Multiparametric and Multinuclear Magnetic Resonance Imaging of Human Breast Cancer: Current Applications

Abstract

The exploration of novel imaging methods that have the potential to improve specificity for the identification of malignancy is still critically needed in breast imaging. Changes in physiologic alterations of soft tissue water associated with breast cancer can be visualized by magnetic resonance (MR) imaging. However, it is unlikely that a single MR parameter can characterize the complexity of breast tissue. Techniques such as multiparametric MR imaging, proton magnetic resonance spectroscopic (MRSI) imaging, and 23Na sodium MR imaging when used in combination provide a comprehensive data set with potentially more power to diagnose breast disease than any single measure alone. A combination of MR, MRSI, and 23Na sodium MR parameters may be examined in a single MR imaging examination, potentially resulting in improved specificity for radiologic evaluation of malignancy.

Keywords

Breast Magnetic Resonance Imaging Sodium MR Spectroscopy Proton ISODATA Cancer Diffusion Neoplasm

References

Wooster

Bignell

Lancaster

Identification of the Breast-Cancer Susceptibility Gene Brca2. Nature 378, 789–792 (1995).

Wooster

Neuhausen

S. L.

Mangion

Localization of a Breast-Cancer Susceptibility Gene, Brca2, to Chromosome 13q12-13. Science 265, 2088–2090 (1994).

Chappuis

P. O.

Nethercot

, and Foulkes

W. D.

Clinico-pathological Characteristics of BRCA1-and BRCA2-related Breast Cancer. Seminars in Surgical Oncology 18, 287–295 (2000).

Cox

L. A.

Chen

, and Lee

Tumor-Suppressor Genes and Their Roles in Breast-Cancer. Breast Cancer Research and Treatment 32, 19–38 (1994).

Miki

Swensen

Shattuckeidens

A Strong Candidate For the Breast and Ovarian-Cancer Susceptibility Gene Brca1. Science 266, 66–71 (1994).

Vogel

V.G.

Breast Cancer Prevention: A Review of Current Evidence. CA Cancer J. Clin. 50, 156–170 (2000).

McPherson

Steel

C. M.

, and Dixon

J. M.

ABC of Breast Diseases — Breast-Cancer — Epidemiology, Risk-Factors, and Genetics. British Medical Journal 309, 1003–1006 (1994).

Richardson

J. L.

Langholz

Bernstein

Burciaga

Danley

, and Ross

R. K.

Stage and Delay in Breast Cancer Diagnosis by Race, Socioeconomic Status, Age and Year. Br. J. Cancer 65, 922–926 (1992).

Umschaden

H. W.

and Haselbach

MR-Mammography: State of the Art and Indications. Acta. Medica. Austriaca. 24, 39–45 (1997).

10.

Gilbert

F. J.

New Screening Techniques for Breast Cancer (MRI). Disease Markers 15, 115–116 (1999).

11.

Lawrence

W. F.

Liang

Mandelblatt

J. S.

Serendipity in Diagnostic Imaging: Magnetic Resonance Imaging of the Breast. J. Natl. Cancer Inst. 90, 1792–1800 (1998).

12.

Weinreb

J. C.

and Newstead

MR-Imaging of the Breast. Radiology 196, 593–610 (1995).

13.

Berg

W. A.

and Gilbreath

P. L.

Multicentric and Multifocal Cancer: Whole-breast US in Preoperative Evaluation. Radiology 214, 59–66 (2000).

14.

Braeuning

M. P.

and Pisano

E. D.

New Modalities in Breast Imaging: Digital Mammography and Magnetic Resonance Imaging. Breast Cancer Res Treat 35, 31–38 (1995).

15.

Hardy

J. R.

Powles

T. J.

Judson

How Many Tests are Required in the Diagnosis of Palpable Breast Abnormalities?

Clin Oncol (R Coll Radiol) 2, 148–152 (1990).

16.

Smith

R. A.

Mettlin

C. J.

Davis

K. J.

, and Eyre

American Cancer Society Guidelines for the Early Detection of Cancer. CA Cancer J Clin 50, 34–49 (2000).

17.

Harris

K. M.

and Vogel

V. G.

Breast Cancer Screening. Cancer and Metastasis Reviews 16, 231–262 (1997).

18.

Kaiser

W. A.

MR Mammography. MedicaMundi 36, 168–82 (1991).

