Seminars in Nuclear Medicine
Volume 31, Issue 3 , Pages 177-190 , July 2001

The value of Ga-67 scintigraphy and F-18 fluorodeoxyglucose positron emission tomography in staging and monitoring the response of lymphoma to treatment

  • Rachel Bar-Shalom

      Affiliations

    • Department of Nuclear Medicine, Rambam Medical Center, Haifa, Israel
    • Division of Nuclear Medicine, Department of Radiology, The New York Presbyterian Hospital, Weill-Medical College of Cornell University, New York, NY, USA
    • Corresponding Author InformationAddress reprint requests to Rachel Bar-Shalom, MD, Department of Nuclear Medicine, Rambam Medical Center, Haifa 35254, Israel.
  • ,
  • Maya Mor

      Affiliations

    • Department of Nuclear Medicine, Rambam Medical Center, Haifa, Israel
    • Division of Nuclear Medicine, Department of Radiology, The New York Presbyterian Hospital, Weill-Medical College of Cornell University, New York, NY, USA
  • ,
  • Nikolai Yefremov

      Affiliations

    • Department of Nuclear Medicine, Rambam Medical Center, Haifa, Israel
    • Division of Nuclear Medicine, Department of Radiology, The New York Presbyterian Hospital, Weill-Medical College of Cornell University, New York, NY, USA
  • ,
  • Stanley J. Goldsmith

      Affiliations

    • Department of Nuclear Medicine, Rambam Medical Center, Haifa, Israel
    • Division of Nuclear Medicine, Department of Radiology, The New York Presbyterian Hospital, Weill-Medical College of Cornell University, New York, NY, USA

