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Annals of Surgical Oncology 8:234-240 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Internal Mammary Lymph Node Drainage Patterns in Patients With Breast Cancer Documented by Breast Lymphoscintigraphy

David R. Byrd, MD, Lisa K. Dunnwald, BS, David A. Mankoff, MD, PhD, Benjamin O. Anderson, MD, Roger E. Moe, MD, Raymond S. Yeung, MD, Erin K. Schubert, BA and Janet F. Eary, MD

From the Department of General Surgery (DRB, BOA, REM, RSY), Section of Surgical Oncology, and the Division of Nuclear Medicine (LKD, DAM, EKS, JFE), University of Washington Medical Center, Seattle, Washington.

Correspondence: Dr. David R. Byrd, Dept. of Surgery Box 356410, University of Washington Medical Center, 1959 N.E. Pacific St., Seattle, WA 98195; Fax: 206-543-8136; E-mail: byrd{at}u.washington.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Metastases to internal mammary lymph nodes (IMN) may occur in patients with breast cancer and may alter treatment recommendations. The purpose of this study was to identify the frequency of IMN drainage in patients undergoing breast lymphoscintigraphy and sentinel lymph node dissection (SLND).

Methods: The combined technique of peritumoral injection of radiocolloid and Lymphazurin blue for SLND was performed on 220 patients. All patients underwent preoperative lymphoscintigraphy before SLND. Lesion location by quadrant included: 110 upper outer (UOQ), 49 lower outer (LOQ), 30 upper inner (UIQ), 24 lower inner (LIQ), and 7 central.

Results: Drainage to any nodal basin was observed in 184 of 220 patients (84%). IMN drainage was documented in 37 of 220 (17%) of patients. IMN drainage without evidence of axillary drainage occurred in 2 of 220 patients(1%). Drainage to the IMN based on quadrant location of the lesion was as follows: UOQ, 10%; LOQ, 27%; UIQ, 17%; LIQ, 25%; and central, 29%.

Conclusions: Internal mammary lymph node drainage shown by breast lymphoscintigraphy is common. Tumors in all quadrants may drain to IMNs, although drainage is significantly more common from quadrants other than the UOQ. Further studies are needed to determine whether lymphoscintigraphy drainage patterns identify patients at the highest risk for IMN metastases who may benefit from radiotherapy.

Key Words: Internal mammary • Lymphoscintigraphy • Sentinel lymph node • Breast cancer


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sentinel lymph node dissection (SLND) is rapidly evolving as the preferred technique for staging the axilla in patients with invasive breast carcinoma. High success rates of axillary sentinel lymph node (SLN) identification have been reported using perilesional or subdermal injections of vital blue dye, radiocolloid, and combined techniques.1–4 Although vital blue dye does not routinely lead to the preoperative recognition of alternative drainage patterns, preoperative breast lymphoscintigraphy with an anterior chest view after radiocolloid injection can reveal potential regional drainage sites outside of the axilla.

The most important drainage site outside of the axilla is the internal mammary lymph node (IMN) chain. Freedman and colleagues5 have extensively reviewed the historical and recent data regarding IMNs in breast cancer. These authors note that only a subset of tumors have potential drainage to the IMN chain. In addition, the clinical recurrence rate in the IMN chain is rare, even in axillary node-positive patients treated by modified radical mastectomy (MRM) and adjuvant systemic therapy alone.5–9 Past studies of extended radical mastectomy (ERM) in operable breast cancer showed a prevalence of positive IMNs in 8% to 20% of patients, but the axilla also was involved in most of these patients. Randomized, prospective trials have failed to show a survival benefit in patients undergoing ERM as opposed to MRM.10–12 However, in several other series, patients harboring regional metastases in both the axillary and internal mammary lymph nodes had a worse prognosis than did patients with isolated axillary metastases.11,13–15

