|
Advertisement |
|
|
||
 |
|
|||||
|
|||||
|
 |
||||||
|
||||||
|
||||||
|
© 1999 American Society for Clinical Oncology Report of an International Workshop to Standardize Response Criteria for Non-Hodgkin's LymphomasFrom the National Cancer Institute, Bethesda, MD; Stanford University, Palo Alto, CA; Centre Hospitalier Lyon-Sud, Lyon, France; Dana-Farber Cancer Institute, Boston, MA; Loyola University, Maywood, IL; British Columbia Cancer Agency, Vancouver, British Columbia, Canada; St. Bartholomew's Hospital, London, England; University of Nebraska, Omaha, NE; IDEC Corporation, San Diego, CA; Universiteit Utrecht, Utrecht, the Netherlands; M.D. Anderson Cancer Center, Houston, TX; Roswell Park Cancer Institute, Buffalo, NY; Klinikum Großhadern, Munich, Germany; Memorial Sloan-Kettering Cancer Center, New York, NY; Massachusetts General Hospital, Boston, MA; and Sharp Memorial Hospital, San Diego, CA. Address reprint requests to Bruce D. Cheson, MD, National Cancer Institute, Executive Plaza North, Rm 741, Bethesda, MD 20892; email chesonb{at}ctep.nci.nih.gov
ABSTRACT: Standardized guidelines for response assessment are needed to ensure comparability among clinical trials in non-Hodgkin's lymphomas (NHL). To achieve this, two meetings were convened among United States and international lymphoma experts representing medical hematology/oncology, radiology, radiation oncology, and pathology to review currently used response definitions and to develop a uniform set of criteria for assessing response in clinical trials. The criteria that were developed include anatomic definitions of response, with normal lymph node size after treatment of 1.5 cm in the longest transverse diameter by computer-assisted tomography scan. A designation of complete response/unconfirmed was adopted to include patients with a greater than 75% reduction in tumor size after therapy but with a residual mass, to include patients—especially those with large-cell NHL—who may not have residual disease. Single-photon emission computed tomography gallium scans are encouraged as a valuable adjunct to assessment of patients with large-cell NHL, but such scans require appropriate expertise. Flow cytometric, cytogenetic, and molecular studies are not currently included in response definitions. Response rates may be the most important objective in phase II trials where the activity of a new agent is important and may provide support for approval by regulatory agencies. However, the goals of most phase III trials are to identify therapies that will prolong the progression-free survival, if not the overall survival, of the treated patients. We hope that these guidelines will serve to improve communication among investigators and comparability among clinical trials until clinically relevant laboratory and imaging studies are identified and become more widely available.
STANDARDIZED RESPONSE criteria are essential for the conduct of clinical research. They facilitate interpretation of data, comparisons of the results among various clinical trials, and identification of new agents with promising activity, and provide a framework on which to evaluate new biologic and immunologic insights into the diseases being studied. The availability of uniform guidelines ensures a reliable analysis of comparable patient groups among studies and acquisition of similar data. Response criteria have been developed for patients with chronic lymphocytic leukemia,1,2 acute myelogenous leukemia,3 and Hodgkin's disease (HD),4 and criteria are now standardized for solid tumors.5 In 1987, Dixon et al6 emphasized the need for uniform reporting of end points in clinical trials of patients with non-Hodgkin's lymphomas (NHL); of particular importance were the complete remission rate, survival, time to treatment failure, and time to relapse of complete responders. Their recommendations were met with controversy that remained unresolved.7 Therefore, although the need for common reporting was obvious, the precise definitions of several major end points were neither provided nor uniformly adopted. A consequence is that there are currently no standardized response criteria for patients with NHL. Recognizing this need, several United States lymphoma investigators from National Cancer Institute (NCI)–sponsored cooperative groups, the NCI, and the pharmaceutical industry collaborated in an effort to resolve the issues regarding response assessment in NHL. The result was a preliminary document that was subsequently reviewed and approved by European lymphoma experts.8,9 Eventually, a workshop was held at the NCI on February 25 to 26, 1998, with a subsequent meeting on May 16, 1998, to come to consensus on a standardized set of guidelines for response assessment in adult patients with indolent and aggressive NHL. This report presents the recommendations from the NCI-sponsored international working group. These represent, to a large extent, a consensus among the participants, rather than being conclusions based on a body of data. However, until such data are available, we hope these standardized guidelines will serve as a basis for measuring the activity of new therapies and facilitating comparisons among the results of clinical trials.
