F 2005 American Association for Cancer Research.
doi:10.1158/1078-0432.CCR-05-1378
Mammaglobin as Molecular Marker
of Breast Cancer (Micro)Metastases
To the Editor: In a recent issue of Clinical Cancer Research ,
two articles (1,2) addressed the use of PCR to detect micro-
metastases from breast cancer either in lymph nodes (1) or in
peripheral blood (2). Both articles found mammaglobin (mam)
to be an excellent marker for this. However, neither article, in
our view, has appropriately considered the effect of the wide
range of expression levels of mam in the primary tumor, and
the association of mam expression with particular tumor
characteristics, on these results.
Mikhitarian et al. (1) diluted the RNA of a metastasis-positive
axillary lymph node with RNA from normal lymph nodes and
used microarray analyses to find mam as the gene with highest
sensitivity. In addition, TFF1 was found as an additional novel
marker. However, for this experiment, a positive lymph node
was chosen based on its 5.3 Â 10
7
– fold overexpression of
mam. We have shown that in the primary breast tumor mam
levels can vary over 10,000-fold (3). Thus, if Mikhitarian et al.
had chosen a tumor that had a lower level of mam expression,
other genes might have been found to have a better detection
rate. Of note, the broad shoulder in the frequency distribution
in Fig. 1 of their article is in agreement with the wide range of
mam expression in primary tumors.
The authors discuss the fact that TFF1 expression in the
primary tumor is positively associated with estrogen receptor
and progesterone receptor status. We have described a similar,
strong association of mam with estrogen receptor and
progesterone receptor status. This then may account for the
fact that TFF1 is found as a novel marker by these authors, as
the tumor chosen for this experiment was selected based on its
mam overexpression, and as both these markers are correlated
with estrogen receptor status.
Reinholz et al. (2) used a PCR for mam to detect breast cancer
cells in peripheral blood samples. Of the patients with breast
cancer in this article, a majority (77%) had an estrogen
receptor – positive tumor. This patient selection would favor the
selection of mam as a sensitive marker for circulating breast
cancer cells, considering the particular association of mam
expression with just these tumor characteristics (3).
Paul N. Span
Fred C.G.J. Sweep
Department of Chemical Endocrinology,
Radboud University Nijmegen Medical
Center, Nijmegen, the Netherlands
References
1. Mikhitarian K, Gillanders WE, Almeida JS, et al. An innovative microarray strategy
identities informative molecular markers for the detection of micrometastatic breast
cancer. Clin Cancer Res 2005 May 15;11:3697 ^ 704.
2. Reinholz MM, Nibbe A, Jonart LM, et al. Evaluation of a panel of tumor markers for
molecular detection of circulating cancer cells in women with suspected breast
cancer. Clin Cancer Res 2005 May 15;11:3722 ^ 32.
3. Span PN, Waanders E, Manders P, et al. Mammaglobin is associated with low-
grade, steroid receptor-positive breast tumors from postmenopausal patients, and
has independent prognostic value for relapse-free survival time. J Clin Oncol 2004
Feb 15;22:691 ^ 8.
I n Response: We thank Dr. Span for interest in our article
(1) and for insightful comments. Although Dr. Span has
correctly pointed out that there is wide range of mammaglobin
(mam) expression levels in primary breast cancers, it still remains
the single best marker for the detection of metastatic and
micrometastatic breast cancer (2, 3). The frequency distribution
analyses in our article confirm that the tissue specificity of mam is
exquisite and there is almost no expression in normal lymph
nodes (or peripheral blood; ref. 4). We have recently completed
an interim analysis of a multi-institutional prospective cohort
study (Minimally Invasive Molecular Staging of Breast Cancer)
designed to assess the clinical relevance of molecular detection of
micrometastatic disease in axillary lymph nodes (ALN) of breast
cancer patients. In this study, mam was overexpressed in ALN
from 79% of patients with pathology-positive ALN and in ALN
from 23% of patients with pathology-negative ALN (3).
Although this is higher than any other molecular marker, the
heterogeneity of gene expression in primary breast cancer is a
good argument for the use of multimarker panels.
Although there is evidence that mam expression is higher in
estrogen receptor–positive tumors (5), mam also seems to be an
excellent molecular marker for metastatic disease derived from
estrogen receptor–negative tumors. Results of the Minimally
Invasive Molecular Staging of Breast Cancer study reveal that
mam is overexpressed in ALN from 80% of patients with
pathology-positive ALN and estrogen receptor–positive tumors
(n = 108) and in ALN from 72% of patients with pathology-
positive ALN and estrogen receptor–negative tumors (n = 29).
With respect to Dr. Span’s comment regarding tissue
selection, we chose an ALN containing metastatic breast
cancer that highly expressed mam as an internal positive control
for the novel dilutional microarray strategy. Identi-
fication and validation of trefoil factor 1 as a marker for
micrometastatic breast cancer provides additional evidence
that this strategy can identify novel molecular markers. We
agree with Dr. Span that selection of an ALN known to over-
express mam may have affected microarray results. However,
in addition to the study described in the article, we have
done dilutional microarray analyses on two pathology-positive
ALN that did not overexpress mam with the goal of identifying
novel molecular markers that complement mam in the detection
of micrometastatic breast cancer. Although trefoil factor 1 was
again one of the most overexpressed genes in one of the ALN, we
also identified several other potential breast cancer markers.
Kaidi Mikhitarian
William E. Gillanders
David J. Cole
Michael Mitas
Department of Surgery, Medical
University of South Carolina,
Charleston, South Carolina
Letters to the Editor
www.aacrjournals.org Clin Cancer Res 2005;11(19) October 1, 2005 7043
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