19.

Feig

S. A.

Decreased Breast Cancer Mortality through Mammographic Screening: Results of Clinical Trials. Radiology 167, 659–665 (1988).

20.

Fischer

Kopka

, and Grabbe

Breast Carcinoma: Effect of Preoperative Contrast-enhanced MR Imaging on the Therapeutic Approach. Radiology 213, 881–88 (1999).

21.

Rosenberg

R. D.

Hunt

W. C.

Williamson

M. R.

Effects of Age, Breast Density, Ethnicity, and Estrogen Replacement Therapy on Screening Mammographic Sensitivity and Cancer Stage at Diagnosis: Review of 183, 134 Screening Mammograms in Albuquerque, New Mexico. Radiology 209, 511–518 (1998).

22.

Poplack

S. P.

Tosteson

A. N.

Grove

M. R.

Wells

W. A.

, and Carney

P. A.

Mammography in 53,803 Women from the New Hampshire Mammography Network. Radiology 217, 832–840 (2000).

23.

Mandelson

M. T.

Oestreicher

Porter

P. L.

Breast Density as a Predictor of Mammographic Detection: Comparison of Interval- and Screen-detected Cancers. J. Natl. Cancer. Inst. 92, 1081–1087 (2000).

24.

Kacl

G. M.

Liu

Debatin

J. F.

Garzoli

Caduff

R. F.

, and Krestin

G. P.

Detection of Breast Cancer with Conventional Mammography and Contrast-enhanced MR Imaging. Eur. Radiol. 8, 194–200 (1998).

25.

Stavros

A. T.

Thickman

Rapp

C. L.

Dennis

M. A.

Parker

S. H.

, and Sisney

G. A.

Solid Breast Nodules: Use of Sonography to Distinguish Between Benign and Malignant Lesions. Radiology 196, 123–134 (1995).

26.

Baker

J. A.

and Soo

M. S.

Breast US: Assessment of Technical Quality and Image Interpretation. Radiology 223, 229–238 (2002).

27.

Heywang

S. H.

Wolf

Pruss

Hilbertz

Eiermann

, and Permanetter

MR Imaging of the Breast with Gd-DPTA: Use and Limitations. Radiology 171, 95–103 (1989).

28.

Orel

S. G.

Schnall

M. D.

Powell

C. M.

Staging of Suspected Breast-Cancer — Effect of MR-Imaging and MR-Guided Biopsy. Radiology 196, 115–122 (1995).

29.

Orel

S. G.

High-resolution MR Imaging for the Detection, Diagnosis, and Staging of Breast Cancer. Radiographics 18, 903–912 (1998).

30.

Orel

S. G.

and Schnall

M. D.

MR Imaging of the Breast for the Detection, Diagnosis, and Staging of Breast Cancer. Radiology 220, 13–30 (2001).

31.

Kriege

Brekelmans

C. T.

Boetes

Efficacy of MRI and Mammography for Breast-Cancer Screening in Women with a Familial or Genetic Predisposition. N. Engl. J. Med. 351, 427–437 (2004).

32.

Jacobs

M. A.

Barker

P. B.

Bottomley

P. A.

Bhujwalla

Bluemke

D. B.

Proton MR Spectroscoptic Imaging of Human Breast Cancer: A Preliminary Study. J. Magn. Reson. Imaging 19, 68–75 (2004).

33.

Jacobs

M. A.

Barker

P. B.

Argani

Ouwerkerk

Bhujwalla

Z. M.

, and Bluemke

D. B.

Combined Dynamic Contrast and Spectroscopic Imaging of Human Breast Cancer. J. Magn. Reson. Imaging XX, in press (2005).

34.

Heywang

S. H.

Bassermann

Fenzl

MRI of the Breast — Histopathologic Correlation. Eur. J. Radiol. 7, 175–182 (1987).

35.

Adams

A. H.

Brookeman

J. R.

Merickel

M. B.

Breast Lesion Discrimination Using Statistical Analysis and Shape Measures on Magnetic Resonance Imagery. Comput Med Imaging Graph 15, 339–349 (1991).

36.

Kerslake

R. W.

Carleton

P. J.

Fox

J. N.

Dynamic Gradientecho and Fat-suppressed Spin-echo Contrast-enhanced MRI of the Breast. Clin. Radiol. 50, 440–454 (1995).

37.