In general, each major cooperative cancer treatment group with active clinical investigations in NHL has developed its own means of assessing and describing response rates and duration. Unfortunately, the differences among these criteria are sufficient to result in substantial confusion (Table 1). Moreover, the guidelines currently in use have tended to have their basis in solid tumor criteria, which are not always applicable to NHL. NHLs share a number of common features that are distinct from other neoplasms, are relatively specific, and mandate a separate set of criteria.
Lymph Node Biopsies Whenever possible, an excisional-node biopsy of a suspicious lymph node should be performed for the initial diagnosis of lymphoma. A core-needle biopsy may suffice to document relapse or transformation in a patient with a previous indolent NHL. Pappa et al10 performed needle biopsies on 106 patients, 51 with low-grade lymphoma, 24 with high-grade NHL, 16 with diagnosed HD, and 15 with no diagnosis. The disease was infradiaphragmatic in 92 patients and supradiaphragmatic in 14. A biopsy was diagnostic and yielded information that guided initial treatment in 88 of 106 patients (83%). When the biopsy was performed at the time of a suspected recurrence, a different histology was diagnosed in 33 of 80 patients, leading to a change in treatment plans for 31 patients. This procedure was accurate in making the diagnosis of histologic transformation in 16 of 18 cases. Investigators from Israel11 reported the results of 1,500 computed tomography (CT)-guided core-needle biopsies with which the diagnosis of lymphoma was made in 100 patients, 71 with NHL and 29 with HD. Previous diagnoses of NHL and HD were known in 24% and 31% of patients, respectively. The results of the needle biopsy were adequate to direct therapy in 86% of cases. Although core biopsies are probably more accurate than fine-needle aspirations, the role of both procedures remains controversial; precise classification of the lymphoma may be difficult, and the procedure requires an appropriate level of skill. For example, the sample was inadequate in 15 of 51 (29.4%) indolent lymphomas in the Pappa series.10 Other problems with this procedure can be anticipated in distinguishing nodular versus diffuse histologies, in lesions with substantial fibrosis or sclerosis, in cases of T-cell NHL, T-cell–rich B-cell NHL, or in lymph nodes only partially involved with lymphoma, particularly in patients with HD.
Bone Marrow Evaluation Lack of uniformity in the interpretation of bone marrow aspirates and biopsies represents a major problem. Among patients with a low-grade lymphoma, the differential diagnosis between bone marrow involvement and benign lymphoid aggregates can be difficult. Bone marrow biopsies should be scored as positive (unequivocal cytologic or architectural evidence of malignancy), negative (no aggregates or only a few well-circumscribed lymphoid aggregates), or indeterminate (increased number or size of aggregates without cytologic or architectural atypia). The bone marrow report should be reported not only as positive or negative for lymphoma, but the percentage of invasion and the lymphoma subtype should be indicated, the latter to describe any discordance with the nodal disease. Patients whose bone marrow is histologically normal but with a small clonal B-cell population detected by flow cytometry should be considered to have a normal bone marrow until there are clinical studies that demonstrate a different outcome for this group.
