NEWS IN PHLEBOLOGY - MINERVA MEDICA

EDIZIONI MINERVA MEDICA

NEWS IN PHLEBOLOGY

C. ALLEGRA - P.L. ANTIGNANI - E. KALODIKI

ANTIGNANI nuovo progetto.indd 1 01/08/13 13:52

ISBN: 978-88-7711-778-6

© 2013 – EDIZIONI MINERVA MEDICA S.p.A. – Corso Bramante 83/85 – 10126 Turin (Italy)www.minervamedica.it / e-mail: [email protected]

All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means.


Dear Readers,It was with great honor and pride that I received the assignment to write a few lines on this important

scientific publication in the phlebology field. Lately, we have been observing a quick development of new knowledge in phlebology. In fact, many pathophysiology, anatomical, diagnosis and therapy principles have deeply improved in

the past decades. For many years the vascular surgeons preferred to dedicate to the arterial pathologies rather than to the

venous disease, regarded as trivial. But, the new technologies such as the ultrasound Doppler, laser, radiofrequency, foam sclerotherapy,

the better quality of the elastic stockings and bandages associated to a reduction of invasive surgical pro-cedures, increased the interest in the phlebology field.

Recently published papers showed a high incidence of the venous pathology as well as a great social economic burden. These findings also contributed to influence doctors’ decisions and interest into phle-bology.

This book aims to present the new findings on the venous disease. It includes chapters on new ana-tomical and physiological findings, along with new challenges of microcirculation and the genesis of the disease. It also describes new diagnosis and treatment methods which range from the traditional to the most modern. Finally, the great venous complex syndromes and coagulation disorders, such as throm-boembolism, have been here discussed.

Therefore, this is an indispensable reference book also useful in phebology courses. My congratulations to the authors for this great project and their hard work.

Angelo Scuderi President of UIP

Foreword


I was very glad when Pier Luigi Antignani, on behalf of the authors of “News in Phlebology”, asked me to write the preface to this book.

Usually it is not easy to present the work of colleagues if you have been working with them for a long time and you share solid ties and mutual professional esteem.

However, in this case it is different, so it is easier to present a book that completes in such an exemplary way a scientific and training path that began many years ago.

The Italian College of Phlebology, of which I was appointed President this year, under the leadership of its founder Claudio Allegra began to focus on the scientific, social and cultural aspects of phlebology, centered on training and education.

“News in Phlebology” is, in this historical moment, the most comprehensive and updated text on training and information regarding venous and lymphatic diseases.The authors’ vast experience and the ability of such an international and outstanding “parterre” to captivate the reader are the premise of a worldwide success.

Stefano de Franciscis President of the Italian College of Phlebology

Preface


Giovanni Battista aGusVascular Surgery, Department of Clinical Sciences and Community Health, University of Milan, Italy

Claudio alleGraMaster of Vascular Diseases, S. Giovanni Addolorata Hospital, Rome, Italy

simone altoBelliDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

leonardo aluiGiCenter and School of Echography, Maggiore Hospital, Bologna, Italy

GiusePPe maria andreozziAngiology Care Unit of University Hospital of Padua, Italy

Pier luiGi antiGnaniVascular Centre, Nuova Villa Claudia, Rome, Italy

alessandro aPollonioAngiology - AUSL Viterbo, Italy

enriCo arosioVascular Rehabilitation Unit, Department of Medicine, University of Verona, Italy

Guido arPaiaOut-Patients Unit of Angiology, Desio and Vimercate General Hospital, Vimercate (MB), Italy

Clive BeGGsMedical Biophysics Laboratory, University of Bradford, UK

FaBrizio Benedetti-valentiniDepartment of Vascular Surgery, Sapienza University of Rome, Italy

