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22 Oil Contrast Lymphangiography
12. Cambria RA, Bender CE, Hauser MF. Lymphoscintigraphy and lymphangiography. In:
Gloviczki P, Yao JST, eds. Handbook of Venous Disorders. Guidelines of the American Venous
Forum. New York: Chapman and Hall Medical; 1996:580-599.
13. Collins PS, Villavicencio JL, Abreu SH. Abnormalities of lymphatic drainage in lower extrem-
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18. Barret T, Choyke PL, Kobayashi H. Imaging of the lymphatic system: new horizons. Contrast
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189
Chapter 23
Fluorescent Microlymphangiography
Claudio Allegra, Michelangelo Bartolo, and Anita Carlizza
Like the blood capillaries, the lymphatic microvessels are formed by a thin layer of
endothelial cells resting on a delicate basal membrane. This structure, particularly at
the initial segment, is widely fenestrated. The cells are anchored to filaments which,
as interstitial pressure increases, are believed to open the fenestrations and allow the
lymph to enter the lymphatic microvessel.
tion is formed by two superficial networks joined by small perpendicular vessels
through which the lymph drains from the superficial into the deep network. This
deep network is connected by channels that run in a perpendicular direction from
the skin downward to the lymphatic precollectors.
rently conceptualized as an integral component of a drainage network originating
from the venous end of microcirculation. Together with the venous portion of the
capillary circulation and the interstitium, it constitutes a single system that may be
defined as a functional microcirculatory unit.
tems work together; they are connected by tiny lymphovenous anastomoses that
activate when the pressure in the lymphatic system rises.
will lead to functional overload in the lymphatic system that may result in dynamic
insufficiency because the fluid overload exceeds the transport capacity of the lymphatics. In these conditions, lymphangiopathy develops and, in turn exacerbating
edema, which is no longer only of venous, but also of lymphatic, origin.
With today’s technologies, the initial lymphatics in any body compartment can
be visualized to study microlymphatic vessel morphology, diameter, and permeability; number of microlymphatic loops; and extension of the contrast halo from the
injection site. Contrast enhancement of microlymphatics is obtained by injecting
0.01 mL of fluorescein isothiocyanate dextran 150,000 into the subderma under
fluorescence videomicroscopy using a microsyringe (approximately 0.2 mm).
The images are recorded on a videocassette and then processed by computer to
visualize the data.
1,2
The cutaneous microlymphatic circula-
1-3
The lymphatic system is cur-
2-6
The venous and the lymphatic sys-
7-9
Persistent venous stasis
3,10-15
1,16-18
C. Allegra (*)
Angiology Department, San Giovanni Hospital, Rome, Italy
B.-B. Lee et al. (eds.), Lymphedema,
DOI 10.1007/978-0-85729-567-5_23, © Springer-Verlag London Limited 2011
191
192 C. Allegra et al.
Microlymphography in Healthy Individuals, in Chronic Venous Disease, and in Lymphedema (Table 23.1)
Because microlymphography permits the visualization and study of microlymphatic
vessels, it can be employed to study lymphatic pathophysiology in common microand macrocirculatory diseases. In healthy individuals, few microlymphatics are
ordinarily visualized because there is good drainage of contrast material into the
deep lymphatic circulation16 (Fig. 23.1). Involvement of the microlymphatics in
chronic venous disease (CVD) offers a characteristic microlymphatic pattern, displaying an increased number of loops and typical fragmentation
In early-stage lymphedema, the number of microlymphatic loops is particularly
high and the microlymphatic pressure is much higher than the normal range. This
finding can be interpreted as a mechanism of initial insufficiency (Fig. 23.3).
In long-standing lymphedema, the microlymphatics cannot be seen because of
the presence of fibrosis
1,23
(Fig. 23.4).
Microlymphography calculates the following parameters:
1. Number of open or available lymphatic vessels
2. Morphology of open or available lymphatic vessels
3. Permeability of available lymphatic vessels
4. Superficial diffusion of contrast material from the injection site (mm)
5. Diameter of available lymphatic vessels (micron)
6. Intralymphatic pressure (mmHg)
7. Interstitial pressure
1,19,20
(Fig. 23.2).
1,21,22
When the data from dynamic capillaroscopy and capillary blood velocity (CBV)
are combined with microlymphography, a more complete picture can be obtained
for understanding the pathophysiology of a microcirculatory unit.
1-3,5,8,16,17
Measurement of Microlymphatic Pressure
During the 1960s microcirculatory pressure was measured directly using micropipettes (at least 15 mm in diameter). With this passive method, the time needed to
measure pressure was about 10 s.24 The large micropipettes altered the delicate pressure balance inside the microlymphatics, rendering measurement extremely difficult. A significant advance in measuring intramicrolymphatic pressure came in the
1970s when Marcos Intaglietta created the Servo Nulling System, a device that permitted active pressure measurement with real-time response (0.05 s).25 The micropipettes in this system were less than half the diameter of the old ones (about 7 mm).