Response in patients with lymphomas is most often defined on the basis of a regression in the size of enlarged lymph nodes or confluent lymph node masses; therefore, it is critical to determine how small an involved node must become after treatment to be considered "normal." A number of studies have attempted to determine the normal range of node size in patients without lymphoid malignancies. The size of lymph nodes in normal individuals as determined by CT scanning or at autopsy varies to a minor degree with the location of the node. In general, however, the upper limit has been considered to be approximately 1 cm in measurement of the short axis.14-20 In an autopsy series,18 there was a difference among mediastinal regions, with upper limits ranging from 8 to 12 mm in the short axis, with greater variation in the long axis. In another autopsy series,21 lymph nodes ranged in size from 5 mm in one region to 8 to 10 mm in others. Several studies have also looked at the size of abdominal nodes on CT scan in patients with either blunt trauma or benign or malignant diseases other than lymphoma.14,15 Values varied by region from 8 to 11 mm, but with some normal pelvic nodes as large as 15 mm. Based on these data, at the time of diagnosis, a lymph node that is greater than 1 cm in its longest transverse diameter should be considered compatible with involvement by NHL.
The question of lymph node size criteria becomes more problematic when assessing response in patients with NHL. The tumor mass in lymphoma patients is usually located within a normal structure, a lymph node, which it may replace either partially or completely. After effective treatment, this mass may decrease in size, and what remains may have the size and appearance of a normal lymph node, but it does not disappear. Unfortunately, it is common that as tumor-involved nodes shrink in size after treatment, fibrosis, necrosis, or inflammation results in a persistent enlargement of that node, although it may be histologically uninvolved by tumor.22 It may also be difficult to interpret response in a group of nodes that were initially enlarged and matted together and appeared as a mass, but that broke up into several smaller nodal masses after treatment. We elected to be consistent with the criteria of 1.5 cm for the cross-sectional diameter of nodes established for HD at the Cotswolds meeting.4 However, nodes that are Another major problem in the interpretation of response to treatment has been that persistence of residual masses after chemotherapy does not necessarily indicate residual disease.25-28 Residual intra-abdominal masses are particularly problematic because of their common occurrence in patients with NHL. As many as 30% to 50% of patients with a large intra-abdominal mass at presentation and for whom the physical examination is normal after therapy will have a residual mass. Residual radiographic abnormalities tend to be more common in patients with large-cell NHL than in patients with a follicular low-grade histology. Fuks et al25 reported 100 patients with advanced NHL of various histologies who were treated with either cyclophosphamide, vincristine, and prednisone or cyclophosphamide, doxorubicin, vincristine, and prednisone. After treatment there were 33 CRs and 38 partial remissions (PRs). In 20 of the PRs, all physical and chemical evidence of disease had returned to normal; however, a lymphangiogram, gallium scan, sonogram, or CT suggested residual disease. When those patients were subjected to restaging laparotomy, disease was detected in only four patients (20%). Surbone et al27 reviewed 241 patients with aggressive NHL treated at the NCI between 1977 and 1986. Of the 72 patients (33%) with an abdominal mass at diagnosis, 29 (40%) were left with a radiologically detectable, stable residual mass that had decreased when compared with the initial diagnostic evaluation, but with no other clinical or laboratory evidence of disease. Patients with bulky masses (> 10 cm) before treatment were more likely to experience this circumstance. Residual masses were evaluated by laparotomy (n = 10), needle aspiration (n = 6), autopsy (n = 6), or clinical and radiographic evaluation only (n = 7). All needle aspirations and autopsies were negative. One laparotomy was positive in a patient in whom a preceding needle aspiration had been inadequate. Therefore, there was no evidence of disease detected in 21 of 22 (95%) cases on pathologic examination of the residual mass, and none of these patients subsequently relapsed. Of seven patients who were observed clinically, five were alive and free of disease from 2 to 9 years, but the other two patients relapsed. In a comparison of prednisone, methotrexate, doxorubicin, cyclophosphamide, and etoposide (ProMACE)/mechlorethamine, vincristine, procarbazine, and prednisone with ProMACE/cytarabine, bleomycin, vincristine, and methotrexate with leucovorin conducted at the NCI, restaging laparotomy was abandoned because 95% of residual abdominal masses did not contain lymphoma.28 The manner in which patients with residual masses are assigned into response categories has varied widely among studies. In some series, responses in patients with residual masses were reclassified at a future time, depending on the subsequent behavior of the mass.29 In a trial conducted by the NCI of Canada Clinical Trials Group, a CR required a return of all nodes to less than 1 cm, unless larger nodes were negative by histologic examination.30 Some investigators have used terms such as "probable CR."31,32 Coiffier et al33 reported that 553 of 737 (75%) patients with aggressive NHL experienced disappearance of clinical and laboratory evidence of disease, although 150 (27%) had a persistent mediastinal or abdominal mass on CT scan. There was no difference in time to relapse or survival between those with or without a residual mass (relapse rates 24% and 26%, respectively); as a result, they retroactively included such cases within the CR category if morphologic evidence of NHL was not available or if the size of the mass did not change after two courses of treatment. Several investigators recommend that a large abdominal or mediastinal mass that undergoes greater than 50% reduction in size and remains stable for 2 to 4 months should not prevent classification as a CR given the absence of all other measurable disease,27-29,31,32,34 whereas a cut-off of 75% is used by others.33
The following criteria are considered anatomic definitions (Table 2). In the future, as additional radiographic, laboratory, and functional studies become more widely available and clearly demonstrate predictive value, they may be recommended as well.
