Key words vascular - interventional procedures - vascular malformations
Introduction
Vascular anomalies (VAs) are a rare disease. According to the classification of the
International Society for the Study of Vascular Anomalies (ISSVA), as proposed by
Mulliken and Glowacki in 1982 [1 ], they can be divided into two main groups: vascular tumors and vascular malformations
[2 ]. Vascular malformations arise from dysmorphogenesis and mostly occur sporadically
but also may be based on germinal mutation [3 ]. They are also classified by their rheological characteristics as slow-flow and
fast-flow lesions [4 ]. Slow-flow lesions include capillary, lymphatic, and venous malformations, while
arteriovenous malformations, for example, are fast-flow lesions [3 ].
Simple slow-flow vascular anomalies, including venous malformations (VM) and lymphatic
malformations (LM), are usually present at birth and do not regress spontaneously.
They can affect multiple tissue levels (cutaneous, subcutaneous, intramuscular, fatty
tissue, and bone) [3 ]
[5 ]
[6 ]. Skin discoloration and swelling are main clinical symptoms [5 ]
[6 ]
[7 ]. While superficial VMs are often accompanied by a prominent blue skin discoloration,
LMs can show a red or brown skin color [6 ]. Especially VMs tend to grow during childhood and puberty [3 ]
[8 ]. In the case of thrombophlebitis and muscular or articular involvement, VMs can
cause pain [8 ]. The primary treatment is sclerotherapy [3 ]
[8 ]
[9 ]
[10 ]. For peripheral VMs involving extremities, compression garments are a main pillar
of conservative treatment [10 ]
[11 ].
Arteriovenous malformations (AVMs) are mainly congenital like VMs and LMs and seldom
acquired on a secondary basis, like uterine AVMs after caesarean section or trauma
[12 ]
[13 ]. Blushed skin, local warmth, and bruit are typical clinical findings of AVMs but
their clinical detection is often hampered in the urogenital and perineal region.
Complications, in the case of progression, can include ulceration or bleeding and
cardiac insufficiency. AVMs need close monitoring. Indication for intervention is
the prevention of local ulceration with infection and cardiopulmonary insufficiency
[3 ]
[9 ].
Urogenital and perineal vascular anomalies are very rare. In the literature there
is very little data on overall incidence. In general, they account for 2–3 % of all
VAs [14 ]
[15 ]
[16 ]
[17 ]. Diagnosis may be delayed because of the rather inconspicuous manifestation site
or the patients’ inability to disclose clinical and sexual symptoms to the treating
physician. The spectrum of findings can vary from cosmetic concerns to deformities
[15 ]
[18 ], including local swelling with physical impairment such as difficulty walking or
exercising [12 ]. Furthermore, hematuria or rectal bleeding may increase local discomfort when the
urinary tract or the rectum wall is involved [13 ].
Awareness of vascular anomalies of the urogenital tract and perineal region with their
pattern of spread, organ manifestation, and complications is therefore indispensable
for adequate diagnosis and treatment.
Methods and Materials
Out of all patients with vascular anomalies who presented to our Interdisciplinary
Center of Vascular Anomalies from 2014 to 2021, patients with vascular malformations
of the pelvis and urogenital tract were identified and included in this retrospective
analysis. For all patients consulted and treated in our Vascular Anomaly Center (VAC),
an informed consent sheet signed by the patient was mandatory and an ethical approval
decision from the local ethic committee was present. The clinical information, including
classification of the vascular malformation, anatomical location, symptoms, pain intensity,
imaging modalities, therapies prior to admission to the VAC and following treatment,
was taken from the clinical record. Venous malformations were classified according
to their Puig stage [19 ] and arteriovenous malformations by their Schobinger stage [20 ].
Depending on their anatomical site, the vascular anomalies were subdivided into three
major groups ([Fig. 1 ]).
Fig. 1 Overview of the classification of anatomical regions.Abb. 1 Überblick über die Einteilung der anatomischen Regionen.
The clinical symptoms were categorized into seven main groups: pain, swelling, bleeding,
physical impairment, sexual dysfunction, discoloration of the skin, and bruit/pulsation.
Sexual dysfunction included not only physical but also psychological problems like
self-consciousness. Pain intensity was classified on a numeric scale ranging from
0 to 10 for adults and on a visual scale for children. Imaging modalities for the
vascular anomalies included ultrasound, X-ray, computed tomography scan (CT), magnetic
resonance imaging (MRI), and transcatheter angiography. Finally, treatment options
were classified into three major categories: “no treatment at all”, “treatment” (sclerotherapy,
embolization, conservative therapy with compression garments, surgery) and “other
procedures” (diagnostic biopsy and follow-up appointments).
