DOI: 10.1148/rg.241025713
(Radiographics. 2004;24:121-145.)
© RSNA, 2004
Clinical Breast Lymphoscintigraphy: Optimal Techniques for Performing Studies, Image Atlas, and Analysis of Images1
Borys R. Krynyckyi, MD,
Chun K. Kim, MD,
Martin R. Goyenechea, MD,
Peggy T. Chan, MD,
Zhuang-Yu Zhang, PhD and
Josef Machac, MD
1 From the Department of Radiology, Mount Sinai School of Medicine, New York, NY. Received August 14, 2002; revision requested November 18; final revision received August 21, 2003; accepted August 22. All authors have no financial relationships to disclose. Address correspondence to B.R.K., Department of Radiology, Box 1141, Mount Sinai Medical Center, One Gustave L. Levy Pl, New York, NY 10029-6574 (e-mail: syrob@msn.com).
 |
Abstract
|
|---|
Breast lymphoscintigraphy is increasingly performed before surgery to delineate the drainage to the sentinel node (SN) in the axilla. On the basis of the histologic status of harvested SNs, the disease status of the entire axilla can be predicted. This prediction allows a more limited dissection to be performed while maintaining staging accuracy comparable with that of classic axillary lymph node dissection. Lymphoscintigraphy assists surgeons in harvesting the SN during gamma probe–assisted axillary biopsy or dissection and provides a wide field of view survey, among other benefits. When certain injection protocols are used, lymphoscintigraphy can be performed in the afternoon before surgery the next morning, thus minimizing disruptions of tight surgical schedules. Image acquisition can be optimized and SN activity can be maximized by means of such factors as parameters for preparation of the radiotracer, injection techniques, energy settings for the gamma camera, breast displacement maneuvers, and techniques for marking and outlining the patient’s body. The ultimate goals are to delineate the true SN, maximize activity in the node for facilitated removal (even at next-day surgery), and deliver the information to the surgeon without delaying the surgical schedule.
© RSNA, 2004
Index Terms: Breast neoplasms, metastases, 07.33 • Breast neoplasms, radionuclide studies, 00.12161 • Breast neoplasms, staging, 00.32 • Lymphatic system, neoplasms, 997.8331 • Lymphatic system, radionuclide studies, 997.12961
|
LEARNING OBJECTIVES
|
|---|
After reading this article and taking the test, the reader will be able to:
- Discuss the theory behind select biopsy of sentinel lymph nodes in the setting of breast cancer and some of the issues associated with the procedure.
- Describe the technique of performing lymphoscintigraphy and methods of optimizing the procedure and the resulting images.
- Identify some of the patterns that can be seen at lymphoscintigraphy and their meanings.
|
Introduction
|
|---|
The goal of breast cancer treatment is to minimize the extent of tissue disruption while facilitating survival. Breast-conserving surgery (vs modified radical mastectomy) for appropriately small tumors with no reduction in survival has become well established (1,2). The staging and control of disease have been intimately associated with axillary lymph node dissection (ALND) as a method to detect metastatic spread of disease (potentially altering patient care) while providing regional control of disease in the axilla. After removal of diseased nodes, a prolongation in long-term survival has been suggested (3,4). In its classic form, ALND involves extensive dissection of most of the level I, II, and III nodes. It can lead to significant morbidity in the form of lymphedema and other conditions (5,6). With the trend toward earlier detection of less advanced disease, a completely negative axilla is being found more frequently, making the morbidity associated with ALND a less acceptable occurrence.
As with breast-conserving surgery, methods to lessen the negative effect of staging the axilla while still providing regional control have been developed. The sentinel node (SN) concept is a major advance toward this goal. As a staging technique to reduce the dissection field and postsurgical morbidity, sentinel lymph node biopsy has been validated for melanoma and now is being applied to breast carcinoma (7,8). The concept is based on the assumption of an orderly progression of tumor from the primary lesion through the lymphatic channels to the first lymph node encountered along those channels (the SN), which then becomes the site of the earliest distant metastases. A low skip rate, which refers to metastasis bypassing the first node to lodge in a more distant node downstream, has been observed in many studies. This allows the SN to provide an accurate prediction of the status of the entire axilla with respect to metastases without the need for extensive dissection of more distant nodes past the SN. By harvesting only the SN and any immediately adjacent nodes, a reduction in morbidity can be achieved while accurately predicting metastatic spread and the potential need for ALND for regional control when metastases are present (3,9).
By injecting a dye or radiocolloid around the region of the primary breast lesion, the lymphatic drainage of that region to the first node along the lymphatic pathways (the SN) can be deduced, either by dissection of the lymphatic pathways in the case of dye or with a gamma camera or handheld gamma probe sensitive to the emissions of the radiocolloid. The initial injection of radiocolloid around the primary breast lesion, its progression along the lymphatic channels, and phagocytosis by macrophages in the SNs is the basis of imaging with the planar gamma camera. Mapping out the lymphatic drainage prior to surgery to assist the surgeon in facilitating removal of the SN is the goal of the lymphoscintigraphy specialist.
The technique of lymphoscintigraphy offers several benefits to the surgeons: The wide field of view gamma camera images the entire chest, with the axillary and internal mammary node regions in one field of view. It can also facilitate detection of intramammary nodes in the breast itself. Lymphoscintigraphy can "map out" diffusion zones emanating from injection sites (interstitial diffusion of radiotracer away from the injection site) and can help identify SNs close to or partly hidden by these diffusion fields, especially when the sitting or standing position is used. This position is not readily available when the handheld gamma probe is used during surgery. The occasionally complex three-dimensional distribution of SNs is also delineated, which facilitates their removal, as well as the presence of secondary distant echelon nodes.
In addition, lymphoscintigraphy can alert the surgeons to "end-on" effects and dilated areas of prominent lymphatic channels, which might mistakenly be construed to represent SNs, by mapping out these findings and preparing the surgeons for the type of findings they might encounter with the handheld probe in this region. Surface contamination, which might be erroneously construed to represent SNs, is easily revealed with orthogonal views and triangulation methods. The activity will appear to reside at the surface in these situations. Surgeons just learning the intraoperative technique appreciate the information lymphoscintigraphy provides. Use of a large field of view camera in the initial survey along with the reference points provided by triangulation markings on the patient’s body facilitate surgical planning and assist the surgeon in use of the handheld probe. Failure to visualize an SN during lymphoscintigraphy alerts the surgical team that blue dye and traditional ALND might be needed.
Several of the technical issues in lymphoscintigraphy were previously presented (5,10,11). In this article, we present additional suggestions and further practical refinements that we have arrived at by performing daily clinical procedures. Our experience has also allowed us to observe the wide range of possible patterns of lymphatic drainage, which are discussed mainly in the figure legends. Specific topics discussed include the radiopharmaceutical preparation, injection techniques, additional injection site issues, pain control, techniques for preventing contamination, massaging the breast, image acquisition parameters, arm positioning and breast displacement maneuvers, triangulation techniques and body marking and outlining, internal mammary SNs, reasons to strive for a "hot" node, combined and hybrid injection techniques, blue dye and special staining of SNs, and factors affecting visualization and detection of SNs.
|
Radiopharmaceutical Preparation
|
|---|
In the United States, the only available radiotracer formulation as a lymphoscintigraphic agent is technetium-99m sulfur colloid, which can be filtered or unfiltered. The smaller filtered preparation (100 or 200 nm) (Acrodisc syringe filter; Pall, Ann Arbor, Mich) generally achieves better lymphatic penetration and is commonly used. Unfiltered preparations have a range of sizes that is difficult to categorize due to multiple preparation and measurement variables that affect the reported size range, but most particles (>75%) are probably 100–1,000 nm in diameter (8). It has been suggested that unfiltered preparations decrease diffusion from the lesion injection site (increased diffusion could potentially obscure closely adjacent nodes) but, in theory, at the expense of decreased delivery of activity to the SN for the same reasons. In addition, larger particles would limit the number of echelon nodes (nodes downstream of the first SN) seen along the lymphatic chain, although it has been suggested that harvesting echelon nodes along with the SN decreases the false-negative rate (12–14). A high specific activity preparation has been reported to further improve performance (15,16). Tc-99m nanocolloid, which is used outside the United States, has a much smaller average particle range, with almost all particles less than 100 nm in diameter (8).
|
Injection Techniques
|
|---|
This is perhaps the most controversial aspect of performing lymphoscintigraphy. Multiple injection techniques exist (Fig 1), with several proponents for each technique in the literature.
View larger version (28K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 1. Different sites of injection. Right: Drawing shows multiple potential injection sites in the right breast, with the injection patterns altered when close to the axilla. A, For uncomplicated lesions, injections can be performed at two to four perilesional locations. B, Lumpectomy sites can be injected at two to six locations, with a minimum of one injection on each side of the scar. C, When lesions are close to the axilla, it is reasonable to shift portions of the total injected dose away from the regions closest to the axilla to diminish the negative effects of injection site diffusion, which could hide adjacent SNs. Top left: Dermal injections are usually performed at the skin directly above the lesion, whereas areolar injections can be performed anywhere in the areola or at the aspect of the areolar-cutaneous junction closest to the lesion.
|
|
Perilesional Injections
Probably the most common technique used in the United States (8), perilesional (also called intraparenchymal or peritumoral) injections are administered generally around the lesion and can include injections deeper or superficial to the plane of the lesion (but the term usually signifies injections on the side of the lesion). Typically, two to four injections of an equally divided dose are performed. The number of injections can beincreased for very large lesions. Lumpectomy site injections call for at least two injections, one on each side of the scar, with multiple injections reported to increase the rate of node visualization (17) (Figs 1, 2). Final images are usually obtained 45 minutes to 1–2 hours or more after injection, as activity reaches the SN slowly as it diffuses through tissues to reach lymphatic vessels. Perilesional injections are more forgiving of position compared with intralesional injections, as discussed later. A greater mass of surrounding breast tissue undergoes injection, which has more lymphatic drainage compared with the tumor itself.
View larger version (124K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 2a. (a) Anterior midstudy image of the left breast, obtained after concurrent perilesional and intradermal injections, shows a tortuous lymphatic pathway leading to the SN from the injection sites (IS). (b) Anterior end-of-study image of the right side of the chest, obtained in another patient after injections into the upper (U) and lower (L) tissues flanking a lumpectomy scar and at the areolar-cutaneous junction (arrow), shows several nodes in the axilla (SNs).
|
|
View larger version (124K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 2b. (a) Anterior midstudy image of the left breast, obtained after concurrent perilesional and intradermal injections, shows a tortuous lymphatic pathway leading to the SN from the injection sites (IS). (b) Anterior end-of-study image of the right side of the chest, obtained in another patient after injections into the upper (U) and lower (L) tissues flanking a lumpectomy scar and at the areolar-cutaneous junction (arrow), shows several nodes in the axilla (SNs).
|
|
Total volumes of injected material generally range from just below 1 mL to a maximum of 8–16 mL (4). These large volumes were proposed as a method to open up lymphatic junctions and allow radiotracer to enter the channels. Others suggest that extreme volumes are not physiologic and even raise the question of tumor spread if such volumes are administered intralesionally (8,18,19). A more modest volume of 3–4 mL is probably adequate. Breast size also dictates the volume of injection, with smaller volumes recommended for small breasts and larger volumes for large breasts. A wide range of activity levels are used, typically 200 µCi (7.4 MBq) to 2–3 mCi (74–111 MBq), with a maximum of 10 mCi (370 MBq) in one study (20).