CR requires the following:
2. All lymph nodes and nodal masses must have regressed to normal size (  1.5 cm in their greatest transverse diameter for nodes > 1.5 cm before therapy). Previously involved nodes that were 1.1 to 1.5 cm in their greatest transverse diameter before treatment must have decreased to 1 cm in their greatest transverse diameter after treatment, or by more than 75% in the sum of the products of the greatest diameters (SPD). 3. The spleen, if considered to be enlarged before therapy on the basis of a CT scan, must have regressed in size and must not be palpable on physical examination. However, no normal size can be specified because of the difficulties in accurately evaluating splenic and hepatic size. For instance, spleens thought to be of normal size may contain lymphoma, whereas an enlarged spleen may not necessarily reflect the presence of lymphoma but variations in anatomy, blood volume, the use of hematopoietic growth factors, or other causes. The determination of splenic volume or splenic index by CT scan are cumbersome and not widely used.35,36 Any macroscopic nodules in any organs detectable on imaging techniques should no longer be present. Similarly, other organs considered to be enlarged before therapy due to involvement by lymphoma, such as liver and kidneys, must have decreased in size. 4. If the bone marrow was involved by lymphoma before treatment, the infiltrate must be cleared on repeat bone marrow aspirate and biopsy of the same site. The sample on which this determination is made must be adequate (  20 mm biopsy core). Flow cytometric, molecular, or cytogenetic studies are not considered part of routine assessment to document persistent disease at the present time. These studies should only be incorporated into trials examining important research questions. CR/unconfirmed (CRu) includes those patients who fulfill criteria 1 and 3 above, but with one or more of the following features:
2. Indeterminate bone marrow (increased number or size of aggregates without cytologic or architectural atypia). PR requires the following:
50% decrease in SPD of the six largest dominant nodes or nodal masses. These nodes or masses should be selected according to the following features: (a) they should be clearly measurable in at least two perpendicular dimensions, (b) they should be from as disparate regions of the body as possible, and (c) they should include mediastinal and retroperitoneal areas of disease whenever these sites are involved. 2. No increase in the size of the other nodes, liver, or spleen. 3. Splenic and hepatic nodules must regress by at least 50% in the SPD. 4. With the exception of splenic and hepatic nodules, involvement of other organs is considered assessable and not measurable disease. 5. Bone marrow assessment is irrelevant for determination of a PR because it is assessable and not measurable disease; however, if positive, the cell type should be specified in the report, eg, large-cell lymphoma or low-grade lymphoma (ie, small, lymphocytic small cleaved, or mixed small and large cells). 6. No new sites of disease. Stable disease is defined as less than a PR (see above) but is not progressive disease (see below). Relapsed disease (CR, CRu) requires the following:
50% in the size of previously involved sites. 2. 50% increase in greatest diameter of any previously identified node greater than 1 cm in its short axis or in the SPD of more than one node. Progressive disease (PR, nonresponders) requires the following:
50% increase from nadir in the SPD of any previously identified abnormal node for PRs or nonresponders. 2. Appearance of any new lesion during or at the end of therapy.
