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Aggressive Non-Hodgkin Lymphoma: Early Prediction of Outcome with ⁶⁷Ga Scintigraphy¹

¹ From the Departments of Nuclear Medicine (D.F., R.B.S., M.M., A.F., G.M.K., O.I.), Oncology (N.H., R.E.), and Radiology (D.G.), Rambam Medical Center, Haifa 35254, Israel. Received November 20, 1998; revision requested February 11, 1999; revision received April 22; accepted July 27. Address reprint requests to D.F.

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To evaluate use of gallium 67 scintigraphy early during chemotherapy to predict the outcome in patients with aggressive non-Hodgkin lymphoma.

MATERIALS AND METHODS: Among 118 patients, ⁶⁷Ga scintigraphy was performed after one cycle of chemotherapy in 51 patients, after a median of 3.5 cycles in 97 patients, and both in 30 patients. Computed tomography (CT) was performed after a median of 3.5 cycles of treatment in 87 patients. The failure-free survival was compared between patients with positive or negative ⁶⁷Ga or CT scans by using the log-rank test. Multivariate analysis helped determine the relation between ⁶⁷Ga scintigraphic and CT findings and the outcome.

RESULTS: The differences in failure-free survival between patients with positive versus negative ⁶⁷Ga scans after one cycle of treatment (P < .001) and at midtreatment (P < .001) were significant. There was no statistically significant difference in failure-free survival between patients with positive versus negative CT findings during treatment. In multivariate analysis, ⁶⁷Ga scintigraphy after one cycle (P < .045) and at midtreatment (P < .006) was an independent factor associated with outcome.

CONCLUSION: Gallium 67 scintigraphic findings after one cycle of chemotherapy and at midtreatment are predictive of outcome in patients with aggressive non-Hodgkin lymphoma. CT findings are not predictive. Early ⁶⁷Ga scintigraphy during chemotherapy is a good indicator of patients who may benefit from a change to a more aggressive treatment. A future study is necessary to investigate the potential effect of early change of treatment.

Index terms: Gallium, radioactive, 99.12962 • Lymphoma, 99.8343 • Lymphoma, CT, 99.12912 • Lymphoma, SPECT, 99.12962 • Lymphoma, radionuclide studies, 99.12962, 99.12974 • Treatment planning, 99.8343

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
There is now considerable evidence to show that gallium 67 scintigraphy after induction therapy helps to determine whether an individual patient with aggressive non-Hodgkin lymphoma has reached a complete response (1–3). This is especially important when a residual mass is present at computed tomography (CT) after treatment. Although such a mass may sometimes contain cancer cells, it may consist only of fibrotic and necrotic tissue, which does not take up ⁶⁷Ga and which disappears without treatment over time. Patients with a mass consisting only of fibrotic and necrotic tissue have reached complete response (1–5). When there is uptake of ⁶⁷Ga after the end of treatment, outcome is poor (1–3).

In this study, we assessed the value of ⁶⁷Ga scintigraphy performed not after but rather early in treatment to predict the outcome in patients with aggressive non-Hodgkin lymphoma. This appears reasonable since ⁶⁷Ga is an in vivo indicator of tumor viability (4). If early during treatment patients with positive ⁶⁷Ga scans have a poorer prognosis than patients with negative ⁶⁷Ga scans, then the treatment in them should be changed to a potentially more effective one. We were interested if this could be achieved by restaging with ⁶⁷Ga scintigraphy at midtreatment or even after only one cycle of chemotherapy. There has been some anecdotal evidence that ⁶⁷Ga scintigraphy performed during treatment can be used to predict outcome (6).

We performed this study to evaluate the use of ⁶⁷Ga scintigraphy after one cycle of chemotherapy and at midtreatment to predict the outcome in patients with aggressive non-Hodgkin lymphoma. The prediction of outcome with CT findings at midtreatment was compared with the prediction of outcome with ⁶⁷Ga scintigraphy.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patients
One hundred eighteen patients who had gallium-avid non-Hodgkin lymphoma before treatment between 1987 and 1997 were prospectively included in the study population and underwent 148 ⁶⁷Ga scintigraphic examinations. Gallium 67 scintigraphic studies have been approved by our institution's Helsinki Committee; the details of the study were explained to the patients by the treating physicians, and the patients gave their informed consent. The number of patients who underwent ⁶⁷Ga scintigraphy after one cycle of treatment, after a median of 3.5 cycles (range, two to five cycles), or both is shown in Table 1. To evaluate the response, ⁶⁷Ga scintigraphy at the end of treatment was used, as is routine.

