Elsevier

Surgical Oncology

Volume 17, Issue 3, September 2008, Pages 247-252
Surgical Oncology

Review
Significance of micrometastases in prostate cancer

https://doi.org/10.1016/j.suronc.2008.05.002Get rights and content

Abstract

Pelvic lymph node metastases have been considered the most potent factor associated with disease recurrence in patients undergoing radical prostatectomy for localized prostate cancer. Routine pathological examination, however, can miss micrometastatic tumor foci in the lymph nodes of patients with prostate cancer, resulting in confused tumor staging and clinical decision-making. Accordingly, intensive efforts have been made to develop a procedure for efficaciously detecting micrometastases in pelvic lymph nodes using several kinds of molecular and histopathological techniques targeting genes specifically expressed in the prostate, such as prostate-specific antigen and prostate-specific membrane antigen. Although some of these techniques have been shown to achieve significantly higher sensitivity for detecting micrometastatic prostate cancer cells in surgically removed pelvic nodes during radical prostatectomy than conventional pathological examination, there have not been any methods introduced into clinical practice. In this review, we attempted to summarize recent advances in the field of “micrometastases” in prostate cancer in order to clarify the clinical significance of micrometastases in patients undergoing radical prostatectomy and to suggest limitations to be overcome before developing a reliable model for clinical application.

Introduction

Of several clinicopathological parameters, pelvic lymph node metastasis has been regarded as the most important factor predicting disease recurrence in patients with clinically localized prostate cancer who underwent radical prostatectomy. Patients with organ-confined prostate cancer have a favorable prognosis and a low-risk of disease recurrence after radical prostatectomy, while biochemical recurrence, characterized by a continuously increasing serum prostate-specific antigen (PSA) value, is observed in approximately 10% of patients in this subgroup [1], [2], [3], [4], which is often associated with the eventual development of clinically significant metastases. It is, thus, possible that micrometastatic disease is already present in some of these patients at the time of surgery. Since routine microscopic examination of dissected lymph node specimens can miss small cancer foci [5], [6], [7], this may partially account for the presence of histologically undetectable micrometastases in the pelvic lymph nodes. In fact, a number of studies have demonstrated that higher sensitivity for detecting micrometastatic cancer cells in surgically removed pelvic lymph nodes at radical prostatectomy can be achieved by several molecular and histolopathological techniques targeting genes specifically expressed in the prostate [8], [9], [10], [11], [12], [13]. We also reported the usefulness of a fully competitive reverse transcriptase-polymerase chain reaction (RT-PCR) targeting prostate-specific antigen (PSA) and prostate-specific membrane antigen (PSMA) genes for the detection of micrometastatic prostate cancer cells in the pelvic lymph nodes [14], [15]. To date, unfortunately, none of these methods have been introduced into clinical practice due to various limitations, such as a high false–positive rates and complicated procedures. In addition to technical aspects for detecting micrometastatic cancer cells, it would be important to characterize the clinical significance of identifying such occult disease. However, it remains controversial whether the presence of micrometastatic cancer cells in the pelvic lymph nodes really has an adverse impact on the prognosis of patients with prostate cancer.

Considering these findings, this article reviews recent progress in the detection of micrometastases in pelvic lymph nodes obtained from patients with prostate cancer, focusing on the following topics: (1) comparison among several techniques for detecting micrometastases; (2) suitable marker genes targeted by these techniques; (3) clinical significance of micrometastases detected in the pelvic nodes; (4) limitations of these techniques; and (5) application of these techniques to peripheral blood or bone marrow.

Section snippets

RT-PCR

The main problems in conventional histopathological evaluation of lymph node specimens are sampling error and poor sensitivity for detecting small tumor foci; therefore, a number of investigators have applied RT-PCR assay to the detection of micrometastatic cancer cells in order to overcome the limitations of routine pathological examinations [16], [17]. Theoretically, RT-PCR assay is suitable for the identification of minute amounts of mRNA coding for proteins specifically expressed in the

Target genes for detecting micrometastatic prostate cancer cells

There are several genes that are rarely expressed outside the prostate gland [33], [34], [35], [36], [37], [38], that thus have the potential to be optimal candidates as specific markers for the detection of prostate cancer cells. In fact, PSA and/or PSMA have traditionally been used as target genes for detecting micrometastases of prostate cancer, since expression of the PSA and PSMA genes is exclusively restricted to prostate epithelial cells, and this high specificity makes it possible to

Clinical significance of micrometastases in patients with prostate cancer

To introduce novel molecular and histological techniques for detecting micrometastases in patients with prostate cancer, it seems to be critical to determine whether the outcomes of these assays correlate with clinicopathological findings, including the prognosis. It would be difficult to fairly evaluate the outcomes of these assays, since several kinds of assays were used by various research groups, and each assay consisted of complex, multistage technical steps, and even in the same assay,

Technical limitations for detecting micrometastases

There are a number of issues to be overcome associated with the detection of micrometastases by novel molecular and immunohistochemical assays before these assays can be introduced into urological clinical practice. The ideal assay would detect the presence of a critical number of prostate cancer cells correlating with eventual disease progression based on a procedure that is as simple as possible.