Response Assessment
2. A bone marrow aspirate and biopsy should only be performed to confirm a CR if they were initially positive or if it is clinically indicated by new abnormalities in the peripheral blood counts or blood smear.
End Points
Follow-up For patients on clinical studies, time points for monitoring disease status should be standardized. Patients on clinical trials should be reassessed after completion of treatment at a minimum of every 3 months for 2 years, then every 6 months for 3 years, and then annually for at least 5 years. For patients with large-cell NHL, few recurrences occur beyond that point. However, there is a continuous risk of relapse for patients with a follicular histology. These intervals may vary with specific treatments, protocols, or unique drug characteristics. Minimum testing at follow-up visits should include history, physical examination for lymphadenopathy, abdominal masses, or organomegaly, and blood tests including a complete blood cell count and LDH. Additional blood tests and imaging studies may be added for relevant clinical indications, but specific tests cannot be currently recommended for the reasons discussed previously in this article. The uniformity of reassessment will provide reasonable comparability among clinical trials without demanding excessive testing of unproven value. Despite the difficulties associated with detection of clinically relevant evidence of relapse or progression, some uniformity of follow-up examinations is desirable across clinical trials so that time and disease state–related end points, such as failure-free, disease-free, and relapse-free survival, can be compared. It is obvious, for example, that a follow-up protocol requiring extensive reevaluation every 2 months will produce different apparent intervals for those end points compared with one requiring the same testing annually, even if the true times to events are the same.
A number of additional diagnostic studies have been proposed to evaluate response or disease progression but are not currently required.
Gallium Scanning Vose et al39 found that the 1-year failure-free survival for patients with a positive SPECT gallium scan after high-dose chemotherapy with autologous transplantation for diffuse aggressive NHL was 15% compared with a 3-year failure-free survival of 47% for patients with a negative scan. Although the predictability of gallium studies was rather modest, they were more accurate than CT scanning. However, the procedure was not predictive of outcome for patients with a follicular NHL. Janicek et al44 found that early restaging with 67Ga scans was useful in predicting those patients who were most likely to experience prolonged disease-free survival after treatment with an augmented cyclophosphamide, doxorubicin, vincristine, and prednisone regimen. Further prospective study of SPECT gallium scanning is highly desirable. Unfortunately, until this procedure becomes more universally available and uniformly reproducible, it cannot be required as part of routine response assessment for all clinical trials. SPECT gallium scans should be considered part of standard practice at centers with expertise in performing the study in clinically relevant situations (eg, to distinguish masses with viable tumor from fibrosis). Functional studies such as SPECT gallium scans would not be considered as part of the anatomic assessment of response using the guidelines previously discussed, but they should be reported in the results of the clinical trial. Several recent studies have suggested a potential role for positron emission tomography (PET) scanning in monitoring response to therapy.46 However, other studies suggest that the cost-benefit ratio of gallium plus CT is more favorable than MRI.47 An interesting research question would involve a prospective comparison of SPECT gallium scanning with PET scans in the assessment of residual masses.
Additional Measures of Bone Marrow Assessment In conclusion, the goal of clinical research in NHL is to improve the survival of our patients. Therefore, the most important end points of clinical trials in NHL should be overall survival and failure-free survival (time to treatment failure and event-free survival). In phase II trials, particularly in the setting of relapsed and refractory disease where the activity of a new agent may be the most important objective, response rates are important and may provide support for approval by regulatory agencies. On the other hand, the goals of most phase III trials are to identify therapies that will prolong the progression-free survival, if not the overall survival, of the treated patients. Response rates will continue to be ambiguous and subject to considerable controversy as long as we are required to base guidelines on consensus opinion of clinical data rather than on more precise and reliable measures of minimal residual disease. Moreover, particularly in the follicular NHL, incremental increases in response rates have not uniformly translated into prolonged time to treatment failure or survival. It will be important to apply the current guidelines prospectively in several large trials and to critically evaluate their usefulness. The current selection of normal node size after therapy was arbitrary, and what is needed are correlations between a variety of normal lymph node sizes and outcome. Residual lymphoma mass also remains a difficult problem; nevertheless, retroactive assignment of responses is confusing and subject to bias. Clearly, a residual mass in a patient with a large-cell lymphoma, in whom the disease may have been cured, has different implications from a patient with a follicular lymphoma, in whom the mass may remain stable for months but will inevitably progress. To improve response assessment, we strongly encourage the use of SPECT gallium scanning in patients with large cell-lymphoma. As more is learned about the biology and immunology of these diseases, and as additional clinically relevant laboratory and imaging studies are identified and become more widely available, modifications of these guidelines may be required. Until that time, we hope that these guidelines will serve to improve communication among investigators and comparability among clinical trials.