Problems with diffusion zone activity obscuring the SNs after injections close to the axilla can occur, especially if the primary lesion is located in the upper outer quadrant, close to the axillary nodes. The perilesional injection technique is one of the few that will delineate internal mammary nodes to any extent (Figs 3, 4). Deeper injections and small breast size have been associated with an increased rate of internal mammary node visualization. These two factors are most likely related to the proximity between the injection site and the deeper lymphatic channels draining to the internal mammary nodes (21).
View larger version (141K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 3. Importance of multiangle views in assessing overlap. Top: Anterior and lateral backlit end-of-study images of the left side of the chest show the injection sites (IS) and SNs. An internal mammary SN (IM) is also noted. Bottom: Images show an overlap effect for both the injection sites and the SNs, depending on the view.
|
|
View larger version (121K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 4a. Sequence of consecutive anterior images. (a) Image obtained before "LymphoBoost" (LB) injection (injection at the areolar-cutaneous junction) shows a perilesional injection site (IS), internal mammary SNs (IM), and an axillary SN (arrow). The liver activity is due to capillary penetration or partial vascularization of the radiotracer dose during injections. (b) Image obtained after lymphoboost (LB) injection shows marked augmentation of axillary SN activity with additional nodes noted (arrow). (c, d) Images obtained with the arm up (c) or down (d) show a marked effect of arm position on the perceived locations of the SNs and the injection site with a potential corresponding shift in the surface markings. The position of the internal mammary SNs (arrow) remains fixed. (Reprinted, with permission, from reference 5.)
|
|
View larger version (127K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 4b. Sequence of consecutive anterior images. (a) Image obtained before "LymphoBoost" (LB) injection (injection at the areolar-cutaneous junction) shows a perilesional injection site (IS), internal mammary SNs (IM), and an axillary SN (arrow). The liver activity is due to capillary penetration or partial vascularization of the radiotracer dose during injections. (b) Image obtained after lymphoboost (LB) injection shows marked augmentation of axillary SN activity with additional nodes noted (arrow). (c, d) Images obtained with the arm up (c) or down (d) show a marked effect of arm position on the perceived locations of the SNs and the injection site with a potential corresponding shift in the surface markings. The position of the internal mammary SNs (arrow) remains fixed. (Reprinted, with permission, from reference 5.)
|
|
View larger version (152K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 4c. Sequence of consecutive anterior images. (a) Image obtained before "LymphoBoost" (LB) injection (injection at the areolar-cutaneous junction) shows a perilesional injection site (IS), internal mammary SNs (IM), and an axillary SN (arrow). The liver activity is due to capillary penetration or partial vascularization of the radiotracer dose during injections. (b) Image obtained after lymphoboost (LB) injection shows marked augmentation of axillary SN activity with additional nodes noted (arrow). (c, d) Images obtained with the arm up (c) or down (d) show a marked effect of arm position on the perceived locations of the SNs and the injection site with a potential corresponding shift in the surface markings. The position of the internal mammary SNs (arrow) remains fixed. (Reprinted, with permission, from reference 5.)
|
|
View larger version (129K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 4d. Sequence of consecutive anterior images. (a) Image obtained before "LymphoBoost" (LB) injection (injection at the areolar-cutaneous junction) shows a perilesional injection site (IS), internal mammary SNs (IM), and an axillary SN (arrow). The liver activity is due to capillary penetration or partial vascularization of the radiotracer dose during injections. (b) Image obtained after lymphoboost (LB) injection shows marked augmentation of axillary SN activity with additional nodes noted (arrow). (c, d) Images obtained with the arm up (c) or down (d) show a marked effect of arm position on the perceived locations of the SNs and the injection site with a potential corresponding shift in the surface markings. The position of the internal mammary SNs (arrow) remains fixed. (Reprinted, with permission, from reference 5.)
|
|
The exact anatomic location of the injection is at times obscure in the literature, with terms such as subcutaneous or subdermal occasionally used, mainly in Europe. These terms vaguely refer to injections somewhere above the tumor but below the skin (subdermal), which could also be classified as perilesional in certain instances if the lesion is very close to the skin surface.
Cutaneous Injections
Cutaneous injections are generally delivered into the skin above the lesion, at a depth varying from just at or below the dermis (subdermal) to as shallow as possible (creating a wheal or blister). The question whether these surface injections delineate the same nodes as perilesional injections is controversial (Fig 5). This difference is indisputable where internal mammary nodes are concerned, which are not delineated by surface injections to any significant extent (0%–3%). In contrast, multiple authors have shown no significant difference for axillary node visualization or harvesting (outside the internal mammary node basins), claiming that the same axillary nodes are drained to, an "all roads lead to Rome" concept (22–24). Some authors have detected subtle differences, with discongruent nodes noted (not including internal mammary basin nodes) (20,25, 26).
View larger version (83K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 5a. Potential connections between lymph nodes and lymphatic channels. (a) Drawing of a lymph node shows serial connections to germinal centers and alternate connections that mostly bypass the germinal centers, running through the node or on the surface without connecting (19). (b) Diagrams show a serial connection (which is most common) and an alternate parallel connection, which has reduced flow compared with that of serial connections. (c) Anterior midstudy image of the left side of the chest, obtained after perilesional and skin injections, shows a bright focus and a fainter focus (arrow), which appeared simultaneously. The latter is closer to the tumor in the breast and potentially represents a node fed through a side parallel connection or a node that is only partially visualized due to replacement by metastases. Because the fainter focus intensified over time and persisted on delayed views, ectasia was less likely. (d) Diagrams show possible connections between a tumor and lymph nodes. PL = perilesional injection site. 1, Perilesional injection demonstrates the SN and a more distant axillary echelon node. 2, Surface injection leads to augmentation of the nodes seen after the perilesional injection. EN = echelon node. 3, Surface injection leads to augmentation of the nodes seen after the perilesional injection, with additional foci appearing proximally, upstream from the originally delineated SNs. This appearance could represent pooling of activity in a dilated area, that is, a pseudo-SN (PSN) or a reverse echelon node (REN). A reverse echelon node is an upstream node that is distinct from the primary SN seen after the initial perilesional injection and that receives activity only from the surface injection. It is usually closer to the tumor and technically is not part of the tumor drainage, since it is not seen with the original perilesional injection but only after the surface injection. The more distant true SN is almost always augmented by surface injections, since it is downstream along the lymphatic chain. 4, Surface injection leads to activity bypassing the true SN because the lymphatic channels are not connected at that point. There is also demonstration of a distant echelon node, which might not contain tumor. The former finding is referred to as a missed SN (MSN) if no perilesional injection was performed; the latter finding is potentially referred to as a false SN (FSN) or a false-negative node (FNN) (5,25). (e) Anterior midstudy image of the left side of the chest, obtained after perilesional and areolar-cutaneous junction injections, shows activity tracking to the same sentinel and echelon nodes along different pathways. Such an "all roads lead to Rome" pattern is seen most of the time with combination injections. (Fig 5a reprinted, with permission, from reference 19; Fig 5d reprinted, with permission, from reference 5.)
|
|
View larger version (21K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 5b. Potential connections between lymph nodes and lymphatic channels. (a) Drawing of a lymph node shows serial connections to germinal centers and alternate connections that mostly bypass the germinal centers, running through the node or on the surface without connecting (19). (b) Diagrams show a serial connection (which is most common) and an alternate parallel connection, which has reduced flow compared with that of serial connections. (c) Anterior midstudy image of the left side of the chest, obtained after perilesional and skin injections, shows a bright focus and a fainter focus (arrow), which appeared simultaneously. The latter is closer to the tumor in the breast and potentially represents a node fed through a side parallel connection or a node that is only partially visualized due to replacement by metastases. Because the fainter focus intensified over time and persisted on delayed views, ectasia was less likely. (d) Diagrams show possible connections between a tumor and lymph nodes. PL = perilesional injection site. 1, Perilesional injection demonstrates the SN and a more distant axillary echelon node. 2, Surface injection leads to augmentation of the nodes seen after the perilesional injection. EN = echelon node. 3, Surface injection leads to augmentation of the nodes seen after the perilesional injection, with additional foci appearing proximally, upstream from the originally delineated SNs. This appearance could represent pooling of activity in a dilated area, that is, a pseudo-SN (PSN) or a reverse echelon node (REN). A reverse echelon node is an upstream node that is distinct from the primary SN seen after the initial perilesional injection and that receives activity only from the surface injection. It is usually closer to the tumor and technically is not part of the tumor drainage, since it is not seen with the original perilesional injection but only after the surface injection. The more distant true SN is almost always augmented by surface injections, since it is downstream along the lymphatic chain. 4, Surface injection leads to activity bypassing the true SN because the lymphatic channels are not connected at that point. There is also demonstration of a distant echelon node, which might not contain tumor. The former finding is referred to as a missed SN (MSN) if no perilesional injection was performed; the latter finding is potentially referred to as a false SN (FSN) or a false-negative node (FNN) (5,25). (e) Anterior midstudy image of the left side of the chest, obtained after perilesional and areolar-cutaneous junction injections, shows activity tracking to the same sentinel and echelon nodes along different pathways. Such an "all roads lead to Rome" pattern is seen most of the time with combination injections. (Fig 5a reprinted, with permission, from reference 19; Fig 5d reprinted, with permission, from reference 5.)
|
|
View larger version (164K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 5c. Potential connections between lymph nodes and lymphatic channels. (a) Drawing of a lymph node shows serial connections to germinal centers and alternate connections that mostly bypass the germinal centers, running through the node or on the surface without connecting (19). (b) Diagrams show a serial connection (which is most common) and an alternate parallel connection, which has reduced flow compared with that of serial connections. (c) Anterior midstudy image of the left side of the chest, obtained after perilesional and skin injections, shows a bright focus and a fainter focus (arrow), which appeared simultaneously. The latter is closer to the tumor in the breast and potentially represents a node fed through a side parallel connection or a node that is only partially visualized due to replacement by metastases. Because the fainter focus intensified over time and persisted on delayed views, ectasia was less likely. (d) Diagrams show possible connections between a tumor and lymph nodes. PL = perilesional injection site. 1, Perilesional injection demonstrates the SN and a more distant axillary echelon node. 2, Surface injection leads to augmentation of the nodes seen after the perilesional injection. EN = echelon node. 3, Surface injection leads to augmentation of the nodes seen after the perilesional injection, with additional foci appearing proximally, upstream from the originally delineated SNs. This appearance could represent pooling of activity in a dilated area, that is, a pseudo-SN (PSN) or a reverse echelon node (REN). A reverse echelon node is an upstream node that is distinct from the primary SN seen after the initial perilesional injection and that receives activity only from the surface injection. It is usually closer to the tumor and technically is not part of the tumor drainage, since it is not seen with the original perilesional injection but only after the surface injection. The more distant true SN is almost always augmented by surface injections, since it is downstream along the lymphatic chain. 4, Surface injection leads to activity bypassing the true SN because the lymphatic channels are not connected at that point. There is also demonstration of a distant echelon node, which might not contain tumor. The former finding is referred to as a missed SN (MSN) if no perilesional injection was performed; the latter finding is potentially referred to as a false SN (FSN) or a false-negative node (FNN) (5,25). (e) Anterior midstudy image of the left side of the chest, obtained after perilesional and areolar-cutaneous junction injections, shows activity tracking to the same sentinel and echelon nodes along different pathways. Such an "all roads lead to Rome" pattern is seen most of the time with combination injections. (Fig 5a reprinted, with permission, from reference 19; Fig 5d reprinted, with permission, from reference 5.)