Patients were treated with the following chemotherapeutic combinations: Seventy-five patients received cyclophosphamide, doxorubicin hydrochloride, vincristine sulfate, and prednisone, or CHOP; 16 patients received prednisone, methotrexate, leucovorin calcium, vincristine sulfate, doxorubicin hydrochloride, cyclophosphamide, and etoposide or mechlorethamine hydrochloride, vincristine sulfate, procarbazine hydrochloride, and prednisone, or ProMACE/MOPP; five patients received CHOP and etoposide, or CHOPE; and 22 patients received other chemotherapeutic combinations.

CT was performed in 89 patients after a median of 3.5 cycles (range, two to six cycles). In two patients, CT was not performed at the time of initial diagnosis; therefore, CT results in 87 patients were included in the final analysis. Each patient underwent a complete reevaluation within 3 weeks of ⁶⁷Ga scintigraphic and CT studies. Treatment failure was diagnosed when the patient did not achieve a complete response after treatment and had tumor progression. A recurrence of disease after a continuous clinical remission, which was a minimum of 4 weeks without evidence of disease since the end of treatment, was also considered treatment failure. Failure-free survival was defined as the duration of survival without progression of disease from the start of treatment. The results of ⁶⁷Ga scintigraphy were compared with the results of CT. Treatment in none of the patients was changed on the basis of the results of ⁶⁷Ga scintigraphy or CT during treatment.

Imaging
⁶⁷Ga scintigraphic and CT images were each evaluated independently before and during treatment with a prospective, blind reading. ⁶⁷Ga scintigraphic images were interpreted by one or more of three of the authors (D.F., R.B.S., and O.I.), and CT scans were read by one author (D.G.). The original reading of the images as it appeared in the file was used to determine whether ⁶⁷Ga scintigraphic and CT findings were positive or negative during treatment. ⁶⁷Ga scintigraphic findings were evaluated as negative or positive for the presence of disease. Abnormal uptake of ⁶⁷Ga at scintigraphy in regions that normally do not take up ⁶⁷Ga was considered to indicate disease (1,2,6,8,9). Gallium 67 scintigraphy was performed as previously described (2,6). Adult patients received an intravenous injection of 8 mCi (296 MBq) of gallium 67 citrate. Children received 75 µCi (2.77 MBq) per kilogram of body weight.

Planar imaging and single photon emission CT (SPECT) were performed at 48 hours. Additional views were always obtained 7–14 days after injection, when abdominal activity interfered with the interpretation of ⁶⁷Ga scintigraphic images and when it was not clear if abnormal uptake of ⁶⁷Ga was present on the early scans. Scintigraphy was performed by using either a digital SPECT camera with a large rectangular field of view (model SP-6; Elscint, Haifa, Israel) or a dual-head digital camera (Helix or Varicam; Elscint). Triple energy peaks of ⁶⁷Ga at 93, 184, and 300 keV were used. A parallel-hole, medium-energy collimator was used with the single-head camera, and a special collimator for ⁶⁷Ga scintigraphy was used with the dual-head cameras. Planar anterior and posterior views with 500–1,000 K counts per view were obtained. Whole-body scanning with the dual-head camera was performed for 20 minutes at 48 hours after injection and for 26 minutes in the delayed studies.

SPECT was performed by using a 360° rotation with 60 projections 6° apart, which resulted in an accumulation of 3.5–8.0 x 10⁶ counts for the whole study. A matrix of 64 x 64, and a Metz filter with parameters 3 and 14 were used. Data were reconstructed by using an SP-1 or XP computer (Elscint). Tomograms were obtained in the transverse, sagittal, and coronal planes. SPECT images of the head, neck, thorax, abdomen, and pelvis were obtained in all patients at 48 hours after injection. When necessary, SPECT was performed up to 7 days after the injection. Areas of abnormal uptake of ⁶⁷Ga clearly separated from normal structures and unexplained by another cause were considered positive. Diffuse lung uptake (8), parahilar uptake (9), focal uptake in fractured ribs, and uptake in the colon were findings not considered to indicate the presence of lymphoma.

CT (Twin Flash scanner; Elscint) of the chest, abdomen, and pelvis was performed before treatment and during treatment (median, 3.5 cycles of chemotherapy; range, two to six cycles) in each of the 87 patients. Scans of the head and neck or extremities were also obtained. The section thickness for the neck was 2.5–3.0 mm; that for the chest, abdomen, and pelvis was 10.0 mm. In patients with lymphoma of the nasopharynx and oropharynx, coronal sections were added. For the chest, a separate window for lungs and mediastinum was used. Patients received 80 mL of contrast medium (iopamidol [Iopamiro; Bracco, Milan, Italy]) as a bolus. Only a normal CT finding or a decrease of 90% or more in tumor mass as compared with the pretreatment size were read as negative for the presence of disease.

