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21 Combined Role of Diagnostic Imaging Modalities
179
MRI and Lymphangiomatosis?
Lohrmann et al.28 confirmed the utility of MRI in 15 patients with diffuse lymphangiomatosis, using magnetic resonance lymphangiography with T1-weighted 3D
spoiled gradient-echo and a T2-weighted 3D-TSE sequence.
MRI and Lymphangiomas?
Because MRI accurately predicts subsequent intraoperative findings and accurately
demonstrates lymphatic architecture at different tissue levels, Liu et al.21 consider
MRI the diagnostic modality of choice in lymphangioma. In contrast, Dubois et al.29
suggest that Doppler ultrasound should be the initial imaging technique, and that MRI
can be used to evaluate the extent of the lesion(s) prior to treatment. Kuhlmann et al.30
preferred MR imaging when intravenous contrast material cannot be given for CT.
Lymphoscintigraphy and/or MRI?
Our estimation of the relative advantages and drawbacks of lymphoscintigraphic
and MRI imaging techniques is presented in Table 21.2. To summarize, MRI techniques offer good anatomical resolution, but are more expensive and up until now,
have been used in only relatively small series of patients. Additionally, the potential
renal toxicity of the imaging contrast agent must be considered. On the other hand,
lymphoscintigraphic techniques have been evaluated on very large series of patients
and are (relatively) less expensive, but require radiation exposure and offer reduced
anatomical resolution. Because MRI lymphangiography requires intradermal injections, we considered its functional contributions lower than those of the lymphoscintigraphic techniques where the tracer is injected subcutaneously,
be more useful in stage 0–2 lymphedema.
1,31
which may
Table 21.2 Lymphoscintigraphic and MRI techniques: the pros and cons
LySc SPECT CT LySc MRI Lymphangio MRI
Overall anatomical
contribution
Functional imaging
of the lymphatic system
Value established
in large series?
Potential limitations Pregnant? Obese, claustrophobia, pace-maker,
Irradiation + ++ /–/ /−/
Potential toxicity of
the imaging agent
Cost + ++ +++ ++++
+ ++ +++ ++++
+++ +++ +? ++?
++++ + ++ +?
metallic prosthesis…availability
of the imaging agent?
/–/ /–/ /−/ +? (kidneys?)
180 P. Bourgeois
Conclusions
Conventional oil-contrast lymphography has, in the past, been the mainstay for lymphatic imaging. Lymphoscintigraphy now more easily permits imaging of peripheral lymphatic vessels and provides insight into lymph flow dynamics. It is
indispensable for patients with known or suspected lymphatic circulatory disorders
to confirm the diagnosis and to delineate the pathogenesis and evolution of lymphedema. In several cases, the injection of radiolabeled colloids at the root of the
edematous limbs will demonstrate lymphatic collateralization pathways and provide useful information for the physical therapists. In patients with lymhadenodysplasia, with reflux and/or leakage of lymph and/or chyle and with suspected
abnormalities at the level of the thoracic duct, SPECT-CT lymphoscintigraphy is
useful in providing detailed anatomy of the abnormalities. PET-CT after injection of
18F-DG is efficacious in patients with secondary lymphedema and/or increased
serum tumor markers. Patients with a provisional diagnosis of peripheral lymphatic
dysfunction or idiopathic edema after lymphoscintigraphy should undergo, in select
cases, MR imaging to verify diagnostic accuracy, pinpoint the specific abnormality,
and help guide subsequent therapy, especially surgery.32 MR imaging will also complement lymphoscintigraphy in the monitoring and treatment of more complex lymphatic circulatory disorders, whereas CT will facilitate catheter-guided percutaneous
sclerosis or obliteration of specific lymphangiectasia or lymphangioma syndromes.
The choice of technique, either alone or in combination, must be made by taking
into account the clinical presentation and the diagnostic and/or therapeutic questions being addressed (Table 21.1).
References
1. Bourgeois P. Critical analysis of the literature on the lymphoscintigraphic investigations of the
limb edemas. Eur J Lymphology Relat Probl. 1996;6:1-9.