GiusePPe BianChiniIsituto Dermopatico dell’Immacolata, Center of Vascular Anomalies, Rome, Italy

salvino BilanCiniVascular Diseases Studies Center JF Merlen, Frosinone, Italy

marisa BoniFaCioVascular Medicine, S. Giovanni Hospital, Rome, Italy

daniel BrandãoFaculty of Medicine, University of Porto, Hospital CUF, Porto, Portugal

matteo BuCalossiDepartment of Vascular Surgery, Valdisieve Clinic, Pontassieve (Florence), Italy

alBerto CaGGiatiVascular Medicine Study Center, Rome, Italy

daniele CamilliVascular Surgery, Policlinico Di Liegro, Rome, Italy

sante CamilliVascular Surgery, Private Surgery, Rome, Italy

GiusePPe CamPoreseUnit of Angiology, University Hospital of Padova, Italy

enriCo CaPotortiAngiology Unit, Hematology Oncology Department - AUSL, Viterbo, Italy

JosePh antony CaPriniNorthShore University HealthSystem, Evanston, IL, USA Department of Surgery, University of Chicago Pritzker School of Medicine, Chicago, IL, USA

marCo CardoneSan Giovanni Battista Hospital – ACISMOM, Rome, Italy

anita CarlizzaUnit of Angiology - S.Giovanni-Addolorata Hospital, Rome, Italy

FaBrizio CheGaiDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

antonio ChiaravallotiDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

authors


NEWS IN PHLEBOLOGY • AutHOrSviii

Claude GillotURDIA Anatomy Research Unit, University Paris Descartes, Paris, France

laura GreCoDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

GiorGio GuarneraUnit of Vascular Surgery, Istituto Dermopatico dell’Immacolata (IDI – IRCCS ), Rome, Italy

luiGi iraCeDepartment of Vascular Surgery, Sapienza University of Rome, Italy

evi KalodiKiVascular Surgery Department Ealing Hospital and Imperial College, London SW7 2AZ, UK - Thrombosis and Haemostasis Research Laboratory, Loyola University Medical Centre, Maywood, IL, USA

James laredoVein Center, George Washington University Hospital, Washington DC, USA

ByunG BoonG leeDepartment of Surgery, George Washington University, Washington DC, USA

GianFranCo lessianiInternal Medicine, Universty of Chieti, Italy

massimo luCChiVascular Diseases Studies Center JF Merlen, Frosinone, Italy

steFano manCiniDepartment of Medical, Surgical Sciences and Neurosciences, University of Siena, Siena (Italy)

armando mansilhaFaculty of Medicine, University of Porto, Hospital CUF, Porto, Portugal

FaBrizio marianiDepartment of Vascular Surgery, Valdisieve Clinic, Pontassieve (Florence), Italy

omBretta martinelliDepartment of Vascular Surgery, Sapienza University of Rome, Italy

raul mattassiClinical Institute Humanitas “Mater Domini”, Centre for Vascular Malformations, Castellanza (VA), Italy

eriCa meneGattiVascular Diseases Centre, University of Ferrara, Italy

sandro miCheliniSan Giovanni Battista Hospital - ACISMOM, Rome, Italy

lodoviCo miChelottiSan Giovanni Battista Hospital - ACISMOM, Rome, Italy

alessandro CinaDepartment of Radiological Sciences, “Agostino Gemelli” Hospital, Catholic University of Sacred Heart, Rome, Italy

GreGorio CinaMaster in Phlebology “Agostino Gemelli” Hospital, Catholic University of Sacred Heart, Rome, Italy

daniele CitraroDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

andré Cornu-thenardSaint-Antoine Hospital, Paris, France

Giovanni davìInternal Medicine, Universty of Chieti, Italy

Costantino del GiudiCeDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

miChelanGelo maria di salvoAngiology Unit, “Vittorio Emanuele” University Clinic, Ferrarotto Hospital, Catania, Italy

silvia d’onoFrioDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

seBastiano FaBianoDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

alessandro FaillaSan Giovanni Battista Hospital – ACISMOM, Rome, Italy

GiaComo FaillaAngiology Unit, “Vittorio Emanuele” University Clinic, Ferrarotto Hospital, Catania, Italy

PierGiorGio FalaPPaInterventional Radiology-Department of Surgery, Bambino Gesù Children’s Hospital IRCCS, Rome, Italy