Current clinical approaches to breast cancer do not include sampling the IMN. Nevertheless, renewed interest in the IMN chain has developed due to recent reports showing improved survival in large randomized clinical trials in which postmastectomy radiation included the internal mammary field.16–18 Ideally, IMN radiotherapy would be based on the documentation of IMN metastases. However, there has not been a reliable technique to identify patients with IMN drainage prior to surgery and thus to direct biopsy in patients at risk for metastases. This difficulty was highlighted in a recent article with accompanying editorial reviewing IMN radiation therapy in breast cancer.5,19 Early attempts at directed IMN biopsy were limited to patients with medial hemispheric lesions, because it was widely believed that lateral hemispheric tumors would not drain to the IMNs. This opinion contradicts the infrequently cited work by Turner-Warwick20 and others,21–23 who conducted early studies of breast lymphoscintigraphy using intramammary injections of radiolabeled gold and other elements in the breasts of volunteers without known cancers. In these studies, the internal mammary chain was shown to be an important pathway of lymphatic drainage from both the medial and lateral regions of the breast.

Several investigators using radiocolloid lymphoscintigraphy to guide axillary SLND in breast cancer patients observed IMN chain drainage. Results are summarized in Table 1, showing a range from 0% to 35%, with a median of 17%. Isolated IMN drainage, without axillary drainage, appears to be rare. The large study by Krag et al.24 identified a drainage rate of 4%; however this study used radiocolloid and a hand-held gamma probe for SLN localization without lymphoscintigraphy prior to surgical mapping. Van der Ent and colleagues25 attempted IMN retrieval in 15 patients. Others have attempted excisional biopsy of the IMN in a small number of patients, with a selected number of cases reporting positive nodes.5,24,26 Investigators using lymphoscintigraphy and subdermal or intradermal injections of radiocolloid before SLND report little or no frequency of IMN drainage using this injection technique.4,27


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  		TABLE 1. Lymphatic drainage to the IMN chain detected by lymphoscintigraphy
 
Our study was undertaken to determine the frequency of internal mammary lymph node drainage by breast lymphoscintigraphy using standard gamma camera imaging techniques. This study differs from earlier reports in either the larger number of patients studied or the inclusion of lymphoscintigraphy as opposed to gamma probe mapping without imaging to identify IMN drainage. Lymphoscintigraphic imaging is likely to be superior to hand-held gamma probe measurements to observe drainage to nodal basins outside of the axilla. The purpose of this study was to identify patients who should be considered for further evaluation of the IMNs by other imaging methods or tissue biopsy.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
From October 1996 through November 1999, preoperative lymphoscintigraphy was performed on 220 patients (219 women and 1 man) undergoing lymphatic mapping and axillary SLND for breast carcinoma. The mean age was 55 years (range, 26–88 years). All patients had a preoperative diagnosis of invasive breast carcinoma (n = 211) or ductal carcinoma in situ (n = 9). Patients with a confirmed diagnosis of DCIS included in this study had a high clinical suspicion of invasive disease and therefore were offered SLND. TNM staging was determined by final pathology unless the patient underwent neoadjuvant (preoperative) chemotherapy, in which case staging was based on clinical findings. The primary lesion size in this patient population was as follows: 9 Tis lesions; 145 T1 lesions (<= 2 cm); 52 T2 lesions (2–5 cm); 12 T3 lesions; and 2 T4 lesions. The location of the primary tumor was recorded at the initial preoperative visit and noted on the lymphatic mapping Nuclear Medicine request form. Among the 220 patients, there were 110 lesions located in the upper outer quadrant (UOQ) of the breast, 49 in the lower outer quadrant (LOQ), 30 in the upper inner quadrant (UIQ), and 24 in the lower inner quadrant (LIQ). Seven patients had subareolar or centrally located lesions. One hundred and twenty-two tumors were palpable masses or palpable cavities from recent excisional biopsy, and 98 were nonpalpable abnormalities requiring mammography or ultrasound localization for excision as part of planned breast conservation surgery. Diagnosis before the definitive breast procedure was by core needle biopsy in 167 patients. Thirty-seven patients had a prior excisional biopsy for diagnosis, 14 patients had prior neoadjuvant chemotherapy for locally advanced breast cancer, and two patients had both prior excisional biopsy and neoadjuvant chemotherapy (Table 2). One hundred and twenty-two patients underwent sentinel lymph node biopsy with axillary dissection as part of an initial study to validate our axillary sampling approach, and 98 patients underwent sentinel lymph node biopsy without completion node dissection. Protocol patients signed informed consent documents approved by the University of Washington Human Subjects and Radiation Safety Committees.