We compared and evaluated the differences between VMs and AVMs regarding variability
and number of symptoms and pain intensity. In a second step we assessed diagnostic
imaging tools and extracted treatment indication, based on the entire clinical information
available.
For the statistical analysis the Fisher’s exact test, Wilcoxon-Mann-Whitney-test,
and the Cochran-Armitage test for trend were used.
Results
Patients
Out of 537 patients, all 25 with congenital vascular malformations of the pelvis and
urogenital tract were included in the retrospective analysis: 10 female (40 %) and
15 male (60 %) patients with a mean age of 37.6 (ranging from 6 to 77 years).
Malformation Characteristics
The diagnosis was venous malformation in 10 (40 %) patients ([Fig. 2 ], [3 ], [4 ]), lymphatic malformation in 5 (20 %) patients ([Fig. 5 ]), and arteriovenous malformation in 10 (40 %) patients ([Fig. 6 ]). 34 % of malformations were located in the perineal/gluteal region, while 32 %
involved the lesser pelvis and the external genitalia each. One AVM (2 %) was located
in the kidney.
Fig. 2 Venous malformation of the left scrotum and the perineal and gluteal area. Axial
T2 TIRM (Turbo Inversion Recovery Magnitude) MRI sequence in a male patient with hyperintense
clusters of venous malformations.Abb. 2 Venöse Malformation des Skrotums sowie der Perineal- und Glutealregion links. Axiale
T2-TIRM (Turbo Inversion Recovery Magnitude)-Sequenz im MRT eines männlichen Patienten
mit hyperintensen Cluster einer venösen Malformation.
Fig. 3 Retroperitoneal venous malformation with encasement of the rectum in a male patient
on a sagittal T2 TSE (Turbo Spin Echo) MRI image. Compact hyperintense mass anterior
and posterior to the rectal fossa.Abb. 3 retroperitoneale venöse Malformation mit Ummauerung des Rektums bei einem männlichen
Patienten in einem sagittalen T2-TSE (Turbo Spin Echo)-MRT-Bild. Kompakte hyperintense
Masse ventral und dorsal im perirektalen Raum.
Fig. 4 Adolescent female patient with a venous malformation of the left labia majora and
the mons pubis.Abb. 4 venöse Malformation der Labia majora links und des Mons pubis bei einer jugendlichen
Patientin.
Fig. 5 Lymphatic malformation in the lesser pelvis of a male patient on an axial T2 TIRM
(Turbo Inversion Recovery Magnitude) MRI view with multiple hyperintense, partially
septate parts of an LM.Abb. 5 lymphatische Malformation im kleinen Becken eines männlichen Patienten auf einer
T2-TIRM (Turbo Inversion Recovery Magnitude)-Sequenz im MRT mit Darstellung einer
hyperintensen, multiseptierten Malformation.
Fig. 6 Arteriovenous malformation of the left gluteal area in a male patient with subcutaneous
and muscular involvement and mass aspect on an arterial phase CT scan after application
of intravenous contrast agent.Abb. 6 Darstellung einer arteriovenösen Malformation der Glutealregion links mit subkutaner
und intramuskulärer Ausdehnung bei einem männlichen Patienten in einer Computertomografie
mit arterieller Kontrastmittelphase.
The external genitalia were more often affected by VMs (58 %). In a sub-analysis comparing
AVMs to VMs, there was a significant difference (p = 0.0198) in the involvement of
the external genitalia, which was present in 7 VMs, whereas only one AVM demonstrated
involvement of this specific region. There was a slight predominance of the left side
of the body. 9 AVMs were classified as Schobinger stage II and one AVM was assigned
to stage I. Four VMs were classified into Puig stage I, three were assigned to stage II,
and another three were classified as stage III.
The distribution of anatomical location was almost homogenous between the lesser pelvis,
external genitalia, and perineal/gluteal region ([Table 1 ]). In the lesser pelvis and perineal/gluteal region, the distribution between VM
and AVM was almost equal with 6 AVMs vs. 5 VMs and 5 AVMs vs. 4 VMs. An overview of
the cohort characteristics is available in [Table 1 ].
Table 1
Overview of cohort characteristics.Tab. 1 Überblick der Kohorten-Charakteristika.
