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Modified Alcian blue enhances the intraoperative diagnosis of sentinel lymph node metastasis in invasive lobular carcinoma: a prospective study.

Sentinel lymph node (SLN) biopsy is routinely done in women with a diagnosis of invasive breast cancer to determine the presence or absence of axillary metastasis. It is a minimally invasive technique that involves selectively removing axillary lymph nodes that have been identified through various mapping techniques. An intraoperative diagnosis of SLN metastasis facilitates definitive axillary staging because it allows the surgeon to perform a completion axillary dissection during the same surgery if a SLN is found to be positive for metastatic cells. (1,2) The sensitivity of intraoperative diagnosis has been especially low in connection with the metastases and micrometastases of invasive lobular carcinoma (ILC). (3-5) Immunohistochemistry (IHC) (6-10) as well as polymerase chain reaction (PCR) methods have enhanced the detection of positive results from SLNs in breast cancer. (11-13) However, these methods are time consuming and labor intensive. They also increase anesthesia time for patients and cost per surgery because of increased time in the operating room. Because lobular carcinoma cells produce mucin that can be detected by Alcian blue special stain on formalin-fixed, paraffin-embedded (FFPE) tissue section, (14-16) we sought to examine the possibility of modifying this stain to be used on touch preparation (TP) of SLN in patients with ILC.


Standardization of Modified Alcian Blue Stain

Modifying conventional Alcian blue (pH 2.5; Poly Scientific, Bay Shore, New York) required multiple steps. All steps were carried out by using a known ILC that expressed mucin proven by conventional Alcian blue stain on FFPE tissue. In this study, conventional Alcian blue stain on a FFPE case of primary ILC was performed in anticipation of receiving fresh tissue containing metastatic tumor to the ovary. On receiving the metastatic ILC to ovary specimen, fresh scrapings from the tumor cells were used for all steps (scraping was performed right before starting each experiment). One slide was stained with hematoxylin-eosin (H&E) to verify the presence of tumor cells. The main 3 steps were modified in a stepwise fashion. With FFPE specimens, the procedure usually takes more than 38 minutes: First, the slide is immersed in 3% glacial acetic acid for 3 minutes, then stained with Alcian blue (pH 2.5) for 30 minutes, and finally counterstained with nuclear fast red for 5 minutes. The process was modified as follows: First, Alcian blue time was decreased to 20, 10, 5, 3, 2, and 1 minute, keeping all other times the same (glacial acetic acid [Poly Scientific] and nuclear fast red [also called Kernechtrot, Poly Scientific). At the 2 minute to 1 minute cutoff, the staining started to become negative. Therefore, the 2-minute time was fixed, and the rest of the procedure was carried out by decreasing nuclear fast red to glacial acetic acid times of 2 minutes to 3 minutes, 1 minute to 3 minutes, and 2 minutes to 2 minutes. The stain remained positive only when the 2 minute to 3 minute time was used. Therefore, the following steps were considered optimal for the purpose of the study:

1. Prepare slides by touching the cut section of SLN.

2. Transfer slides to 95% ethanol for 2 minutes.

3. Transfer slides to 3% glacial acetic acid solution for 2 minutes.

4. Transfer slides to Alcian blue stain (pH 2.5) for 2 minutes.

5. Rinse in tap water for 30 seconds.

6. Transfer to nuclear fast red solution for 3 minutes.

7. Rinse in tap water for 30 seconds.

8. Dehydrate with 2 changes each of 95% and 100% ethanol, then clear in xylene, and add a coverslip.

Standard Procedure for Intraoperative Diagnosis Staining and Reporting Process and Reading Conventional Staining

