Journal of Sex & Marital Therapy

ISSN: 0092-623X (Print) 1521-0715 (Online) Journal homepage: https://www.tandfonline.com/loi/usmt20

Transperineal Ultrasound Visual Feedback Assisted

Pelvic Floor Muscle Physiotherapy in Women With
Deep Infiltrating Endometriosis and Dyspareunia:
A Pilot Study

Simona Del Forno, Alessandro Arena, Martina Alessandrini, Valentina

Pellizzone, Jacopo Lenzi, Diego Raimondo, Paolo Casadio, Aly Youssef,
Roberto Paradisi & Renato Seracchioli

To cite this article: Simona Del Forno, Alessandro Arena, Martina Alessandrini, Valentina
Pellizzone, Jacopo Lenzi, Diego Raimondo, Paolo Casadio, Aly Youssef, Roberto Paradisi &
Renato Seracchioli (2020): Transperineal Ultrasound Visual Feedback Assisted Pelvic Floor Muscle
Physiotherapy in Women With Deep Infiltrating Endometriosis and Dyspareunia: A Pilot Study,
Journal of Sex & Marital Therapy, DOI: 10.1080/0092623X.2020.1765057

To link to this article: https://doi.org/10.1080/0092623X.2020.1765057

Published online: 24 Jun 2020.

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JOURNAL OF SEX & MARITAL THERAPY
https://doi.org/10.1080/0092623X.2020.1765057

Transperineal Ultrasound Visual Feedback Assisted Pelvic Floor

Muscle Physiotherapy in Women With Deep Infiltrating
Endometriosis and Dyspareunia: A Pilot Study
Simona Del Fornoa, Alessandro Arenaa, Martina Alessandrinia, Valentina Pellizzonea,
Jacopo Lenzib, Diego Raimondoa, Paolo Casadioa, Aly Youssefc , Roberto Paradisia,
and Renato Seracchiolia
a
Gynaecology and Human Reproduction Physiopathology Unit, DIMEC, S. Orsola Hospital, University of
Bologna, Bologna, Italy; bDepartment of Biomedical and Neuromotor Sciences, University of Bologna,
Bologna, Italy; cObstetrics and Feto-Maternal Medicine, DIMEC, S. Orsola Hospital, University of Bologna,
Bologna, Italy

ABSTRACT
A prospective study with the aim to evaluate the effects of pelvic floor
physiotherapy was conducted among women with deep infiltrating endo-
metriosis (DIE) and associated dyspareunia. At initial evaluation superficial
and deep dyspareunia were assessed using a numerical rating scale, and
levator hiatus area (LHA) was assessed with 3-D/4-D transperineal ultra-
sound. Women underwent five individual sessions of ultrasound visual
feedback assisted pelvic floor physiotherapy. One month after the therapy,
dyspareunia and LHA were reassessed and compared with pre-therapy
data. Pelvic floor physiotherapy seems to improve both superficial and
deep dyspareunia and pelvic floor muscle relaxation in women with DIE.

Introduction
Endometriosis is a chronic inflammatory disease, defined as the presence of endometrial glands
and stroma outside the uterine cavity. It affects up to 6% to 10% of reproductive-age women and
it is associated with chronic pelvic pain and/or infertility, due to long-lasting inflammation, adhe-
sions, and anatomical distortion (Clement, 2007; Giudice, 2010). The most severe form of the dis-
ease is deep infiltrating endometriosis (DIE), when endometriotic implants penetrate under the
peritoneal surface and can involve the rectovaginal septum, the uterosacral ligament and the para-
metria, the rectum, the ureters, and the bladder (Chapron et al., 2006; Uccella et al., 2018;
Seracchioli et al., 2008). The deep localization is strongly associated with severe chronic pelvic
pain, dysmenorrhea, dyspareunia, and dyschezia but also with bladder, sexual, and bowel dysfunc-
tion (Cornillie, Oosterlynck, Lauweryns, & Koninckx, 1990; Seracchioli et al., 2007; Kondo et al.,
2011), impairing health and quality of life of women during reproductive age (Cornillie et al.,
1990; Marinho et al., 2017). Various studies evaluated sexual activity in women with endometri-
osis, demonstrating the presence of sexual dysfunction, due to dyspareunia; lower number of sex-
ual intercourses per month; greater feelings of guilt toward the partner; and fewer feelings of
femininity, with consequent worsened quality of sexual life (Attaran, Falcone, & Goldberg, 2002;
Mabrouk et al., 2012; Fritzer et al., 2013; Di Donato et al., 2014). The close connection between
DIE and deep dyspareunia (pain in the vagina and in the pelvis during sexual intercourse) has