Total
AVM (n = 10)
VM (n = 10)
LM (n = 5)
Sex
n = 25
Male
15 (60 %)
6 (40 %)
5 (33 %)
4 (27 %)
Female
10 (40 %)
4 (40 %)
5 (50 %)
1 (10 %)
Imaging
n = 61
MRI
24 (39 %)
10 (42 %)
9 (38 %)
5 (21 %)
Ultrasound
20 (33 %)
5 (25 %)
10 (50 %)
5 (25 %)
CT
12 (20 %)
7 (58 %)
5 (42 %)
0
Diagnostic Angiography
5 (8 %)
4 (80 %)
1 (20 %)
0
Location
n = 38
Lesser pelvis
12 (32 %)
6 (50 %)
5 (42 %)
1 (8 %)
External genitalia
12 (32 %)
1 (8 %)
7 (58 %)
4 (33 %)
Perineal/gluteal Area
13 (34 %)
5 (38 %)
4 (31 %)
4 (31 %)
Others
1 (3 %)
1 (100 %)
0
0
Clinical Symptoms
The main clinical symptom in our patient cohort was pain (96 %). All of these patients
complained of continuous episodes of pain which were problematic and resulted in consultation
at our VAC. Patients with VMs and LMs suffered from a higher subjective pain level,
their mean intensity was 5.7/10 (VM) and 6.0/10 (LM), compared to patients with AVMs
who experienced an average pain level of 4.5/10. Physical impairment (76 %) and local
swelling (72 %) were also very common symptoms. Physical impairment included difficulty
or inability to walk an appropriate distance (more than 500 meters), to stand for
a prolonged period, to be seated in a vertical position, or to exercise without pain.
Less common symptoms included skin discoloration, bleeding complications of the vascular
malformation, bruit and pulsation, and sexual dysfunction. There were no documented
events of altered cardiac output or heart failure in connection with an AVM, based
on echocardiography examination results. [Table 2 ] gives an overview of the clinical symptoms per vascular malformation.
Table 2
Overview of clinical symptoms.Tab. 2 Überblick klinischer Symptome.
Symptom
Total
AVM (n = 10)
VM (n = 10)
LM (n = 5)
Pain
24 (96 %)
10 (100 %)
10 (100 %)
4 (80 %)
Swelling
18 (72 %)
5 (50 %)
9 (90 %)
4 (80 %)
Bleeding
4 (16 %)
1 (10 %)
3 (30 %)
0
Physical impairment
19 (76 %)
8 (80 %)
9 (90 %)
2 (40 %)
Sexual dysfunction
4 (16 %)
1 (10 %)
3 (30 %)
0
Skin discoloration
10 (40 %)
2 (20 %)
6 (60 %)
2 (40 %)
Bruit/pulsation
4 (16 %)
4 (40 %)
0
0
A sub-analysis comparing AVMs to VMs showed a significant difference in the number
of symptoms per patient (mean 3.0 (VM) vs. 1.7 (AVM); trend test p = 0.0129). Patients
with VMs complained of overall more symptoms compared to patients with fast-flow vascular
anomalies. According to the pathophysiological characteristics, solely patients with
AVMs described local bruit and pulsation as a clinical symptom.
Imaging Modalities
The most commonly used imaging modality was MRI in 24 (96 %) patients receiving cross-sectional
examination followed by ultrasound which was performed in 20 (80 %) patients. CT and
transcatheter angiography were significantly less common. None of the patients underwent
conventional X-ray as a diagnostic tool. Several patients presented at our VAC with
imaging studies that had not been performed in-house. These findings correlate with
the existing recommendation for imaging of vascular anomalies which has been established
and published previously [10 ]
[21 ]
[22 ]
[23 ].
Treatments
Before admission to the VAC, 12 external treatments were found in the records of our
patient population: 6 surgical interventions (3 VMs, 3 LMs), 1 sclerotherapy (VM),
3 transcatheter embolization procedures (AVMs) and 2 diagnostic biopsies (1 VM, 1
AVM). 14 (56 %) patients had not received any treatment previously.
After consulting the VAC, 14 (56 %) patients were conservatively managed or underwent
minimally invasive therapy. 5 of these patients had been treated for their vascular
malformation before at another institution, 4 with different therapeutic approaches.
At the VAC, 10 (40 %) patients underwent sclerotherapy ([Fig. 7 ]), 3 (12 %) received transcatheter embolization, and 1 (4 %) patient was managed
conservatively. Follow-up appointments were scheduled for 11 (44 %) patients who did
not require immediate treatment. Overall, there were 5 patients who had not undergone
therapy for their vascular malformation prior to consultation at the VAC and did not
have any indication for therapy, according to the VAC consultation.