Each lymph node was serially sectioned and touch preparations were made and stained with H&E, modified Diff-Quik Giemsa stain, or both (based on an assigned pathologist preference) for intraoperative diagnosis. The pathologist then reported the SLN findings as positive, negative, or atypical. Intraoperative diagnosis was made without the modified Alcian blue finding. For the H&E stain, TP slides were first fixed in 100% alcohol and then transferred sequentially to the following solutions (with the time of immersion), tap water (30 seconds), hematoxylin (1 minute), 70% alcohol (10 seconds), twice in 90% alcohol (10 seconds, each), 100% alcohol (10 seconds), eosin (30 seconds), 90% alcohol (10 seconds), 100% alcohol (10 seconds), and finally twice in xylene (10 seconds, each) before applying coverslip. For the Diff-Quik Giemsa stain, TP slides were fixed in methanol for 30 seconds, cleared with water for 10 seconds, dipped 25 times in solution 1 (xanthene dye-eosin Y), dipped 25 times in solution 2 (thiazine dyemethylene blue, Azure A), then rinsed with water and moved consecutively to 95% ethanol, 100% ethanol, and xylene before applying a coverslip. Each case was read by one assigned pathologist among 10 different pathologists. All conventionally stained slides were then reviewed by one pathologist (T.K.) prospectively and retrospectively in a blinded fashion to the modified Alcian blue findings.

Modified Alcian Blue Staining Process

The staining procedure was setup in the frozen section room. Patients with a diagnosis of ILC or mammary carcinoma with ductal and lobular features on a needle core biopsy who were scheduled for lumpectomy with SLN surgery were eligible for the study. Patients undergoing SLN biopsy were identified the day before the procedure, and their pathology reports were reviewed to determine eligibility. E-cadherin (clone 36B5, Dako, Carpinteria, California; dilution, 1:50 DakoCytomation high pH, targeted silver retrieval) stain was performed on the excisional biopsy. Cases that stained positive (ductal phenotype) were excluded from the study. Each lymph node was serially sectioned, and TPs were made and stained with H&E, Diff-Quik Giemsa, or both for intraoperative diagnosis. To avoid sampling bias, one TP from the same area that was sampled for intraoperative diagnosis was sampled for the modified Alcian blue staining.

Comparing Conventional Staining and Modified Alcian Blue Results With Permanent Section Results

Alcian blue (pH 2.5) stain was used on the FFPE section of lymph nodes staining positive to compare the staining with the TPs stained with modified Alcian blue, and were reported as negative or positive. All permanent lymph node sections were stained with cytokeratin (AE 1/3, Dako; dilution, 1:100 with proteinase K similar to the silver retrieval). For AE 1/3 and Ecadherin staining, sections were cut at 5 mm, placed on charged slides, and dried in a 60[degrees]C oven for 1 hour. On return to room temperature, the slides were deparaffinized in 3 changes of xylene and rehydrated using graded alcohols. Endogenous peroxidase activity was quenched with aqueous 3% hydrogen peroxide for 15 minutes and washed with phosphate-buffered saline and 0.05% Tween-20 (PBS-T). Antigen retrieval was then performed. After a PBS-T wash, casein 0.03% (in PBS-T) was used as a block for 30 minutes, and then the primary antibody was applied to the slides and left for 30 to 60 minutes. The PBS-T wash was followed by a biotinylated secondary antibody for 30 minutes, and the PBS-T was followed by a streptavidin complex for 30 minutes. The PBS-T was used as a wash, and the chromagen 3,3'-diaminobenzidine (Dako) was applied for 5 minutes (the color reaction product was brown). The slides were counterstained with hematoxylin and recorded as either positive or negative. The size of the tumor metastasis was measured based on American Joint Committee on Cancer recommendations. (17)

Clinical and Pathologic Findings

Patients' age and tumor size were recorded. Tumors were subtyped based on the World Health Organization classification, (18) as classic, solid, alveolar, pleomorphic (with histiocytoid or apocrine differentiation), or as a mixed pattern (classic and one or more subtype). A modified Bloom-Richardson grading system was used to grade tumors (from grade 1 to grade 3).

Statistical Analyses

Accuracy is defined as the ratio of correct test results (true-positive and true-negative) divided by the total number of tests (true-positive + true-negative + false-positive + false-negative). Sensitivity is defined as the ratio of true-positive test results divided by the sum of the true-positive and false-negative results. Specificity is defined as the ratio of true-negative test results divided by the sum of the true-negative and false-positive results. Data were compiled using Microsoft Access database software (Microsoft, Redmond, Washington). Statistical analyses were made with GraphPad InStat software (version 3.05; GraphPad Software, San Diego, California).