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  		TABLE 2. Patient characteristics (n = 220)
 
Lymphoscintigraphy
All patients underwent breast lymphoscintigraphy on the day of the SLND in the Nuclear Medicine suite. The full imaging and sentinel lymph node location and identification procedure has been described previously.28 Briefly, patients received a midplane, peritumoral, intraparenchymal injection of 1 mCi filtered 99mTc-sulfur colloid in a total 6 to 10 ml volume in four quadrants surrounding either the primary breast tumor or the breast tumor biopsy site. For nonpalpable lesions, a single 6- to 10-ml injection was made through a localization needle using a catheter placed under mammographic or ultrasound guidance. Lymphoscintigraphy was performed using a standard single-head gamma camera (GE Starcam 300 AC or GE Starcam 2000 XCT) equipped with a high resolution collimator. All patients were imaged immediately postinjection until an axillary SLN was visualized or for a maximum of 2 to 3 hours postinjection, with the exception of four patients who were injected the evening before the planned SLND. For these cases, one immediate postinjection image was acquired, and a mark was made on the skin if a SLN was visualized. Whether or not a node was identified on imaging the prior evening, the patient returned to Nuclear Medicine the following morning for delayed imaging and skin marking of the SLN. Following SLN axillary imaging and marking, a static anterior thorax image was acquired in all patients to document drainage to internal mammary lymph nodes (Fig. 1). An additional marker image was acquired identifying the sternal notch and the xiphoid process to depict the location of any IMNs seen on lymphoscintigraphy. All lymphoscintigraphy studies were interpreted prospectively by a board-certified Nuclear Medicine specialist.



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  		FIG. 1. Lymphoscintigraphy in a patient with a lower outer quadrant tumor demonstrating drainage to a sentinel lymph node in the axilla (closed arrow) in addition to drainage to an internal mammary lymph node (open arrow).

 
Sentinel Lymph Node Dissection
All patients underwent axillary lymphatic mapping and SLND 1 to 18 hours after breast lymphoscintigraphy. The sentinel lymph node in the axilla was identified using a combined technique of peritumoral blue dye (3–5 ml isosulfan blue) injection and a hand-held gamma probe (Neoprobe, Neoprobe Corp., Dublin, OH; Navigator, U.S. Surgical Corp, Norwalk, CT). All initial protocol patients had the SLN identified, removed, and sent separately at the time of a planned levels I and II completion axillary node dissection. After April 1998, our practice plan changed to SLND without completion axillary dissection for patients with T1 primary tumors (<= 2 cm) diagnosed by core needle biopsy for whom the SLN was found to be without metastatic disease.29 These patients underwent completion axillary node dissection if any SLN was found to harbor metastatic disease on frozen section or permanent pathology. Internal mammary lymph nodes were not sampled as part of our protocol.

Statistical Methods
Differences in the rate of IMN drainage as a function of primary tumor site or tumor size were tested for statistical significance by analyzing contingency tables using the Pearson {chi}2 analysis. The frequency of IMN drainage versus the presence or absence of axillary nodal metastases also was tested using the Pearson {chi}2 statistic. All statistical analyses were performed using the JMP statistical package (SAS Institute, Cary, NC).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Lymphoscintigraphy
Lymphoscintigraphy successfully identified lymphatic drainage to any lymph node basin in 184 of 220 patients (84%). Drainage to the axilla was seen in 182 of 220 patients (83%). Drainage to one or more IMNs was seen in 37 of 220 patients (17%) overall and in 37 of 184 patients (20%) when lymphoscintigraphy was successful. Isolated IMN drainage only was demonstrated in 2 of 220 patients (1%). The location of the primary tumor in these two patients was the UOQ in one and the LOQ in the other.