Jawed FareedDepartment of Pathology and Pharmacology, Thrombosis and Haemostasis Research Laboratory, Loyola University Medical Centre, Maywood, IL, USA

alessandro FiorentinoSan Giovanni Battista Hospital – ACISMOM, Rome, Italy

roBerto FloreAngiology Department, Catholic University of the Sacred Heart, Rome, Italy

massimo GalluCCiUnit of Angiology, San Giovanni Addolorata Hospital, Rome, Italy


• iX

Giovanni simonettiDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

matteo steFaniniDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

FranCesCo stilloCenter of Vascular Anomalies, Guarnieri Clinic, Rome, Italy

mauro tamBuriniCenter and School of Echography, Maggiore Hospital, Bologna, Italy

lorenzo tessariFoundation Glauco Bassi, Trieste, Italy

mirKo tessariVascular Diseases Centre, University of Ferrara, Italy

Paolo tondiAngiology Department, Catholic University of the Sacred Heart, Rome, Italy

Jean-François uhlURDIA Anatomy Research Unit, University Paris Descartes, Paris, France

massimo vaGhiHospital “G. Salvini”, Centre for Vascular Malformations, Garbagnate Milanese, Milan, Italy

Paolo zamBoniVascular Diseases Centre, University of Ferrara, Italy

PierluiGi edGard molloUnit of Angiology P.O. Anagni ASL Frosinone, Italy

Giovanni monetaSan Giovanni Battista Hospital – ACISMOM, Rome, Italy

FederiCa natoniMolecular Biology Unit, Hematology Oncology Department - AUSL, Viterbo, Italy

dominique niKiDepartment of Diagnostic Imaging, Molecular Imaging, Interventional Radiology and Radiotherapy, University of Rome “Tor Vergata”, Italy

FranCesCo Paolo PalumBoVascular Surgery, Vulnologic Center, Palermo, Italy

rita PePeUnit of Angiology, S. Eugenio Hospital, ASL RmC, Rome, Italy

Gloria PessinaMolecular Biology Unit, Hematology Oncology Department - AUSL, Viterbo, Italy

FederiCa PomellaBranca Angiologia, Poliambulatorio Specialistico SUMAI ASL Frosinone, Italy

manlio PriorVascular Rehabilitation Unit, Department of Medicine, University of Verona, Italy

didier rastelSelurl Philangio, Grenoble, France


Contents

Part 1 – General ConCePts ..............................................................................................................................  1

1. Clinical embryology of the venous bed of the lower limbs  ...................................................................................  1Alberto Caggiati

2. anatomy of the venous system of the lower limb  ...............................................................................................................  5Jean-François Uhl, Claude Gillot

3. Physiology of the venous system of the lower limbs  ..................................................................................................... 15Salvino Bilancini

4. venous endothelium, endothelial inflammation and dysfunction  ........................................................... 17Paolo Tondi

Part 2 – ChroniC venous disease  ......................................................................................... 22

5. terminology, classifications and severity scoring  ................................................................................................................ 22Claudio Allegra

6. the CeaP classification and its evolution  ..................................................................................................................................... 28Pier Luigi Antignani

7. the role of scores in the management of chronic venous disease ......................................................... 33Pier Luigi Antignani

8. the magnitude of the problem  ....................................................................................................................................................................... 38Claudio Allegra

9. socioeconomic aspects  ................................................................................................................................................................................................. 40Claudio Allegra

10. etiopathogenesis  ..................................................................................................................................................................................................................... 41Massimo Lucchi

11. Patients with chronic venous disease-related symptoms without signs: prevalence and hypotheses on pathophysiology  .................................................................................................................. 46Claudio Allegra

12. non-invasive diagnosis  ................................................................................................................................................................................................... 51Pier Luigi Antignani

13. drug therapy .................................................................................................................................................................................................................................. 55Claudio Allegra, Pier Luigi Antignani

14. medical compression therapy in 2013: what’s new?  ........................................................................................................ 59André Cornu-Thenard, Didier Rastel

15. is there still space for open surgery?  ...................................................................................................................................................... 65Gregorio Cina

16. endovascular treatment procedure  ......................................................................................................................................................... 69Giovanni Battista Agus

17. ultrasound guided foam sclerotherapy  .............................................................................................................................................. 73Massimo Gallucci


NEWS IN PHLEBOLOGY • CONtENtSXii

18. varicose veins of the lower limbs: a comparison of endoluminal techniques “the choice”  .............................................................................................................................................................................................. 77LorenzoTessari