CONTACT Simona Del Forno simona.delfo@gmail.com; simona.delforno2@unibo.it Gynaecology and Human

Reproduction Physiopathology Unit, Department of Medical and Surgical Sciences, DIMEC, S.Orsola Hospital, University of
Bologna, Massarenti 13, 40138 Bologna, Italy.
ß 2020 Taylor & Francis Group, LLC
2 S. DEL FORNO ET AL.

been already investigated (Montanari et al., 2013; Ferrero et al., 2005), but only few studies
focused the attention on superficial dyspareunia (pain occurring in or around the vaginal
entrance) in women with endometriosis. In particular, Yong et al. demonstrated that endometri-
osis is a risk factor for the coexisting presence of deep dyspareunia and superficial dyspareunia/
provoked vesitibulodynia (Yong, Sadownik, & Brotto, 2015). Moreover, superficial dyspareunia
seems to be highly prevalent in women with endometriosis, especially DIE, and in most cases
appears to be concomitant with deep dyspareunia (Mabrouk et al., 2020).
Chronic pelvic pain syndromes like endometriosis may be associated with an increased pelvic
floor muscle tone, suggesting a role of the pelvic floor in the pathogenesis of the pain (Stratton,
Khachikyan, Sinaii, Ortiz, & Shah, 2015; Butrick, 2009). Three- and 4-D transperineal ultrasound
has been recently introduced for the evaluation of pelvic floor muscle (PFM) though the assess-
ment of the levator hiatus area (LHA), with the advantages of being a dynamic, safe, cheap, and
highly reproducible method (Youssef et al., 2016; Dietz, 2017). The LHA, which is delimited by
the puborectalis muscle, symphysis pubis, and inferior pubic ramus, represents a valuable param-
eter for the assessment of pelvic floor morphometry both at rest and during dynamic maneuvers
(PFM contraction and Valsalva maneuver), comparable to digital palpation (Van Delft, Thakar, &
Sultan, 2015; Youssef et al., 2016; Dietz, 2017).
Our group has previously analyzed the PFM using 3-D and 4-D transperineal ultrasound in
patients with endometriosis, demonstrating a reduced LHA in women with DIE compared to con-
trols (Raimondo et al., 2017) or to women with isolated ovarian endometriosis (Mabrouk et al.,
2018), suggesting the presence of an increased PFM tone, in particular in women with superficial
dyspareunia (Mabrouk et al., 2020). These findings encouraged us to propose to women with DIE
and associated dyspareunia pelvic floor physiotherapy as a new therapeutic strategy. Pelvic floor
physiotherapy is, in fact, a valid and noninvasive treatment available for the management of PFM
dysfunction (including pelvic pain syndromes, vestibulodynia, pelvic organ prolapse, urinary and
fecal incontinence, obstructed defecation, and sexual dysfunction) (Dietz, 2017; Arnouk et al.,
2017). Nonetheless, PFM physiotherapy has never been studied in women with endometriosis.
Our study aimed to evaluate the effects of PFM physiotherapy in women with DIE and dys-
pareunia using 3-D/4-D transperineal ultrasound as visual feedback technique.

