Abstract
Although some reports with computed tomography and bone scintigraphy are available in the literature, the distinct epidemiologic description of skeletal metastatic pattern of various tumors is still lacking. This study uses a novel approach to identify skeletal metastases from magnetic resonance imaging (MRI) data to describe metastatic pattern in common malignancies. A retrospective analysis of 130 cancer patients (42 lung, 56 breast, 11 prostate cancers; 21 multiple myeloma) with vertebral metastases and without disseminated disease, and whom underwent a whole body 3Tesla MRI investigation (Discovery MR750w), was carried out. Multiple myeloma had the most commonly disseminated metastatic disease (95 %) compared to lung (28 %), breast (44 %) and prostate (71 %) cancers. Lung cancer was related to more frequent pedicle involvement compared to breast or prostate cancer (29, 9 and 0 %, p < 0.05). Pathologic fracture was mainly associated with multiple myeloma (43 %). The prevalence of lung cancer metastases was more frequent in the lumbal spine (81 %), as well as particular in C7, D7, D8, D9 and L1, compared to breast cancers. Most differences among tumors were detected in the extravertebral osseous metastatic pattern (p < 0.05). The highest frequency of extravertebral skeletal metastases was present in multiple myeloma (28 to 76 %). Brain metastasis was more frequent in lung cancer compared to breast cancers (35 % vs. 17 %, p < 0.05). Significant differences in the skeletal metastatic pattern among common malignancies were demonstrated with MRI.
Similar content being viewed by others
References
Vineis P, Wild CP (2014) Global cancer patterns: causes and prevention. Lancet 383:549–557
Sciubba DM, Gokaslan ZL (2006) Diagnosis and management of metastatic spine disease. Surg Oncol 15:141–151
Sundaresan N, Boriani S, Rothman A, Holtzman R (2004) Tumors of the osseous spine. J Neurooncol 69:273–290
White AP, Kwon BK, Lindskog DM, Friedlaender GE, Grauer JN (2006) Metastatic disease of the spine. J Am Acad Orthop Surg 14:587–598
Witham TF, Khavkin YA, Gallia GL, Wolinsky JP, Gokaslan ZL (2006) Surgery insight: current management of epidural spinal cord compression from metastatic spine disease. Nat Clin Pract Neurol 2:87–94
Memon AG, Jaleel A, Aftab J (2006) Pattern of prostatic carcinoma metastases in bones detected by bone scans using Technitium 99m methyl dipohsphate (Tc99m MDP) imaging technique. Pak J Med Sci 22:180–183
Morgan JWM, Adcock KM, Donohue RE (1990) Distribution of skeletal metastases in prostatic and lung cancer. Urology 36:31–34
Coleman RE, Rubens RD (1987) The clinical course of bone metastases from breast cancer. Br J Cancer 55:61–66
Coleman RE (1997) Skeletal complications of malignancy. Cancer 80:1588–1594
Bubendorf L, Schöpfer A, Wagner U, Sauter G, Moch H, Willi N, Gasser TC, Mihatsch MJ (2000) Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 31:578–583
Marulanda GA, Mont MA, Lucci A, Letson GD, Khakpour N (2008) Orthopedic surgery implications of breast cancer. Expert Rev Anticancer Ther 8:949–956
Black P (1979) Spinal metastasis: current status and recommended guidelines for management. Neurosurgery 5:726–746
Scutellari PN, Addonisio G, Righi R, Giganti M (2000) Diagnostic imaging of bone metastases. Radiol Med 100:429–435
Sciubba DM, Petteys RJ, Dekutoski MB, Fisher CG, Fehlings MG, Ondra SL, Rhines LD, Gokaslan ZL (2010) Diagnosis and management of metastatic spine disease. A review. J Neurosurg Spine 13:94–108