Kuhl

C. K.

Klaschik

Mielcarek

Gieseke

Wardelmann

, and Schild

H. H.

Do T2-weighted Pulse Sequences Help with the Differential Diagnosis of Enhancing Lesions in Dynamic Breast MRI?

J. Magn. Reson. Imaging 9, 187–196 (1999).

38.

Heywang

S. H.

Hahn

Schmidt

MR Imaging of the Breast Using Gadolinium-DTPA. J. Comput. Assist. Tomogr. 10, 199–204 (1986).

39.

Kaiser

W. A.

and Zeitler

MR Imaging of the Breast: Fast Imaging Sequences With and Without Gd-DTPA. Preliminary Observations. Radiology 170, 681–686 (1989).

40.

Gilles

Guinebretiere

J. M.

Shapeero

L. G.

Assessment of Breast Cancer Recurrence with Contrast-enhanced Subtraction MR Imaging: Preliminary Results in 26 Patients. Radiology 188, 473–478 (1993).

41.

Harms

S. E.

Flamig

D. P.

Hesley

K. L.

MR Imaging of the Breast with Rotating Delivery of Excitation Off-resonance: Clinical Experience with Pathological Correlation. Radiology 187, 493–501 (1993).

42.

Kelcz

and Santyr

Gadolinium-enhanced Breast MRI. Crit. Rev. Diagn. Imaging 36, 287–338 (1995).

43.

Heywang-Kobrunner

S. H.

Viehweg

Heinig

Kuchler

Contrast-enhanced MRI of the Breast: Accuracy, Value, Controversies, Solutions. Eur. J. Radiol. 24, 94–108 (1997).

44.

Kuhl

C. K.

Mielcareck

Klaschik

Dynamic Breast MR Imaging: Are Signal Intensity Time Course Data Useful for Differential Diagnosis of Enhancing Lesions?

Radiology 211, 101–110 (1999).

45.

Heywang-Kobrunner

S. H.

Haustein

Pohl

Contrast-enhanced MR Imaging of the Breast: Comparison of Two Different Doses of Gadopentetate Dimeglumine. Radiology 191, 639–646 (1994).

46.

Gribbestad

I. S.

Nilsen

Fjosne

H. E.

Kvinnsland

Haugen

O. A.

Rinck

P. A.

Comparative Signal Intensity Measurements in Dynamic Gadolinium-enhanced MR Mammography. J. Magn. Reson. Imaging 4, 477–480 (1994).

47.

Orel

S. G.

Schnall

M. D.

LiVolsi

V. A.

, and Troupin

R. H.

Suspicious Breast Lesions: MR Imaging with Radiologic-pathologic Correlation. Radiology 190, 485–93 (1994).

48.

Boetes

Barentsz

J. O.

Mus

R. D.

MR Characterization of Suspicious Breast Lesions with a Gadolinium-enhanced TurboFLASH Subtraction Technique. Radiology 193, 777–781 (1994).

49.

Orel

S. G.

Differentiating Benign from Malignant Enhancing Lesions Identified at MR Imaging of the Breast: Are Time-signal Intensity Curves an Accurate Predictor?

Radiology 211, 5–7 (1999).

50.

Sinha

and Sinha

Functional Magnetic Resonance of Human Breast Tumors: Diffusion and Perfusion Imaging. Ann. NY Acad. Sci. 980, 95–115 (2002).

51.

Guo

Cai

Y. Q.

Cai

Z. L.

Differentiation of Clinically Benign and Malignant Breast Lesions Using Diffusion-weighted Imaging. J. Magn. Reson. Imaging 16, 172–178 (2002).

52.

Sinha

Lucas-Quesada

F. A.

Sinha

DeBruhl

, and Bassett

L. W.

In Vivo Diffusion-weighted MRI of the Breast: Potential for Lesion Characterization. J. Magn. Reson. Imaging 15, 693–704 (2002).

53.

Moseley

M. E.

Kucharczyk

Mintorovitch

Diffusion-weighted MR Imaging of Acute Stroke: Correlation with T2-weighted and Magnetic Susceptibility-enhanced MR Imaging in Cats. American Journal of Neuroradiology 11, 423–429 (1990).

54.

Le Bihan

Breton

Lallemand

Grenier

Cabanis

, and Jeantet

M. Laval

MR Imaging of Intravoxel Incoherent Motions: Application to Diffusion and Perfusion in Neurologic Disorders. Radiology 161, 401–407 (1986).

