Vascular conflicts in andrology. Part 2. Lower level arteryovenous conflicts

Full Text

ILIAC VENOUS COMPRESSION SYNDROME

Compression of the left common iliac vein between the right common iliac artery and the fifth lumbar vertebra, and fibrous adhesions in it were first described by the German pathologist R. Virchow in 1851 [1]. R. Virchow noted that deep ileofemoral thrombosis occurred on the left five times more often than on the right. Fibrous adhesions (synechiae) in the compressed iliac vein represent an inevitable pathogenetic link in this disease (Fig. 1).

 

Fig. 1. Synechiae (adhesions) in the lumen of the left common iliac vein according to H. Mitsuoka et al. (2013)

Рис. 1. Шварты (синехии, спайки) в просвете левой общей подвздошной вены по H. Mitsuoka et al. (2013)

 

The left common iliac vein compression syndrome is often called the May – Thurner syndrome in the English language literature. In 2006, R.M. Burke et al. first described a right-sided May – Thurner syndrome in a 62-year-old patient who had deep venous thrombosis with pulmonary artery thromboembolism for four years; therefore, a filter was inserted into the inferior vena cava [2].

PREVALENCE

In 1908, J.P. McMurrich revealed an obstruction of the left common iliac vein in 31.25% of 32 autopsy cases [3] and in 30% of 57 autopsy cases [4]. In 1943, W.E. Ehrich and E.B. Krumbhaar detected an obstruction of the left common iliac vein in 23.8% of 412 autopsy cases. It is possible that minor obstruction was noted in 4% of cases and that other abnormalities in the iliac veins were registered in 1.8% of cases [5]. In 1957, R. May and J. Thurner in conducting the autopsy of 430 corpses revealed the pressing of the left common iliac vein by the right common iliac artery to the body of the fifth vertebra in 19–22% of cases [6]. D. Negus et al. (1968), while examining 100 patients registered obstruction of the left common iliac vein in 14% of cases [7]. N. Usui et al. (1978) detected tunica media hypertrophy and fibrous adhesions in the left common iliac vein in 50% of cases during the autopsy of 90 corpses and only in one of them was found in the right common iliac vein [8]. According to H.C. Baron et al. (2000), asymptomatic compression of the left common iliac vein in the adult population occurs in 16–20% of cases [9].

Thus, iliac venous compression is a widespread pathology.

CLASSIFICATION

From the clinician’s point of view, the compression of iliac veins can be thrombotic or non-thrombotic. Previously, physicians mainly focused on diagnosing and treating the thrombotic compression.

Variants of non-thrombotic iliac vein lesions (NIVL) were described by S. Raju and P. Neglen in 2006 [10]. The authors identified four variants of arteriovenous conflicts:

1) classical left-sided proximal compression due to left common iliac vein compression by the right common iliac artery (left proximal NIVL);

2) right-sided proximal compression due to compression of the right common iliac vein by the right common iliac artery (right proximal NIVL);

3) left-sided distal compression due to compression of the left external iliac vein by the left internal iliac artery (left distal NIVL);

4) right-sided distal compression due to compression of the right external iliac vein by the right common iliac artery (right distal NIVL).

A classification of morphological changes in the left common iliac vein in May – Thurner syndrome was proposed by U.B. Jeon et al. (2010), in which type I indicated focal compression of the right common iliac artery, type II indicated diffuse atrophy of the left common iliac vein, and type III indicated cicatricial obliteration of the left common iliac vein [11]. During the autopsy of 28 corpses (12 men and 16 women), with mean age of 82.5 years, H. Mitsuoka et al. (2013) established two variants of aortic abnormalities at the intersection of the right common iliac artery, where group A included complete or partial compression of the right common iliac artery by the left common iliac vein (low level aortic bifurcation) in 19 (67.9%) of 28 corpses and group B included compression of the inferior vena cava by the right common iliac artery (high-level aortic bifurcation) in 9 (32%) of the 28 corpses [12]. R. Englund (2017) examined and treated 61 patients with compression of the left common iliac vein, and proposed his classification based on the phlebography results (Table 1) [13]. The author also stated that the indication for angioplasty and stenting was stage 2 in 20% of cases, stage 3 in 100%, stage 4a in 71.4%, and stage 4b in 75% of cases.