We appreciate the efforts of Javier Garcia-Conde (Hospital Clinico Universitario, Valencia, Spain), Alessandro Gianni (Instituto Nazionale Tumori, Milan, Italy), and Robert Marcus (Addenbrooke's Hospital, Cambridge, England).
1. Cheson BD, Bennett JM, Rai KR, et al: Guidelines for clinical protocols for chronic lymphocytic leukemia: Report of the NCI-sponsored Working Group. Am J Hematol 29:152-163, 1988[Medline]
2.
Cheson BD, Bennett JM, Grever M, et al: National Cancer Institute-Sponsored Working Group guidelines for chronic lymphocytic leukemia: Revised guidelines for diagnosis and treatment. Blood 87:4990-4997, 1996 3. Cheson BD, Cassileth PA, Head DR, et al: Report of the NCI-sponsored workshop on definitions of diagnosis and response in acute myeloid leukemia. J Clin Oncol 8:813-819, 1990[Abstract] 4. Lister TA, Crowther D, Sutcliffe SB, et al: Report of a committee convened to discuss the evaluation and staging of patients with Hodgkin's disease: Cotswolds Meeting. J Clin Oncol 7:1630-1636, 1989[Abstract] 5. Therasse P, Eisenhauer E, Wanders J, et al: Evaluation of response to treatment in solid tumors. Can the methodology be harmonized and simplified? Ann Oncol 2:25, 1998 (suppl) (abstr)
6.
Dixon DO, McLaughlin P, Hagemeister FB, et al: Reporting outcomes in Hodgkin's disease and lymphoma. J Clin Oncol 5:1670-1672, 1987 7. Anderson JR, Propert KJ, Harrington DP: Guidelines for reporting outcomes of lymphoma trials. J Clin Oncol 6:559-560, 1988 (letter)[Medline] 8. Horning S, Cheson B, Peterson B, et al: Response criteria (RC) and quality assurance (QA) of responses in the evaluation of new therapies for patients with low-grade lymphoma (LGNHL). Proc Am Soc Clin Oncol 16:18a, 1997 (abstr 61) 9. Grillo-López AJ, Horning S, Cheson B, et al: Development of response criteria (RC) for low-grade or follicular lymphomas (LG/FNHL) and application in a 166 patient study. Exper Hematol 25:732, 1997 (abstr 17) 10. Pappa VI, Hussain HK, Raeznek RH, et al: Role of image-guided core-needle biopsy in the management of patients with lymphoma. J Clin Oncol 14:2427-2430, 1996[Abstract] 11. Ben-Yehuda D, Polliack A, Okon E, et al: Image-guided core-needle biopsy in malignant lymphoma: Experience with 100 patients that suggests the technique is reliable. J Clin Oncol 14:2431-2434, 1996[Abstract] 12. Coller BS, Chabner BA, Gralnick HR: Frequencies and patterns of bone marrow involvement in non-Hodgkin's lymphomas: Observations on the value of bilateral biopsies. Am J Hematol 3:105-119, 1977[Medline] 13. Bitran JD, Golomb HM, Ultmann JE, et al: Non-Hodgkin's lymphoma, poorly differentiated lymphocytic and mixed cell types: Results of sequential staging procedures, response to therapy, and survival of 100 patients. Cancer 42:88-95, 1978[Medline]
14.