2. Szuba A, Shin WS, Strauss HW, Rockson S. The third circulation: radionuclide lymphoscin-
tigraphy in the evaluation of lymphedema. J Nucl Med. 2003;44:43-57.
3. Scarsbrook AF, Ganeshan A, Bradley KM. Pearls and pitfalls of radionuclide imaging of the
lymphatic system. Part 2: evaluation of extremity lymphoedema. Br J Radiol. 2007;80:219-226.
4. Pecking AP, Albérini JL, Wartski M, Edeline V, Cluzan RV. Relationship between lymphoscin-
tigraphy and clinical findings in lower limb lymphedema: towards a comprehensive staging.
Lymphology. 2008;41:1-10.
5. Bourgeois P, Munck D, Becker C, Leduc O, Leduc A. Reevaluation of a three-phase lympho-
scintigraphic investigation protocol for the lower limb-edemas. Eur J Lymphology Relat Probl.
1996;6:10-21.
6. Bourgeois P, Belgrado JP. Interest of lymphoscintigraphic investigations in the post-therapeu-
tic upper limb edemas [abstract]. Eur J Nucl Med Mol Imaging. 2009;36:S215.
7. Li LY, Zhao QX, Luo WC. An analysis of 30 cases of chylothorax and chyloperitoneum
[Article in Chinese]. Zhonghua Nei Ke Za Zhi. 1991;30:347-349, 382.
8. Howarth D, Gloviczki P. Lymphoscintigraphy and lymphangiography of lymphangiectasia.
J Nucl Med. 1998;39:1635-1638.
21 Combined Role of Diagnostic Imaging Modalities
9. Nishiyama Y, Yamamoto Y, Mori Y, et al. Usefulness of Technetium-99m human serum albu-
min lymphoscintigraphy in chyluria. Clin Nucl Med. 1998;23:429-431.
10. Pui MH, Yueh TC. Lymphoscintigraphy in chyluria, chyloperitoneum and chylothorax. J Nucl
Med. 1998;39:1292-1296.
11. Wells RG, Ruskin JA, Sty JR. Lymphoscintigraphy: lower extremity lymphangioma. Clin Nucl
Med. 1986;11:523.
12. Boxen I, Zhang ZM, Filler RM. Lymphoscintigraphy for cystic hygroma. J Nucl Med.
1990;31:516-518.
13. Okizaki A, Shuke N, Yamamoto W, et al. Protein-loss into retroperitoneal lymphangioma:
demonstration by lymphoscintigraphy and blood-pool scintigraphy with Tc-99m-human serum
albumin. Ann Nucl Med. 2000;14:131-134.
14. Kuang-Tao Y. Detection of chylothorax and cervical cystic hygroma in hydrops fetalis using
lymphoscintigraphy. Clin Nucl Med. 2006;31:205-206.
15. Marotel M, Cluzan R, Pascot M, Ghabboun S, Alliot F, Lasry JL. CT findings in 150 cases of
lower extremity lymphedema. J Radiol. 1998;79:1373-1378.
16. Wunderbaldinger P, Paya K, Partik B, et al. CT and MR imaging of generalized cystic lymp-
hangiomatosis in pediatric patients. AJR Am J Roentgenol. 2000;174:827-832.
17. Witte CL, Witte MH, Unger EC, et al. Advances in imaging of lymph flow disorders.
Radiographics. 2000;20:1697-1719.
18. Pecking AP, Mechelany-Corone C, Pichon MF. 1959–1999: from serum markers to 18-FDG in
oncology: the experience of the René-Huguenin Center [Article in French]. Pathol Biol (Paris).
2000;48:819-824.
19. Klerkx WM, Bax L, Veldhuis WB, et al. Detection of lymph node metastases by gadolinium-
enhanced magnetic resonance imaging: systematic review and meta-analysis. J Natl Cancer
Inst. 2010;102:244-253.
20. Lu Q, Xu J, Liu N. Chronic lower extremity lymphedema: a comparative study of high-resolu-
tion interstitial MR lymphangiography and heavily T2-weighted MRI. Eur J Radiol.