Statistical Analysis
The duration of failure-free survival was calculated by using the Kaplan-Meier method. Failure-free survival was compared between negative and positive ⁶⁷Ga scintigraphic and negative and positive CT findings by using the log-rank test. The relation between failure-free survival and ⁶⁷Ga scintigraphic and CT findings was determined by using univariate analysis with the log-rank test. Patients with CT information missing from the files were excluded from the analysis. P values of less than .05 were considered to represent a statistically significant difference. Multivariate analysis was performed by using the Cox regression method to determine if ⁶⁷Ga scintigraphic findings after one cycle of treatment and at midtreatment were independently associated with failure-free survival. The same was attempted with CT findings.

	RESULTS

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Of the 118 patients included in the study, 61 (52%) had continuous clinical remission for a median ± SD of 37 months ± 28 (range, 12–123 months). Fifty-seven patients (48%) had treatment failure after a median failure-free period of 9 months ± 13 (range, 1–57 months); 30 of these patients had relapse, 22 did not achieve a complete response and had tumor progression, and five had a partial response followed by tumor progression.

Results of ⁶⁷Ga scanning and CT during treatment are summarized in Table 2. The outcomes in patients are compared with ⁶⁷Ga scintigraphic and CT findings in Table 3. There was a statistically significant difference in failure-free survival between patients with positive ⁶⁷Ga scans and patients with negative ⁶⁷Ga scans after one cycle of treatment (P < .001) and at midtreatment (P < .001). Eighty-one percent of patients with negative ⁶⁷Ga scans after one cycle of treatment and 63% of patients with negative ⁶⁷Ga scans at midtreatment remained in complete response. In patients with positive ⁶⁷Ga scans after one cycle and at midtreatment, 71% and 74%, respectively, had treatment failure.

Adding relevant CT results to ⁶⁷Ga scintigraphic results did not change the statistical significance of the difference in failure-free survival between patients with positive and patients with negative ⁶⁷Ga scintigraphic findings after one cycle or at midtreatment. The Kaplan-Meier failure-free survival curves for patients with positive findings and patients with negative findings of ⁶⁷Ga scintigraphy after one cycle of chemotherapy or at midtreatment or of CT at midtreatment are shown in the Figure.

View larger version (15K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Graphs of failure-free survival versus time in patients with non-Hodgkin lymphoma who have (a) positive or negative 67Ga scintigraphic findings after one cycle of chemotherapy, (b) positive or negative 67Ga scintigraphic findings at midtreatment, and (c) positive or negative CT findings at midtreatment. In a and b, there is a statistically significant (P < .001) difference in failure-free survival between the two groups. In c, there is no statistically significant difference (P = N.S) in failure-free survival between the two groups.

View larger version (15K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Graphs of failure-free survival versus time in patients with non-Hodgkin lymphoma who have (a) positive or negative 67Ga scintigraphic findings after one cycle of chemotherapy, (b) positive or negative 67Ga scintigraphic findings at midtreatment, and (c) positive or negative CT findings at midtreatment. In a and b, there is a statistically significant (P < .001) difference in failure-free survival between the two groups. In c, there is no statistically significant difference (P = N.S) in failure-free survival between the two groups.

View larger version (15K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Graphs of failure-free survival versus time in patients with non-Hodgkin lymphoma who have (a) positive or negative 67Ga scintigraphic findings after one cycle of chemotherapy, (b) positive or negative 67Ga scintigraphic findings at midtreatment, and (c) positive or negative CT findings at midtreatment. In a and b, there is a statistically significant (P < .001) difference in failure-free survival between the two groups. In c, there is no statistically significant difference (P = N.S) in failure-free survival between the two groups.

Two other Cox regression models were evaluated for one of the two ⁶⁷Ga scintigraphic examinations during treatment. When ⁶⁷Ga scintigraphic results after one cycle were ignored, ⁶⁷Ga scintigraphic results at midtreatment remained a significant prognostic factor (P < .006). In the other model, when the results of ⁶⁷Ga scintigraphy at midtreatment were ignored and the role of ⁶⁷Ga scintigraphy after one cycle was assessed, it was again a good prognostic determinator (P < .045).

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
About 50%–60% of the patients with aggressive non-Hodgkin lymphoma achieve prolonged survival and a cure (10,11). In our study population, 61 of the 118 patients (52%) with non-Hodgkin lymphoma did not have treatment failure for the duration of the study. Efforts are now being made to improve the outcome in patients who do not achieve a continuous clinical remission with more aggressive treatment (10–14). The earlier an ineffective treatment is stopped and a more appropriate one is instituted, the better the chances for tumor response and longer failure-free survival.