 

Table 1 / Таблица 1

Classification of iliac venous compression according to R. Englund (2017) [13]

Классификация подвздошной венозной компрессии по R. Englund (2017) [13]

Signs	Stage 0	Stage 1	Stage 2	Stage 3	Stage 4a	Stage 4b
Compression	–	+	+	+	+	+
Obstruction	–	–	+	+	+	+
Collateralization	–	–	+	+	+	+
Fibrous adhesions	–	–/+	–/+	+	+	+
Adjacent venous segment	–	–	–	–	+	+
Distal venous segment (popliteal, femoral)	–	–	–	–	–	+

 

Analysis of MRI data of the inferior vena cava and small pelvic vessels, as well as contrast CT scan of the abdominal cavity organs in 225 patients with bilateral varicocele, varicose veins of the pelvic organs, and May – Thurner syndrome between the ages of 17 and 69 years (on average 33.8 years) enabled to propose a topographic and anatomical classification of variants for compression of the iliac veins [14]. According to this classification, there are six compression variants:

1) central proximal represented by high bifurcation of the aorta, when the right common iliac artery compresses the lower part of the inferior vena cava before it divides into iliac veins;

2) central distal represented by high bifurcation of the aorta, in which the right common iliac artery compresses the lower part of the inferior vena cava at the site of its division into the iliac veins;

3) left proximal, when the right common iliac artery compresses the left common iliac vein (May – Thurner syndrome);

4) left distal represented by compression of the left external and/or left internal iliac artery by the left external iliac vein;

5) right proximal represented by compression of the right common iliac artery by the right common iliac vein; and

6) right distal represented by compression of the right external and/or right internal iliac artery of the right external iliac vein.

S.A. Rizvi et al. (2018) from January 2013 to December 2014 performed 268 angioplasty surgeries and stenting procedures in 210 patients with non-thrombotic compression of the iliac veins. Bilateral stent placement was performed in 58 patients, and 173 (64.6%) surgeries were performed on women [15]. In addition, only in 42.6% of cases was the classic May – Thurner syndrome identified (Table 2).

 

Table 2 / Таблица 2

Localization of ileofemoral stenosis according to S.A. Rizvi et al. (2018) [15]

Локализация илеофеморального стеноза по S.A. Rizvi et al. (2018) [15]

Venous system segment	On the right, %	On the left, %
Proximal segment of the common iliac vein	24.3	42.6
Middle segment of the common iliac vein	11.3	27
Distal segment of the common iliac vein	7.8	1.6
Proximal segment of the external iliac vein	24.3	7.4
Middle segment of the external iliac vein	24.3	17.2
Distal segment of the external iliac vein	6.1	1.6
Proximal segment of the common femoral vein	1.7	2.5

 

When processing MRI data of the inferior vena cava and small pelvic vessels with 3D reconstruction, which does not determine the iliac compression localization but its severity, we made a decision on the feasibility of identifying the four stages of this disease [16] (Fig. 2).

 

Fig. 2. Stages of the ileal venous compression syndrome (May–Thurner Syndrome) according to MRI of the vena cava inferior and pelvic blood vessels with 3D reconstruction according to A.A. Kapto (2018): stage 1 – compression of the left common iliac vein; stage 2 – compression of the left common iliac vein with its dilatation; stage 3 – compression of the left iliac vein with the closure of the vessel walls in its central part and with its dilatation; stage 4 – pronounced and extended narrowing of the left common iliac vein lumen

Рис. 2. Стадии синдрома подвздошной венозной компрессии (синдрома Мея – Тюрнера) по данным МРТ нижней полой вены и сосудов малого таза с 3D-реконструкцией по А.А. Капто (2018): 1-я стадия — компрессия левой общей подвздошной вены; 2-я стадия — компрессия левой общей подвздошной вены с ее дилатацией; 3-я стадия — компрессия левой подвздошной вены со смыканием стенок сосуда в центральной его части и с ее дилатацией; 4-я стадия — выраженное и протяженное сужение просвета левой общей подвздошной вены

 

We identified four stages of the May – Thurner syndrome, based on the presence and severity of collateral circulation while performing the ileocavagraphy (Fig. 3) [16].