Fig. 7 Periinterventional phlebography of a labial venous malformation of a female patient
prior to sclerotherapy.Abb. 7 periinterventionelle Phlebographie einer venösen Malformation der rechten Labie.
Complete therapeutic response after minimally invasive therapy, transcatheter embolization
for AVMs and sclerotherapy for VMs and LMs, was achieved in 9 (69 %) patients. In
3 (23 %) patients a partial response was documented. Only 1 patient with a VM reported
no clinical response to sclerotherapy. Clinical outcome was evaluated according to
patient findings and diagnostic findings during follow-up appointments, which had
been documented in the patient records.
The overview of the patients’ entire treatment history is provided in [Table 3 ].
Table 3
Overview of treatment history.Tab. 3 Überblick der therapeutischen Maßnahmen.
Total
AVM (n = 10)
VM (n = 10)
LM (n = 5)
Treatment before VAC n = 26
None
14 (54 %)
6 (43 %)
6 (43 %)
2 (14 %)
Sclerotherapy
1 (4 %)
0
1 (100 %)
0
Embolization
3 (12 %)
3 (100 %)
0
0
Surgery
6 (23 %)
0
3 (50 %)
3 (50 %)
Diagnostic biopsy
2 (8 %)
1 (50 %)
1 (50 %)
0
Treatment in VAC n = 25
Sclerotherapy
10 (40 %)
0
8 (80 %)
2 (20 %)
Embolization
3 (12 %)
3 (100 %)
0
0
Conservative
1 (4 %)
0
1 (100 %)
0
Follow-up
11 (44 %)
7 (64 %)
1 (9 %)
3 (27 %)
Results after therapy in VAC n = 25
Complete regression
9 (36 %)
3 (33 %)
4 (44 %)
2 (22 %)
Partial regression
3 (12 %)
0
3 (100 %)
0
No response
1 (4 %)
0
1 (100 %)
0
Recurrence
0
0
0
0
No follow-up possible
1 (4 %)
0
1 (100 %)
0
No treatment in VAC
11 (44 %)
7 (64 %)
1 (9 %)
3 (27 %)
In the sub-analysis comparing AVMs to VMs, follow-up appointments instead of immediate
minimally invasive therapy were significantly (p = 0.0198) more common in patients
with AVMs compared to patients with VMs. Therapy of VMs compared to AVMs required
frequent therapeutic sessions with a maximum of 4 sclerotherapy sessions compared
to 1 embolization treatment session for AVMs (p = 0.0055).
Discussion
With an incidence of 1.5 %, vascular malformations represent a rare disease [24 ], and the involvement of the urogenital tract and perineal region is even less common
with an incidence of only 2–3 % of vascular anomalies overall [15 ]
[16 ]
[17 ]. Over a period of 6 years, only 25 of 537 patients were diagnosed with a vascular
malformation of the pelvis or urogenital tract at our institution. Yet, one has to
assume that the number of undiagnosed urogenital vascular anomalies is much higher
due to the number of patients that remain undetected in the general clinical workflow,
unless they present at a dedicated center. Comparable data from Vogel et al. [17 ] describe 60 vascular malformations of the female external genitalia among 3186 female
patients with vascular anomalies, collected over 10 years via a database search. Kulungowski
et al. [16 ] report 105 vascular malformations of the male genitalia among 3889 male patients
over 15 years, also collected with a database search. In comparison to the literature,
our data was not extracted by a database search but is based on clinically symptomatic
patients that consulted our VAC.
The reported symptoms of our patient cohort are similar to the cohort of Willihganz-Lawson
et al. [15 ], who analyzed patients with genitourinary and perineal vascular malformations and
also reported functional problems and pain as the most common and leading symptoms.
Other than in our cohort, their mean age was 28 months with a predominance of the
female gender. Their cohort included patients under the age of 18 from the multidisciplinary
Vascular Anomalies Program at Seattle Children’s Hospital.