55.

Benveniste

Hedlund

, and Johnson

Mechanism of Detection of Acute Cerebral Ischemia in Rats by Diffusion-weighted Magnetic Resonance Microscopy. Stroke 23, 746–754 (1992).

56.

Minematsu

Fisher

Sotak

C. H.

Davis

M. A.

, and Fiandaca

M. S.

Diffusion Weighted Magnetic Resonance Imaging: Rapid and Quantitative Detection of Focal Brain Ischemia. Neurology 42, 235–240 (1992).

57.

Hoehn-Berlage

Norris

Kohno

Mies

Leibfritz

, and Hossmann

Evolution of Regional Changes in Apparent Diffusion Coefficient During Focal Ischemia of Rat Brain: The Relationship of Quantitative Diffusion NMR Imaging to Reduction in Cerebral Blood Flow and Metabolic Disturbances. Journal of Cerebral Blood Flow & Metabolism 15, 1002–1011 (1995).

58.

Liu

K. F.

Tatlisumak

Regional Variations in the Apparent Diffusion Coefficient and the Intracellular Distribution of Water in Rat Brain During Acute Focal Ischemia. Stroke 32, 1897–1905 (2001).

59.

Degani

Gusis

Weinstein

Fields

, and Strano

Mapping Pathophysiological Features of Breast Tumors by MRI at High Spatial Resolution. Nat. Med. 3, 780–782 (1997).

60.

Roebuck

J. R.

Cecil

K. M.

Schnall

M. D.

Lenkinski

R. E.

Human Breast Lesions: Characterization with Proton MR Spectroscopy. Radiology 209, 269–275 (1998).

61.

Kvistad

K. A.

Bakken

I. J.

Gribbestad

I. S.

Characterization of Neoplastic and Normal Human Breast Tissues with In Vivo (1)H MR Spectroscopy. J. Magn. Reson. Imaging 10, 159–164 (1999).

62.

Cecil

K. M.

Schnall

M. D.

Siegelman

E. S.

, and Lenkinski

R. E.

The Evaluation of Human Breast Lesions with Magnetic Resonance Imaging and Proton Magnetic Resonance Spectroscopy. Breast Cancer Res. Treat 68, 45–54 (2001).

63.

Yeung

D. K.

Cheung

H. S.

, and Tse

G. M.

Human Breast Lesions: Characterization with Contrast-enhanced In Vivo Proton MR Spectroscopy — Initial Results. Radiology 220, 40–46 (2001).

64.

Katz-Brull

Lavin

P. T.

, and Lenkinski

R. E.

Clinical Utility of Proton Magnetic Resonance Spectroscopy in Characterizing Breast Lesions. J. Natl. Cancer Inst. 94, 1197–1203 (2002).

65.

Kim

J. K.

Park

S. H.

Lee

H. M.

In Vivo 1H-MRS Evaluation of Malignant and Benign Breast Diseases. Breast 12, 179–182 (2003).

66.

Huang

Fisher

P. R.

Dulaimy

Tudorica

L. A.

O'Hea

Button

T. M.

Detection of Breast Malignancy: Diagnostic MR Protocol for Improved Specificity. Radiology 232, 585–591 (2004). [Epub Jun 17, 2004].

67.

Jacobs

M. A.

Bluemke

D. B.

Bhujwalla

Marano

, and Barker

P. B.

A Model to Differentiate Benign From Malignant Breast Tumors using Multiparametric MRI with Histological Correlates. Proceedings of the International Society of Magnetic Resonance 9th Scientific Meeting, 18th Annual Meeting. Glasgow, Scotland UK 9, 563 (2001).

68.

Jacobs

M. A.

Barker

P. B.

Bluemke

D. A.

Benign and Malignant Breast Lesions: Diagnosis with Multiparametric MR Imaging. Radiology 229, 225–232 (2003).

69.

Haase

Frahm

Hanicke

, and Matthaei

H-1-Nmr Chemical-Shift Selective (Chess) Imaging. Physics in Medicine and Biology 30, 341–344 (1985).

70.

Boada

F. E.

Gillen

J. S.

Shen

G. X.

Chang

S. Y.

, and Thulborn

K. R.

Fast Three Dimensional Sodium Imaging. Magn. Reson. Med. 37, 706–715 (1997).