19. quality of life  ................................................................................................................................................................................................................................. 80Giuseppe Maria Andreozzi

20. Prevention  .......................................................................................................................................................................................................................................... 86Roberto Flore, Paolo Tondi

Part 3 – venous-lymPhatiC vasCular malFormations ................................................................................................................................................ 91

21. Classification  .................................................................................................................................................................................................................................. 91Byung Boong Lee, James Laredo

22. Clinical conditions  ................................................................................................................................................................................................................. 95Francesco Stillo, Giuseppe Bianchini

23. non-invasive diagnostic in malformations  .................................................................................................................................... 99Leonardo Aluigi, MauroTamburini

24. invasive diagnostics  ......................................................................................................................................................................................................... 107Alessandro Cina, Piergiorgio Falappa

25. medical therapy  ..................................................................................................................................................................................................................... 112Sandro Michelini, Marco Cardone, Alessandro Failla, Giovanni Moneta, Lodovico Michelotti, Alessandro Fiorentino

26. surgical treatment  ........................................................................................................................................................................................................... 117Raul Mattassi, Massimo Vaghi

Part 4 – venous thromBosis  .................................................................................................................. 121

27. definition  ......................................................................................................................................................................................................................................... 121Pier Luigi Antignani

28. Pathophysiology  .................................................................................................................................................................................................................... 124Giovanni Davì, Gianfranco Lessiani

29. effective thrombosis prophylaxis using individual risk assessment  .................................................. 128Joseph Antony Caprini

30. Particular aspects of venous thromboembolism and cancer  ..................................................................... 132Pier Luigi Antignani

31. thrombophilia  ........................................................................................................................................................................................................................ 137Gloria Pessina, Federica Natoni, Enrico Capotorti, Alessandro Apollonio

32. non-invasive evaluation  ........................................................................................................................................................................................... 143Pier Luigi Antignani

33. Pharmacologic treatment  .................................................................................................................................................................................... 147Evi Kalodiki, Jawed Fareed

34. Compression therapy  .................................................................................................................................................................................................. 151Guido Arpaia

35. surgical treatment  ........................................................................................................................................................................................................... 154Fabrizio Benedetti-Valentini, Ombretta Martinelli, Luigi Irace

36. quality of life and venous disease  ............................................................................................................................................................ 163Armando Manshila, Daniel Brandão

37. Primary and secondary venous thromboembolism prevention  ............................................................ 169Anita Carlizza

38. treatment of asymptomatic patients with thrombophilia  ............................................................................. 175Leonardo Aluigi, Pier Luigi Antignani


Xiii Contents

Part 5 – Post-thromBotiC syndrome  .............................................................. 181

39. Pathophysiology  .................................................................................................................................................................................................................... 181Marisa Bonifacio

40. Clinics  .................................................................................................................................................................................................................................................... 184Rita Pepe

41. non-invasive diagnosis  ............................................................................................................................................................................................... 186Giuseppe Camporese

42. recent advances in the management of post-thrombotic syndrome. are drugs indicated and efficient?  .......................................................................................................................................................... 192Claudio Allegra, Pier Luigi Antignani

43. Compression therapy  .................................................................................................................................................................................................. 196Fabrizio Mariani, Matteo Bucalossi, Stefano Mancini

44. Physical therapy  .................................................................................................................................................................................................................... 199Manlio Prior, Enrico Arosio

45. surgical therapy  .................................................................................................................................................................................................................... 204Sante Camilli, Daniele Camilli

Part 6 – venous ulCers  ................................................................................................................................................ 207

46. definitions and differential diagnosis  ................................................................................................................................................. 207Pierluigi Edgard Mollo, Federica Pomella

47. news in inflammatory and microcirculatory mechanisms  ............................................................................ 211Pier Luigi Antignani

48. medical therapy  ..................................................................................................................................................................................................................... 215Alessandro Apollonio

49. surgical therapy  .................................................................................................................................................................................................................... 218Giorgio Guarnera

50. dressings of venous ulcers  ................................................................................................................................................................................... 222Giacomo Failla, Francesco Paolo Palumbo, Michelangelo Maria Di Salvo