2010;73:365-373.
21. Liu N, Wang C, Sun M. Noncontrast three-dimensional magnetic resonance imaging vs lym-
phoscintigraphy in the evaluation of lymph circulation disorders: a comparative study. J Vasc
Surg. 2005;41:69-75.
22. Liu NF, Lu Q, Jiang ZH, Wang CG, Zhou JG. Anatomic and functional evaluation of the lym-
phatics and lymph nodes in diagnosis of lymphatic circulation disorders with contrast magnetic resonance lymphangiography. J Vasc Surg. 2009;49:980-987.
23. Notohamiprodjo M, Baumeister RG, Jakobs TF, et al. MR-lymphangiography at 3.0 T – a
feasibility study. Eur Radiol. 2009;19:2771-2778.
24. Lohrmann C, Foeldi E, Langer M. MR imaging of the lymphatic system in patients with lipe-
dema and lipo-lymphedema. Microvasc Res. 2009;77:335-339.
25. Lohrmann C, Pache G, Felmerer G, Foeldi E, Schaefer O, Langer M. Post-traumatic edema of
the lower extremities: evaluation of the lymphatic vessels with magnetic resonance lymphangiography. J Vasc Surg. 2009;49:417-423.
26. Molitch H, Unger E, Witte C, vanSonnenberg E. Percutaneous sclerotherapy of lymp-
hangiomas. Radiology. 1995;194:343-347.
27. Yu DX, Ma XX, Zhang XM, Wang Q, Li CF. Morphological features and clinical feasibility of
thoracic duct: detection with nonenhanced magnetic resonance imaging at 3.0 T. J Magn Reson
Imaging. 2010;32:94-100.
28. Lohrmann C, Foeldi E, Langer M. Assessment of the lymphatic system in patients with diffuse
lymphangiomatosis by magnetic resonance imaging. Eur J Radiol. 2009 Nov 11. [Epub ahead
of print].
29. Dubois J, Garel L. Imaging and therapeutic approach of hemangiomas and vascular malforma-
tions in the pediatric age group. Pediatr Radiol. 1999;29:879-893.
30. Kuhlman JE, Bouchardy L, Fishman EK, Zerhouni EA. CT and MR imaging evaluation of
chest wall disorders. Radiographics. 1994;14:571-595.
181
182 P. Bourgeois
31. Bourgeois P, Leduc O, Belgrado JP, Leduc A. Scintigraphic investigations of the superficial
lymphatic system: quantitative differences between intradermal and subcutaneous injections.
Nucl Med Commun. 2009;30:270-274.
32. Lohrmann C, Felmerer G, Foeldi E, Bartholomä JP, Langer M. MR lymphangiography for the
assessment of the lymphatic system in patients undergoing microsurgical reconstructions of
lymphatic vessels. Microvasc Res. 2008;76:42-45.
33. Bourgeois P, Munck D, Sales F. Anomalies of thoracic lymph duct drainage demonstrated by
lymphoscintigraphy and review of the literature about these anomalies. Eur J Surg Oncol.
2008;34:553-555.
Chapter 22
Oil Contrast Lymphangiography
J. Leonel Villavicencio
Ever since the lymphatic vessels were discovered incidentally in 1622 by Gasparo
Asselius, Professor of Anatomy at Pavia University in Italy,1 the anatomy and physiological functions of these tiny structures have posed a challenge to the investigators
because of their small size and the difficulties involved in visualization. Contrary to
what happens in the arterial and venous systems, where visualization is relatively easy,
visualization of the lymphatic system has been technically challenging. After Asselius’s
description, the lymphatics were the focus of attention of many investigators who used
injections of mercury into cadavers to gain as much knowledge as possible about these
intriguing little vessels. At the Medical–Surgical Military Academy of Austria, founded
in 1785 by Joseph II, 1,192 beautiful anatomical wax models, crafted in Florence at the
end of the eighteenth century, are on public display. Here, unique models of wholebody dissections of the lymphatic system created by the Italian artists can be admired.