|
|
View larger version (23K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 5d. Potential connections between lymph nodes and lymphatic channels. (a) Drawing of a lymph node shows serial connections to germinal centers and alternate connections that mostly bypass the germinal centers, running through the node or on the surface without connecting (19). (b) Diagrams show a serial connection (which is most common) and an alternate parallel connection, which has reduced flow compared with that of serial connections. (c) Anterior midstudy image of the left side of the chest, obtained after perilesional and skin injections, shows a bright focus and a fainter focus (arrow), which appeared simultaneously. The latter is closer to the tumor in the breast and potentially represents a node fed through a side parallel connection or a node that is only partially visualized due to replacement by metastases. Because the fainter focus intensified over time and persisted on delayed views, ectasia was less likely. (d) Diagrams show possible connections between a tumor and lymph nodes. PL = perilesional injection site. 1, Perilesional injection demonstrates the SN and a more distant axillary echelon node. 2, Surface injection leads to augmentation of the nodes seen after the perilesional injection. EN = echelon node. 3, Surface injection leads to augmentation of the nodes seen after the perilesional injection, with additional foci appearing proximally, upstream from the originally delineated SNs. This appearance could represent pooling of activity in a dilated area, that is, a pseudo-SN (PSN) or a reverse echelon node (REN). A reverse echelon node is an upstream node that is distinct from the primary SN seen after the initial perilesional injection and that receives activity only from the surface injection. It is usually closer to the tumor and technically is not part of the tumor drainage, since it is not seen with the original perilesional injection but only after the surface injection. The more distant true SN is almost always augmented by surface injections, since it is downstream along the lymphatic chain. 4, Surface injection leads to activity bypassing the true SN because the lymphatic channels are not connected at that point. There is also demonstration of a distant echelon node, which might not contain tumor. The former finding is referred to as a missed SN (MSN) if no perilesional injection was performed; the latter finding is potentially referred to as a false SN (FSN) or a false-negative node (FNN) (5,25). (e) Anterior midstudy image of the left side of the chest, obtained after perilesional and areolar-cutaneous junction injections, shows activity tracking to the same sentinel and echelon nodes along different pathways. Such an "all roads lead to Rome" pattern is seen most of the time with combination injections. (Fig 5a reprinted, with permission, from reference 19; Fig 5d reprinted, with permission, from reference 5.)
|
|
View larger version (84K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 5e. Potential connections between lymph nodes and lymphatic channels. (a) Drawing of a lymph node shows serial connections to germinal centers and alternate connections that mostly bypass the germinal centers, running through the node or on the surface without connecting (19). (b) Diagrams show a serial connection (which is most common) and an alternate parallel connection, which has reduced flow compared with that of serial connections. (c) Anterior midstudy image of the left side of the chest, obtained after perilesional and skin injections, shows a bright focus and a fainter focus (arrow), which appeared simultaneously. The latter is closer to the tumor in the breast and potentially represents a node fed through a side parallel connection or a node that is only partially visualized due to replacement by metastases. Because the fainter focus intensified over time and persisted on delayed views, ectasia was less likely. (d) Diagrams show possible connections between a tumor and lymph nodes. PL = perilesional injection site. 1, Perilesional injection demonstrates the SN and a more distant axillary echelon node. 2, Surface injection leads to augmentation of the nodes seen after the perilesional injection. EN = echelon node. 3, Surface injection leads to augmentation of the nodes seen after the perilesional injection, with additional foci appearing proximally, upstream from the originally delineated SNs. This appearance could represent pooling of activity in a dilated area, that is, a pseudo-SN (PSN) or a reverse echelon node (REN). A reverse echelon node is an upstream node that is distinct from the primary SN seen after the initial perilesional injection and that receives activity only from the surface injection. It is usually closer to the tumor and technically is not part of the tumor drainage, since it is not seen with the original perilesional injection but only after the surface injection. The more distant true SN is almost always augmented by surface injections, since it is downstream along the lymphatic chain. 4, Surface injection leads to activity bypassing the true SN because the lymphatic channels are not connected at that point. There is also demonstration of a distant echelon node, which might not contain tumor. The former finding is referred to as a missed SN (MSN) if no perilesional injection was performed; the latter finding is potentially referred to as a false SN (FSN) or a false-negative node (FNN) (5,25). (e) Anterior midstudy image of the left side of the chest, obtained after perilesional and areolar-cutaneous junction injections, shows activity tracking to the same sentinel and echelon nodes along different pathways. Such an "all roads lead to Rome" pattern is seen most of the time with combination injections. (Fig 5a reprinted, with permission, from reference 19; Fig 5d reprinted, with permission, from reference 5.)
|
|
Intradermal injections above the lesion result in significantly faster and brighter visualization of SNs than perilesional injections (8,10,11,24). Final imaging can usually be performed after only 30–45 minutes, as the radiotracer reaches SNs much faster due to the rich lymphatic drainage of the skin to the axilla compared with the drainage of the deeper parenchyma of perilesional injections. The average volume of injection is also much less, typically 0.2–1 mL. The amount of activity used is usually also smaller than for perilesional injections, typically ranging from 150 µCi (5.6 MBq) to 1–2 mCi (37–74 MBq). Problems with diffusion from the injection site interfering with the detection of SNs also exist, but this is probably less of a problem than for perilesional injections.
Areolar Region Injections
On the basis of anatomic considerations, that is, the presence of a highly dense subareolar lymphatic plexus that drains the areola to the axilla, use of injections in this region was examined by several authors (25,27–34). Variations in technique exist, with some authors achieving an infiltration of the whole areolar region with radiotracer or using a quadrant-based approach depending on lesion location, whereas others performed injections at a fixed site or variable sites. Different volumes have been used and injected at different depths.
As with skin injections, problems of discongruence between areolar and perilesional injections exist concerning internal mammary node detection, the rate of which is also very low. Issues of potential discongruence similarly exist with areolar injections as for skin injections above the tumor in their ability to delineate the same axillary nodes as perilesional injections. In many studies, these issues were not directly addressed by using radionuclide-only injections, as blue dye was used as a comparative agent instead. However, the rate of complete discongruence, which is defined as a completely missed SN from an areolar-only injection, appears to be very low based on the reported comparative results.
Volumes of injection and activity amounts are typically similar to those for skin injections above the tumor, although some centers have used substantially greater volumes of 4–5 mL over multiple or single subareolar injection sites (27,29, 34). Activity reaches the SN at a similar or even faster rate than for dermal injections above the tumor. In addition, more of the total dose reaches the SN compared with skin injections above the tumor.
Intralesional Injections
Intralesional injections have been performed outside the United States but rarely within the United States. Intralesional injections have been considered by several authors as the most accurate, as they simulate drainage from the tumor itself (35–37). However, there can be poor lymphatic drainage from the lesion because of poor lymphatic permeation of solid tumor tissues (8). In addition, questions have been raised about spread of disease from intratumoral needle tracks and the effects the injected material has on dislodging tumor cells (8).
The main technical problem with this technique is the difficulty of finding the center of the lesion if the lesion is not palpable, is palpable but is small or deep, or is multifocal, without use of special techniques such as ultrasonographic (US) or mammographic guidance. Even if the lesion is palpable, the center is still not easily determined. Whether the increased placement accuracy of the radiotracer (compared with that of other perilesional techniques) truly makes a difference clinically has not been answered adequately. As with other perilesional-type injections, problems with diffusion zone activity obscuring SNs from injections close to the axilla occur, but these problems can be minimized if smaller volumes of injection are used, which typically range from 0.2 to 1 mL.
|
Additional Injection Site Issues
|
|---|
Wire localization poses a challenge in identifying the site to inject, as the location where the wire exits the skin is obviously not the true position of the lesion deep in the breast. Review of mammograms and the surface markings made during US for lesions originally localized with these techniques can help define the general area to inject.
Fluid-filled lumpectomy sites pose their own challenge as to where to inject. Injection into a serosanguineous cavity, which can be very large, will rarely lead to SN visualization. Injection into the tissues surrounding the cavity (or into the skin if surface injections are used) is desirable, but the needle tip position cannot always be reliably guided by plunger withdrawal maneuvers to check for serosanguineous fluid. US guidance can help with the injections. Nevertheless, some investigators have reported reduced rates of SN visualization in these cases, whereas others have not found any differences (17,38,39). Injection into the wall at multiple sites has been suggested to improve performance (17) (Figs 1, 2).
Finally, for any deep injection where the tumor is close to the chest wall, it is important to avoid injection into the pectoral muscle or a breast prosthesis for obvious reasons.
|
Pain Control
|
|---|
Experience has shown a need for routine control of pain during injections. Shallow intradermal injections are more painful than intraparenchymal ones. A topical anesthetic has worked well for us. EMLA cream alone (lidocaine 2.5% and prilocaine 2.5%; Astra Pharmaceuticals, Wayne, Pa) has proved to be effective in controlling local surface pain during injections for all but areolar-cutaneous junction injections (11,16). The cream needs to be applied to the skin for at least 20–30 minutes to be fully effective. For even more sensitive shallow areolar injections, besides use of a topical anesthetic, lidocaine can be added to the injection syringes for additional pain control (as discussed later).
|
Techniques for Preventing Contamination
|
|---|
Good injection technique will prevent contamination and reduce the chance of inappropriately labeling such artifacts as nodes. Methods of avoiding contamination include applying negative pressure to the syringe during withdrawal and immediately dabbing the injection site with a gauze pad. This gauze pad is immediately discarded for a fresh one. Bandaging the site after all injections are completed and keeping the patient’s hands away from the sites will also help (11). Dynamic acquisitions are useful. Contamination will not intensify with time, whereas true SNs will. Adding an air bubble into the syringe on top of the dose will help ensure delivery of the entire dose. Care must be exercised to avoid spraying portions of the dose.
|
Massaging the Breast
|
|---|
Massaging the injection site after injecting the radiotracer has been suggested to improve the distribution of radiotracer and increase SN visualization (8,40). Mild massaging for a short period is probably beneficial. Vigorous and prolonged massaging has been criticized by some as not physiologic and potentially harmful by spreading micrometastases and can lead to contamination if the proper technique is not used (41,42).
|
Acquisition Parameters
|
|---|
We recommend a large field of view gamma camera equipped with a high-resolution collimator. A 256 x 256 matrix can be used to obtain images with high resolution. To eliminate some of the negative effects of scatter from the injection site, the energy window for Tc-99m can be offset upward or dual energy channels can be used (Fig 6) (5,11). The dual-channel method allows a facility to view images in either a combined channel mode or separately to determine the benefit of this technique with any particular camera system. Dynamic image acquisitions for all phases of the study (60-second frames obtained for a 6–15-minute session), if time permits, are suggested for several reasons. Different summations of frames to produce optimal images are then possible. Images presented to the surgeons can be summed to include frames with and without the transmission source outlines when nodes are occasionally faint. Contamination is easier to detect in a dynamically obtained data set. In addition, first-line SNs can be easily differentiated from more distant echelon nodes.