Materials and methods

Patients
A prospective study was conducted between June 2018 and June 2019 at our tertiary-level referral
academic center for endometriosis. We enrolled 10 nulliparous women aged between 18 and 45
years with a clinical and sonographic diagnosis of DIE and associated dyspareunia. Diagnosis of
endometriosis was based on clinical and sonographic findings according to IDEA criteria.
(Guerriero et al., 2016). Data about age, body mass index (BMI), medical history, current or pre-
vious hormonal therapies, and previous surgery were collected. Exclusion criteria included history
of or current genital malignancy, history of or current pelvic organ prolapse, previous surgery for
DIE, congenital or acquired abnormalities of pelvis or pelvic floor, and other causes of chronic
pelvic pain. Women were counseled about the study before the enrollment and written informed
consent was obtained. The study protocol was approved by the local institutional Ethics
Committee (345/2017/O/Sper).

Gynecological examinations
Patients underwent two gynecological examinations, before the pelvic floor physiotherapy (first
examination) and one month after the end of the physiotherapy treatment (follow-up
 JOURNAL OF SEX & MARITAL THERAPY 3

examination). During the first examination, women were asked to rank endometriosis-related
pain symptoms (chronic pelvic pain, dysmenorrhea, dysuria, dyschezia, dyspareunia) with a
numerical rating scale (NRS; score 0–10), with a particular focus on dyspareunia, differentiating
between deep dyspareunia (pain in the vagina and in the pelvis during sexual intercourse) and
superficial dyspareunia (pain occurring in or around the vaginal entrance). Three-D and 4-D
transperineal ultrasound was performed to evaluate LHA at rest, at maximum pelvic floor con-
traction, and during maximum Valsalva maneuver by the same operator. Assessment of pain
symptoms and 3-D and 4-D transperineal ultrasound were repeated one month after the end of
pelvic floor physiotherapy. Moreover, at follow-up examination, women were asked to assess their
satisfaction with the treatment and the usefulness of ultrasonographic visual biofeedback during
the physiotherapy sessions using a 5-item scale (5 ¼ very satisfied, 4 ¼ satisfied, 3 ¼ neither satisfied
nor dissatisfied, 2 ¼ dissatisfied, 1 ¼ very dissatisfied) and a yes/no questionnaire, respectively.

Pelvic floor muscle examination and physiotherapy

A physiotherapist experienced in PFM dysfunction and physiotherapy performed a digital evalu-
ation of the PFM tone, during the first and follow-up examinations. Pubococcygeus and ischiococ-
cygeus muscle tone was assessed bilaterally at rest, during pelvic floor contraction, and relaxation.
After the first examination, women underwent 5 individual sessions of PFM physiotherapy of
30 minutes each at weeks 1, 3, 5, 8, and 11. During the first session, patients received information
about the pelvic floor anatomy and function, with the help of anatomical tables. In each session,
women underwent a Thiele massage, which consists of digital pressure and subsequent elongation
of the musculature in order to relax muscles, restoring normal pelvic tone and the ability to coord-
inate muscle behavior (Arnouk et al., 2017; Oyama et al., 2004). The Thiele massage has been found
to improve pelvic floor myalgia, reduce pain levels, and improve sexual function in individuals with
pelvic floor muscle hypertone, chronic pelvic pain, interstitial cystitis, and dyspareunia (Stein,
Sauder, & Reale, 2019; da Silva et al., 2017; de Souza Montenegro et al., 2010). All the physiother-
apy sessions were assisted with the visual feedback of transperineal ultrasound.

Transperineal ultrasound
After complete bladder emptying, 3-D and 4-D transperineal ultrasound was performed to evalu-
ate LHA at rest, at maximum contraction, and during maximum Valsalva maneuver by the same
operator using the OmniView-VCI technique, as previously described (Youssef et al., 2016). In
particular, 3-D ultrasound provides information about PFM at rest, while 4-D ultrasound pro-
vides information about the dynamic changes of LHA over time during PFM relaxation and con-
traction. All acquisitions were recorded with a Voluson E6 system (GE Healthcare, Zipf, Austria)
using a RAB 8-4-MHz volume transducer, high quality, and wide acquisition angle of 85 . The
convex volumetric ultrasound transducer was translabially positioned in the midsagittal plane,
with patients in lithotomy position, as previously described (Youssef et al., 2016; Dietz, 2017). All
volumes and areas were subsequently evaluated by another investigator, blinded to clinical and
sonographic data, using dedicated software (4-D View 14.4; GE Healthcare). All areas were meas-
ured by tracing the area bordered by the most medial part of the LHA, the symphysis pubis, and
the inferior pubic ramus (Figure 1).