The complex network of small lymphatic capillaries that absorb fluid from
the interstitial space was described by Casley-Smith, who called them “initial lymphatics.”2 They are formed by a single layer of 10 to 60 mm endothelial cells. These
lymphatic capillaries drain into larger valved channels of the dermis and subcutaneous tissues that run along the veins above the muscular fascia. Visualization of the
initial lymphatics was the subject of the 1984 International Symposium in Zurich,
Switzerland, and a publication edited by A. Bollinger, J. Partsch, and J.H.N. Wolfe3
in which demonstration and functional evaluation of superficial lymphatics was
explored using fluorescence microlymphography4 and Iotasul (indirect lymphography).5 Of course, all of these efforts came after the pioneering work of Professor
John B. Kinmonth of Saint Thomas Hospital in London, of whose life the lymphatic
system, its visualization by lymphography, its classification, and its function became
J.L. Villavicencio
Distinguished Professor of Surgery, Department of Surgery,
Uniformed Services, University School of Medicine,
Director Emeritus Venous and Lymphatic Teaching Clinics,
Walter Reed Army and National Naval Medical Centers,
Washington DC and Bethesda, MD, USA
B.-B. Lee et al. (eds.), Lymphedema,
DOI 10.1007/978-0-85729-567-5_22, © Springer-Verlag London Limited 2011
183
184 J.L. Villavicencio
the focus. In the introduction to the first edition of his book in 1972, it is compelling
to read the following citation:
The chief author had the good fortune to work in the years after the war with Professor Sir
James Patterson Ross at St Bartholomew’s Hospital. At that time there was no satisfactory
clinical method of investigating lymphatic function. Pure speculation reigned. One eminent
authority on vascular diseases even stated that “he doubted if the lymphatics existed, and if they
did they were of no importance.” Another said that such research was valueless: “you won’t
find anything out and if you do, no-one will believe you.” But Sir James was encouraging.
When on a ward round at Bart’s he saw a picture of one of the first successful deep lymphangio-
grams and he said, “don’t lose that slide it is going to be very important.” Much of our early
studies were on patients with lymphedema with aplasia or hypoplasia of the lymphatics. We did
not know it but we had chosen the most difficult subjects for lymphography. Often we felt like
the poet W.B. Yeats, “the fascination of what is difficult has dried the sap out of my veins.”
6
After the groundbreaking investigations of Hudack and McMaster, who injected
patent blue dye intradermally and demonstrated small lymphatics in the skin,7
Servelle in 1944,8 and Kinmonth in 19529 explored the use of patent blue in the
experimental and clinical visualization of the lymphatic vessels. This pioneering
work culminated with the description of the technique of lymphography as a preliminary step to the visualization of the dermal and subcutaneous lymphatics.
Cannulation of these vessels and injection of contrast materials produced some of
the first radiological imaging of the lymphatic vessels. Kinmonth devoted the following 25 years of his life to the study of the lymphatic system and the development
of techniques of lymphatic visualization that produced the first lymphangiographic
and clinical classification of lymphedemas. By the time he published his book, he
had performed more than 2,000 direct lymphographies. This author had the privilege to have met Professor Kinmonth and to have worked with him in 1957 during
a visit to his close friend, and my mentor, Professor Richard Warren of the Peter
Bent Brigham Hospital in Boston. Professor Kinmonth gave me a small bag containing several grams of patent blue violet powder (also known as Patent Blue V,
Alphazurine 2G ) with detailed instructions on how to prepare an 11% sterile aqueous solution of the vital dye whose capacity to diffuse into the tissues and be
absorbed by the lymphatics was higher than that of other vital dyes. Professor
Kinmonth’s visit sparked my life-long interest in the lymphatic system and my
efforts to study the lymphatic system in different edema-producing conditions. An
apparatus of my own design to measure the intra-lymphatic pressure (lymphomanometer) and perform direct visual and radiological lymphography was constructed
and used in different types of lymphedema (Fig. 22.1). The results of my investigations on lymphatic pressure are beyond the scope of this chapter.