View larger version (73K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 6a. (a) Anterior images obtained with dual energy channels. The image obtained with the lower channel shows little useful information, but the image obtained with the higher channel shows a partly hidden SN. (b) Lateral images of another patient obtained with dual energy channels. The image obtained with the lower channel shows shallow angle scatter from the arm, but the image obtained with the higher channel shows an SN (arrow), which is no longer obscured by the scatter.
|
|
View larger version (78K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 6b. (a) Anterior images obtained with dual energy channels. The image obtained with the lower channel shows little useful information, but the image obtained with the higher channel shows a partly hidden SN. (b) Lateral images of another patient obtained with dual energy channels. The image obtained with the lower channel shows shallow angle scatter from the arm, but the image obtained with the higher channel shows an SN (arrow), which is no longer obscured by the scatter.
|
|
Injections in the skin above the tumor or at the areola can create a rapidly changing pattern, with prominent transient lymphatic channels, bolus streaming, and areas of ectasia that manifest as transient accumulation of activity in focally dilated lymphatic channels, producing focal "hot spots." These can be potentially confusing to interpret for centers just starting to perform lymphoscintigraphy. In these cases, dynamic and delayed imaging can help identify true SNs, which become brighter over time (Figs 7–9) (5,11). Finally, viewing in cine mode, as is also done with gastrointestinal bleeding studies, makes use of the mind’s ability to better detect subtle differences in patterns when the data are presented dynamically (43).
View larger version (109K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 7a. Early (a) and late (b) anterior images of the left side of the chest show an SN (arrow) and the injection site (IS). There is also an "inverted J"-type pattern, which represents a lymphatic channel that courses above the SN before turning inferiorly, deep to the SN. Potential causes of this pattern include pathways in the skin plexus that follow a large, cranially bulging breast before connecting to the deeper plexus of axillary lymphatics (dashed curve in b). Other possible causes include upward "tenting" of lymphatics due to a raised arm position, thus producing an inflection point, or alternate pathways secondary to complete replacement of nodes by the tumor. (Reprinted, with permission, from reference 5.)
|
|
View larger version (147K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 7b. Early (a) and late (b) anterior images of the left side of the chest show an SN (arrow) and the injection site (IS). There is also an "inverted J"-type pattern, which represents a lymphatic channel that courses above the SN before turning inferiorly, deep to the SN. Potential causes of this pattern include pathways in the skin plexus that follow a large, cranially bulging breast before connecting to the deeper plexus of axillary lymphatics (dashed curve in b). Other possible causes include upward "tenting" of lymphatics due to a raised arm position, thus producing an inflection point, or alternate pathways secondary to complete replacement of nodes by the tumor. (Reprinted, with permission, from reference 5.)
|
|
View larger version (143K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 8. Anterior midstudy image of the right side of the chest shows the injection site (IS) and an SN. There is also a focus of activity in the breast (arrow), which was excised. Histologic analysis demonstrated that the focus was a dilated lymphatic channel. No node was found. Such foci are known as pseudo-SNs. They usually disappear on delayed images and do not intensify over time.
|
|
View larger version (110K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 9a. (a) Anterior early image of the left side of the chest shows a focus of activity (arrow). This is not an SN but a lymphatic channel seen "end on," which can be erroneously interpreted as an SN because of the end-on effect. (b-d) Multiangle sequence of images presented from anterior (b) to lateral (d) shows the end-on effect. The lymphatic channel appears as an arch leading from the injection site to an SN, which is mostly hidden on the anterior images (a and b) by the injection site. D = dermal injection site, P = perilesional injection site. (Reprinted, with permission, from reference 5.)
|
|
View larger version (75K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 9b. (a) Anterior early image of the left side of the chest shows a focus of activity (arrow). This is not an SN but a lymphatic channel seen "end on," which can be erroneously interpreted as an SN because of the end-on effect. (b-d) Multiangle sequence of images presented from anterior (b) to lateral (d) shows the end-on effect. The lymphatic channel appears as an arch leading from the injection site to an SN, which is mostly hidden on the anterior images (a and b) by the injection site. D = dermal injection site, P = perilesional injection site. (Reprinted, with permission, from reference 5.)
|
|
View larger version (67K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 9c. (a) Anterior early image of the left side of the chest shows a focus of activity (arrow). This is not an SN but a lymphatic channel seen "end on," which can be erroneously interpreted as an SN because of the end-on effect. (b-d) Multiangle sequence of images presented from anterior (b) to lateral (d) shows the end-on effect. The lymphatic channel appears as an arch leading from the injection site to an SN, which is mostly hidden on the anterior images (a and b) by the injection site. D = dermal injection site, P = perilesional injection site. (Reprinted, with permission, from reference 5.)
|
|
View larger version (82K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 9d. (a) Anterior early image of the left side of the chest shows a focus of activity (arrow). This is not an SN but a lymphatic channel seen "end on," which can be erroneously interpreted as an SN because of the end-on effect. (b-d) Multiangle sequence of images presented from anterior (b) to lateral (d) shows the end-on effect. The lymphatic channel appears as an arch leading from the injection site to an SN, which is mostly hidden on the anterior images (a and b) by the injection site. D = dermal injection site, P = perilesional injection site. (Reprinted, with permission, from reference 5.)
|
|
Images should be obtained in both the anterior and lateral projections, with an oblique (45°) projection suggested as an alternative to lateral views (with breast displacement performed for any of the projections when warranted). Oblique views also allow the camera head to come closer to select nodes, potentially improving resolution. Occasionally, the position of the nodes in the body is such that even these three views are unsatisfactory. In these rare cases, multiangle views can be obtained every 20° (over a 100°–120° range), with the images played back dynamically in cine fashion.
Artifacts occasionally occur. Their delineation during lymphoscintigraphy, and subsequent relaying of the information to the surgeons, will usually prevent any confusion that might occur during use of the handheld probe (Figs 10, 11).
View larger version (145K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 10. Anterior end-of-study image of the right side of the chest shows a prominent SN (arrow) above the injection site. The activity in the salivary gland, thyroid gland, and stomach is due to free pertechnetate. The free pertechnetate could be secondary to faulty synthesis of the radiocolloid, radiolytic decomposition of the radiocolloid over time, or oxidation. Sources of free pertechnetate also include high "carrier" levels of Tc-99 in the elution and inadequate reaction conditions (ie, incorrect mixing order, low heating temperature, or short heating time). Surgeons must be alerted to a slightly increased background level and organ activity. However, these findings will not hamper harvesting of SNs.
|
|
View larger version (114K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 11a. Rare leakage patterns. (a) Lateral end-of-study image of the right side of the chest shows leakage of the radiotracer along a localization wire with pooling at the wire tip (arrow). (b) Anterior end-of-study image of the right side of the chest, obtained in another patient after perilesional injection 4 cm from the tip of the nipple, shows activity in a lactiferous channel leading to the nipple tip (arrow). After the injection, some of the radiotracer had squirted out of the nipple. IM = internal mammary SNs.
|
|
View larger version (193K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 11b. Rare leakage patterns. (a) Lateral end-of-study image of the right side of the chest shows leakage of the radiotracer along a localization wire with pooling at the wire tip (arrow). (b) Anterior end-of-study image of the right side of the chest, obtained in another patient after perilesional injection 4 cm from the tip of the nipple, shows activity in a lactiferous channel leading to the nipple tip (arrow). After the injection, some of the radiotracer had squirted out of the nipple. IM = internal mammary SNs.
|
|
|
Arm Positioning and Breast Displacement Maneuvers
|
|---|
The position of the arm has a profound effect on the surface markings placed on the patient’s body due to shifting positions of tissue and skin at different levels (Figs 4, 12) (5,11). The position of the arm should approximate that used during surgery, which is usually perpendicular to the long axis of the body. However, this will cause physical interference with the camera head when one tries to obtain lateral views. Two compromises can be used: First, the arm can be raised above the perpendicular surgical position, allowing a reasonably close camera head position in the lateral projection but with some minor distortion of surface markings when the arm is brought back to its "native" position during surgery. As an alternative, the camera head position can be adjusted to 45° (oblique projection) from the anterior position to allow clearance of the arm, which now can be in the perpendicular surgical position. However, this makes triangulation slightly more difficult, as the angles between projections are smaller than 90°.
View larger version (101K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 12a. (a) Anterior end-of-study images show bilateral lesions and a small amount of free pertechnetate (in the thyroid gland, salivary glands, and stomach), which is useful as a positional reference. On each side, the distance from the perilesional injection site to the node varies with the position of the patient, increasing when the patient stands and when the arms are lowered. Delineation of axillary nodes increases as overlap decreases when the patient stands and when the arms are lowered. In addition, the breasts move medially when the patient stands. (b) Anterior images show a marked shift in the positions of the combined perilesional-areolar injection site and the axillary nodes (vertical dashed line) when the patient is standing with the arm out versus supine with the arm up. However, there is no change in the position of an internal mammary node (horizontal dashed line). When the patient is supine with the arm up, axillary nodes tend to bunch up, the distance between the injection site and the nodes decreases, and the breast moves laterally.
|
|
View larger version (139K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 12b. (a) Anterior end-of-study images show bilateral lesions and a small amount of free pertechnetate (in the thyroid gland, salivary glands, and stomach), which is useful as a positional reference. On each side, the distance from the perilesional injection site to the node varies with the position of the patient, increasing when the patient stands and when the arms are lowered. Delineation of axillary nodes increases as overlap decreases when the patient stands and when the arms are lowered. In addition, the breasts move medially when the patient stands. (b) Anterior images show a marked shift in the positions of the combined perilesional-areolar injection site and the axillary nodes (vertical dashed line) when the patient is standing with the arm out versus supine with the arm up. However, there is no change in the position of an internal mammary node (horizontal dashed line). When the patient is supine with the arm up, axillary nodes tend to bunch up, the distance between the injection site and the nodes decreases, and the breast moves laterally.
|
|
In addition, elevation of the ipsilateral shoulder 45° with a triangular foam wedge, a modified oblique view of the axilla, has been suggested as a method of shifting the breast tissues medially by gravity, thereby pulling them away from the SNs as well as bringing specific SNs closer to the camera. When scintigraphy is performed with the camera head parallel to the floor, improved resolution and SN detection compared with a simple anterior-only view are possible (44). Surgeons must be made aware of these maneuvers so that they can adjust their interpretation of the body surface markings. In some patients, raising the arm above the head for lateral views actually brings the injection site closer to the axillary nodes compared with the surgical arm position, an unwanted effect. There is also a tendency for axillary nodes to bunch up when the arm is in the raised position compared with the surgical arm position, with the best separation often occurring when the patient is standing or sitting (Figs 4, 12).