References 

  1. Edward CL, Hayes RL. Tumor scanning with Ga-67 citrate. J Nucl Med. 1969;10:103–105
  2. Hayes RL, Nelson B, Swartzendruber DC, et al. Gallium-67 localization in rat and mouse tumors. Science. 1970;167:289–290
  3. Iosilevsky G, Front D, Bettman L, et al. Uptake of Gallium-67 citrate and [2–3H] deoxyglucose in the tumor model, following chemotherapy and radiotherapy. J Nucl Med. 1985;26:278–282
  4. Israel O, Front D. Lymphoma. In: Aklolun C, Tauxe WN editor. Nuclear Oncology. ed 1. Berlin: Springer Verlag; 1999;
  5. Sohn MH, Jones BJ, Whiting JH, et al. Distribution of Gallium-67 in normal and hypotransferrinemic tumor-bearing mice. J Nucl Med. 1993;34:2135–2143
  6. McLaughlin AF, Southee AE. Gallium scintigraphy in tumor diagnosis and management. In: Murray IPC, Ell PJ editor. Nuclear Medicine in Clinical Diagnosis and Treatment. ed 1. New York: Churchill Livingstone; 1994;
  7. Nejmeddine F, Raphael M, Martin A, et al. Ga-67 scintigraphy in B-cell non-Hodgkin's lymphoma: Correlation of Ga-67 uptake with histology and transferrin receptor expression. J Nucl Med. 1999;40:40–45
  8. Johnson GS, Go MF, Benua RS, et al. Gallium-67 citrate imaging in Hodgkin's disease: Final report of cooperative group. J Nucl Med. 1977;18:692–698
  9. Andrews GA, Hubner KF, Greenlaw RH. Ga-67 citrate imaging in malignant lymphoma: Final report of cooperative group. J Nucl Med. 1978;19:1013–1019
  10. Seabold JE, Votau ML, Keyes JW, et al. Gallium-67 citrate scanning. Arch Intern Med. 1976;136:1370–1374
  11. Rudders RA, McCaffrey JA, Kahn PC. The relative roles of gallium-67-citrate scanning and lymphangiography in the current management of malignant lymphoma. Cancer. 1997;40:1439–1443
  12. Longo DL, Schilsky RL, Blei L, et al. Gallium-67 scanning: Limited usefulness in staging patients with non-Hodgkin's lymphoma. Am J Med. 1980;68:695–700
  13. Bekerman C, Hoffer PB, Bitran JD. The role of gallium-67 in the clinical evaluation of cancer. In: Semin Nucl Med. 25:1985;p. 72–103
  14. Anderson KC, Leonard RCF, Canellos GP, et al. High-dose gallium imaging in lymphoma. Am J Med. 1983;75:327–331
  15. Front D, Israel O, Epelbaum R, et al. Ga-67 SPECT before and after treatment of lymphoma. Radiology. 1990;175:515–519
  16. Tumeh SS, Rosenthal DS, Kaplan WD, et al. Lymphoma: Evaluation with Ga-67 SPECT. Radiology. 1987;164:111–114
  17. Galss RB, Fernbach SK, Conway JJ, et al. Gallium scintigraphy in American Burkitt lymphoma: Accurate assessment of tumor load and prognosis. AJR Am J Roentgenol. 1985;145:671–676
  18. Brown ML, O'Donnell JB, Thrall JH, et al. Gallium-67 seintigraphy in untreated and treated non-Hodgkin lymphomas. J Nucl Med. 1978;19:875–879
  19. Hoffer P. Status of gallium-67 in tumor detection. J Nucl Med. 1980;21:394–398
  20. Sandrock D, Lastoria S, Magrath IT, et al. The role of gallium-67 scintigraphy in patients with small, non-cleaved cell lymphoma. Eur J Nucl Med. 1993;20:119–122
  21. Waxman AD, Eller D, Ashook G, et al. Comparison of gallium-67 citrate and thallium-201 scintigraphy in peripheral and intrathoracic lymphoma. J Nucl Med. 1996;37:46–50
  22. Gallamini A, Biggi A, Fruttero A, et al. Revisiting the prognostic role of gallium scintigraphy in low-grade non-Hodgkin's lymphoma. Eur J Nucl Med. 1997;24:1499–1506
  23. Ben-Haim S, Bar-Shalom R, Israel O, et al. Utility of gallium-67 scintigraphy in low-grade non-Hodgkin's lymphoma. J Clin Oncol. 1996;14:1936–1942
  24. Jochelson M, Mauch P, Balikian J, et al. The significance of the residual mediastinal mass in treated Hodgkin's disease. J Clin Oncol. 1985;3:637–640
  25. Radford JA, Cowan RA, Flanagan M, et al. The significance of residual mediastinal abnormality on the chest radiograph following treatment for Hodgkin's disease. J Clin Oncol. 1988;6:940–946
  26. Surbone A, Longo DL, DeVita VT, et al. Residual abdominal massess in aggressive non-Hodgkin's lymphoma after combination chemotherapy: Significance and management. J Clin Oncol. 1988;6:1832–1837
