils platform was utilized a 2.7 Fr Progreat Terumo (Terumo Medical, Tokyo, Japan) was used to delivery. A sandwich technique was preferred in all cases with pushable coils used after distal injection of 3% sodium tetradecyl sulphate (STS), prepared as a foam according to the Tessari method, with a maximum dose per procedure as 10 ml [15]. The complete occlusion with of the entire length of incompetent vein prevent possible future recanalization. Coils common sizes used range from 8 mm to 20 mm, generally oversized to prevent migration. Internal iliac veins were embolized with the same sandwich technique in cases where a venous reflux was confirmed at phlebography during Valsalva maneuver. Final phlebography control after embolization is undertaken to confirm vessel occlusion. In patients with symptomatic uterine myomas, a bilateral uterine artery embolization (UAE) was carried out in the same session. All procedures were performed by an interventional radiology radiologist with more than 5 years of experience. The primary cause of PCS was ovarian vein reflux highlighted in 29 patients (90.6%) (Fig. 2) and internal iliac vein reflux in 1 patient (3.2%); in 3 patients (9.3%) phlebography demonstrated a combination of both. Ovarian vein embolization was performed in 28 patients (87.5%) and iliac vein embolization in 2 patients (6.25%). Findings from pelvic phlebography with fluoroscopy and therapeutic details are summarized in Table 3.

Table 3

Diagnostic and procedural data of patients
Phlebographic findings
Ovarian vein reflux, n (%)	29 (90.6)
Internal vein reflux, n (%)	11 (34.3)
Vulvar vein reflux	1 (3.1)
Main pathology
Ovarian vein insufficiency, n (%)	28 (87.5)
Internal iliac vein insufficiency, n (%)	1 (3.2)
Both	3 (9.3)
Treatment
Ovarian vein embolization, n (%)	28 (87.5)
Left, n (%)	24 (75)
Right, n (%)	12 (37.5)
Bilateral, n (%)	8 (25)
Internal iliac vein embolization, n (%)	2 (6.25)
Left, n (%)	1 (3.25)
Right, n (%)	1 (3.25)

sEMG signal Recording Technique. sEMG signal was recorded in each patient from the left and right sides of the pelvic floor in a dorsal lithotomy position with adhesive electrodes. The study of the sacral evoked potentials was carried out with a manual bipolar stimulator with cathode in the paraclitoral site and recording using surface electrodes in the parietal region CZ (-2 cm) – FPZ according to the international 10–20 system, with square wave stimulation of the duration of 0.5 msec, intensity 3–4 times the sensory threshold, frequency 1.5 Hz, 151 impedance < 5 kOhm, bandwidth 1 Hz-3 kHz, 200 stimuli. The latency of the P40 response (n.v. 37.68 ± 2.60 msec) and the P1-N1 amplitude (n.v. 3.64 ± 1.01µV) were evaluated. The anal pudendal reflex was evaluated with a manual bipolar stimulator with the cathode positioned in the paraclitoral site and recording by means of coaxial needle electrodes from the external anal sphincter muscle. The latency of the R1 early response was evaluated (n.v.<45 msec).

Study endpoints and definition. Primary clinical success was defined as the change in symptoms severity following 6-months endovascular therapy. Symptoms relief was divided in three categories relating to its improvement: 1. Complete freedom from PCS symptoms; 2. Improvement with residual symptoms; 3. No improvement or changes of symptoms.

Secondary clinical outcome was defined as a difference in the sEMG study between the single parameters studied before and after endovascular treatment.

Technical success was defined as the successful endovascular procedure with no further evidence at imaging of reflux.

Safety outcome was defined as the prevalence of peri and post-operative complications, categorized according to CIRSE guidelines [16].