Dorfman RE, Alpern MB, Gross BH, et al: Upper abdominal lymph nodes: Criteria for normal size determined with CT. Radiology 180:319-322, 1991 15. Einstein DM, Singer AA, Chilcote WA, et al: Abdominal lymphadenopathy: Spectrum of CT findings. Radiographics 11:457-472, 1991[Abstract]
16.
Glazer GM, Gross BH, Quint LE, et al: Normal mediastinal lymph nodes: Number and size according to American Thoracic Society mapping. AJR Am J Roentgenol 144:261-265, 1985 17. Hopper KD, Kasales CJ, Van Slyke MA, et al: Analysis of interobserver and intraobserver variability in CT tumor measurements. AJR Am J Roentgenol 187:851-854, 1996
18.
Kiyono K, Sone S, Sakai F, et al: The number and size of normal mediastinal lymph nodes: A postmortem study. AJR Am J Roentgenol 150:771-776, 1988
19.
Steinkamp HJ, Hosten N, Richter C, et al: Enlarged cervical lymph nodes at helical CT. Radiology 191:795-798, 1994
20.
van den Brekel MWM, Castelijns JA, Snow GB: Detection of lymph node metastases in the neck: Radiologic criteria. Radiology 192:617-617, 1994
21.
Genereux GP, Howie JL: Normal mediastinal lymph node size and number: CT and anatomic study. AJR Am J Roentgenol 142:1095-1100, 1984 22. Lewis E, Bernardino ME, Salvador PG, et al: Post-therapy CT-detected mass in lymphoma patients: Is it viable tissue? J Comput Assist Tomogr 6:792-795, 1982[Medline] 23. Grillo-López AJ, McLaughlin P, Cheson BD, et al: First report on the application of the new response criteria (RC) proposed for NHL: The Rituximab pivotal trial. Proc Am Soc Clin Oncol (in press) 24. Grillo-López AJ, Cheson B, Horning S, et al: Response criteria (RC) for NHL: Importance of "normal" lymph node (LN) size and correlations with response. Blood 92:412a, 1998 (abstr 1701) (suppl 1) 25. Fuks JZ, Aisner J, Wiernik PH: Restaging laparotomy in the management of the non-Hodgkin lymphomas. Med Pediatr Oncol 10:429-438, 1982[Medline] 26. Stewart FM, Williamson BR, Innes DJ, et al: Residual tumor masses following treatment for advanced histiocytic lymphoma. Cancer 55:620-623, 1985[Medline] 27. Surbone A, Longo DL, DeVita VT Jr, et al: Residual abdominal masses in aggressive non-Hodgkin's lymphoma after combination chemotherapy: Significance and management. J Clin Oncol 6:1832-1837, 1988[Abstract]
28.
Longo DL, DeVita VT Jr, Duffey PL, et al: Superiority of ProMACE-CytaBOM over ProMACE-MOPP in the treatment of advanced diffuse aggressive lymphoma: Results of a prospective randomized trial. J Clin Oncol 9:25-38, 1991
29.
Waits TM, Greco FA, Greer JP, et al: Effective therapy for poor-prognosis non-Hodgkin's lymphoma with 8 weeks of high-dose-intensity combination chemotherapy. J Clin Oncol 11:943-949, 1993
30.
Meyer RM, Quirt IC, Skillings JR, et al: Escalated as compared with standard doses of doxorubicin in BACOP therapy for patients with non-Hodgkin's lymphoma. N Engl J Med 329:1770-1776, 1993 31. Zuckerman KS, LoBuglio AF, Reeves JA: Chemotherapy of intermediate- and high-grade non-Hodgkin's lymphomas with a high-dose doxorubicin-containing regimen. J Clin Oncol 8:248-256, 1990[Abstract]
32.
Zuckerman KS, Case DC Jr, Gams RA, et al: Chemotherapy of intermediate- and high-grade non-Hodgkin's lymphomas with an intensive epirubicin-containing regimen. Blood 82:3564-3573, 1993 33. Coiffier B, Gisselbrecht C, Herbrecht R, et al: LNH-84 regimen: A multicenter study of intensive chemotherapy in 737 patients with aggressive malignant lymphoma. J Clin Oncol 7:1018-1026, 1989[Abstract]
34.