 

Fig. 3. Stages of May–Thurner syndrome according to ileocavagraphy depending on the presence and intensity of collateral circulation according to A.A. Kapto (2018): 1 – lack of contrast in the pelvic veins; 2 – contrasting of the pelvic veins; 3 – contrasting of the pelvic veins with the flow of contrast into the contralateral right common iliac vein; 4 – contrasting of the pelvic veins with the flow of contrast into the right common iliac vein and ascending lumbar veins on the left

Рис. 3. Стадии синдрома Мея – Тюрнера по данным илеокаваграфии в зависимости от наличия и выраженности коллатерального крово­обращения по А.А. Капто (2018): 1 — отсутствие контрастирования вен таза; 2 — контрастирование вен таза; 3 — контрастирование вен таза с перетоком контраста в контралатеральную правую общую подвздошную вену; 4 — контрастирование вен таза с перетоком контраста в правую общую подвздошную вену и восходящие поясничные вены слева

 

Clinical manifestations

The natural course of the iliac vein compression syndrome is a prerequisite for the development of ileofemoral thrombosis. In 1965, F.B. Cockett and M.L. Thomas described 35 patients with ileofemoral thrombosis in combination with compression of the iliac vein. The detailed clinical presentation of ileofemoral thrombosis in patients with the iliac vein compression syndrome is known as the Cockett syndrome, according to the name of the author who described the clinical presentation of the disease [17, 18].

Hypertension in the system of the left common iliac vein due to its compression between the right common iliac artery and the body of the fifth lumbar vertebra (May – Thurner syndrome) causes venous congestion of the pelvic organs (Fig. 4) and counterpulsation through the vein of the musculus cremaster into the uviform plexus of the testicle and its epididymis (ileospermic varicocele) (Fig. 5).

 

Fig. 4. Antegrade ileocavagraphy. Non-thrombotic compression of the left renal vein. Collateral circulation and pronounced venous congestion of the pelvic organs

Рис. 4. Антеградная илеокаваграфия. Нетромботическая компрессия левой почечной вены. Коллатеральное кровообращение и выраженное венозное полнокровие органов малого таза

 

Fig. 5. Retrograde phlebotesticulography of a patient with Nutcracker syndrome and May–Thurner syndrome. Contrasting the left common iliac vein through the cremaster vein

Рис. 5. Ретроградная флеботестикулография пациента с Nut­cracker syndrome и синдромом Мея – Тюрнера. Контрастирование левой общей подвздошной вены через кремастерную вену

 

B.L. Coolsaet (1980) presented the results of the angiographic examination of 67 patients with left-sided varicocele [19]. Three types of varicocele were identified using the intravenous angiography of the kidneys in the internal testicular and common iliac veins:

1) in the internal testicular vein;

2) in the extrafunicular veins, which was caused by obstruction of the common iliac vein where they flow;

3) in both systems simultaneously (Fig. 6).

 

Fig. 6. Classification of varicocele according to B.L. Coolsaet (1980): I – renospermic type; II – ileospermic type; III – mixed type

Рис. 6. Классификация варикоцеле по B.L. Coolsaet (1980): I — реносперматический тип; II — илеосперматический тип; III — смешанный тип

 

A.I. Neimark et al. (2013) proposed to distinguish two types of varicocele: 1) isolated varicocele with minimal hemodynamic disorders in the right testis without involvement of the prostate gland in the pathological process; and 2) varicocele in combination with pelvic congestion, in which the disorders affect not only the left testicle, but also the contralateral testis and prostate [20].

In both Nutcracker and May – Thurner syndromes, venous plethora of the prostatic plexus is noted. In May – Thurner syndrome, bilateral varicocele occurs as a rule, and according to TRUS, bilateral varicose veins of the prostatic plexus is noted (Fig. 7)

 

Fig. 7. Transrectal ultrasound imaging of the prostate of patient K., 33 years old, with bilateral stage 3 varicocele and May–Thurner syndrome. Prostate volume – 22.3 cm3 . The maximum diameter of the veins on the left is 10.9 and 18.3 mm, on the right – 12.5 mm. Chronic calculous prostatitis

Рис. 7. ТРУЗИ простаты пациента К., 33 года, с двусторонним варикоцеле 3-й стадии при синдроме Мея – Тюрнера. Объем простаты — 22,3 см³. Максимальный диаметр вен слева —10,9 и 18,3 мм, справа — 12,5 мм. Хронический калькулезный простатит

 

Diagnostics

The diagnosis of varicose veins of the pelvic organs is verified using TRUS in the presence of criteria such as varicose veins of the paraprostatic plexus of more than 5 mm and/or the presence of blow-out in the Valsalva test with duplex angioscanning [21]. In 2017, we proposed a classification of prostatic varicose veins (Table 3) [22].