This prospective study took place at Roswell Park

Cancer Institute (Buffalo, New York) for the 2006 to 2008

period. A total of 31 patients were included; a total of 121 SLNs were examined (the median number of SLNs per patient was 4). Patients' ages ranged from 35 to 87 years, with median of 62 years. Tumor sizes were between 0.1 and 8 cm, with a median of 2 cm. Histologically, there were 14 cases (45%) with a modified Bloom-Richardson grade 1, 16 cases (52%) with grade 2, and 1 case (3%) with grade 3. There were 23 cases (74%) subtyped as classic, 3 (10%) as solid, 3 (10%) as mixed (classic and trabecular), and 2 (6%) as pleomorphic types (histiocytic).

Morphology of False-Negative Cases by Conventional Staining

False-negative cases were retrospectively reviewed. The false-negativity was due to either the presence or the rare, but convincingly positive, cells that were missed, or to the loosely cohesive, low nuclear-grade cells that resembled benign histiocytes (Figure 1). Three lymph node samples in 2 patients (patients 7 and 8; Table 1) were false-negatives by conventional staining and by modified Alcian blue. Reviewing those slides revealed no convincing evidence of the presence of tumor cells with either stain. The tumor metastases measured 0.9, 1, and 1.8 mm, respectively.


Morphology of Modified Alcian Blue Staining in ILC

Positive cells showed one of the following staining patterns (Figure 2): (1) an eccentric targetoid, with blue, mucinous globules; (2) overlapping, dense, blue, homogenous globules, present in touch preparations with tumor nuclei; (3) 1 or 2 dotlike globules, with homogenous, dense, blue material (Figure 2, A); (4) a detached targetoid, with blue, mucinous globules (Figure 2, B); (5) homogenous, blue, mucinous globules, surrounded by tumor cells (Figure 2, C); or faint, irregular, eccentrically located, mucinous material (Figure 2, D).

Interpreting Modified Alcian Blue TPs

First, at screening magnification (X10), we looked for blue staining, which might be plasma cells, mast cells, muciphages, or positive lobular carcinoma cells. On higher magnification (X 20 or X 40), positive tumor cells showed a distinctive staining pattern (as discussed above; Figure 3).


Plasma Cells.--Plasma cells showed cytoplasmic, blue granules that completely or partially surrounded a "cartwheel" nucleus (Figure 3, A). This morphology was considered a positive internal control throughout the study.

Muciphages.--Mucinous material in the muciphages was either small, fragmented, dotlike, irregular material (Figure 3, B), or a more diffuse, ragged, faint-blue material that surrounded at least 50% of the nuclear contour (Figure 4, A).


Extracellular Immunoglobulin.--Extracellular immunoglobulin material, in comparison with mucinous material, was denser and more bluish (Figure 4, B). Two features can be used to differentiate this material from mucinous material. First, the extracellular immunoglobulin was more of the extracellular material seen between the nuclei, and second, evaluating the harboring nuclei showed they are relatively smaller than the tumor cells.

Nuclear Overlapping.--Nuclear overlapping is usually easily solved by moving the focusing up and down. Also, higher magnification shows the benign features of the nuclei (Figures 4, C and D).

Results of Comparing the Modified Alcian Blue With the Intraoperative Diagnosis and the SLN Permanent Sections

The test results for patients with a finding of at least one positive SLN are outlined in Table 1. There were a total of 18 positive SLN results in 11 patients. Although the modified Alcian blue test results showed 15 of 18 positive SLN samples (83.3%) with an accuracy of 97.3%, conventional staining results showed 10 of 18 (55.6%) positive SLN samples with an accuracy of 92.8% (Table 2). Tumor metastasis size ranged from 0.9 to 15 mm, with median of 4.5 mm. Micrometastasis (<2.0 mm) was present in 6 of 18 positively stained SLN samples. All 6 SLN samples with micrometastases, in addition to 2 SLN samples with macrometastases, produced false-negative results with conventional staining. Modified Alcian blue staining showed 3 of the 6 micrometastases (50%) and all the macrometastases. One case had weak conventional Alcian blue staining on a permanent section and weak modified Alcian blue on a TP (Figure 2, D and inset). If cytoplasmic staining was used exclusively in making the diagnosis, that case would have been misdiagnosed as negative for metastases. We noticed that such staining can be seen in muciphages (Figure 4, A and inset). One way to avoid this pitfall is to compare the tumor nucleus with the muciphage nucleus. Modified Alcian blue also has the advantage of maintaining the morphologic details of the nuclei.