Follow-up and clinical outcome. Median follow-up was 8 months (range 6–10 months). Clinical improvement was demonstrated in 29 patients (90%) with 15 patients (46%) having complete resolution of symptoms. In 3 patients (9.3%), endovascular treatment did not improve symptoms. One patient had history of endometriosis with previous multiple surgical laparoscopic interventions. The second one had previous history of sacral trauma with associated a significant increase of R1 latency of the anal pudendal reflex, directly related with a neuronal impairment. The last one had previous history of urolithiasis with different previous urological procedure. In one case with no resolution of vulvar varices after ovarian sclero-embolization, the patient underwent to direct percutaneous STS foam sclerotherapy with complete resolution. The latency values of P40 response pre-treatment are slight reduced compared to normal value; compared to pre-treatment value, the latency of P40 response was slight increased after treatment but not with a statistical significance. An increase of P1-N1 signal amplitude in PCS was demonstrated; moreover, a reduction of signal amplitude after PCS treatment was demonstrated but with no statistical significance. There was no statistically difference before and after endovascular treatment in study of R1 latency of the anal pudendal reflex. The sEMG values pre and after embolization are summarized in Table 4. Complications due to endovascular procedure occurred in 4 patients (12.5%): in 2 patient (6.25%) partial coil migration into inferior vena cava in one patient and in left renal vein in another one was promptly retrieved by snaring techniques during endovascular procedure (Grade 1 CIRSE classification); 2 patient (6.25%) suffered mild symptoms of pelvic thrombophlebitis successfully treated with low molecular weight heparin (LMWH) (Grade 3 CIRSE Classification).

Table 4

The sEMG values evaluated pre- and after- PCS sclero-embolization.
sEMG signals	Pre-embolization	After embolization	p value
Latency p40 response	32.85 ± 1.40 msec	34.05 ± 2.30 msec	≥ 0.05
P1-N1 amplitude	4.26 ± 0.96 µV	3.96 ± 0.85 µV	≥ 0.05
Anal pudendal reflex	40 ± 2 msec	39 ± 3 msec	≥ 0.05

CPP has a worldwide population prevalence of 15% in female population between 18 and 50 years and in 61% of cases the etiology is unexplained. Labeling pelvic pain patients with single pathologic diagnoses such as PCS may hinder treatment efforts; however, a prevalence estimated around 30% of PCS in CPP patients has been demonstrated [17].

The pathogenesis of PCS is still unclear, but it has been demonstrated its multifactorial nature. Pregnancy hyper flow venous condition, in terms of gonadal and pelvic plexus dilated, due to estrogen level vasodilator effects could one of the pathogenetic factor involved. A main role, in addition, is related to a valve incompetence development and/or stenosis/obstruction onset of the draining veins [18]. The type 1 Greiner’s classification PCS treated in our study, that is a non-obstructive left ovarian vein insufficiency and reflux, is the most common pathophysiological cause with a prevalence of more than 50% of cases. In 2021 Meissner et al. proposed the Symptoms-Varices-Pathophysiology (SVP) classification of pelvic venous disorders: however, its effective role in determining treatment has still to be demonstrated [19]. A novel PCS management strategy proposed an association between a simple screening tool - the PCS score - that gynecologists and primary care physicians could use, and an accurate noninvasive imaging; this synergy, also used in our study, seems to improve the PCS diagnosis and successful rate treatment [14].

A non-invasive imaging study is mandatory in PCS management strategy, primarily to confirm the clinical suspect of PCS and secondly to exclude other CPP causes [17]. Ultrasound (US), both transabdominal and transvaginal, with colour Doppler imaging and Doppler spectral analysis should be used in PCS diagnosis. A dilated and tortuous pelvic vein (diameter > 6 mm), a slow blood flow (< 3cm/s) or reversal caudal flow, a dilated arcuate veins and polycystic changes in the ovaries are the ultrasound diagnostic criteria for PCS diagnosis [20]. MRI represent the first line of investigation, providing better imaging of the many causes of CPP and, due to the patient young age, should be preferred to Computed Tomography (CT) given the absence of ionizing radiation. MRI has shown a sensitivity and specificity of 88% and 67%, respectively, in demonstration of ovarian veins congestion. However, CT and MRI studies are both performed in supine position, thus being able to underestimate venous dilation compared to US and phlebography where provocative maneuvers could be employed. In our cases, a prior MRI study with demonstration of pelvic venous congestion for ovarian veins and MR angiography sequence with detection of vein dilatation and reflux was mandatory [21]. Catheter phlebography still remains the gold standard for PCS diagnosis, but its diagnostic role is reserved only in cases when noninvasive studies are inconclusive [22].

PCS treatments proposed and used in time are multiple and include conservative, psychological, medical, surgical and endovascular options, both in isolation and in combination. An RCT comparing combined hormone suppression and psychotherapy experienced sustained CPP relief with a > 50% reduction 262 in pain score [23]. A medical therapy, alone or in combination with other treatment, didn’t demonstrated a superior efficacy than another but only an increase of adverse symptoms if used in a long-term setting [24]. Surgical treatments include different alternatives including a mini-invasive laparoscopic approach for ovarian veins ligation to a more invasive one as hysterectomy and/or oophorectomy. Only one study published by Gargiulo et al. demonstrated an extraordinary 100% symptoms relief in 23 women treated with a laparoscopic ovarian vein ligation treatment [25]. Finally, hysterectomy, proposed when all other treatments have failed, showed a 22–33% of failure rate in clinical symptoms resolution [26].