  27. (editorial) Canellos GP. Residual mass in lymphoma may not be residual disease. J Clin Oncol. 1988;6:931–933
  28. Israel O, Front D, Lam M, et al. Gallium-67 imaging in monitoring lymphoma response to treatment. Cancer. 1988;61:2439–2443
  29. Wylie BR, Southee AE, Joshua DE, et al. Gallium scanning in the management of mediastinal Hodgkin's disease. Eur J Haematol. 1989;42:344–347
  30. Israel O, Front D, Epelbaum R, et al. Residual mass and negative gallium scintigraphy in treated lymphoma. J Nucl Med. 1990;31:365–368
  31. Drossman SR, Schiff RG, Kronfeld GD, et al. Lymphoma of the mediastinum and neck: Evaluation with Ga-67 imaging and CT correlation. Radiology. 1990;174:171–175
  32. Weiner M, Leventhal B, Cantor A, et al. Gallium-67 scan as an adjunct to computed tomography scans for the assessment of a residual mediastinal mass in pediatric patients with Hodgkin's disease. Cancer. 1991;68:2478–2480
  33. Karimjee S, Brada M, Husband J, et al. A comparison of gallium-67 single photon emission computed tomography and computed tomography in mediastinal Hodgkin's disease. Eur J Cancer. 1992;28A:1856–1857
  34. Kostakoglu L, Yeh SDJ, Portlock C, et al. Validation of gallium-67-citrate single photon emission computed tomography in biopsy-confirmed residual Hodgkin's disease in the mediastinum. J Nucl Med. 1992;33:345–350
  35. Front D, Israel O, Ben-Haim S. The dilemma of a residual mass in treated lymphoma: The role of gallium-67 scintigraphy. In: Freeman L editors. Nuclear Medicine Annual. New York: Raven Press; 1991;
  36. Ionescu I, Brice P, Simon D, et al. Restaging with gallium scan identifies chemosensitive patients and predicts survival of poor-prognosis mediastinal Hodgkin's disease patients. Med Oncol. 2000;17:127–134
  37. Chilton HM, Witcofski RL, Watson NE, et al. Alteration of gallium-67 distribution in tumor-bearing mice following treatment with methotrexate: Concise communication. J Nucl Med. 1981;22:1064–1068
  38. Dambro TJ, Slavin JD, Epstein NF, et al. Loss of radio-gallium from lymphoma after initiation of chemotherapy. Clin Nucl Med. 1992;17:32–33
  39. (editorial) Kaplan WD. Residual mass and negative gallium scintigraphy in treated lymphoma: When is the gallium scan really negative?. J Nucl Med. 1990;31:369–371
  40. Front D, Israel O. The role of Ga-67 scintigraphy in evaluating the results of therapy of lymphoma patients. In: Semin Nucl Med. 25:1995;p. 60–71
  41. Peylan-Ramu N, Haddy TB, Jones E, et al. High frequency of benign mediastinal uptake of gallium-67 after completion of chemotherapy in children with high grade non-Hodgkin's lymphoma. J Clin Oncol. 1989;7:1800–1806
  42. Even-Sapir E, Bar-Shalom R, Israel O, et al. Singlephoton emission computed tomography quantitation of gallium citrate uptake for the differentiation of lymphoma from benign hilar uptake. J Clin Oncol. 1995;13:942–946
  43. Champion PE, Groshar D, Hooper HR, et al. Does gallium uptake in the pulmonary hila predict involvement by non-Hodgkin's lymphoma?. Nucl Med Commun. 1992;13:730–737
  44. (editorial) Israel O, Front D. Benign mediastinal and parahilar uptake of gallium-67 in treated lymphoma: Do we have all the answers?. J Nucl Med. 1993;34:1330–1332
  45. Bar-Shalom R, Israel O, Haim N, et al. Diffuse lung uptake of Ga-67 after treatment of lymphoma: Is it of clinical importance?. Radiology. 1996;199:473–476
  46. (abstr) Israel O, Yefremov N, Mor M, et al. A new technology of combined transmission (CT) and emission (Ga-67) tomography (TET) in the evaluation of patients with lymphoma. J Nucl Med. 2000;41:70P
  47. Front D, Ben-Haim S, Israel O, et al. Lymphoma: Predictive value of Ga-67 scintigraphy after therapy. Radiology. 1992;182:359–363
  48. Hagemeister FB, Purugganan R, Podoloff DA, et al. The gallium scan predicts relapse in patients with Hodgkin's disease treated with combined modality therapy. Ann Oncol. 1994;5(suppl 2):S59–S63