Statistical analysis
Continuous variables were summarized as either mean (standard deviation) or median (range),
while categorical variables were summarized as counts and percentages. Comparisons of NRS
scores and LHA values before and after physiotherapy were performed using Chen’s version of
4 S. DEL FORNO ET AL.

Figure 1. Three-D transperineal ultrasound images of levator hiatus area at rest in the same woman before (upper image) and
after (lower image) pelvic floor physiotherapy, showing an enlargement of the area after the therapy. The dashed lines in yellow
indicate the levator hiatus area.

Johnson’s one-tailed t-test (t2-test), which is suitable for testing the mean of skewed distributions
with small sample sizes (Chen, 1995). The significance level was set at 0.05. All analyses were car-
ried out using Stata software, version 15 (StataCorp, 2017, Stata Statistical Software: Release 15.
College Station, TX: StataCorp LLC).

Results
Baseline characteristics, pharmacological treatment, localizations of the disease, and pain symp-
toms at first examination are reported in Table 1.
As shown in Table 2, mean NRS scores following physiotherapy were significantly reduced, both
for superficial dyspareunia (3.7 ± 3.0 vs. 7.6 ± 2.0, p ¼ 0.0027) and deep dyspareunia (4.4 ± 3.9 vs.
5.0 ± 4.1, p ¼ 0.0385). Comparison of LHA values before and after physiotherapy are illustrated in
Figure 2. As compared to pre-therapy data, mean post-therapy LHA was significantly larger at rest
(11.5 ± 2.4 cm2 vs. 10.4 ± 2.1 cm2, p ¼ 0.0395), at maximum PFM contraction (10.5 ± 2.1 cm2 vs.
9.5 ± 3.0 cm2, p ¼ 0.0278), and at maximum Valsalva maneuver (14.0 ± 2.5 cm2 vs. 12.0 ± 2.2 cm2,
p ¼ 0.0293; see Figure 2).
At follow-up examination, all women declared themselves very satisfied (8/10, 80%) or satisfied
(2/10, 20%) with the physiotherapy treatment, and the majority of women considered the
 JOURNAL OF SEX & MARITAL THERAPY 5

Table 1. Baseline characteristics, pharmacological treatment, localizations of the disease, and

pain symptoms at first examination.
Age (years), mean ± SD 33.4 ± 9.2
BMI (kg/m2), mean ± SD 23.0 ± 4.0
Pharmacological treatment, n (%)
None 2 (20)
Estroprogestinic 4 (40)
Progestinic 4 (40)
Localization, n (%)
Adenomyosis 7 (70)
Ovarian cysts 5 (50)
Anterior nodule 0 (0)
Posterior nodule 10 (100)
Pretreatment symptoms, n (%)
Dysmenorrhea 5 (50)
Chronic pelvic pain 7 (70)
Superficial dyspareunia 10 (100)
Deep dyspareunia 7 (70)
Dysuria 1 (10)
Dyschezia 4 (40)

Table 2. Mean ± standard deviation of superficial and deep dyspareunia measured with the numeric rating scale, before and
after physiotherapy.
Symptoms Before After D p
Superficial dyspareunia 7.6 ± 2.0 3.7 ± 3.0 –3.9 ± 3.4 0.0027
Deep dyspareunia 5.0 ± 4.1 4.4 ± 3.9 –0.6 ± 1.0 0.0385

ultrasonographic visual feedback during sessions useful (9/10, 90%). No women were lost at
follow-up.