Imaging the patient in a prone position with the breast hanging down (gravity "pull") has been suggested as a method of moving the injection site scatter away from the chest and axilla to unmask any SNs close to the injection site. This procedure typically uses a special pad with cutouts to allow the breast to assume a dependent position. Its major disadvantage is that it adds an additional position the patient must be maneuvered through and is different from the position during surgery. The sitting position noted earlier allows gravity to pull attenuating breast tissues and injection site scatter away from the axillary nodes and has been shown to be useful (5,45,46) (Fig 12).
Tape traction allows five degrees of freedom: Pulling is possible in the cranial, caudal, medial, lateral, and anterior (away from the patient) directions (the last direction simulating the prone–breast hanging position mentioned earlier) or any combination of these directions simultaneously, with the patient supine and the camera in the anterior, lateral, or 45° position (Fig 13). The free end of the tape can be held by the operator at any angle or anchored to the camera head or even the opposite chest wall of the patient. Slippage is rarely a problem when generous amounts of a very wide (5 cm) surgical tape with good adhesive properties (Transpore 1527–2; 3M Health Care, St Paul, Minn) are used. Oblique (45°) camera views with tape traction breast displacement medially can be used, similar in effect to the modified oblique view of the axilla noted earlier but with no need to use a wedge. In general, we use this technique only in cases of lesions close to the axilla or when a perceived possibility of a hidden node is not easily resolved on multiangle views or sitting views. Acquisition of sitting views at the end of the study is a recommended option when the injection sites are close to the axilla (Fig 12).
View larger version (112K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 13a. Obscuration of an SN due to injection site activity and the attenuating effects of breast tissues. (a) Lateral end-of-study image of the right side of the chest shows an SN behind the inferior portion of the injection site. (b) Anterior images show that the node (arrows) is mostly hidden due to overlap with the injection site and attenuation effects. (c) Images obtained with the breast displaced cranially and medially show that the injection site overlap has been resolved and some of the attenuation has been eliminated (arrows). Breast displacement will alter the positions of surface markings when the breast is released and must be taken into account.
|
|
View larger version (101K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 13b. Obscuration of an SN due to injection site activity and the attenuating effects of breast tissues. (a) Lateral end-of-study image of the right side of the chest shows an SN behind the inferior portion of the injection site. (b) Anterior images show that the node (arrows) is mostly hidden due to overlap with the injection site and attenuation effects. (c) Images obtained with the breast displaced cranially and medially show that the injection site overlap has been resolved and some of the attenuation has been eliminated (arrows). Breast displacement will alter the positions of surface markings when the breast is released and must be taken into account.
|
|
View larger version (102K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 13c. Obscuration of an SN due to injection site activity and the attenuating effects of breast tissues. (a) Lateral end-of-study image of the right side of the chest shows an SN behind the inferior portion of the injection site. (b) Anterior images show that the node (arrows) is mostly hidden due to overlap with the injection site and attenuation effects. (c) Images obtained with the breast displaced cranially and medially show that the injection site overlap has been resolved and some of the attenuation has been eliminated (arrows). Breast displacement will alter the positions of surface markings when the breast is released and must be taken into account.
|
|
|
Triangulation Techniques and Body Marking and Outlining
|
|---|
Once the SNs are visualized, the patient’s body is marked by using a triangulation technique, which allows the surgeon to deduce the actual three-dimensional position of the SN in the patient’s body by extrapolating from surface markings on the patient. The patient’s body is marked along imaginary lines that intersect the SN somewhere along their length, which emanate perpendicularly from the camera collimator surface and are obtained at two different angles (usually 90° or 45° apart). With these projections, the actual position of the SN in the body can be reasonably deduced by the surgeon using triangulation (Figs 14, 15) (5,11).
View larger version (125K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 14. Anterior end-of-study image of the chest shows bilateral lesions and injection sites (IS). In the right breast, nodes appear in a chain of decreasing intensity (1, 2, and 3) as the radiotracer is successively filtered by macrophages. The first node is the more important SN; the more distant nodes are the echelon nodes. This pattern can occur with any injection method and is often seen with dermal or areolar-cutaneous junction injections. Clavicular or supraclavicular SNs (SC SN) are seen medially on the right; their appearance is possibly due to activity in a distal branching lymphatic channel. In the left breast, two nodes with nearly equal activity are seen. In the rare case of bilateral lesions, use of 90° lateral images should be avoided when the technique is just being learned, as "shine through" of activity in the opposing axillary nodes and breast could complicate image interpretation. Acquisition of 45° oblique images will not produce any significant overlap, and the preferred surgical position (with the arm perpendicular, not raised) can then be used. If such altered image acquisition and body marking are used, the surgeons must be made aware of the altered triangulation pattern needed.
|
|
View larger version (25K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 15. Method of accurately marking the patient’s body by using triangulation. The patient is imaged, and the position of the SN is noted on the monitor screen. An observer, who remains in a fixed position in front of the monitor to avoid parallax error, attaches a small piece of tape (or makes a mark with a nonpermanent marker) over the position of the SN on the monitor screen. A physician, who is holding a radioactive point source in one hand and a color-coded permanent marker in the other, moves the point source into the field of view. The observer, who is sitting or standing in front of the monitor without having moved, then guides the physician (with constant refreshing of the persistent screen image) as the point source is moved along the patient’s body until it is positioned under the reference point on the monitor screen (the tape or nonpermanent mark placed there earlier), at which time the patient’s body is marked by the physician with the color-coded permanent marker. This process is repeated in a different projection, usually 90° or 45°. Keep in mind that displacement of the breast or arm will alter the relationships of the surface markings to the SN (5,11).
|
|
Outlining the patient’s body on the images presented to the surgeon facilitates orientation. The two most common methods use either a cobalt-57 sheet source (122 keV), which is placed behind the patient to create a transmission scan outline of the patient (attenuation by the patient’s body), or a simple point source of activity, which is used to manually outline the edges of the patient’s body. As an alternative, a large syringe (10 mL) filled with radioactive material can be used to "paint" a background of activity behind the patient by using a sweeping motion (Fig 16). An additional outlining technique uses a very broad and low-energy scatter window for the injection site activity within the body to outline the patient’s tissues, but this method is difficult to perform clinically and is sensitive to variations in body habitus (47–49).
View larger version (105K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 16a. (a-c) Lateral images show three methods of outlining the patient’s body. (a) In the recommended and probably most common method, a Co-57 (122-keV) transmission sheet source is placed behind the patient, with the patient (the attenuating mass) between the sheet source and the head of the camera. (b) Radioactive material in a syringe is used to paint a background behind the patient by using an up-and-down motion. It is more difficult to achieve a uniform result with this method, and radiation exposure is an issue. (c) In the edge outlining method, a simple point source of activity (Tc-99m) is used to trace the edges of the patient’s body. However, the inferior surface is not easily traced due to the imaging table. As an alternative, a flexible "tube" line source can be taped to the patient and used as a marker, which will produce similar results. (d) Photograph shows a patient positioned between a Co-57 sheet source and the head of the camera (the method used in a).
|
|
View larger version (104K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 16b. (a-c) Lateral images show three methods of outlining the patient’s body. (a) In the recommended and probably most common method, a Co-57 (122-keV) transmission sheet source is placed behind the patient, with the patient (the attenuating mass) between the sheet source and the head of the camera. (b) Radioactive material in a syringe is used to paint a background behind the patient by using an up-and-down motion. It is more difficult to achieve a uniform result with this method, and radiation exposure is an issue. (c) In the edge outlining method, a simple point source of activity (Tc-99m) is used to trace the edges of the patient’s body. However, the inferior surface is not easily traced due to the imaging table. As an alternative, a flexible "tube" line source can be taped to the patient and used as a marker, which will produce similar results. (d) Photograph shows a patient positioned between a Co-57 sheet source and the head of the camera (the method used in a).
|
|
View larger version (81K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 16c. (a-c) Lateral images show three methods of outlining the patient’s body. (a) In the recommended and probably most common method, a Co-57 (122-keV) transmission sheet source is placed behind the patient, with the patient (the attenuating mass) between the sheet source and the head of the camera. (b) Radioactive material in a syringe is used to paint a background behind the patient by using an up-and-down motion. It is more difficult to achieve a uniform result with this method, and radiation exposure is an issue. (c) In the edge outlining method, a simple point source of activity (Tc-99m) is used to trace the edges of the patient’s body. However, the inferior surface is not easily traced due to the imaging table. As an alternative, a flexible "tube" line source can be taped to the patient and used as a marker, which will produce similar results. (d) Photograph shows a patient positioned between a Co-57 sheet source and the head of the camera (the method used in a).
|
|
View larger version (134K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 16d. (a-c) Lateral images show three methods of outlining the patient’s body. (a) In the recommended and probably most common method, a Co-57 (122-keV) transmission sheet source is placed behind the patient, with the patient (the attenuating mass) between the sheet source and the head of the camera. (b) Radioactive material in a syringe is used to paint a background behind the patient by using an up-and-down motion. It is more difficult to achieve a uniform result with this method, and radiation exposure is an issue. (c) In the edge outlining method, a simple point source of activity (Tc-99m) is used to trace the edges of the patient’s body. However, the inferior surface is not easily traced due to the imaging table. As an alternative, a flexible "tube" line source can be taped to the patient and used as a marker, which will produce similar results. (d) Photograph shows a patient positioned between a Co-57 sheet source and the head of the camera (the method used in a).
|
|
Some newer gamma cameras are equipped with line sources, which are used for transmission attenuation correction and can be adapted to delineate the patient’s outline (47,48). If a Co-57 sheet source is used, a separate outlining energy window centered around 122 keV can be optionally programmed into the camera system (in addition to the separate upwardly offset energy window used to delineate SNs, images of which are displayed and printed separately). This allows use of a weak Co-57 sheet source when a fresh one is unavailable or as a deliberate method to control exposure to technologists (47).
|
Internal Mammary SNs
|
|---|
Internal mammary SNs are seen with intralesional and perilesional injections (Figs 3, 4, 11, 12). As noted earlier, intradermal injections above the tumor and at the areolar region rarely, if ever, allow visualization of internal mammary nodes (8,28–33). This difference is probably due to the fact that the internal mammary nodes receive the main portion of their drainage from deeper lymphatic pathways closer to the chest and distant to superficial injections. Even with perilesional injections, injecting deeper has increased visualization of internal mammary nodes (21,50, 51). Our experience appears to confirm this, with deeper and multilevel perilesional injections having a major effect on the rate of internal mammary node visualization. Also noted was a much higher rate of internal mammary node visualization in women with smaller breasts, both factors suggesting a proximity effect (52). However, some of these studies exclusively used "subtumoral" injections, which in one study demonstrated axillary nodes in only 50% of patients with the probe when referenced against concurrent intradermal dye injections performed in the same patients (51).