Part 7 – sPeCial session  ........................................................................................................................................... 225

51. invasive diagnostic imaging  ................................................................................................................................................................................ 225Giovanni Simonetti, Matteo Stefanini, Antonio Chiaravalloti, Silvia D’Onofrio, Laura Greco, Sebastiano Fabiano

52. Pelvic reflux varicose veins  ................................................................................................................................................................................. 238Salvino Bilancini

53. a novel plethysmographic method for assessment of cerebral venous drainage  .............................................................................................................................................................................. 240Paolo Zamboni, Erica Menegatti, MirkoTessari, Clive Beggs

54. Percutaneous treatment of deep vein thrombosis  ...................................................................................................... 249Giovanni Simonetti, Matteo Stefanini, Costantino Del Giudice, Simone Altobelli, Fabrizio Chegai, Sebastiano Fabiano

55. the treatment of varicocele and pelvic congestion syndrome   ............................................................. 256Giovanni Simonetti, Sebastiano Fabiano, Daniele Citraro, Dominique Niki, Antonio Chiaravalloti, Matteo Stefanini


1CliniCal embryology of the venous bed

of the lower limbsA. CAGGIATI

Part 1General ConCePts

■■ General

The development of the venous bed of the lower limbs is divided into three stages.

Early embryonic phase. – The first phase is char-acterized by the presence of a network of undiffer-entiated vessels that simultaneously supply blood to and drain blood from the precursors of the limb.1

Late embryonic phase. – Subsequently, the mi-crovessels functionally differ from each other in arteries and veins, while still retaining morpholog-ically similar walls.1 The course of the veins is slow to stabilize and undergoes continuous phenomena of regression and fusion, as well as the gemmation of new collectors. At the end of the first trimester of pregnancy, the venous vessels appear different

in structure and stabilized in the course. This will be maintained during both the intra- and extra-uterine life.

Fetal phase. – In the second and third trimes-ter of intrauterine life, the definitive veins undergo remodeling phenomena regarding their size, struc-ture of the wall and valvulization. These remod-eling phenomena will continue even after birth (Figure 1.1).

■■ early emBryoniC Phase, alias retiCular Phase

In the early embryonic stage, a network of un-differentiated vessels supply and at the same time drain the precursor of the limb (Figure 1.2).2 If a developmental arrest occurs at this stage, real ve-

Figure 1.1 �– �Development �of �the �venous �bed.Extra-truncular

malformations

Truncularmalformations

Anatomicalvariations

Undifferentiatedvessels

Differarantiatedbut instable vessels

Undifferentiatedvessels

with stable path

Vascularremodelling

Fetal period

Embryonicphase

1CliniCal embryology of the venous bed

of the lower limbsA. CAGGIATI


NEWS IN PHLEBOLOGY • GENErAL CONCEPtS2

nous trunks will not be formed as the vascular bed maintains the primitive undifferentiated reticular form. These vessels retain all of the evolutionary potential of mesenchymal cells and these malfor-mations may therefore appear or worsen at any age, even after birth (due to hormonal phenomena or local trauma). Since in these cases the main ve-nous trunks are free of significant alterations, these developmental defects are called extratruncular ve-nous malformations which must therefore be con-sidered real embryonic tissue remnants of meso-dermal origin that retain the characteristics of the mesenchymal cells (angioblasts).1 This explains why these lesions carry a significant risk of recur-rence, especially after partial excision or incom-

plete treatment. Besides hemodynamic impact, extratruncular lesions may be present as infiltrat-ing lesions possibly causing mechanical compres-sion to surrounding tissues and organs.