Clinical symptoms of urogenital and perineal vascular malformations include those
of other vascular anomalies but are often accompanied by increased physical and sexual
impairment which may lead to deterioration of the patient’s life quality. In female
patients, menses and pregnancy can worsen clinical symptoms [13 ]. In fact, in females with uterine vascular malformations, not only abnormal bleeding
but also pregnancy loss and fertility issues may be encountered [25 ]
[26 ]. This requires dedicated interdisciplinary management of women with vascular malformations,
especially during and after pregnancy. Unfortunately, there is hardly any literature
to be found on multicenter analysis of this patient population. A case report by Serrano
et al. indicates higher miscarriage rates in pregnant females with venous anomalies
due to higher coagulation activity in the form of localized intravascular coagulopathy
(LIC) which may progress to life-threatening disseminated intravascular coagulation
(DIC) [27 ]. However, with dedicated multidisciplinary management and close monitoring, successful
pregnancy outcomes can be achieved [28 ]
[29 ].
An interesting observation in our patient cohort was the significant difference in
the number of symptoms associated with the vascular malformations. Patients with VMs
suffered from at least 3 various symptoms, unlike patients with AVMs (clinical symptoms
overview in [Table 2 ]). A possible explanation could be the distribution of anatomic manifestation. Most
likely, symptoms are more extensive when the vascular malformation is localized at
the cutaneous or subcutaneous tissue level rather than intrapelvic. The external genitalia
were more often involved in the case of VMs than AVMs. Also, localized thrombosis
and thrombophlebitis, commonly observed by us in VMs, and infections in LMs, created
recurrent painful episodes whereas in AVMs, due to the high-flow characteristics,
clinical symptoms were hardly found in these patients.
A similar clinical symptom complex can be observed in patients with chronic pelvic
pain (CPP). There are several underlying causes of CPP. The spectrum of clinical findings
based on the underlying etiology has been published extensively [30 ]
[31 ]. One example of a vascular disorder not associated with vascular malformations leading
to CPP is the pelvic congestion syndrome ([Fig. 8 ]) in female patients. Although similar in clinical presentation, VMs and pelvic congestion
syndrome represent two fundamentally different entities. The underlying causes of
CPP must be differentiated from congenital vascular malformations because of the different
clinical management and therapeutic approach.
Fig. 8 Example of a female patient with clinical pelvic congestion syndrome. A Coronal venous contrast phase CT scan showing a dilated left ovarian vein [white
arrow] and dilated uterine venous plexus [blue arrow]. B Fluoroscopy after embolization of the left ovarian vein with coils.Abb. 8 Beispiel einer Patientin mit einem Pelvic-Congestion-Syndrom. A Coronare Abbildung einer venösen Kontrastmitteldarstellung in der Computertomographie
mit Darstellung der dilatierten linken Ovarialvene [weißer Pfeil] und einem dilatierten
parauterinen Venenplexus links [blauer Pfeil]. B Fluoroskopie nach Embolisation der linken Ovarialvene mit Coils.
The clinical assessment of pelvic vascular anomalies can be hampered by the fact that
urogenital symptoms are not immediately evident compared to vascular anomalies in
other regions of the body. Regarding the therapeutic spectrum, compression garments,
as a mainstay for the treatment of peripheral VMs, can be difficult. Indication for
minimally invasive treatment with sclerotherapy for VMs and LMs as well as transcatheter
embolization for AVMs also depends on the extent of clinical symptoms and the experience
of the treating interventional radiologist. The primary indication for treatment in
our study group was pain and physical impairment. Bleeding complications were hardly
encountered in our cohort. Overall, only 4 of 25 patients had a history of bleeding
complication related to the vascular malformation. Therefore, minimally invasive therapies
are usually performed in an elective setting. Vital indication for intervention is
very rare.
To ensure the right management of urogenital and perineal vascular malformations,
it is essential to detect the underlying vascular anomaly early and provide adequate
therapy. Management should be performed in a dedicated center. According to the extent
and location of the vascular malformation and the patient’s age and condition, the
integral therapy should include interdisciplinary teamwork with gynecologists, urologists,
hematologists, and interventional radiologists [32 ].
Despite the rarity of these vascular anomalies, underassessment should be avoided
and focused diagnosis and treatment should be initiated in a combined clinical effort.
Conclusion
In conclusion, our study gives an overview of a rare condition and the clinical presentation
of patients with vascular malformation of the pelvis and urogenital tract in order
to improve knowledge and patient management. Despite the fact that vascular malformations
of the perineal area and urogenital tract are a rare disease, especially urologists
and gynecologists might be confronted with VA patients in their daily clinical work.
Delayed diagnosis often leads to deterioration of clinical symptoms as well as inadequate
treatment resulting in progression of the vascular malformation. Nonetheless, it is
important to rule out inflammatory and tumorous causes. Subsequently, VA patients
should be referred to a VAC for management and adequate treatment.