Metastatic lobular carcinoma, as a histologic subtype of breast carcinoma, remains a challenge for histopathologic evaluation. (4,19) It metastasizes to the lymph nodes in a scattered fashion, without severe cytologic atypia. Metastatic cells tend to fill the sinuses, mimicking sinus histiocytosis. (19) On TPs, these cells are even more difficult to interpret because they resemble histiocytes. A variable proportion of cells have intracytoplasmic lumina containing demonstrable sialomucins with the mucicarmine and Alcian blue stains. (14-16) When that region is prominent, the cells have a signet ring configuration. (20) With the aforementioned stains, it is often possible to detect the small amount of secretion in the nonsignet ring cells. (21) Many methods have aimed at increasing the accuracy of the SLN intraoperative diagnosis, including special stains, IHC, and PCR. Special stains have included the toluidine blue, (10,22) Papanicolaou, (23) Diff-Quik, (24) and Giemsa (25) stains, all of which attempted to improve the nuclear morphology. Immunohistochemistry methods for increasing the accuracy have included applied cytokeratin staining. (6-10) Quantitative and nonquantitative, real-time PCR tests have targeted the presence of tumor-specific molecules, like cytokeratin 19 and mammaglobin. (11-13) None of these methods took advantage of the lobular carcinoma cells, which in most cases, produce mucin, and which can be detected by special stains including Alcian blue. (16)

Several factors encouraged us to use the lobular carcinoma cell trait of producing mucin to develop a fast, reliable staining process, aiming for an easy, accessible, and specific target of intracytoplasmic mucin. These factors included the difficulty of assessing SLN TP in patients with ILC by conventional staining, the variable and conflicting results regarding the use of variable procedures (TP versus frozen section), and the limitations of the most sensitive methods (IHC and PCR), which include the relative difficulty, the need for technical expertise, and the relatively lengthy process involved. Although IHC procedures take from 15 to 20 minutes, (9,10) a PCR takes about 36 to 46 minutes.8 We, therefore, thought of modifying the Alcian blue stain so that it could be used for SLN intraoperative diagnosis in patients with ILC. We ran a few validating tests on fresh ILC samples and gradually decreased the time of various steps to reach the highest sensitivity within the shortest period (11 minutes). We also tried mucicarmine, but that was unsuccessful. Invasive ductal carcinoma, particularly modified Bloom-Richardson grades 2 and 3, is easier to interpret. These tumors express mucin and are more difficult to detect (detection rate, 20%) with conventional Alcian blue (pH 2.5) than is ILC (detection rate, 90%). (16) Therefore, we excluded these cases from our study.


Our main finding was that modified Alcian blue staining in SLN TPs can enhance the accuracy of detecting metastatic lobular carcinoma cells compared with conventional staining, including H&E and Diff-Quik Giemsa. Although both methods had a specificity of 100%, modified Alcian blue was considerably better than conventional staining in sensitivity and in decreasing the rate of false-negatives. The false-negative rate can sometimes be as high as 67%. (26) At our institution, although the false-negative rate is reported in the literature as 46%, (27) our current false-negative rate is 27% (data not published). Therefore, given our better performance, this method might prove valuable at other institutions as well.

There are few studies that examine ILC only. Therefore, it is difficult to compare our results with what has been published. Creager et al, (5) used H&E and Diff-Quik Giemsa and reported a sensitivity rate of 52%, a specificity rate of 100%, and an accuracy rate of 82%. Those results are consistent with what ours were when we used conventional staining. However, in our series, using modified Alcian blue staining increased the specificity and accuracy. Leikola et al (10) examined 2 cohorts of patients with ILC, one using toluidine blue stain and one using IHC. They found that, when compared with the toluidine blue, IHC enhanced the diagnostic findings of positive lymph nodes (66% versus 87%, respectively). By comparing those results with our data, the modified Alcian blue appears to be equal to IHC.