Endovascular management of PCS is recommended with a level 2B evidence by the Society of Vascular Surgery: “We suggest treatment of pelvic congestion syndrome and pelvic varices with coil embolization, plugs, or trans-catheter sclerotherapy, used alone or together” [27]. Our study confirms the actual literature about the difference rate between technical success (almost always described above 95%) and clinical success (usually between 58% and 100%), regardless of the embolic agent. To date, there have not been any randomized study comparing clinical success using different embolic agents for PCS endovascular treatment. The choice of embolic agent is generally operator dependent with no different outcome described with use of a specific agent [17]. Moreover, such a high technical success with a low complication rate allows us to conclude that endovascular techniques are safe and effective in PCS syndrome tretment.

Clinical outcome is in line with previous literature and it could be considered as overall positive. 90% of patients showed a clinical improvement with 46% of patients having complete resolution of symptoms; in only 3 patients (9.3%), endovascular treatment did not improve symptoms. A recent meta-analysis demonstrated a short-term outcome similar to our study, showing a clinical improvement in 88% of patients and a 6–32% of patients that not experienced any symptom relief [28]. Another comprehensive review in 2018 stated that of the 1308 patients included in the study about 75% reported an early symptoms relief after embolization [29].

CPP and other clinical condition of the pelvic floor (i.e., fecal incontinence, organ prolapse, etc…) are closely associated with disfunction of the pelvic floor musculature PFM, so that sEMG could be a useful tool to assess patients’ clinical conditions [11]. In our study, the baseline value of the latency of p40 response and P1-N1 signal amplitude confirm that a slight muscular hypertonia is associated with CPP due to PCS; however, these values after PCS endovascular treatment point out that this correlation, is not directly connected with venous insufficiency, but there are subtle other pathologies related that should be studied further. The R1 latency of the anal reflex comparison show no difference between pre and after treatment; this type of evaluation is directly related with neuronal impairment that is highlighted in only one patient. The results obtained prove that sEMG can reveal alterations in the PFM electrophysiology associated with CPP related to PCS and provide clinicians with objective information that can help them to better evaluate CPP patients’ condition, thus allowing more efficient management of this complex syndrome. Future studies of PCS-related pelvic pain should also evaluate central mediators of vascular tone, perhaps by employing biofeedback or stress reduction. Anxiety and depression in this group of women has long been recognized with much debate as to whether this cause or effect. Farquhar et al. postulated that in a population of PCS patients, only women on combined hormone suppression and psychotherapy experienced sustained CPP relief, pointing out that overlapping neurological and hormonal factors can influence pain symptom expression [23].

Even though the sample size was homogenous, our study has several limitations. First, the sample size studied was small. Second, the evaluation only of patients with a type 1 Greiner’s classification PCS, makes the population more homogeneous, ruling out patients with type 2 and 3 of PCS syndrome, that asses more than 40% of patients with PCS. Third, all patients were recruited by only one interventional radiology center that could bring a selection bias. Last, the absence of a comparison healthy population studied with sEMG. However, given the absence in literature of a randomized controlled trials on management and treatment strategy of PCS with also sEMG study of PFM, our data may provide a reference for a future trial.

Currently, the management of women with chronic pelvic pain is suboptimal, with only 40% of affected women being referred to a dedicated specialist. Endovascular therapy should be chosen over a less effective medical (psychotropic, hormonal or venoactive drugs) and a more invasive surgical approach, highlighting that PCS is a multifactorial disease where vein disease is only one side of a more complex pathology [4]. The slight differences found between PFM activity in PCS patients prior and after endovascular treatment prove that sEMG could be a useful tool for a selected patients and more studies are necessary for identify its role in CPP clinical diagnosis and management.

This study was performed in line with the principles of the Declaration of Helsinki;
All human and animal studies have been approved by the appropriate ethics committee and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments;
Informed consent was obtained from all individual participants included in the study;
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request;
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript;
The authors have no relevant financial or non-financial interests to disclose;
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by G. F., C. M., N. R.. The first draft of the manuscript was written by C. F. and C. A. and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript;
The authors declare that they have no conflict of interest.

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Chronic pelvic pain in congestion pelvic syndrome: clinical impact and electromyography pelvic floor activity prior and after endovascular treatment

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