If internal mammary node visualization were to be deemed important, then multidepth perilesional or subtumoral injections would need to be performed. However, the need to detect internal mammary nodes is questionable, as many surgeons do not routinely explore the chest even if internal mammary nodes are identified (53) but might alter radiation treatment if their presence is detected. The controversy continues on the benefits of increased staging accuracy from harvesting internal mammary nodes at the expense of additional dissection morbidity, with issues of altered treatment (radiation to the internal mammary chain) based on their presence without histologic proof (no harvesting) also being debated. The reader is referred to several views on each side (54–60).
|
Why Strive for a Hot Node?
|
|---|
At times, detection of the SN is difficult due to low activity levels in the node. This is more of a problem with perilesional injections than surface injections. Obtaining a "hotter" SN has several advantages: The most important is in the group of patients who have surgery scheduled on the day following lymphoscintigraphy the previous afternoon. The 2-day protocol has evolved as a means to perform surgery very early in the morning, when imaging facilities performing lymphoscintigraphy are closed, and to preserve tight surgical schedules without creating delays that add to hospital costs, which occur when the entire operating room team is waiting for a patient. In addition, surgery can be delayed past noon the following day, when activity in SNs further decays by several half-lives, seriously increasing the difficulty of finding them. Achieving hotter SNs offsets the physical decay of the radiotracer. An SN that is easier to find with a probe at the surface because it is hotter provides a direct and faster approach to the SN and potentially reduces the amount of dissection needed for its removal (morbidity) while saving time.
Arguments similar to this, in addition to the increased rates of SN detection hotter nodes provide, probably account for the reasons surface injections have gained popularity in some centers and reflect the increased efficiency of delivering the radiotracer to the SNs. A brighter SN is produced by surface injections, as opposed to simply resorting to a higher perilesional dose of activity with the associated negative diffusion effects and resultant exposure issues for the team (5,24).
|
Combined and Hybrid Injection Techniques
|
|---|
Because perilesional injections by themselves can produce weak visualization of SNs with the Tc-99m formulations of sulfur colloid available in the United States, in 1999 we began to use a combination of radiocolloid injection methods to increase the probability of detecting nodes (10,11). Perilesional injections of radiocolloid can be combined with intradermal injections of radiocolloid above the tumor or with injections in the areolar region (10,11,61). It is our opinion that a protocol that combines perilesional injections with surface injections covers all theoretical bases and provides the "hottest" achieved nodes for any amount of total activity injected. Others have also used combinations of radiotracer-only injections, combining perilesional injections with dermal or areolar injections with good results (25,62).
Our preferred approach to hybrid combination injections uses a variant of areolar injections, dubbed "LymphoBoost," in which shallow injections are performed at the areolar-cutaneous junction (61). The technique is described later and in Figure 17. Shifting part of the total radionuclide dose to lymphoboost injection and away from the perilesional injection site will markedly increase the percentage of total injected activity reaching the SN. Because of its efficiency, lymphoboost injection demonstrates SNs much faster and produces nodes that are brighter for any given injected activity compared with cutaneous injections over the lesion or perilesional injections. There is less of a problem with injection site diffusion interfering with axillary SNs after lymphoboost injection than after perilesional injections close to the axilla, where the negative effects of diffusion would be greatest (Figs 1, 4–6, 13, 17).
View larger version (121K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 17a. Use of the lymphoboost technique in the left breast. (a) Anterior image obtained before lymphoboost (LB) injection shows the sites of combined perilesional (PL) and intradermal (ID) injections and an SN. (b) Anterior end-of-study image, obtained with Co-57 backlighting after lymphoboost injection, shows marked augmentation of the SN, as well as additional second- and third-tier echelon nodes of lesser intensity. The diffusion field does not extend significantly toward the axilla. (c-f) Sequence of dynamic lateral images, obtained over 6 minutes just before (c), during (d, e), and after (f) lymphoboost injection, show augmentation of activity in the SN (* in f) even before the syringe is empty. A prominent lymphatic channel leading to the node is seen.
|
|
View larger version (133K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 17b. Use of the lymphoboost technique in the left breast. (a) Anterior image obtained before lymphoboost (LB) injection shows the sites of combined perilesional (PL) and intradermal (ID) injections and an SN. (b) Anterior end-of-study image, obtained with Co-57 backlighting after lymphoboost injection, shows marked augmentation of the SN, as well as additional second- and third-tier echelon nodes of lesser intensity. The diffusion field does not extend significantly toward the axilla. (c-f) Sequence of dynamic lateral images, obtained over 6 minutes just before (c), during (d, e), and after (f) lymphoboost injection, show augmentation of activity in the SN (* in f) even before the syringe is empty. A prominent lymphatic channel leading to the node is seen.
|
|
View larger version (113K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 17c. Use of the lymphoboost technique in the left breast. (a) Anterior image obtained before lymphoboost (LB) injection shows the sites of combined perilesional (PL) and intradermal (ID) injections and an SN. (b) Anterior end-of-study image, obtained with Co-57 backlighting after lymphoboost injection, shows marked augmentation of the SN, as well as additional second- and third-tier echelon nodes of lesser intensity. The diffusion field does not extend significantly toward the axilla. (c-f) Sequence of dynamic lateral images, obtained over 6 minutes just before (c), during (d, e), and after (f) lymphoboost injection, show augmentation of activity in the SN (* in f) even before the syringe is empty. A prominent lymphatic channel leading to the node is seen.
|
|
View larger version (114K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 17d. Use of the lymphoboost technique in the left breast. (a) Anterior image obtained before lymphoboost (LB) injection shows the sites of combined perilesional (PL) and intradermal (ID) injections and an SN. (b) Anterior end-of-study image, obtained with Co-57 backlighting after lymphoboost injection, shows marked augmentation of the SN, as well as additional second- and third-tier echelon nodes of lesser intensity. The diffusion field does not extend significantly toward the axilla. (c-f) Sequence of dynamic lateral images, obtained over 6 minutes just before (c), during (d, e), and after (f) lymphoboost injection, show augmentation of activity in the SN (* in f) even before the syringe is empty. A prominent lymphatic channel leading to the node is seen.
|
|
View larger version (115K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 17e. Use of the lymphoboost technique in the left breast. (a) Anterior image obtained before lymphoboost (LB) injection shows the sites of combined perilesional (PL) and intradermal (ID) injections and an SN. (b) Anterior end-of-study image, obtained with Co-57 backlighting after lymphoboost injection, shows marked augmentation of the SN, as well as additional second- and third-tier echelon nodes of lesser intensity. The diffusion field does not extend significantly toward the axilla. (c-f) Sequence of dynamic lateral images, obtained over 6 minutes just before (c), during (d, e), and after (f) lymphoboost injection, show augmentation of activity in the SN (* in f) even before the syringe is empty. A prominent lymphatic channel leading to the node is seen.
|
|
View larger version (111K):
[in this window]
[in a new window]
[Download PPT slide]
|
Figure 17f. Use of the lymphoboost technique in the left breast. (a) Anterior image obtained before lymphoboost (LB) injection shows the sites of combined perilesional (PL) and intradermal (ID) injections and an SN. (b) Anterior end-of-study image, obtained with Co-57 backlighting after lymphoboost injection, shows marked augmentation of the SN, as well as additional second- and third-tier echelon nodes of lesser intensity. The diffusion field does not extend significantly toward the axilla. (c-f) Sequence of dynamic lateral images, obtained over 6 minutes just before (c), during (d, e), and after (f) lymphoboost injection, show augmentation of activity in the SN (* in f) even before the syringe is empty. A prominent lymphatic channel leading to the node is seen.
|
|
In theory, the technique by itself would be susceptible to the same problems as intradermal and other areolar injection techniques regarding the rare case of axillary node discongruence compared with perilesional injections. However, an extremely low rate (1% to <2%) of complete axillary node discongruence (completely different axillary "SNs" delineated by the different injection techniques) has been noted by us in over 400 patients since we began using the technique of lymphoboost and perilesional injections performed at the same time (unpublished data). This discongruence is less significant with this combination injection technique, as both "SNs" are visible and available for removal, that is, the true SN is not missed (61).
The lymphoboost technique consists of a single 0.6–1.0-mL injection of 100% filtered sulfur colloid at the aspect of the areolar-cutaneous junction closest to the lesion site and directed toward the nipple (Figs 1, 4, 17). This junction is best described as the border where the normal skin changes texture and color to become the areola. The injection is performed over 1–2 minutes with the bevel down and as close to the surface as possible at less than a 45° angle. An extrathin (30-gauge) and short (
-inch) needle (30G1/2 PrecisionGlide Needle; Becton, Dickinson, Franklin Lakes, NJ) is used, as this gauge makes it easier to control initial skin penetration by producing less resistance during initial puncture (preventing "depth overshoot"). Lidocaine is added to the syringes (0.1 mL of a 2% solution), since use of a topical anesthetic alone is not enough to control pain.
We continue to use perilesional injections for theoretical reasons of "direct drainage," to address any discongruence between injection techniques, and to delineate internal mammary SNs. Lymphoboost injection is performed as soon as an SN is seen after the perilesional injections or if time pressures arise. As an alternative, if no SN is visualized after the perilesional injections, a repeat perilesional injection or a very shallow cutaneous injection above the lesion can be tried before lymphoboost injection is performed.
|
Blue Dye and Special Staining of SNs
|
|---|
Blue dye has frequently been used during surgery to delineate the SN (62). The method consists of injecting the dye into the tissues surrounding the primary lesion (or less commonly into the skin or areola) and then quickly dissecting along lymphatic pathways to the SN before the dye has had a chance to dissipate uniformly into surrounding tissues, at which time a decrease in the contrast between stained nodes and surrounding tissues would have occurred, hampering detection. When used with radiotracer-guided sentinel lymph node biopsy, the addition of dye has increased the success rate for finding SNs, has lowered the false-negative rate, and tended to increase the number of nodes harvested in numerous studies (63–67). This combination is used by most surgeons (>85%) (53). More often than not, the SN is hot and stained, with occasional nodes found that are only hot and even rarer nodes that are stained but not hot (68).
The disadvantage of dye resides in time pressures inherent in the technique as well as the added dissection that it entails if performed as a primary guide to finding the SN. More commonly, the dye is used as a "check" between methods. If an SN is not both hot and blue, then a search for the "other" SN is more aggressively pursued. Dye can be injected at the same or a different location compared with the radiotracer (eg, perilesional, intradermal, areolar). Some consider the blue dye technique optional, since low false-negative rates have been suggested with combination hybrid radiocolloid injection techniques only (62).