  49. King SC, Reiman RJ, Prosnitz LR. Prognostic importance of restaging gallium scans following induction chemotherapy for advanced Hodgkin's disease. J Clin Oncol. 1994;12:306–311
  50. Vose JM, Bierman PJ, Anderson JR, et al. Single-photon emission computed tomography gallium imaging versus computed tomography: Predictive value in patients undergoing high-dose chemotherapy and autologus stem-cell transplantation for non-Hodgkin's lymphoma. J Clin Oncol. 1996;14:2473–2479
  51. Salloum E, Brandt DS, Caride VJ, et al. Gallium scans in the management of patients with Hodgkin's disease: A study of 101 patients. J Clin Oncol. 1997;15:518–527
  52. Bogart JA, Chung CT, Mariados NF, et al. The value of gallium imaging after therapy for Hodgkin's disease. Cancer. 1998;82:754–759
  53. Cooper DL, Caride VJ, Zloty M, et al. Gallium scans in patients with medistinal Hodgkin's disease treated with chemotherapy. J Clin Oncol. 1993;11:1092–1098
  54. Cooper DL, Neumann RD, Caride VJ. A critical assessment of the prognostic value of gallium-67 scintigraphy in lymphoma. In: Freeman LM editors. Nuclear Medicine Annual. Philadelphia, PA: Lippincott-Raven; 1998;
  55. Weeks JC, Yeap BY, Canellos GP, et al. Value of follow-up procedures in patients with large-cell lymphoma who achieve a complete remission. J Clin Oncol. 1991;9:1196–1203
  56. DeVita VT, Hellman S, Jaffe ES. Hodgkin's disease. In: DeVita VT, Hellman S, Rosenberg SA editor. Cancer Principles and Practice of Oncology. ed 4. Philadelphia, PA: Lippincott-Raven; 1993;
  57. Armitage JO, Weisenburger DD, Hutchins M, et al. Chemotherapy for diffuse large-cell lymphoma: Rapidly responding patients have more durable remissions. J Clin Oncol. 1986;4:160–164
  58. Vose JM, Armitage JO, Bierman PJ, et al. Salvage therapy for relapsed or refractory non-Hodgkin's lymphoma utilizing autologous bone marrow transplantation. Am J Med. 1989;87:285–288
  59. Front D, Bar-Shalom R, Epelbaum R, et al. Early detection of lymphoma recurrence with gallium-67 scintigraphy. J Nucl Med. 1993;34:2101–2104
  60. Shipp MA, Harrington DP. A predictive model for aggressive non-Hodgkin's lymphoma. The International Non-Hodgkin's Lymphoma Prognostic Factors Project. N Engl J Med. 1993;329:987–994
  61. Hasenclever D, Diehl V. A prognostic score for advanced Hodgkin's disease. N Engl J Med. 1998;339:1506–1514
  62. Verdonck LF, Van Putten WLJ, Hagenbeek A, et al. Comparison of CHOP chemotherapy with autologous bone marrow transplantation for slowly responding patients with aggressive non-Hodgkin's lymphoma. N Engl J Med. 1995;332:1045–1051
  63. Kaplan WD, Jochelson MS, Herman TS, et al. Gallium-67 imaging: A predictor of residual tumor viability and clinical outoome in patients with diffuse large-cell lymphoma. J Clin Oncol. 1990;8:1966–1970
  64. Janicek M, Kaplan W, Neuberg D, et al. Early restaging gallium scans predict outcome in poor-prognosis patients with aggressive non-Hodgkin's lymphoma treated with high-dose CHOP chemotherapy. J Clin Oncol. 1997;15:1631–1637
  65. Gasparini M, Bombardieri E, Castellani M, et al. Gallium-67 scintigraphy evaluation of therapy in non-Hodgkin's lymphoma. J Nucl Med. 1998;39:1586–1590
  66. Front D, Bar-Shalom R, Mor M, et al. Hodgkin disease: Prediction of outcome with Ga-67 scintigraphy after one cycle of chemotherapy. Radiology. 1999;210:487–491
  67. Front D, Bar-Shalom R, Mor M, et al. Aggressive non-Hodgkin lymphoma: Early prediction of outcome with Ga-67 scintigraphy. Radiology. 2000;214:253–257
  68. Link MP, Shuster JJ, Donaldson SS, et al. Treatment of children and young adults with early-stage non-Hodgkin's lymphoma. N Engl J Med. 1997;337:1259–1266
  69. Magrath I. Limiting therapy for limited childhood non-Hodgkin's lymphoma. N Engl J Med. 1997;337:1304–1305
  70. Warburg O. The metabolism of tumors. NY: Smith RR; 1931;
  71. Weber G. Biochemical strategy of cancer cells and the design of chemotherapy. GHA Clowes memorial lecture. Cancer Res. 1983;43:3466–3492