Visual Lymphography and Radiological Lymphography
Visual lymphography is performed by injecting 0.1–0.3 mL of patent blue dye
through a fine needle (27-gauge) into two to three interdigital spaces of the foot or
hand. Gentle massage and active movements of the foot/hand are recommended to
22 Oil Contrast Lymphangiography
a
b
Fig. 22.1 (a) Direct
lymphography after
lymphomanometry. This
photograph shows a
lymphatic vessel cannulation
on the dorsum of the foot
after injection of 0.2 mL of
aqueous solution of patent
blue violet into each of three
interdigital spaces of the foot.
(b) A 1-mm ID diameter
micro-pipette attached by one
end to a plastic tube
connected to a syringe and a
U water manometer and by
the other to a 30-gauge
needle. After the lymphatic
pressure determination, a
slow injection of ultrafluid
lipiodol was performed by
gradual turning of the metal
piston on the syringe plunger
185
facilitate dye absorption and proximal progression. In patients with lymphatic truncal or nodal obstruction, a fine reticular cutaneous pattern (dermal backflow) may
appear 5–15 cm proximal to the site of injection (Fig. 22.2). In addition to the detection of dermal backflow, visual lymphography is widely used intra operatively to
facilitate the surgical identification of the lymphatic trunks travelling next to the
greater saphenous vein or the superficial veins of the upper extremity in patients
subjected to lymphovenous anastomosis or other lymphatic/node reconstruction
procedures. The injection of patent blue can be performed in other areas of the body,
such as the neck, testes (lymphocele, hydrocele), axilla, pelvis, etc., to visualize
nodes or lymph trunks.
Radiological Lymphography
After the dye injection has been absorbed by the lymphatics, one often may detect
the blue lymph channels through the skin. A small transverse incision on the dorsum of the foot or hand is carefully performed using gentle strokes of the scalpel.
186 J.L. Villavicencio
a
b
Fig. 22.2 (a) Reflux of the
dye to the skin is called
“dermal backflow” and is
strongly suggestive of
lymphatic obstruction.
(b) Visual lymphography.
The interdigital injection of
0.2 mL of an 11% aqueous
solution of patent blue violet
into three to four web spaces
produced this image
Magnification using 4+ surgical loupes or a 6+ surgical microscope is of great value
in identifying the lymphatic trunks and distinguishing them from the neighboring
veins. The lymphatic trunks appear stained in beautiful blue against the yellowish
contrast of the fatty tissue. Dissection of the lymphatic is done carefully, freeing its
anterior and lateral aspects and leaving the posterior segment intact to serve as a
support for the cannulation. We used a # 30-gauge hypodermic needle with four
small side holes in its distal 5 mm. The lateral holes drilled by a watchmaker
decrease the resistance to the injection of the contrast material.
Oil Contrast Lymphography
Oil soluble contrast materials such as ultrafluid lipiodol were used extensively in
direct lymphography. Lipiodol contains 38% of iodine and is more viscous than its
aqueous counterpart, “Conray” 280 or 420. The injection must be performed very
slowly, using automatic injectors (1 mL every 6–7 min). A total of no more that
10 mL of lipiodol should be injected. The progress of the dye is monitored by serial
22 Oil Contrast Lymphangiography
187
radiographs. The calf and thigh are massaged to assist the oil in its centripetal flow
and further radiographs are taken at intervals of several hours. The contrast material
has the disadvantage of producing inflammation of the vessels and, often, obstruction of the lymphatics. The latter complication is responsible for possible obstruction and lack of visualization of surgical lymphovenous anastomosis and thus,
difficulty in assessing the patency and benefits of the procedure. Oil lymphography
may also produce allergies and, on occasion, oil embolization, manifested by dyspnea, pyrexia, and slight hemoptysis. In spite of its risks, the procedure was extensively used throughout the world and was instrumental in the development of a
lymphedema classification. The Kinmonth classification was based on clinical,
lymphangiographic and histopathological studies. He described:
(a) The normal lymphatic system
(b) Hypoplasia of the lymphatic trunks
(c) Aplasia of the trunks and lymph nodes
(d) Hyperplasia or varicose dilatations of the lymph trunks
Primary lymphedemas have aplasia or hypoplasia of trunks with or without node
aplasia. Secondary lymphedemas have abnormal patterns of lymph transport secondary to damage to the lymph trunks or to the nodes, such as in lymphadenectomy
for malignancy and/or radiation.