Special stains that demonstrate specific features of cancer cells are routinely used after the SNs have been harvested. These techniques tend to be labor-intensive. Because of the workload involved, they are usually applied only to select nodes per patient, that is, the SNs. By using sentinel lymph node biopsy, the optimal nodes are chosen for this more thorough examination. Spe- cial stains, in addition to the routine hematoxylin-eosin (H-E) method, include cytokeratin immunohistochemistry of epithelial markers on cancer cells, which can be detected in minute quantities in the form of micrometastases (as small as several cells) and can easily be missed with H-E alone (68,69). Reverse transcriptase polymerase chain reaction markers, which allow detection of tumor-specific messenger RNA sequences, have also been used but are less popular (70,71). Conventional frozen section techniques are being challenged by touch imprint techniques, which use different staining methods that have evolved for more rapid analysis of specimens during the time of surgery (72,73). Finally, even traditional H-E staining can be improved if fine serial sectioning is performed, but this is practical only if limited to the SNs because of the workload involved.
|
Factors Affecting Visualization and Detection of SNs
|
|---|
Numerous patient features have been noted to affect visualization of axillary SNs. Advanced age, large breast size, excisional biopsies, and primary lesions located in the upper outer quadrant close to the axilla have been noted to decrease the intensity of SN visualization and/or the success rate of SN harvesting (5,24,44,65). Diffusion effects from perilesional injections could hide SNs close to the injection site. Complete replacement of the SN by tumor could potentially prevent radiocolloid from entering. In fact, the rate of metastatic disease is higher in patients with nodes not visualized during lymphoscintigraphy than in patients with a node seen during lymphoscintigraphy (74). Nonvisualization of the SN has been associated with the presence of metastasis or an increasing number of invaded axillary nodes, increasing age, and vascular invasion in the primary tumor (74). Lumpectomy procedures can disrupt lymphatic pathways (especially with scars located between intradermal or areolar injection sites and SNs). Debris from a resulting hematoma can prevent local diffusion or overload lymphatic channels. Injection into a hematoma or seroma cavity at the lumpectomy site will fail to delineate SNs. Injection into the pectoral muscle or into a breast prosthesis will likely not delineate SNs. In theory, a pacemaker could also hide a node due to attenuation on certain views.
Massage, possibly high specific activity preparations, and especially surface injections have been noted to increase detection or node intensity, as described earlier (10,11,16,24,74–76). Dose and volume effects are less clearly established, but smaller particles have been noted to delineate a greater number of echelon nodes.
As noted earlier, skin injections fail to delineate internal mammary nodes to any extent. Internal mammary node detection appears to be enhanced by deeper perilesional injections (underneath the tumor). Internal mammary nodes are also more frequently seen in younger patients and those with small breasts. Primary lesions located medially and inferiorly in the breast also favor internal mammary node visualization. Most of these findings could be explained by the effects of proximity to the deeper internal mammary drainage channels (21,50–52).
|
Conclusions
|
|---|
Although great variation exists in techniques, a practical approach based on theoretical and observed results can produce SN visualization with great intensity for a given amount of activity administered. This is important when surgery is planned for the next day. Combined injection techniques exist, which are used by some centers. Patterns of lymphatic drainage are varied, with lymphoscintigraphy providing assistance to the surgeons during SN harvesting. It is the role of the lymphoscintigraphy imaging specialist to accurately delineate the SNs while avoiding the interpretation pitfalls that might be seen with normal variants, artifacts, and the rare complex three-dimensional presentations of SNs.
|
Footnotes
|
|---|
See the commentary by Dillehay
following this article.
Abbreviations: ALND = axillary lymph node dissection,
SN = sentinel node
|
References
|
|---|
- Veronesi U, Cascinelli N, Mariani L, et al. Twenty-year follow-up of a randomized study comparing breast conserving surgery with radical mastectomy for early breast cancer. N Engl J Med 2002; 347:1227-1232.[Abstract/Free Full Text]
- Fisher B, Anderson S, Bryant J, et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med 2002; 347:1233-1241.[Abstract/Free Full Text]
- Keshtgar MR, Ell PJ. Clinical role of sentinel-lymph-node biopsy in breast cancer. Lancet Oncol 2002; 3:105-110.[CrossRef][Medline]
- Krag D. Why perform randomized clinical trials for sentinel node surgery for breast cancer? Am J Surg 2001; 182:411-413.[CrossRef][Medline]
- Krynyckyi BR, Kim CK, Shafir MK, Mosci K, Machac J. Breast cancer and its management: the utility and technique of lymphoscintigraphy. In: Freeman LM, eds. Nuclear medicine annual, 2003. Philadelphia, Pa: Lippincott Williams & Wilkins, 2003; 131-169.
- Burak WE, Hollenbeck ST, Zervos EE, et al. Sentinel lymph node biopsy results in less postoperative morbidity compared with axillary lymph node dissection for breast cancer. Am J Surg 2002; 183:23-27.[CrossRef][Medline]
- Mariani G, Gipponi M, Moresco L, et al. Radioguided sentinel lymph node biopsy in malignant cutaneous melanoma. J Nucl Med 2002; 43:811-827.[Abstract/Free Full Text]
- Mariani G, Moresco L, Viale G, et al. Radioguided sentinel lymph node biopsy in breast cancer surgery. J Nucl Med 2001; 42:1198-1215.[Abstract/Free Full Text]
- Strickland AH, Beechey-Newman N, Steer CB, Harper PG. Sentinel node biopsy: an in depth appraisal. Crit Rev Oncol Hematol 2002; 44:45-70.[Medline]
- Krynyckyi BR, Firestone M, Eskandar Y, et al. Dual method injection technique for breast lymphoscintigraphy to maximize visualization of sentinel nodes (abstr). J Nucl Med 2000; 41:281.
- Krynyckyi BR, Miner M, Ragonese JM, Firestone M, Kim CK, Machac J. Technical aspects of performing lymphoscintigraphy: optimization of methods used to obtain images. Clin Nucl Med 2000; 25:978-985.[CrossRef][Medline]
- Wong SL, Edwards MJ, Chao C, et al. Sentinel lymph node biopsy for breast cancer: impact of number of sentinel nodes removed on false negative rate. J Am Coll Surg 2001; 192:684-689.[CrossRef][Medline]
- Schrenk P, Rehberger W, Shamiyeh A, Wayand W. Sentinel node biopsy for breast cancer: does the number of sentinel nodes removed have an impact on the accuracy of finding a positive node? J Surg Oncol 2002; 80:130-136.[CrossRef][Medline]
- McCarter MD, Yeung H, Fey J, Borgen PI, Cody HS, 3rd. The breast cancer patient with multiple sentinel nodes: when to stop? J Am Coll Surg 2001; 192:692-697.[CrossRef][Medline]
- Gommans GM, van Dongen A, van der Schors TG, et al. Further optimization of 99mTc-Nanocoll sentinel node localization in carcinoma of the breast by improved labeling. Eur J Nucl Med 2001; 28:1450-1455.[CrossRef][Medline]
- Krynyckyi BR, Zhang ZY, Kim CK, Lipszyc H, Mosci K, Machac J. Effects of high specific activity sulfur colloid preparations on sentinel node count rates. Clin Nucl Med 2002; 27:92-95.[CrossRef][Medline]
- Feldman SM, Krag DN, McNally RK, et al. Limitation in gamma probe localization of the sentinel node in breast cancer patients with large excisional biopsy. J Am Coll Surg 1999; 188:248-254.[CrossRef][Medline]
- Uren RF, Thompson JF, Howman-Giles RB. Sentinel lymph node biopsy in breast cancer. Lancet 1998; 352:1472-1473.[Medline]
- Tanis PJ, Nieweg OE, Valdes Olmos RA, Kroon BB. Anatomy and physiology of lymphatic drainage of the breast from the perspective of sentinel node biopsy. J Am Coll Surg 2001; 192:399-409.[CrossRef][Medline]
- Van der Ent FW, Kengen RA, Van der Pol HA, et al. Sentinel node biopsy in 70 unselected patients with breast cancer: increased feasibility by using 10 mCi radiocolloid in combination with a blue dye tracer. Eur J Surg Oncol 1999; 25:24-29.[CrossRef][Medline]
- Paganelli G, Galimberti V, Trifiro G, et al. Internal mammary node lymphoscintigraphy and biopsy in breast cancer. Q J Nucl Med 2002; 46:138-144.[Medline]
- Borgstein PJ, Meijer S, Pijpers R. Intradermal blue dye to identify the sentinel lymph node in breast cancer. Lancet 1997; 349:1668-1669.[Medline]
- Linehan DC, Hill AD, Akhurst T, et al. Intradermal radiocolloid and intraparenchymal blue dye injection optimize sentinel node identification in breast cancer patients. Ann Surg Oncol 1999; 6:450-454.[Abstract]
- McMasters KM, Wong SL, Martin RC, 2nd, et al. Dermal injection of radioactive colloid is superior to peritumoral injection for breast cancer sentinel lymph node biopsy: results of a multiinstitutional study. Ann Surg 2001; 233:676-687.[CrossRef][Medline]
- Roumen RM, Geuskens LM, Valkenburg JG. In search of the true sentinel node by different injection techniques in breast cancer patients. Eur J Surg Oncol 1999; 25:347-351.[CrossRef][Medline]
- Rettenbacher L, Kassmann H, Galvan G, Menzel C, Reitsamer R, Holzmannhofer J. Lymphoscintigraphy in breast cancer patients: comparison of peritumoural and intradermal injection. Nuklearmedizin 2000; 39:152-155.[Medline]
- Klimberg VS, Rubio IT, Henry R, Cowan C, Colvert M, Korourian S. Subareolar versus peritumoral injection for location of the sentinel lymph node. Ann Surg 1999; 229:860-864.[CrossRef][Medline]
- Mertz L, Mathelin C, Marin C, et al. Subareolar injection of 99m-Tc sulfur colloid for sentinel nodes identification in multifocal invasive breast cancer. Bull Cancer 1999; 86:939-945.[Medline]
- Kern KA, Rosenberg RJ. Preoperative lymphoscintigraphy during lymphatic mapping for breast cancer: improved sentinel node imaging using subareolar injection of technetium 99m sulfur colloid. J Am Coll Surg 2000; 191:479-489.[CrossRef][Medline]
- Alazraki N, Styblo T, Grant S, et al. Optimum injection methods (peritumoral [PT], subdermal [SD] and periareolar [PA]) to image sentinel lymph nodes (SLNs) in breast cancer (abstr). J Nucl Med 2001; 42:116.
- Gambir S, Azad M, Barlow R, et al. Tumor quadrant and depth independent subareolar injection of 99mTc-albumin colloid (AC) and blue dye (BD) in detection of sentinel lymph node/s (SLN) in breast carcinoma (abstr). J Nucl Med 2001; 42:116.