With later refinements to the Servo Nulling System (Model 5a created in 1990) and
positioning of a preamplifier near the micropipette, the pressure could be measured
with much smaller micropipettes (about 1 mm in diameter).
pettes of only 1 micron in diameter led the way to detailed study of intramicrolymphatic
26
The use of micropi-
23 Fluorescent Microlymphangiography
Capillary blood
Interstitial
pressure
Lymphatic
capillary pressure
in human skin
Lymphatic
capillary
diameter
193
velocity
(mmHg)
(mmHg)
(micron)
Superficial
diffusion of
Table 23.1 Microlymphography in chronic venous disease, in lymphedema and in healthy controls
contrast material
from injection site
(mm)
Morphology
interrupted,
broken Permeability
No. of open or
available lymphatics
CEAP 2–3 16.8 ± 8.2 + + n.a. 72.77 ± 17.3 6.7 ± 2.6 1.47 ± 1.7 0.34 ± 0.1
Controls 6.6 ± 5 − – 7.8 ± 2.6 62.3 ± 7.4 4.19 ± 1 0.65 ± 1.6 0.38 ± 0.7
CEAP 4–6 13.8 ± 8 ++ ++ n.a. 88.5 ± 19.6 5.51 ± 2.4 0.29 ± 0.1
Lymphedema > 30 − + 22.1 ± 13.1 >100 n.a. 4.33 ± 1.7 n.a.
n.d. n.d. +++++ n.a. n.d. n.d. n.d. n.a.
in fibrosis
+ present, − absent, n.d. not determinable, n.a. not available, CVD chronic venous disease, plus or minus values are the means ± SD
Lymphedema
194 C. Allegra et al.
Fig. 23.1 Microlymphography in a healthy
subject
Fig. 23.2 Microlymphography in chronic venous
disease, CEAP 2–3
Fig. 23.3 Microlymphography in lymphedema
23 Fluorescent Microlymphangiography
Fig. 23.4 Microlymphography in fibrosis
195
pressure. Pressure is measured for at least 1 min at baseline conditions with the
patient supine and having rested for at least 30 min beforehand.
Studies by Allegra et al. using the system have improved our knowledge of the
pathophysiology of the lymphatic circulation in healthy subjects and in patients
with chronic venous disease, lymphedema, and other vascular conditions.
19,20,22,23
Besides intramicrolymphatic pressure, this method can be used to measure interstitial pressure in healthy individuals and in those with chronic venous disease and
lymphedema.
Lymphatic Vasomotion and Lymphatic Flow Motion
Several important findings were discovered by chance. After having recorded thousands of microlymphographs and fast-forwarded several images, we noticed that it
was sometimes possible to recognize, even with the naked eye, flow movement inside
the microlymphatics. We digitized several microlymphographs and observed and
measured lymphatic flow. For the first time, the velocity of lymphatic flow was visualized and measured in vivo in a human. We noted two different types of intramicrolymphatic flow: a very slow granular flow, which we termed “lymphatic flow motion”
(about 10 ± 4 m/s), and a pulsating, “stop and go” flow pattern, faster than the former
(about 91 ± 58 m/s), with periodic accelerations, which we termed “lymphatic vasomotion.” The periodicity of the flow accelerations was about 1 min ± 25 s.
We were unable to visualize either type of flow pattern in healthy subjects; however, in patients with CVD (CEAP 2,3) we sometimes found a pulsating flow (lymphatic vasomotion) in the proximity of the precollectors, but never granular flow
196 C. Allegra et al.
(lymphatic flow motion). In patients with soft edema, we more often found a granular flow pattern, but rarely a periodic flow pattern in the proximity of the precollec-
19,20,22,23
tors
That granular flow pattern is visible only in a setting of soft lymphedema,
but not in patients with CVD or healthy subjects; it may be linked to an increase in
the superficial flow that compensates for obstruction of normal deep flow.
In the setting of lymphedema, the presence of a pulsating flow (lymphatic vasomotion) is related to deep drainage because of the opening of the precollectors,
probably resulting from critical pressure levels. As regards CVD, the pulsating flow
pattern is related to similar dynamics, even if the underlying pathophysiological
mechanism is failure of the microlymphatic system and increased interstitial pressure due to capillary stasis.
19,20,22,23
In healthy subjects, neither flow pattern is detected
since the lymph flows not in the superficial, but, rather, in the deep network through
the collectors and therefore cannot be visualized. Recent developments in monitoring and studying lymphatic flow have provided insights into the pathophysiology of
lymphatic circulation (Table 23.1).
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