Khanna AJ, Shindle MK, Wasserman BA, Gokaslan ZL, Gonzales RA, Buchowski JM, Riley LH 3rd (2005) Use of magnetic resonance imaging in differentiating compartmental location of spinal tumors. Am J Orthop (Belle Mead NJ) 34:472–476
Kakhki VR, Anvari K, Sadeghi R, Mahmoudian AS, Torabian-Kakhki M (2013) Pattern and distribution of bone metastases in common malignant tumors. Nucl Med Rev Cent East Eur 16:66–69
Cossigny D, Quan GM (2012) In vivo animal models of spinal metastasis. Cancer Metastasis Rev 31:99–108
Schaberg J, Gainor BJ (1985) A profile of metastatic carcinoma of the spine. Spine (Phila Pa 1976) 10:19–20
Weigert F, Reiser M, Pfändner K (1987) Imaging of neoplastic changes in the spine using MR tomography]. Rofo 146:123–30
Bubendorf L, Schöpfer A, Wagner U, Sauter G, Moch H, Willi N, Gasser TC, Mihatsch MJ (2000) Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 31:578–583
Bohlman HH, Sachs BL, Carter JR, Riley L, Robinson RA (1986) Primary neoplasms of the cervical spine. Diagnosis and treatment of twenty-three patients. J Bone Joint Surg Am 68:483–494
Hart RA, Boriani S, Biagini R, Currier B, Weinstein JN (1997) A system for surgical staging and management of spine tumors. A clinical outcome study of giant cell tumors of the spine. Spine (Phila Pa 1976) 22:1773–1782
Lee C, Jung C (2012) Metastatic spinal tumor. Asian Spine J 6:71–87
Shackman R, Harrison CV (1948) Occult bone metastases. Br J Surg 35:385–389
Algra PR, Heimans JJ, Valk J, Nauta JJ, Lachniet M, Van Kooten B (1992) Do metastases in vertebrae begin in the body or the pedicles? Imaging study in 45 patients. AJR Am J Roentgenol 158:1275–1279
Abdel-Wanis ME, Solyman MT, Hasan NM (2011) Sensitivity, specificity and accuracy of magnetic resonance imaging for differentiating vertebral compression fractures caused by malignancy, osteoporosis, and infections. J Orthop Surg (Hong Kong) 19:145–150
Arguello F, Baggs RB, Duerst RE, Johnstone L, McQueen K, Frantz CN (1990) Pathogenesis of vertebral metastasis and epidural spinal cord compression. Cancer 65:98–106
Asdourian PL, Weidenbaum M, DeWald RL, Hammerberg KW, Ramsey RG (1990) The pattern of vertebral involvement in metastatic vertebral breast cancer. Clin Orthop Relat Res 250:164–170
Coleman RE (2006) Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 12:6243–6249
Bundred N, Walker RA, Ratcliffe WA, Warwick J, Morrison JM, Ratcliffe JG (1992) Parathyroid hormone related protein and skeletal morbidity in breast cancer. Eur J Cancer 28:690–692
Koenders P, Beex LV, Langens R, Kloppenborg PW, Smals AG, Benraad TJ (1991) Steroid hormone receptor activity of primary human breast cancer and pattern of first metastasis. Breast Cancer Res Treat 18:27–32
Yuh WT, Quets JP, Lee HJ, Simonson TM, Michalson LS, Nguyen PT, Sato Y, Mayr NA, Berbaum KS (1996) Anatomic distribution of metastases in the vertebral body and modes of hematogenous spread. Spine (Phila Pa 1976) 21:2243–2250
Zhou Q, Zu L, Li L, Chen X, Chen X, Li Y, Liu H, Sun Z (2014) Screening and establishment of human lung cancer cell lines with organ-specific metastasis potential. Zhongguo Fei Ai Za Zhi 17:175–182
Melton LJ 3rd, Kyle RA, Achenbach SJ, Oberg AL, Rajkumar SV (2005) Fracture risk with multiple myeloma: a population-based study. J Bone Miner Res 20:487–493