- Winzer KJ, Geworski L, Zander A, Muller J, Munz DL. Prospective intraindividual comparative study of peritumoral and subareolar application of 99mTc nanocolloid in sentinel node (SN) detection in breast cancer (abstr). J Nucl Med 2001; 42:117.[Abstract/Free Full Text]
- Kern KA. Breast lymphatic mapping using subareolar injections of blue dye and radiocolloid: illustrated technique. J Am Coll Surg 2001; 192:545-550.[CrossRef][Medline]
- Tuttle TM, Colbert M, Christensen R, et al. Subareolar injection of 99mTc facilitates sentinel lymph node identification. Ann Surg Oncol 2002; 9:77-81.[Abstract/Free Full Text]
- Valdes-Olmos RA, Jansen L, Hoefnagel CA, et al. Evaluation of mammary lymphoscintigraphy by a single intratumoral injection for sentinel node identification. J Nucl Med 2000; 41:1500-1506.[Abstract/Free Full Text]
- Tanis PJ, Deurloo EE, Valdes Olmos RA, et al. Single intralesional tracer dose for radio-guided excision of clinically occult breast cancer and sentinel node. Ann Surg Oncol 2001; 8:850-855.[Abstract/Free Full Text]
- Doting MH, Jansen L, Nieweg OE, et al. Lymphatic mapping with intralesional tracer administration in breast carcinoma patients. Cancer 2000; 88:2546-2552.[CrossRef][Medline]
- Miner TJ, Shriver CD, Jaques DP, Maniscalco-Theberge ME, Krag DN. Sentinel lymph node biopsy for breast cancer: the role of previous biopsy on patient eligibility. Am Surg 1999; 65:493-498.[Medline]
- Haigh PI, Hansen NM, Qi K, Giuliano AE. Biopsy method and excision volume do not affect success rate of subsequent sentinel lymph node dissection in breast cancer. Ann Surg Oncol 2000; 7:21-27.[Abstract]
- Bass SS, Cox CE, Salud CJ, et al. The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer. J Am Coll Surg 2001; 192:9-16.[CrossRef][Medline]
- Rosser RJ. A point of view: trauma is the cause of occult micrometastatic breast cancer in sentinel axillary lymph nodes. Breast J 2000; 6:209-212.[CrossRef][Medline]
- Rosser RJ. Sentinel lymph nodes and postinjection massage: it is premature to reject caution (letter). J Am Coll Surg 2001; 193:338-339.[Medline]
- Maurer AH, Rodman MS, Vitti RA, Revez G, Krevsky B. Gastrointestinal bleeding: improved localization with cine scintigraphy. Radiology 1992; 185:187-192.[Abstract/Free Full Text]
- Haigh PI, Hansen NM, Giuliano AE, Edwards GK, Ye W, Glass EC. Factors affecting sentinel node localization during preoperative breast lymphoscintigraphy. J Nucl Med 2000; 41:1682-1688.[Abstract/Free Full Text]
- Uren RF, Howman-Giles R, Renwick SB, Gillett D. Lymphatic mapping of the breast: locating the sentinel lymph nodes. World J Surg 2001; 25:789-793.[CrossRef][Medline]
- Pierini A, Dworkin HJ. Is the upright position more sensitive than the supine position in breast cancer sentinel node lymphoscintigraphy? Clin Nucl Med 2001; 26:823-825.[CrossRef][Medline]
- Krynyckyi BR, Kim CK, Goyenechea M, Machac J. Methods to outline the patient during lymphoscintigraphy (letter). J Nucl Med 2003; 44:992.[Free Full Text]
- Clarke E, Notghi A, Harding K. Improved body-outline imaging technique for localization of sentinel lymph nodes in breast surgery. J Nucl Med 2002; 43:1181-1183.[Abstract/Free Full Text]
- Fujii H, Yamashita H, Nakahara T, et al. Outlining the body contour using the scattered photons in lymphoscintigraphy for sentinel nodes (abstr). J Nucl Med 2000; 41:279.
- Paganelli G, Galimberti V, Trifiro G, et al. Internal mammary node lymphoscintigraphy and biopsy in breast cancer. Q J Nucl Med 2002; 46:145-151.[Medline]
- Shimazu K, Tamaki Y, Taguchi T, et al. Lymphoscintigraphic visualization of internal mammary nodes with subtumoral injection of radiocolloid in patients with breast cancer. Ann Surg 2003; 237:390-398.[CrossRef][Medline]
- Krynyckyi BR, Chun H, Kim HH, Eskandar Y, Kim CK, Machac J. Factors affecting visualization rates of internal mammary sentinel nodes during lymphoscintigraphy. J Nucl Med 2003; 44:1387-1393.[Abstract/Free Full Text]
- Lucci A, Jr, Kelemen PR, Miller C, 3rd, Chardkoff L, Wilson L. National practice patterns of sentinel lymph node dissection for breast carcinoma. J Am Coll Surg 2001; 192:453-458.[CrossRef][Medline]
- Cserni G, Szekeres JP. Internal mammary lymph nodes and sentinel node biopsy in breast cancer. Surg Oncol 2001; 10:25-33.[CrossRef][Medline]
- Noguchi M. Internal mammary sentinel node biopsy for breast cancer: is it practicable and relevant? Oncol Rep 2002; 9:461-468.[Medline]
- Veronesi U, Marubini E, Mariani L, et al. The dissection of internal mammary nodes does not improve the survival of breast cancer patients: 30-year results of a randomised trial. Eur J Cancer 1999; 35:1320-1325.
- Bevilacqua J, Gucciardo G, Cody H, et al. A selection algorithm for internal mammary sentinel lymph node biopsy in breast cancer. Eur J Surg Oncol 2002; 28:603-614.[CrossRef][Medline]
- Dupont E, Cox CE, Nguyen K, et al. Utility of internal mammary lymph node removal when noted by intraoperative gamma probe detection. Ann Surg Oncol 2001; 8:833-836.[Abstract/Free Full Text]
- Tanis PJ, Nieweg OE, Valdes Olmos RA, et al. Impact of non-axillary sentinel node biopsy on staging and treatment of breast cancer patients. Br J Cancer 2002; 87:705-710.[CrossRef][Medline]
- Kern KA. A rational approach to internal mammary node biopsy in the era of lymphatic mapping for breast cancer. J Surg Oncol 2002; 79:5-9.[CrossRef][Medline]
- Krynyckyi BR, Kim CK, Mosci K, et al. Areolar-cutaneous "junction" injections to augment sentinel node count activity. Clin Nucl Med 2003; 28:97-107.[CrossRef][Medline]
- Feezor RJ, Kasraeian A, Copeland EM, 3rd, et al. Sequential dermal-peritumoral radiocolloid injection for sentinel node biopsy for breast cancer: the University of Florida experience. Am Surg 2002; 68:684-688.[Medline]
- Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994; 220:391-398.[Medline]
- Cox CE, Pendas S, Cox JM, et al. Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg 1998; 227:645-653.[CrossRef][Medline]
- Cody HS, Fey J, Akhurst T, et al. Complementarity of blue dye and isotope in sentinel node localization for breast cancer: univariate and multivari- ate analysis of 966 procedures. Ann Surg Oncol 2001; 8:13-19.[Abstract/Free Full Text]
- McMasters KM, Tuttle TM, Carlson DJ, et al. Sentinel lymph node biopsy for breast cancer: a suitable alternative to routine axillary dissection in multi-institutional practice when optimal technique is used. J Clin Oncol 2000; 18:2560-2566.[Abstract/Free Full Text]
- Alazraki NP, Styblo T, Grant SF, Cohen C, Larsen T, Aarsvold JN. Sentinel node staging of early breast cancer using lymphoscintigraphy and the intraoperative gamma-detecting probe. Semin Nucl Med 2000; 30:56-64.[CrossRef][Medline]
- Dowlatshahi K, Fan M, Bloom KJ, et al. Occult metastases in the sentinel lymph nodes of patients with early stage breast carcinoma: a preliminary study. Cancer 1999; 86:990-996.[CrossRef][Medline]
- Motomura K, Komoike Y, Inaji H, et al. Multiple sectioning and immunohistochemical staining of sentinel nodes in patients with breast cancer. Br J Surg 2002; 89:1032-1034.[CrossRef][Medline]
- Bostick PJ, Huynh KT, Sarantou T, et al. Detection of metastases in sentinel lymph nodes of breast cancer patients by multiple-marker RT-PCR. Int J Cancer 1998; 79:645-651.[CrossRef][Medline]
- Krag DN, Weaver DL. Pathological and molecular assessment of sentinel lymph nodes in solid tumors. Semin Oncol 2002; 29:274-279.[CrossRef][Medline]
- Salem AA, Douglas-Jones AG, Sweetland HM, Newcombe RG, Mansel RE. Evaluation of axillary lymph nodes using touch imprint cytology and immunohistochemistry. Br J Surg 2002; 89:1386-1389.[CrossRef][Medline]
- Creager AJ, Geisinger KR. Intraoperative evaluation of sentinel lymph nodes for breast carcinoma: current methodologies. Adv Anat Pathol 2002; 9:233-243.[CrossRef][Medline]
- Brenot-Rossi I, Houvenaeghel G, Jacquemier J, et al. Nonvisualization of axillary sentinel node during lymphoscintigraphy: is there a pathologic significance in breast cancer? J Nucl Med 2003; 44:1232-1237.[Abstract/Free Full Text]
- Bass SS, Cox CE, Salud CJ, et al. The effects of postinjection massage on the sensitivity of lymphatic mapping in breast cancer. J Am Coll Surg 2001; 192:9-16.
- Celliers L, Mann GB. Alternative sites of injection for sentinel lymph node biopsy in breast cancer. ANZ J Surg 2003; 73:600-604.[CrossRef][Medline]
Related Article
-
Invited Commentary • Authors' Response
- Gary L. Dillehay, Borys R. Krynyckyi, and Chun K. Kim
RadioGraphics 2004 24: 139-145.
[Full Text]
[PDF]
This article has been cited by other articles:
|
|
|
|
 
M. Thompson, S. Korourian, R. Henry-Tillman, L. Adkins, S. Mumford, M. Smith, and V. S. Klimberg
Intraoperative Radioisotope Injection for Sentinel Lymph Node Biopsy
Ann. Surg. Oncol.,
November 1, 2008;
15(11):
3216 - 3221.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Madsen, P. Gobardhan, V Bongers, M Albregts, J. Burgmans, P De Hooge, J Van Gorp, and T. van Dalen
The Impact on Post-surgical Treatment of Sentinel Lymph Node Biopsy of Internal Mammary Lymph Nodes in Patients with Breast Cancer
Ann. Surg. Oncol.,
April 1, 2007;
14(4):
1486 - 1492.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A F Scarsbrook, A Ganeshan, and K M Bradley
Pearls and pitfalls of radionuclide imaging of the lymphatic system. Part 1: sentinel node lymphoscintigraphy in malignant melanoma
Br. J. Radiol.,
February 1, 2007;
80(950):
132 - 139.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. P. Povoski, J. O. Olsen, D. C. Young, J. Clarke, W. E. Burak, M. J. Walker, W. E. Carson, L. D. Yee, D. M. Agnese, R. V. Pozderac, et al.
Prospective Randomized Clinical Trial Comparing Intradermal, Intraparenchymal, and Subareolar Injection Routes for Sentinel Lymph Node Mapping and Biopsy in Breast Cancer
Ann. Surg. Oncol.,
November 1, 2006;
13(11):
1412 - 1421.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. R. Krynyckyi, S. Sata, I. Zolty, C. K. Kim, and K. Knesaurek
Reducing Exposure from 57Co Sources During Breast Lymphoscintigraphy by Optimizing Energy Windows and Other Suggested Enhancements of Acquisition and the Display of Images
J. Nucl. Med. Technol.,
December 1, 2004;
32(4):
198 - 205.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S H Kim, J Shim, C K Kim, J Machac, and B R Krynyckyi
Reverse echelon node and a lymphatic ectasia in the same patient during breast lymphoscintigraphy: the importance of injection and imaging technique
Br. J. Radiol.,
December 1, 2004;
77(924):
1053 - 1056.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S Sata, K Knesaurek, and B R Krynyckyi
Effective dose in sentinel lymph node imaging
Br. J. Radiol.,
August 1, 2004;
77(920):
709 - 709.
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. L. Dillehay, B. R. Krynyckyi, and C. K. Kim
Invited Commentary * Authors' Response
RadioGraphics,
January 1, 2004;
24(1):
139 - 145.
[Full Text]
[PDF]
|
|
|
Top
Abstract
LEARNING OBJECTIVES