During our experiences with this staining, we were able to record variable staining morphologies and possible pitfalls. More prospective studies on larger cohorts are required to validate our results as well as to explore more possible staining morphologies and pitfalls. However, we believe that using this stain could be of tremendous help in interpreting the most morphologically challenging cases, particularly in small, remote, community hospitals that have less access to more advanced methodologies as well as less expertise in this field.


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Thaer Khoury, MD; Deborah Malik, MS; Cathy Fan, MD; Dongfeng Tan, MD; Swati Kulkarni, MD

Accepted for publication January 15, 2010.

From the Departments of Pathology (Drs Khoury and Fan and Ms Malik) and Surgical Oncology (Dr Kulkarni), Roswell Park Cancer Institute, Buffalo, New York; and the Department of Pathology, M. D. Anderson Cancer Center, Houston, Texas (Dr Tan).

The authors have no relevant financial interest in the products or companies described in this article.

Reprints: Thaer Khoury, MD, Roswell Park Cancer Institute, Elm and Carlton Streets, Buffalo, NY 14263 (e-mail:
Table 1. Characteristics of Positively Stained Lymph Node Metastasis
in Invasive Lobular Carcinoma Cases

Case SLN Size of
No. No. CS MAB IHC Metastasis, mm

1 1 0 1 1 5.0
2 1 + + + 8.0
 2 + + + 4.0
3 1 2 + + 4.0
4 1 + + + 11.0
5 1 2 + + 1.4
 2 + + + 5.0
6 1 2 + + 1.5
 2 2 + + 1.0
7 1 0 0 1 0.9
8 1 2 2 + 1.0
 2 2 2 + 1.8
 3 + + + 9.0
 4 + + + 8.0
9 1 + + + 15.0

10 1 + + + 6.0
 2 + + + 4.0
11 1 + + + 8.0
Total 18 10 15 18 0.9-15.0 (4.5) (a)

Case Tumor
No. Size, cm SBR Type

1 7.5 1 Classic
2 2.5 1 Classic

3 2.3 2 Classic
4 6.0 1 Classic
5 1.8 2 Solid

6 3.0 2 Classic

7 0.7 2 Classic
8 2.0 1 Classic

9 1.7 2 Pleomorphic,
10 2 2 Classic

11 2.3 2 Classic
Total 0.7-7.5 (2.3) (a)

Case Signet [AB.sup.+]
No. Ring, % Cells, %

1 5 30
2 40 60

3 40 60
4 1 20
5 10 10

6 0 5

7 10 10
8 1 20

9 5 90

10 5 20

11 30 30

Abbreviations: AB, Alcian blue; CS, conventional staining; ER-PR,
estrogen receptor-progesterone receptor; IHC, immunohistochemistry;
MAB, modified Alcian blue; SBR, modified Bloom-Richardson score; SLN,
sentinel lymph node.

(a) Range (median).

Table 2. Comparison of the Detection Rate of Sentinel Node Metastasis
Intraoperatively With Hematoxylin-Eosin, Modified Alcian Blue, and
Permanent Section Immunohistochemistry Staining

 Per-Patient Basis (N = 31)

Characteristic Final (a) MAB CS Final

Positive results 11 10 (b) 7 18
Negative results 20 21 24 (c) 103
False-negatives 1 4
False-positives 0 0 (c)
Sensitivity 90.9 63.6 (c)
Specificity 100 100
Accuracy 96.8 87.1

 Per-Node Basis (N = 121)

Characteristic MAB CS

Positive results 15 (b) 10
Negative results 106 111 (c)
False-negatives 3 (b) 8
False-positives 0 0 (c)
Sensitivity 83.3 55.6 (c)
Specificity 100 100
Accuracy 97.3 92.8

Abbreviations: CS, conventional staining; MAB, modified Alcian blue.

(a) Hematoxylin-eosin and immunohistochemistry on tissue sections.

(b) False-negative because of micrometastases.

(c) Atypical diagnosis in 2 patients, 1 has 1 lymph node, and 1 has 2
lymph nodes.
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Author:Khoury, Thaer; Malik, Deborah; Fan, Cathy; Tan, Dongfeng; Kulkarni, Swati
Publication:Archives of Pathology & Laboratory Medicine
Article Type:Clinical report
Date:Oct 1, 2010
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