■■ late emBryoniC staGe, alias trunCular Phase

The first vessels that differentiate into veins de-velop along the margins of the limb bud and take their name of marginal veins, one medial and one lateral (Figure 1.3).3 A vascular central axis which accompanies the so-called “axial nerve”, (the sci-atic nerve for the lower limb) develops later. The artery and vein called “sciatic” course at the center of the limb bud and gradually assume the pre-dominant hemodynamic role. Subsequently the “pre-axial” nerve (ventrally to the sciatic) and the “post-axial” nerve (dorsally to the sciatic) also de-velop in the precursor of the limb, both accom-panied by a dense venous plexus (Figure 1.4). In particular, the pre-axial nerve is the femoral nerve and the femoral vein and the great saphenous vein will develop from the venous plexus that accom-panies it. The post-axial nerve corresponds instead to the lesser ischiatic nerve (alias, the cutaneous posterior femoral nerve) and the small saphenous vein and its thigh extension 4 will develop from the venous plexus that accompanies it. These three systems are connected by anastomoses from which important structures such as the deep femoral vein and popliteal artery develop. Once the pre-axial and post-axial systems develop, the hemody-

Figure 1.2 �– �The �network �of �undifferentiated �vessels �that �supply �and �drain �the �precursor �of �the �limb.

Figure 1.3 �– �Drawing �rep-resenting �the �vasculature �of �the �pig �embryo �upper � limb �at �a �stage �corresponding �to �the �fifth �week �of � intrauter-ine �life �in �humans �(modified �from: �Woollard, �1922).


1 • CLINICAL EmBrYOLOGY Of tHE vENOuS BEd Of tHE LOWEr LImBS 3

namic role of the axial system decreases and the axial vein itself regresses to the simple function of vena nervorum.

Note. The exact evolutionary sequence of the venous system is not well known. It should, in fact, be noted that most of the studies on venous embryology of the limbs were not performed on humans but on other mammals or other species. In some cases the upper limb has been studied. In addition, most of our knowledge comes from studies conducted more than a century ago, based on sporadic observations that were not repeated or verified over time.

The “truncular form” of venous malformations occurs when development stops during the “late stage” of the embryonic development. It consists of a persistent fetal remnant vessel (e.g. the sciatic or the lateral marginal veins) or as a defective vessel trunk (e.g. venous aneurysm, webs or stenosis of large veins). Truncular lesions do not grow or pro-liferate because the abnormal vessel lost the em-bryonic characteristics of the mesenchimal cells. In turn, truncular lesion may imply more serious hemodynamic consequences than extratruncular ones.

Fetal stage

During the second and third trimester of intra-uterine life the course of the veins is stable.

Changes occurring in this period affect vein morfology and functionality. These changes de-pend on hemodynamic, physiologic or pathologic phenomena, and may therefore continue even after birth. Already fifty years ago, the Swiss Anatomist Rickenbacher stated: “The definitive venous patterns develop to facilitate those segments of the venous net which represent favourable hemodynamic shunts. In turn, unfavourable shunts are demolished”. There-fore, these phenomena, therefore, determine the true final appearance of the venous bed, as it will be present in the adult. Changes occurring during this long period have not been considered by emi-nent venous embryologists.

The main changes that occur during the fetal period relate to the caliber, connections and valvu-lations of the definitive veins.

Variations in caliber are frequent in normal veins, especially in superficial ones.5, 6 As an exam-ple, the caliber of a normal saphenous vein ranges between 2 mm and 6 mm. Segmental hypoplasia and aplasia of the saphenous trunks are more fre-quent in varicose limbs. This led to the assumption that saphenous aplasia may be a predisposition to the onset of varicose veins.6

The great anatomical variability between indi-viduals concerns the pattern of connections of the main veins, the most striking example being the saphenous endings (Figure 1.5) where the connec-tions of tributaries with main trunks are crucial for the pathophysiology and treatment of varicose disease.7, 8

Finally, the greatest inter-individual differences concern the different number of valves found in normal veins.9, 10 Venous valves (VV) appear at 3-4 months of intrauterine life, especially in the vessels adjacent to the heart and muscles. The VV increase in number during the prenatal life. Differ-ences with regards to distribution and character-istics of VV in different areas of the human body start during the intrauterine life and continue after birth. In 1981, Maros pointed out that “[…] cer-tain findings suggest a reorganization of the venous valves which are frequently met in fetus. The close relation between hemodynamic mechanisms and the blood guiding structures may explain the changes (dis-appearance or persistence) of venous valves in some areas […]”. According to Kampmeier and Birch, the earliest valves of the lower extremity appear in the deep veins of the femoral trigone and popliteal fossa and in the upper end of the great saphenous vein.11

Figure 1.4 �– �Drawing �representing �the �topography �of �the �embryonic �veins �according �to �the �path �of �the �axial �nerve � �(sciatic).

