Cruikshank was the first to report the lymphatics of the breast in his book published in 1787.25
He used the cadaver of a pregnant woman injecting mercury into the mammary duct from the nipple. He reported seeing by chance mercury-filled lymphatics but did not make any diagrams of his findings.
In 1874, Sappey applied the same method,15
injecting mercury into the dermis of a semiputrefied cadaver to identify the superficial lymph vessels. A very thin adult cadaver was used and he described the superficial lymphatic drainage of the torso, dividing it into four territories by a sagittal midline and a horizontal line at the L2 level. The upper torso lymphatics always drained into the ipsilateral axilla (Fig. ). Sappey reported that the lymphatics of the breast collected in a subareolar plexus and then drained towards the axilla via lymph collecting vessels. Sappey’s description of the breast lymphatics was adopted by anatomists and became the theoretical basis for the subareolar injection of dye and/or isotope for lymphatic mapping as part of the sentinel node biopsy for breast cancer more than one century later.13
In 1903, Poirer and Cuneo summarized Sappey’s results.26
They added their results from foetal studies using with Gerota’s method27
using oil painting dye to stain the lymphatics, they reviewed other people’s studies and published a comprehensive anatomy book of the lymphatic system. Poirer and Cuneo’s famous picture of the lymphatics of the breast (Fig. ) was redrawn and is still being used in Gray’s Anatomy.28
Fig. 8. Poirier and Cuneo’s summary diagram of the breast lymph drainage.26 This diagram was composed based on the anatomical and clinical findings of several people, including Sappey.
In 1959, Turner-Warwick performed photographic and radiographic studies of the collecting lymphatics injecting them with iron Prussian blue or radioisotope gold (Au198
) during surgery in breast cancer patients.29
He demonstrated lymphatic pathways that passed direct from the tumor injection site in the breast to the axillary lymph nodes that bypassed the subareolar plexus. He found that all quadrants of the breast drained to the axilla and either the internal mammary or posterior intercostal nodes. He suggested that Sappey had mistaken the mammary duct for a lymphatic vessel, thereby overemphasizing the importance of the subareolar plexus.
The more recent users of lymphoscintigraphy examinations of the breast are also skeptics of the centripetal lymphatic route towards the subareolar plexus. Tanis30
and Uren (Uren RF: personal communication, May 2007) stated that there is no constant route via the subareolar plexus.
Our current anatomical knowledge of the breast lymphatics still depends on Sappey and Poierer and Cuneo’s diagrams. Since Sappey used thin adult cadavers and Poirer and Cuneo used infant cadavers, the relationship between the superficial lymphatics and the adult breast tissue, and also the relationship of the lymphatic drainage of the breast tissue with that of the surrounding superficial tissues, has not been adequately described. Controversy still exists over the role of the subareolar plexus in the lymphatic drainage of the breast. There has been no concrete evidence of a centripetal anatomical lymphatic pathway that drains the breast tissue towards the subareolar plexus and then, via this plexus, towards the sentinel node.
Our direct injection technique, however, gives a comprehensive image of the lymphatic system in individual specimens. Each lymph vessel that enters a lymph node can be traced retrogradely to provide an accurate map of the tissue for which that lymph node is “sentinel.” We have photographed, radiographed, and recorded actual lymphatic pathways. In addition, cross-sectional studies have been performed to obtain three-dimensional images of these lymph collecting vessels.
We have shown that some of the torso vessels pass from the periphery through the breast tissue on their way towards the axilla. This is discordant with the conventional understanding that they run just underneath the skin.
We compared the torso lymphatic vessel pathways and breast tissue lymphatic vessel pathways in adult female cadavers. Although our results do not show conclusively that the lymph drainage of the breast tissue is via the collecting lymphatics that pass through or immediately superficial to the breast substance, this is likely to be the case since (i) the lymph collecting vessel has a microporous nature and drains surrounding tissue fluid along its entire course31
and (ii) lymphoscintigraphy in breast cancer patients after peritumoral injection, coupled with similar studies with radioactive gold by Turner-Warwick, usually reveals a direct pathway from the injection site to the axillary lymph node,29
not via a subareolar plexus. Therefore we conclude that the lymph collecting vessels that pass through the breast contribute to breast lymph drainage and must be the same vessels shown in lymphoscintigraphy examinations.
Embryologically, the development of the human peripheral lymphatics is poorly understood. However, the lymphatics of the foetus represent similar arrangements to those of adults.32
We assume that some of the lymph vessels are trapped inside the mammary gland as the breast develops around preexisting superficial lymph collectors. We have color coded a diagram of our dissection to simulate various injection sites in lymphatic mapping and sentinel node biopsy for breast cancer. Figure shows that, if the tracer is injected deep around the purple-colored vessel (lower outer quadrant), it reaches both the green and orange lymph node in the pectoral group. However, if the tracer is injected into the subareolar region or into the lower outer quadrant intradermaly near the tumor, it reaches only the green node. This anatomical analysis suggests a mechanism for false negative sentinel node biopsy since more than one sentinel node drains the breast in this example.
False-negative results following sentinel node biopsy are of the order of 5–10% in different series.34
Reasons given to this have been technical
; either related to:
- The surgeons’ experience with the technique or
- The size of the radioactive tracer which may not reach the lymph node, especially if sited in a peritumoral position.
Our results now offer an anatomical explanation for these false negative results as a distinct third possibility.
Perforating lymphatics that pierce the deep fascia are critical when discussing breast lymph drainage. The lymphatic system is classified conventionally into the superficial system and the deep system because of their relationship to the deep fascia. However, we subdivided the system draining the tissues above the deep fascia into the superficial system and the perforating system (Fig. ). The perforating system is connected to the deep lymphatic system and these collecting vessels have the same appearance as the superficial lymphatics as they course with the internal thoracic blood vessels. Variations of the blood supply to the breast have been reported.38
Therefore, we hypothesize that the perforating lymphatics may have the same variations. This helps explain the fact that in all quadrants of the breast, cancer has the potential to metastasize via the internal mammary lymphatics especially if the tumor is medial or deep in the breast parenchyma.43
It is accepted that intradermal injection of tracer rarely demonstrates the internal mammary lymphatics.10
The variable contribution of perforating lymphatics along the branches of the internal mammary artery to lymphatic drainage of the breast cannot be predicted clinically and therefore the likelihood of sentinel nodes being located along the internal mammary artery is also unpredictable. Our anatomical analysis suggests that accurate lymphatic mapping requires peritumoral injection.
Our concept of the breast lymph drainage, drained by both the perforating lymphatic system and the conventional horizontal superficial lymphatic system with their relationship to the lymphatic system beneath the deep fascia.