 

Table 3 / Таблица 3

Ultrasound classification of varicose veins of the prostate according to A.A. Kapto (2017) [22]

Ультразвуковая классификация варикозного расширения вен простаты по А.А. Капто (2017) [22]

Stage	Stage of varicose veins	Maximum diameter of veins, mm	Blood flow velocity, cm/s	Blood flow velocity during Valsalva test, cm/s
1	Visible	<4	<3	<5
2	Significant	5–10	3–5	5–15
3	Pronoun­ced	>10	>5	>15

 

The iliac venous compression syndrome is verified by MRI of the inferior vena cava or small pelvic vessels, as well as CT of the abdominal organs with contrast enhancement, phlebography, phlebomanometry, and intravascular ultrasound. When processing MRI data of the inferior vena cava and small pelvic vessels and CT scan of the abdominal cavity organs with contrast enhancement, the criteria for iliac venous (vertebroarterial) compression are determined, which include determining the value of the lower lumbar lordosis angle (LLLA) (norm 134.33–136.76°) and diameter of the iliac vein tunnel (IVTD) (norm 4.18–4.50 mm) [23].

The diagnosis of venogenic erectile dysfunction is verified using the IIEF-5 (International Index of Erectile Function 5) questionnaire, as well as ultrasound pharmacodoplerography of the penis and dynamic pharmacocavernosography.

Treatment

Treatment of the left iliac vein compression syndrome (May – Thurner syndrome) is performed by X-ray surgical methods, and includes the following stages:

1) vein puncture (femoral, popliteal);

2) multi-projection intraoperative phlebography to reveal the collateral circulation of the left common iliac vein;

3) balloon angioplasty of the left common iliac vein;

4) implantation of a stent into the left common iliac vein;

5) post-dilation of the stented segment;

6) control phlebography revealing the patency of the left common iliac vein and the absence of collateral circulation.

X-ray surgical angioplasty and stenting of the iliac veins in the treatment of thrombotic disease have been used for the last three decades [24–27]. In addition, X-ray surgical angioplasty and stenting of the iliac veins in the treatment of recurrent varicocele and varicose veins of the pelvic organs in men (chronic pelvic pain syndrome, venogenic erectile dysfunction, chronic prostatitis) have been used since 2017 [28, 29].

Indications for angioplasty and stenting of the iliac veins in andrological patients include the following:

1) severe symptoms from pelvic organs (pain, dysuria, erectile dysfunction);

2) bilateral and/or recurrent varicocele;

3) varicose veins of the prostate gland degree II–III (maximum diameter of the veins of the prostatic plexus > 5 mm);

4) compression of the iliac veins revealed by MRI and phlebography;

5) collateral circulation of the iliac veins according to phlebography;

6) the pressure gradient in the areas distal and proximal to the stenosis according to frontal phlebomanometry is not less than 4 mmHg;

7) pathospermia and infertility as a consequence of the ileospermic type of varicocele.

From March 2017 to May 2019, we performed endovascular angioplasty and stenting in 70 patients with iliac venous compression, varicose veins of the pelvic organs, and bilateral varicocele with a positive clinical effect. The high clinical efficiency of X-ray endovascular angioplasty and stenting in patients with ileospermatic-type varicocele and varicose veins of the pelvic organs due to iliac venous compression enables to recommend this technique for use in such cases.

Currently, venous erectile dysfunction is not considered as an independent disease and, moreover, as a consequence of varicose dilatation of the dorsal vein of the penis. It is frequently caused by varicose veins of the pelvic organs. J.J. Keller et al. (2012), after analyzing more than 120,000 case histories, concluded that erectile dysfunction occurs five times more frequently in patients with varicocele. Moreover, the greatest prevalence of erectile dysfunction occurs at the age of over 60 years. According to Taiwanese researchers, previous surgical treatment for varicose veins of the spermatic cord reduces the risk of erectile dysfunction by approximately two times [30]. Varicose veins of the pelvic organs in men or pelvic phlebopathy syndrome, includes the following main clinical manifestations:

1) varicocele;

2) varicose veins of the skin of the scrotum, penis and lower extremities;

3) prostatopathy (chronic prostatitis, benign prostatic hyperplasia);

4) venous insufficiency of the penis with the development of venogenic erectile dysfunction;

5) hemorrhoids;

6) chronic pain syndrome;

7) dysuria in the form of obstructive and/or irritative symptoms [22].