Discussion
This is the first study to evaluate pelvic floor physiotherapy as a new therapeutic strategy in
women with DIE and dyspareunia. Pelvic floor physiotherapy seems to improve both superficial
and deep dyspareunia, as well as pelvic floor morphometry evaluated with 3-D and 4-D transperi-
neal ultrasound. In agreement with other authors (Giggins, Persson, & Caulfield, 2013; Dietz,
Wilson, & Clarke, 2001; Ariail, Sears, & Hampton, 2008), the ultrasonographic visual feedback
during physiotherapy sessions was useful for the majority of women. Moreover, all women
declared themselves very satisfied or satisfied with the physiotherapy treatment.
DIE may cause severe pain symptoms and dysfunctions with significant consequences on qual-
ity of life of affected women. In particular, dyspareunia has a high prevalence in women with
endometriosis (32% to 70%) and painful intercourses due to endometriosis occur in up to 2% to
4% of sexually active women, with a severe impairment of sexual health and love life and conse-
quent impact on psychological well-being. Despite that deep and superficial dyspareunia may
have different etiopathogenesis, most of the studies considered dyspareunia as a single entity,
without discriminating between the two symptoms or focused the attention only on deep dyspar-
eunia (Mabrouk et al., 2012; Ferrero et al., 2005; Pluchino et al., 2016). Yong et al. demonstrated
that endometriosis is a risk factor for the coexisting presence of deep dyspareunia and superficial
dyspareunia/provoked vestibulodynia (Yong et al., 2015). Furthermore, in another study from the
same group, the prevalence of pelvic floor tenderness was 40% in a cohort of patients with pelvic
pain, rising to 60% in the subgroup of women with endometriosis (Yong, Mui, Allaire, &
Williams, 2014). Mechanisms explaining the connection among endometriosis, pelvic floor ten-
derness, and dyspareunia are still unclear. Our group previously demonstrated the association of
an increased PFM tone in women with DIE, suggesting PFM physiotherapy as a possible
6 S. DEL FORNO ET AL.

Figure 2. Dot plot combined with box plot showing the distribution of levator hiatus area (LHA) at rest, at maximum pelvic floor
muscle (PFM) contraction and at maximum Valsalva maneuver, before and after physiotherapy.
Notes: The box represents the interquartile range; the triangle and bar inside the box represent the mean and median, respect-
ively; the whiskers represent the range.

therapeutic strategy for symptomatic women. Moreover, in another study, we detected a high
prevalence of the symptom in women with DIE (75.3%) and a correlation of the symptom with a
narrower LHA at 3-D transperineal ultrasound (Mabrouk et al., 2020). All these data prompted
us to treat dyspareunia with pelvic floor physiotherapy in the current view of a dedicated and
tailored therapeutic approach (Vercellini, 2015).
The improvement of painful symptoms remains one of the most important therapeutic targets
in women with endometriosis. Pelvic floor physiotherapy may be proposed as a valid and nonin-
vasive technique, which seems to improve dyspareunia, in particular superficial dyspareunia,
which may not benefit from surgery alone. Another important aspect in the management of
endometriosis is the improvement of women’s psychological well-being and quality of life. In this
perspective, the high grade of satisfaction reported by our women represents one of the major
strengths of the study and encourages us to carry on our research. This is the first study investi-
gating the role of pelvic floor physiotherapy in women with DIE. Moreover, the use of a noninva-
sive and reliable technique, the blinding of the examiner reviewing the sonographic data, and the
prospective design represent other strengths of the study. Our results, which are preliminary, can-
not be generalized because of the small sample size of the study population. This represents the
main limitation of the study, together with the absence of a control group. Moreover, 1-tailed
testing was employed, rather than the typical 2-tailed testing. A randomized controlled trial is
ongoing at our institution in order to evaluate the efficacy of pelvic floor physiotherapy in
women with endometriosis.
 JOURNAL OF SEX & MARITAL THERAPY 7

Conclusions
Our preliminary data suggest that pelvic floor physiotherapy may be useful to improve both
superficial and deep dyspareunia and PFM morphometry in women with DIE. Four-dimensional
transperineal ultrasound may be considered as a valid visual feedback technique to help women
during the physiotherapy sessions.

Acknowledgments
We acknowledge our psychologist Dr. Chiara Ferracuti for reading the paper and providing some advice.

Disclosure statement
The authors report no conflicts of interest and nothing to disclose.

ORCID
Aly Youssef http://orcid.org/0000-0002-9322-2184

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