  72. Bar-Shalom R, Valdivia AY, Balufox MD. PET imaging in oncology. In: Semin Nucl Med. 30:2000;p. 150–185
  73. Paul R. Comparison of fluorine-18-2-fluorodeoxyglucose and gallium-67 citrate imaging for detection of lymphoma. J Nucl Med. 1987;28:288–292
  74. Okada J, Yoshikawa K, Imazeki K, et al. The use of FDG-PET in the detection and management of malignant lymphoma: Correlation of uptake with prognosis. J Nucl Med. 1991;32:686–691
  75. Lapela M, Leskinen S, Minn HRI, et al. Increased glucose metabolism in untreated non-Hodgkin's lymphoma: A study with positron emission tomography and fluorine-18-fluorodeoxyglucose. Blood. 1995;86:3522–3527
  76. Leskinen-Kallio S, Ruotsalainen U, Nagren K, et al. Uptake of carbon-11-methionine and fluorodeoxyglucose in non-Hodgkin's lymphoma: A PET study. J Nucl Med. 1991;32:1211–1218
  77. Rodriguez M, Rehn S, Ahlstrom H, et al. Predicting malignancy grade with PET in non-Hodgkin's lymphoma. J Nucl Med. 1995;36:1790–1796
  78. Jerusalem G, Warland V, Majjar F, et al. Whole-body 18F-FDG-PET for the evaluation of patients with Hodgkin's disease and non-Hodgkin's lymphoma. Nucl Med Commun. 1999;20:13–20
  79. Hoffmann M, Kletter K, Demling M, et al. Positron emission tomography with fluorine-18-2-fluoro-2-deoxy-D-glucose (F18-FDG) does not visualize extranodal B-cell lymphoma of the mucosa-associated lymphoid tissue (MALT)-type. Ann Oncol. 1999;10:1185–1189
  80. Cremerius U, Fabry U, Neuerburg J, et al. Positron emission tomography with 18F-FDG to defect residual disease after therapy for malignant lymphoma. Nucl Med Commun. 1998;19:1055–1063
  81. Newman JS, Francis IR, Kaminski MS, et al. Imaging of lymphoma with PET with 2-[F-18] fluoro-2-deoxy-D-glucose: Correlation with CT. Radiology. 1994;190:111–116
  82. Stumpe KDM, Urbinelli M, Steinert HC, et al. Wholebody positron emission tomography using fluorodeoxyglucose for staging of lymphoma: Effectiveness and comparison with computed tomography. Eur J Nucl Med. 1998;25:721–728
  83. Okada J, Oonish H, Yoshikawa K, et al. FDG-PET for predicting the prognosis of malignant lymphoma. Ann Nucl Med. 1994;8:187–191
  84. Okada J, Yoshikawa K, Itami M, et al. Positron emission tomography using fluorine-18-fluorordeoxyglucose in malignant lymphoma: A comparison with proliferative activity. J Nucl Med. 1992;33:325–329
  85. Hoh CK, Glaspy J, Rosen P, et al. Whole-body FDG-PET imaging for staging of Hodgkin's disease and lymphoma. J Nucl Med. 1997;38:343–348
  86. Bangerter M, Moog F, Buchmann I, et al. Whole-body 2-[18F]-fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) for accurate staging of Hodgkin's disease. Ann Oncol. 1998;9:1117–1122
  87. Bangerter M, Kotzerke J, Griesshammer M, et al. Positron emission tomography with 18-fluorodeoxyglucose in the staging and follow-up of lymphoma in the chest. Acta Oncol. 1999;38:799–804
  88. Kotzerke J, Guhlmann A, Moog F, et al. Role of attenuation correction for fluorine-18 fluorodeoxyglucose positron emission tomography in the primary staging of malignant lymphoma. Eur J Nucl Med. 1999;26:31–38
  89. Klose T, Leidl R, Buchmann I, et al. Primary staging of lymphomas: Cost-effectiveness of FDG-PET versus computed tomography. Eur J Nucl Med. 2000;27:1457–1464
  90. Partridge S, Timothy A, O'Doherty MJ, et al. 2-fluorine-18-fluoro-2-deoxy-D glucose positron emission tomography in the pretreatment staging of Hodgkin's disease: Influence on patient management in a signle institution. Ann Oncol. 2000;11:1273–1279
  91. Kostakoglu L, Goldsmith SJ. Fluorine-18 fluorodeoxyglucose positron emission tomography in the staging and follow-up of lymphoma: Is it time to shift gears. Eur J Nucl Med. 2000;27:1564–1578
  92. Moog F, Bangerter M, Diederichs CG, et al. Lymphoma: Role of whole-body 2-deoxy-2-[F-18]fluoro-D-glucose (FDG) PET in nodal staging. Radiology. 1997;203:795–800