Drainage to the IMNs could be seen with the primary breast tumor located in any quadrant of the breast, including lateral hemispheric lesions (Fig. 2). Quadrants other than the UOQ had 17% to 29% drainage to the IMNs. Analyzing the frequency of IMN drainage using only the subset of 184 patients showing drainage to any basin, the rate of IMN drainage was as follows: UOQ, 11 of 89 patients (12%); UIQ, 5 of 24 patients (21%); LOQ, 13 of 44 patients (30%); LIQ, 6 of 20 patients (30%); and central, 2 of 7 patients (29%).



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  		FIG. 2. Internal mammary lymph node drainage patterns in the breast based on tumor location as documented by lymphoscintigraphy.

 
There was a statistically significant difference (P < .01) when comparing the rate of IMN drainage in the UOQ versus all other quadrants (10% UOQ versus 24% all other quadrants). There was no statistically significant difference within any of the other quadrants (UIQ vs. LIQ vs. LOQ vs. central lesions) (P = .76). There was no association between frequency of IMN drainage and tumor size (P = .20) (Table 3).


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  		TABLE 3. Primary tumor size and frequency of IMN drainage (n = 220)
 
Sentinel Lymph Node Dissection
An axillary SLN was identified in 194 of the 220 patients (88%). The localized SLN was both blue and radioactive in 128 of 194 (66%) cases, blue only in 21 of 194 (11%), and radioactive only in 45 of 194 (23%). Surgical exploration of the IMN chain was not performed. In 173 of 220 cases (79%), a patient was successfully imaged by lymphoscintigraphy, and a SLN was found in surgery. In 21 patients, no SLN was localized by lymphoscintigraphy, but a SLN was identified in surgery. In the group of patients with unsuccessful preoperative nodal imaging, a blue and radioactive lymph node (ex vivo counts higher than 3:1 over axillary bed counts) was found in 9 patients. A discrete blue-stained, nonradioactive lymph node with incoming blue afferent channels was found in 10 patients, and a radioactive-only SLN was found using the gamma probe in 2 patients. In addition, there were 11 patients in whom a SLN was documented by lymphoscintigraphy but could not be localized at the time of surgical resection.

Pathology
Sixty-two of 220 patients overall (28%) had axillary lymph nodes positive for metastases. The frequency of positive axillary nodes based on the size of tumor is summarized in Table 4. Axillary nodal status versus drainage or no drainage to the IMN as documented by lymphoscintigraphy is shown in Table 5. This was not found to be statistically significant (P = .3). After our pilot protocol with concomitant axillary node dissection, sentinel lymph node biopsy was performed without required complete axillary dissection on 122 patients, with a success rate of 93% (113/122). Twenty-two patients in this group had a positive SLN and went on to a completion axillary dissection. In 17 of 22 patients (77%), the SLNs were the only positive node; the mean number of SLNs excised was 2 (range, 1–11).


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  		TABLE 4. Primary tumor size and axillary nodal pathology (n = 220)
 

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  		TABLE 5. Axillary sentinel node pathology and IMN drainage (n = 220)
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Traditional surgical teaching has suggested that only primary tumors in the medial half of the breast drain to the IMN.30 However, it has been known for some time that all four quadrants can have lymphatic pathways to internal mammary lymph nodes. The largest clinical study of extended radical mastectomy suggested that metastases to IMN occurred with equal frequency whether the primary breast tumor was in the inner quadrants (19.1%), the outer quadrants (18%), or the central breast (22.1%).11 Our results using lymphoscintigraphy also suggest that IMN drainage can occur with tumors in any quadrant; however, the UOQ has a significantly lower rate of drainage than all other quadrants, in which IMN drainage frequencies are 17% to 27%. We did not find an association between tumor size and IMN drainage. Isolated drainage to the IMN was a rare event in our series. This is consistent with the previously established finding that most patients with IMN metastases also have axillary metastases.15,31