Song IC, Kim JN, Choi YS, Ryu H, Lee MW, Lee HJ, Yun HJ, Kim S, Kwon ST, Jo DY (2014) Diagnostic and prognostic implications of spine magnetic resonance imaging at diagnosis in patients with multiple myeloma. Cancer Res Treat. doi:10.4143/crt.2014.010
Greenspan SL, Wagner J, Nelson JB, Perera S, Britton C, Resnick NM (2013) Vertebral fractures and trabecular microstructure in men with prostate cancer on androgen deprivation therapy. J Bone Miner Res 28:325–332
Klimo P Jr, Schmidt MH (2004) Surgical management of spinal metastases. Oncologist 9:188–196
Schirrmeister H, Guhlmann A, Elsner K, Kotzerke J, Glatting G, Rentschler M, Neumaier B, Träger H, Nüssle K, Reske SN (1999) Sensitivity in detecting osseous lesions depends on anatomic localization: planar bone scintigraphy versus 18F PET. J Nucl Med 40:1623–1629
Aydinli U, Ozturk C, Bayram S, Sarihan S, Evrensel T, Yilmaz HS (2006) Evaluation of lung cancer metastases to the spine. Acta Orthop Belg 72:592–597
Batson OV (1940) The function of vertebral veins and their role in the spread of metastases. Ann Surg 112:38–149
Bubendorf L, Schöpfer A, Wagner U, Sauter G, Moch H, Willi N, Gasser TC, Mihatsch MJ (2000) Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 31:578–583
Moreno A, Albiach C, Soria R, Vidal V, Gómez R, Antequera M (2014) Oligometastases in prostate cancer: restaging stage IV cancers and new radiotherapy options. Radiat Oncol 9:258
Saitoh H, Yoshida K, Uchijima Y, Kobayashi N, Suwata J, Kamata S (1990) Two different lymph node metastatic patterns of a prostate cancer. Cancer 65:1843–1846
Fabozzi SJ, Schellhammer PF, El-Mahdi AM (1995) Pulmonary metastases from prostate cancer. Cancer 75:2706–2709
Maccauro G, Spinelli MS, Mauro S, Perisano C, Graci C, Rosa MA (2011) Physiopathology of spine metastasis. Int J Surg Oncol 2011:107969
Sugiura H, Yamada K, Sugiura T, Hida T, Mitsudomi T (2008) Predictors of survival in patients with bone metastasis of lung cancer. Clin Orthop Relat Res 466:729–736
Sorensen JB, Hansen HH, Hansen M, Dombernowsky P (1988) Brain metastases in adenocarcinoma of the lung: frequency, risk groups, and prognosis. J Clin Oncol 6:1474–1480
Lagerwaard FJ, Levendag PC, Nowak PJ, Eijkenboom WM, Hanssens PE, Schmitz PI (1999) Identification of prognostic factors in patients with brain metastases: a review of 1292 patients. Int J Radiat Oncol Biol Phys 43:795–803
Riihimäki M, Hemminki A, Fallah M, Thomsen H, Sundquist K, Sundquist J, Hemminki K (2014) Metastatic sites and survival in lung cancer. Lung Cancer 86:78–84
Petrén-Mallmin M, Nordström B, Andréasson I, Nyman R, Jónsson H Jr, Rauschning W, Hemmingsson A (1992) MR imaging with histopathological correlation in vertebral metastases of breast cancer. Acta Radiol 33:213–220
Acknowledgments
We acknowledge the financial support (travel grant) of GE for ADT and DLT and the help of Peter Mechtler in the language editing.
Funding
No funding decrared.
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical approval
For this type of study formal consent is not required.
Author information
Authors and Affiliations
Corresponding author
Additional information
David Laszlo Tarnoki and Adam Domonkos Tarnoki contributed equally to this work.
Rights and permissions
About this article
Cite this article
Tarnoki, D.L., Tarnoki, A.D., Ohlmann-Knafo, S. et al. Pattern of Tumour Spread of Common Primary Tumours as Seen on Magnetic Resonance Imaging. Pathol. Oncol. Res. 22, 79–85 (2016). https://doi.org/10.1007/s12253-015-9975-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12253-015-9975-y