71.

Ouwerkerk

Bleich

K. B.

Gillen

J. S.

Pomper

M. G.

, and Bottomley

P. A.

Tissue Sodium Concentration in Human Brain Tumors as Measured with 23Na MR Imaging. Radiology 227, 529–537 (2003).

72.

Jacobs

M. A.

Knight

R. A.

Windham

J. P.

Identification of Cerebral Ischemic Lesions in Rat Using Eigenimage Filtered Magnetic Resonance Imaging. Brain Research 837, 83–94 (1999).

73.

Windham

J. P.

Abd-Allah

M. A.

Reimann

D. A.

Froelich

J. W.

, and Haggar

A. M.

Eigenimage Filtering in MR Imaging. J Comput Assist Tomogr 12, 1–9 (1988).

74.

Jacobs

M. A.

Knight

R. A.

Soltanian-Zadeth

Unsupervised Segmentation of Multiparameter MRI in Experimental Cerebral Ischemia with Comparison to T2, Diffusion, and ADC MRI Parameters and Histopathological Validation. J. Magn. Reson. Imaging 11, 425–437 (2000).

75.

Soher

B. J.

Hurd

R. E.

Sailasuta

, and Barker

P. B.

Quantitation of Automated Single-voxel Proton MRS Using Cerebral Water as an Internal Reference. Magn. Reson. Med. 36, 335–339 (1996).

76.

Pan

J. W.

Twieg

D. B.

, and Hetherington

H. P.

Quantitative Spectroscopic Imaging of the Human Brain. Magn. Reson. Med. 40, 363–369 (1998).

77.

Michaelis

Merboldt

K. D.

Bruhn

Hanicke

, and Frahm

Absolute Concentrations of Metabolites in the Adult Human Brain In Vivo: Quantification of Localized Proton MR Spectra

Radiology 187, 219–227 (1993).

78.

Kreis

Ernst

, and Ross

Absolute Quantitation of Water and Metabolites in the Human Brain II. Metabolite Concentrations. J. Magn. Reson. B 102, 9–19 (1993).

79.

Barker

P. B.

Soher

B. J.

Blackband

S. J.

Chatham

J. C.

Mathews

V. P.

, and Bryan

R. N.

Quantitation of Proton NMR Spectra of the Human Brain Using Tissue Water as an Internal Concentration Reference. NMR Biomed 6, 89–94 (1993).

80.

Alger

J. R.

Symko

S. C.

Bizzi

Posse

DesPres

D. J.

, and Armstrong

M. R.

Absolute Quantitation of Short TE Brain 1H-MR Spectra and Spectroscopic Imaging Data. J. Comput. Assist. Tomogr. 17, 191–199 (1993).

81.

Bakken

I. J.

Gribbestad

I. S.

Singstad

T. E.

, and Kvistad

K. A.

External Standard Method for the In Vivo Quantification of Choline-containing Compounds in Breast Tumors by Proton MR Spectroscopy at 1.5 Tesla. Magn. Reson. Med. 46, 189–192 (2001).

82.

Jagannathan

N. R.

Kumar

Raghunathan

Coshic

Julka

P. K.

, and Rath

G. K.

Assessment of the Therapeutic Response of Human Breast Carcinoma using In Vivo volume Localized Proton Magnetic Resonance Spectroscopy. Current Science 76, 777–782 (1999).

83.

Delille

J.-P.

Slanetz

P. J.

Yeh

E. D.

Halpern

E. F.

Kopans

D. B.

, and Garrido

Invasive Ductal Breast Carcinoma Response to Neoadjuvant Chemotherapy: Noninvasive Monitoring with Functional MR Imaging — Pilot Study. Radiology 228, 63–69 (2003).

84.

Jacobs

M. A.

Ouwerkerk

Bottomley

P. A.

Multiparameter Proton, Sodium, and Spectroscopic Imaging of Human Breast Cancer. Proceedings of the International Society of Magnetic Resonance 2003; 11th Scientific Meeting, 20th Annual Meeting, Toronto, Canada 2003.

85.

Meisamy

Bolan

P. J.

Baker

E. H.

Neoadjuvant Chemotherapy of Locally Advanced Breast Cancer: Predicting Response with In Vivo 1H MR Spectroscopy — A Pilot Study at 4 T. Radiology 233, 424–431 (2004).