Our study is the largest reported study to date documenting IMN drainage by breast lymphoscintigraphy. Other studies using peritumoral radiocolloid injection and lymphoscintigraphy have found similar results (Table 1). Krag et al.24 reported a lower incidence of drainage to IMN, but their SLN mapping technique used only an intraoperative gamma probe without preoperative lymphoscintigraphy to document IMN drainage. Experience with melanoma mapping suggests that imaging is important to identify areas of drainage when more than one drainage site is possible.32–34 Recent studies from the Memorial Sloan-Kettering Cancer Center reported lymphoscintigraphy results in 200 consecutive breast cancer patients comparing intraparenchymal versus intradermal radiocolloid injection techniques.27 Preoperative lymphoscintigraphy did not show any lymphatic drainage to the IMNs in either of the two groups. The fact that there was no reported drainage in 100 patients receiving intradermal injections can be explained by the absence of skin drainage to IMNs, observed in breast and chest wall skin injections during lymphoscintigraphy for melanoma.33 However, the absence of any IMN drainage after intraparenchymal injection in 100 patients is perplexing, and no explanation is given. A preliminary study using subdermal injections by Veronesi et al.4 reported IMN visualization in 1% of cases.35 The discrepancy with these studies needs clarification before there is universal acceptance of the technique of intradermal or subdermal injections for lymphatic mapping in breast cancer patients.

One limitation of our study is that we did not sample IMN; therefore, we have documented drainage to the IMNs, not IMN metastases. It is evident the incidence of axillary nodal metastases is lower than the number of cases demonstrating axillary lymphatic drainage. Similarly, the rates of IMN metastases cited in the literature are lower than IMN drainage rates. Fifteen of 24 patients studied by Van der Ent et al.25 had a successful biopsy of an internal mammary SLN, and 5 of 15 cases proved positive for IMN metastases. Five patients studied at the Fox Chase Cancer Center with documented lymphatic drainage to the IMN chain by lymphoscintigraphy had open biopsy of the nodes that pathologically proved to be negative.5 Prospective studies are needed to identify the subset of patients at risk for IMN metastases.

Biopsy of the IMN may be more difficult than the axillary node biopsy.26 Removal of IMNs often requires a separate incision in patients receiving breast conservation therapy for the primary tumor and carries a risk of pain, bleeding, and pneumothorax from entry into the pleura. Image-guided fine-needle aspiration may be an alternative method of IMN tissue evaluation if an abnormal node can be seen.

Many authors suggest that biopsy and treatment of the IMN chain does not improve outcome in the general breast cancer patient population. However, the general breast cancer population has a high rate of UOQ lesions, which have a significantly lower rate of IMN drainage by our data. Lymphoscintigraphy can identify the subset of patients who are at risk and may benefit from biopsy and, possibly, radiotherapy. There is renewed interest in chest wall irradiation in axillary node-positive patients who have had mastectomy, with a suggestion of possible benefit in survival.16–18 The IMN nodal chain is not routinely irradiated in patients receiving whole breast or chest wall irradiation unless IMN nodal disease is suspected or known. Potential benefit has been suggested both for local control and survival in subsets of patients who have positive IMN nodes. Information on IMN status is likely to be complementary to axillary lymph node status in the subset of patients who are at an increased risk of IMN metastases. We are beginning a prospective trial to obtain nodal tissue in selected patients at higher risk of harboring IMN metastases. We hope to define subsets of patients where further IMN imaging or intervention is appropriate to improve staging and treatment of breast cancer patients.


   Acknowledgments
 
This work was supported in part by NIH Grant CA72064.

Received for publication June 20, 2000. Accepted for publication October 26, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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