The generally accepted methods of surgical treatment of venogenic erectile dysfunction in most cases are not effective enough; therefore, endophalloprosthetics is most often offered to these patients as the last chance to optimize sexual function. An alternative field in the surgical treatment of venogenic erectile dysfunction is X-ray surgical embolization of the prostatic plexus veins, which has been used all over the world since 1984. The effectiveness of the embolization of the prostatic plexus veins exceeds significantly the effectiveness of other surgeries for venogenic erectile dysfunction, reaching an average of 85% cases according to the literature. According to the surgical approach, all methods of embolization can be divided into two groups, namely antegrade and retrograde embolization of the prostatic plexus veins (Table 4).

 

Table 4 / Таблица 4 Methods of embolization of the veins of the prostatic plexus (indicating authors who first performed operation) Методы эмболизации вен простатического сплетения (с указанием авторов, впервые выполнивших операцию)
X-ray-guided surgical embolization of the prostatic plexus
Antegrade		Retrograde
Incision of v. dorsalis penis	Puncture in v. dorsalis penis	Access through v. femoralis (transfemoral)	Access through v. basilica (transbasilar)
D. Maiza et al. (1984, 1985) [31, 32]; P. Courtheoux et al. (1985, 1986) [33, 34]	J.J. Bookstein, A.L. Lurie (1988) [35]	H.H. Schild et al. (1993) [36]	A.A. Kapto, A.G. Kole­dinsky (2019) [37]

 

From our point of view, retrograde X-ray-guided surgical embolization of the prostatic plexus through the v. basilica (transbasilar approach) access is more convenient, since it does not involve the bending of the intravascular catheter in the ileocaval segment (Fig. 8).

 

Fig. 8. Retrograde X-ray guided surgical embolization of the prostatic plexus by access through v. basilica (transbasilar access). On the left, the prostatic venous plexus and cavernous bodies of the penis in the place of pathological venous drainage are contrasted, on the right – the absence of venous leakage after embolization with Gianturko spirals (Cook Medical, USA)

Рис. 8. Ретроградная рентгенохирургическая эмболизация простатического сплетения доступом через v. basilica (трансбазилярный доступ). Слева контрастируется простатическое венозное сплетение и кавернозные тела полового члена в месте патологического венозного дренажа, справа — отсутствие венозной утечки после эмболизации спиралями Gianturko (Cook Medical, USA)

 

A new promising field of treatment of this pathology is represented by hybrid and combined surgeries that enable to influence both the causes of venogenic erectile dysfunction and the pathological venous drainage formed as a result of these causes. X-ray guided surgical embolization of the prostatic plexus veins alone or in combination with testicular vein embolization and angioplasty and stenting of the iliac vein is possible only at the confluence of urology, andrology, and X-ray surgery. This circumstance led to the expediency of arranging thematic courses for the advanced training of doctors at the Department of Urology of the Center for Training of Medical Workers from 2019.

Additional information

The authors declare no conflicts of interest.

The study had no external funding.

Acknowledgments. The authors express gratitude to Professor Salman Khasunovich Al-Shukri and Professor Igor Valentinovich Kuzmin for their professional attitude and advertence to the problems of vascular andrology.

Author contributions:

A.A. Kapto created the study concept and design and wrote the manuscript. Z.V. Smyslova collected and processed the data, as well as processed the illustrations.

About the authors

Alexandr А. Kapto

Education Center of Medical Workers; RUDN University of the Ministry of Science and Higher Education of the Russian Federation; Multidisciplinary Medical Holding “SM-Clinic”

Author for correspondence.
Email: alexander_kapto@mail.ru

Candidate of Medical Science, Head of the Department of Urology; Associate Professor of the Department of Urology with Courses of Oncology, Radiology and Andrology; Head of the Andrology Center 

Russian Federation, Moscow

Zoja V. Smyslova

Education Center of Medical Workers; RUDN University of the Ministry of Science and Higher Education of the Russian Federation

Email: smyslova.zv@smpost.ru

Candidate of Medical Science, Assistant of the Department of Pediatrics; Director 

Russian Federation, Moscow

References

Supplementary files