C2C

3C4

C4

C5

C5

C6

C7

C8

T1T2

T10

T4

L1L2

S2S3S3

S2

L1L2

L4-S1L3

L4

S2S1 L5

PRE

POST

AX

IAL

PRE

POST

AX

IAL

Pre-axialarea

The axis(sciatic nerve)

Post-axialarea


NEWS IN PHLEBOLOGY • GENErAL CONCEPtS4

Despite the rare cases of the avalvulia syndrome (characterized by the absence of valves in both deep and superficial veins),12 it is quite common to observe great inter-individual differences in the number of venous valves in normal limbs. For ex-ample, the number of valves along the great saphen-ous vein varies between 7.3±2.3 and 2.4±0.83. Con-sidering the relevant hemodynamic role of valves in preventing venous insufficiency, it has been pos-tulated that a lesser number of valves may provoke varicose veins. Similarly, relevant difference in val-vulation have been reported in the area of the ter-minal saphena, common femoral and external iliac veins.7 For example, in 30% of limbs, no valves are located in the femoral or external iliac veins above the saphenous opening. Again, in about 30% of limbs, the pre-terminal valve of the saphenous vein is missing. Both conditions are relevant from the hemodynamic and surgical points of view.13

■■ ConClusion

Changes occurring during the fetal period were poorly considered by eminent embryologists. However, they are responsible for those differenc-es marked as interindividual, regarding the size, number, termination, connections and valvulation

of the main veins occurring even in normal limbs. These changes are of crucial importance in patho-logic conditions like varicose veins.

■■ reFerenCes

1 Lee BB, Bergan J, Gloviczki P, et al. Diagnosis and treatment of venous malformations. Consensus document of the International Union of Phlebol-ogy (IUP)-2009.International Union of Phlebology (IUP). Int Angiol 2009;28:434-51.

2 Lewis FT. The development of the veins in the limbs of rabbit embryo. Am J Anat 1905;5:1-120.

3. McClure CFW, Butler EG. The development of the vena cava inferior in man. Am J Anat 1925:35:331-83.

4. Barberini F, Cavallini A, Caggiati A. The thigh ex-tension of the small saphenous vein: a hypothesis about its significance, based on morphological, em-bryological and anatomo-comparative reports. Ital J Anat Embryol 2006;111:187-98.

5. Ricci S, Caggiati A. Does a double long saphenous vein exists? Phlebology 1999;14:59-64.

6. Caggiati A, Mendoza E. Segmental hypoplasia of the great saphenous vein and varicose disease. Eur J Vasc Endovasc Surg 2004;28:257-61.

7. Caggiati A, Bergan JJ, Gloviczki P, et al. Nomen-clature of the veins of the lower limbs: Extensions, refinements and clinical application. J Vasc Surg 2005;41:719-24.

8. Caggiati A, Bergan JJ, Gloviczki P, et al. Nomencla-ture of the veins of the lower limbs: an international interdisciplinary consensus statement. J Vasc Surg 2002;36:416-22.

9. Basmaijan JV. The distribution of valves in the fem-oral, external iliac and common iliac veins and their relationship to varicose veins. Surg Gynecol Obstet 1952;95:537-42.

10. Caggiati A, Phillips M, Lametschwandtner A, et al. Valves in small veins and venules. Eur J Vasc En-dovasc Surg 2006;32:447-52.

11. Kampmeier OF, Birch LF. The origin and develop-ment of the venous valves, with particular reference to the saphenous district. Amer J Anat 1927;38:451-99.

12. Lindvall N, Lodin A. Congenital absence of valves in the deep veins of the leg. Acta Dermato-Venereo-logica Scand 1961;41:45.

13. Caggiati A, Rosi C, Heyn R, et al. Age-related vari-ations of varicose veins anatomy. J Vasc Surg 2006; 44:1291-5.

Figure 1.5 �– �Variability �of �tributary �veins �number �and �connections �at �the �ending �of �the �great �saphenous �vein.


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