Chopra R, Goldstone AH, Pearce R, et al: Autologous versus allogeneic bone marrow transplantation for non-Hodgkin's lymphoma: A case-controlled analysis of the European Bone Marrow Transplant Group Registry data. J Clin Oncol 10:1690-1695, 1992 35. Strijk SP, Boetes C, Bogman MJJT, et al: The spleen in non-Hodgkin lymphoma: Diagnostic value of computed tomography. Acta Radiol 28:139-144, 1987[Medline]
36.
Breiman RS, Beck JW, Korobkin M, et al: Volume determinations using computed tomography. AJR Am J Roentgenol 138:329-333, 1982 37. Shipp MA, Ambinder RF, Appelbaum FR, et al: NCCN preliminary non–Hodgkin's lymphoma practice guidelines. Oncology (Huntingt) 11:281-346, 1997[Medline] 38. 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 9:1196-1203, 1991[Abstract] 39. 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 autologous stem-cell transplantation for non-Hodgkin's lymphoma. J Clin Oncol 14:2473-2479, 1996[Abstract] 40. Longo DL, Schilsky RL, Blei L, et al: Gallium-67 scanning: Limited usefulness in staging patients with non-Hodgkin's lymphoma. Am J Med 68:695-700, 1980[Medline]
41.
Hill M, Cunningham D, MacVicar D, et al: Role of magnetic resonance imaging in predicting relapse in residual masses after treatment of lymphoma. J Clin Oncol 11:2273-2278, 1993 42. Israel O, Front D, Lam M, et al: Gallium 67 imaging in monitoring lymphoma response to treatment. Cancer 61:2439-2443, 1988[Medline] 43. Kaplan WD, Jochelson MS, Herman TS, et al: Gallium-67 imaging: A predictor of residual tumor viability and clinical outcome in patients with diffuse large-cell lymphoma. J Clin Oncol 8:1966-1970, 1990[Abstract] 44. Janicek M, Kaplan W, Neuberg D, et al: Early restaging gallium scans predict outcome in poor-prognosis patients with aggressivenon-Hodgkin's lymphoma treated with high-dose CHOP chemotherapy. J Clin Oncol 15:1631-1637, 1997[Abstract] 45. Even-Sapir E, Bar-Shalom R, Israel O, et al: Single-photon emission computed tomography quantitation of gallium citrate uptake for the differentiation of lymphoma from benign hilar uptake. J Clin Oncol 13:942-946, 1995[Abstract]
46.
Römer W, Hahauske A-R, Zieger S, et al: Positron-emission tomography in non-Hodgkin's lymphoma: Assessment of chemotherapy with fluorodeoxyglucose. Blood 91:4464-4471, 1998 47. Devizzi L, Maffiolo L, Bonfante V, et al: Comparison of gallium scan, computed tomography, and magnetic resonance in patients with mediastinal Hodgkin's disease. Ann Oncol 8:53-56, 1997
48.
Hoane BR, Shields AF, Porter BA, et al: Detection of lymphomatous bone marrow involvement with magnetic resonance imaging. Blood 78:728-738, 1991
49.
Altehoefer C, Blum U, Bathmann J, et al: Comparative diagnostic accuracy of magnetic resonance imaging and immunoscintography for detection of bone marrow involvement in patients with malignant lymphoma. J Clin Oncol 15:1754-1760, 1997 50. Moog F, Bangerter M, Kotzerke J, et al: 18-F-fluorodeoxyglucose-positron emission tomography as a new approach to detect lymphomatous bone marrow. Blood 16:603-609, 1998
51.
Carr R, Barrington SF, Madan B, et al: Detection of lymphoma in bone marrow by whole-body positron emission tomography. Blood 91:3340-3346, 1998 Submitted October 27, 1998; accepted January 25, 1999. This article has been cited by other articles:
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
TOP
ABSTRACT
INTRODUCTION