Lymphography, as described, provided useful information on anatomy and morphology of the lymphatics. However, the procedure was tedious and time-consuming and requires exquisite patience and skill. It did not provide dynamic information
and its use has been practically abandoned. Like many advances in science, lymphography has been a stepping-stone in the progress toward better technological
procedures. Lymphoscintigraphy was the next step in the effort to obtain visualization and better information on flow dynamics and transport of fluids.
10-13
With the
introduction of technetium-99m human serum albumin and advances in the digital
gamma camera, improved resolution of the entire body lymphatic system was
obtained.
14,15
The lymphoscintigraphy technique as utilized in our department15 requires the
injection of 1 mc of Tc-Sb2 S3 mixed with 0.3–0.5 mL of normal saline, subcutaneously, into three interdigital web spaces of each foot. Before injecting the isotope,
the patient exercises by walking for 5 min. Images are obtained in a gamma camera
at 10 min intervals with a large field of view. Inguinal nodes are usually observed at
or before 30 min. A normal lymphoscintigraphic pattern consists of symmetrical,
bilateral transit of the tracer to the inguinal nodes within 1 h. Abnormal lymphoscintigraphic patterns include dermal backflow, complete obstruction, lymphoceles,
reflux, and lateral channels. Because the tracer enters the lymphatics by diffusion
rather than direct endolymphatic injection, lymphoscintigraphy accurately and reliably depicts the anatomy and function of the lymphatic system.
16
Magnetic resonance imaging (MRI) has shown its value in congenital vascular
anomalies. It has been used in the differential diagnosis of lipedema, venous edema,
and lymphedema. Patients with lymphedema show a typical honeycomb pattern of
the subcutaneous tissue. An advantage of the method is that it is possible to visualize
188 J.L. Villavicencio
the lymphatic trunks or nodes proximal to lymphatic obstruction, something that
lymphoscintigraphy cannot do.
17
There is no doubt in my mind that the field of lymphatic imaging continues to
evolve with the development of newer imaging methods such as positron emission
tomography (PET), dynamic contrast-enhanced MRI (DCE-MRI), and color Doppler
ultrasound (CDUS). These techniques provide structural and functional information
using minimally invasive interstitial imaging techniques with new contrast agents.
As occurs in the field of congenital vascular malformations, multi-modal techniques
might be more appropriate for diagnosing and studying lymphatic diseases.
18
The poor resolution of the conventional diagnostic method of radionuclide-based
imaging has served as the incentive to investigate MRI and new contrast agents in
the anatomical and functional evaluation of the lymphatics and lymph nodes in the
diagnosis of lymphatic circulatory disorders, particularly in primary lymphedema.
In a recent study, contrast-enhanced lymphangiography was performed with a 3.0-T
MR unit after intracutaneous injection of gadobenate dimeglumine into the interdigital webs of the foot. This study demonstrated the possibility of visualizing the
precise anatomy of lymphatic vessels and lymphatic nodes in patients with lymphedema, as well as functional data regarding lymph flow transport in the lymphatic
vessels and nodes.
19
From the direct lymphography of Kinmonth to the current wave of novel
radiological techniques and newer contrast materials, many years of clinical and
experimental investigations have elapsed, always in search of better methods and techniques to discover the true significance of the challenging and elusive lymphatics.
References
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Systems. 2nd ed. London: Edward Arnold; 1982:1-17.
7. Hudack SS, McMaster PD. The lymphatic participation in human cutaneous phenomena.
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Nucl. 1944;26:165.
9. Kinmonth JB. Lymphangiography in man. Clin Sci. 1952;11:13.
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following interstitial injection. Cancer. 1953;6:1238-1240.
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