Current pathological examinations of dissected lymph nodes stained with hematoxylin and eosin have

Application of novel techniques for detecting micrometastases to peripheral blood or bone marrow

In this review, we mainly focused on the detection of micrometastases in pelvic lymph nodes from patients with localized prostate cancer, while intensive studies have also been carried out for identifying disseminated prostate cancer cells to peripheral blood or bone marrow [18], [46], [47], [48], [49], [50], [51], [52].

In 1994, Katz et al. collected blood samples from 319 patients prior to radical prostatectomy and analyzed these using an RT-PCR targeting PSA. They reported that 16% of

Conclusion

Considering the outcomes of analyzing the utility of novel molecular and immunohistochemical assays for the detection of micrometastatic prostate cancer cells, positive findings using these assays may have relevance to the clinical course of patients following radical prostatectomy. However, the optimization of these novel assays is still required to further enhance the sensitivity keeping with reasonable specificity in order to avoid both false–positive and false–negative results as much as

Conflict of interest statement

None declared.

References (52)

  • C.A. Olsson et al.

    Reverse transcriptase-polymerase chain reaction assays for prostate cancer

    Urol Clin North Am

    (1997)
  • B. Straub et al.

    Detection of prostate-specific antigen RNA before and after radical retropubic prostatectomy and transurethral resection of the prostate using “Light-Cycler”-based quantitative real-time polymerase chain reaction

    Urology

    (2001)
  • I.G. McIntyre et al.

    Molecular prediction of progression in patients with conservatively managed prostate cancer

    Urology

    (2001)
  • A. Mejean et al.

    Detection of circulating prostate derived cells in patients with prostate adenocarcinoma is an independent risk factor for tumor recurrence

    J Urol

    (2000)
  • S.A. Boorjian et al.

    Long-term outcome after radical prostatectomy for patients with lymph node positive prostate cancer in the prostate specific antigen era

    J Urol

    (2007)
  • M. Mitas et al.

    Quantitative real-time RT-PCR detection of breast cancer micrometastasis using a multigene marker panel

    Int J Cancer

    (2001)
  • M. Inokuchi et al.

    Quantitative evaluation of metastases in axillary lymph nodes of breast cancer

    Br J Cancer

    (2003)
  • S.F. Shariat et al.

    Comparison of immunohistochemistry with reverse transcription-PCR for the detection of micrometastatic prostate cancer in lymph nodes

    Cancer Res

    (2003)
  • S.F. Shariat et al.

    Detection of clinically significant, occult prostate cancer metastases in lymph nodes using a splice variant-specific RT-PCR assay for human glandular kallikrein

    J Clin Oncol

    (2003)
  • S.R. Potter et al.

    Molecular and immunohistochemical staging of men with seminal vesicle invasion and negative pelvic lymph nodes at radical prostatectomy

    Cancer

    (2000)
  • A.C. Ferrari et al.

    Prospective analysis of prostate-specific markers in pelvic lymph nodes of patients with high-risk prostate cancer

    J Natl Cancer Inst

    (1997)
  • H. Miyake et al.

    Quantitative detection of micrometastases in pelvic lymph nodes in patients with clinically localized prostate cancer by real-time reverse transcriptase-PCR

    Clin Cancer Res

    (2007)
  • H. Miyake et al.

    Significance of micrometastases in pelvic lymph nodes detected by real-time reverse transcriptase polymerase chain reaction in patients with clinically localized prostate cancer undergoing radical prostatectomy after neoadjuvant hormonal therapy

    BJU Int

    (2007)
  • I.G. McIntyre et al.

    The molecular staging of prostate cancer

    BJU Int

    (2004)
  • D.H. Schamhart et al.

    Identification of circulating prostate cancer cells: a challenge to the clinical implementation of molecular biology (review)

    Int J Oncol

    (2005)
  • R.L. Vessella et al.

    A sensitive method for detection of a prostate tumor cell marker using the polymerase chain reaction

    J Urol

    (1992)
  • Cited by (0)

    View full text