  93. Moog F, Bangerter M, Diederichs CG, et al. Extranodal malignant lymphoma: Detection with FDG PET versus CT. Radiology. 1998;206:475–481
  94. Kostakoglu L, Goldsmith SJ. Positron emission tomography in lymphoma: Comparison with computed tomography and gallium-67 single photon emission computed tomography. Clin Lymphoma. 2000;1:67–74
  95. Moog F, Bangerter M, Kotzerke J, et al. 18-F-fluorodeoxyglucose positron emission tomography as a new approach to detect lymphomatous bone marrow. J Clin Oncol. 1998;16:603–609
  96. Carr R, Barrington SF, Madan B, et al. Detection of lymphoma in bone marrow by whole-body positron emission tomography. Blood. 1998;91:3340–3346
  97. Dimitrakopoulou-Strauss A, Strauss LG, Goldschmidt H, et al. Evaluation of tumor metabolism and multidrug resistance in patients with treated lymphoma. Eur J Nucl Med. 1995;22:434–442
  98. (abstr) Bangerter M, Moog F, Griesshammer M, et al. Role of whole-body FDG-PET in predicting relapse in residual masses after treatment of lymphoma. Br J Haematol. 1998;102:148
  99. de Wit M, Bumann D, Beyer W, et al. Whole-body positron emission tomography (RET) for diagnosis of residual mass in patients with lymphoma. Ann Oncol. 1997;8:57–60
  100. Zinzani PL, Magagnoli M, Chierichetti F, et al. The role of positron emission tomography (PET) in the management of lymphoma patients. Ann Oncol. 1999;10:1181–1184
  101. Jerusalem G, Beguin Y, Fassotte MF, et al. Whole-body positron emission tomography using 18F-fluorodeoxyglucose for posttreatment evaluation in Hodgkin's disease and non-Hodgkin's lymphoma has higher diagnostic and prognostic value than classical computed tomography scan imaging. Blood. 1999;94:429–433
  102. Maisey NR, Hill ME, Webb A, et al. Are 18-fluorodeoxyglucose positron emission tomography and magnetic resonance imaging useful in the prediction of relapse in lymphoma residual masses?. Eur J Cancer. 2000;36:200–206
  103. Cremerius U, Fabry U, Kroll U, et al. Clinical value of FDG PET for therapy monitoring of malignant lymphoma—Results of a retrospective study in 72 patients. Nuklearmedizin. 1999;38:24–30
  104. Alavi JB, Benard F, Alavi A. Detection of unsuspected recurrent lymphoma with fluorodeoxyglucose positron emission tomography imaging after induction chemotherapy. Am J Clin Oncol. 1998;21:126–128
  105. (abstr) Front D, Israel O, Mor M, et al. A new technology of combined transmission (CT) and 18F fluorodeoxyglucose (FDG) emission tomography (TET) in the evaluation of cancer patients. J nucl Med. 2000;41:284P
  106. Hoekstra OS, Ossenkoppele GJ, Golding R, et al. Early treatment response in malignant lymphoma, as determined by planar fluorine-18-fluorodeoxyglucose scintigraphy. J Nucl Med. 1993;34:1706–1710
  107. Hoekstra OS, van Lingen A, Ossenkoppele GJ, et al. Early response monitoring in malignant lymphoma using fluorine-18 fluorodeoxyglucose single-photon emission tomography. Eur J Nucl Med. 1993;20:1214–1217
  108. Barrington SF, Carr R. Staging of Burkitt's lymphoma and response to treatment monitored by PET scanning. Clin Oncol. 1995;7:334–335
  109. Romer W, Hanauske AR, Ziegler S, et al. Positron emission tomography in non-Hodgkin's lymphoma: Assessment of chemotherapy with fluorodeoxyglucose. Blood. 1998;91:4464–4471
  110. Wiedmann E, Baican B, Hertel A, et al. Positron emission tomography (PET) for staging and evaluation of response to treatment in patients with Hodgkin's disease. Leuk Lymphoma. 1999;34:545–551
  111. Willkomm P, Palmedo H, Grunwald F, et al. Functional imaging of Hodgkin's disease with FDG-PET and gallium-67. Nuklearmedizin. 1998;37:251–253
  112. (abstr) Kostakoglu L, Leonard JP, Coleman M, et al. Comparison of fluorine-18 fluorodeoxyglucose positron emission tomography (FDG-PET) and gallium-67 scintigraphy in staging and follow-up of patients with lymphoma. Blood. 1999;94:84A

PII: S0001-2998(01)80018-0

doi: 10.1053/snuc.2001.23519

Seminars in Nuclear Medicine
Volume 31, Issue 3 , Pages 177-190 , July 2001