Gallium 67 scintigraphic findings are indicators of cancer cell viability (4) and have been shown to be good indicators of complete response at the end of induction chemotherapy, especially when a residual mass exists at the end of treatment (1–3,6). It has been shown in an anecdotal report on patients (6) and recently in reports on 30 patients with aggressive non-Hodgkin lymphoma and poor prognosis (15) and on 98 patients with Hodgkin disease (16) that ⁶⁷Ga scintigraphy can be used to predict the patient outcome early, before the end of treatment.

In the present study, there was a significant difference in failure-free survival in 118 patients with non-Hodgkin lymphoma between the patients with positive ⁶⁷Ga scintigraphic findings and the patients with negative ⁶⁷Ga scintigraphic findings at midtreatment and as early as the completion of one cycle of chemotherapy. This should lead to a strategy of an early change of an ineffective treatment to a more appropriate one, which will be more suitable for the tumor in the individual patient who does not show a rapid response and in whom ⁶⁷Ga scintigraphic findings remain positive. An early change in treatment, when the tumor load of nonsensitive cells is still not large, has a better chance of being effective. Effective chemotherapy delivered early could increase the number of patients who will respond completely, who will have a prolonged failure-free survival, and who will even be cured.

Response to the treatment of tumors is heterogeneous, even in patients with the same histologic findings. Gallium 67 scintigraphy can be used to monitor the response of the tumor cells in each patient to the particular combination chemotherapy received. While clinical prognostic factors (12,17) provide information on outcome, abnormal, early ⁶⁷Ga scintigraphic findings indicate that the cancer in the individual patient is not sensitive to the particular chemotherapeutic combination the patient receives at the time of the examination. Of course, it must be realized that ⁶⁷Ga scintigraphy, although showing a statistically significant difference in failure-free survival between patients with positive and patients with negative findings, does not allow one to identify all patients who will develop treatment failure. Some patients with negative ⁶⁷Ga scintigraphic studies early during treatment may still develop tumor progression or relapse. There is at present no technique that can depict small deposits of cells that can cause relapse after months or years.

Although the evaluation with ⁶⁷Ga scintigraphy is not ideal, it appears to show early the overall state of the cancer before a large load of chemotherapy-resistant cancer cells may develop at the end of protocol treatment or later. The results of the present study are complementary to those in patients with Hodgkin disease (16), in whom negative ⁶⁷Ga scintigraphic findings can be used to determine in which patients the dose of chemotherapy can potentially be reduced. Positive ⁶⁷Ga scintigraphic findings of aggressive non-Hodgkin lymphoma can be used to select patients who need a more aggressive treatment. There is now evidence that aggressive treatment can be effective sometimes. It is necessary in the future to examine if early selection with ⁶⁷Ga scintigraphy increases survival in patients whose conditions do not respond early.

Findings of the present study further show that CT findings are not good indicators of early tumor response (1,5). Evaluation of response with CT is based on the change in tumor size. Using CT findings as a criterion for early response results in inclusion of an unacceptable number of patients with a residual mass who therefore are expected to have a poor outcome and who need a change in treatment but who actually achieve complete response. The change in the size of a mass does not necessarily indicate nonresponse to treatment. Tumor size at each point in time during treatment is the result of the equilibrium between the clearing of necrotic and fibrotic tissue from the tumor after the death of sensitive cancer cells because of treatment and the growth of resistant cells. CT does not necessarily show a return to normal size in patients with complete response. ⁶⁷Ga scintigraphy shows only viable tumor cells and therefore indicates the state of viable cancer in the tumor mass (1,4).

Findings of a number of previous studies (1,2,6,14) have shown that CT cannot be used to predict outcome after treatment in patients with high-grade aggressive non-Hodgkin lymphoma. Adding relevant CT data to ⁶⁷Ga scintigraphic data does not change the results. This is similar to the results of Vose et al (14) in patients undergoing high-dose chemotherapy and autologous stem-cell transplantation, where CT was not useful.

It is concluded that ⁶⁷Ga scintigraphy may be used early during treatment in patients with aggressive non-Hodgkin lymphoma to predict outcome. In the future, ⁶⁷Ga scintigraphy should be tested to determine the need to change to a more suitable treatment at an early stage. It remains now to be seen if an early change in treatment in patients with positive ⁶⁷Ga scintigraphic findings after one cycle and during treatment will indeed improve the outcome. A prospective two-arm study is now necessary to compare failure-free survival in patients with positive ⁶⁷Ga scintigraphic findings during treatment who will continue to receive conventional treatment and failure-free survival in patients with positive findings in whom treatment will be changed to a more aggressive and potentially more effective one.

	Footnotes

 
Author contributions: Guarantor of integrity of entire study, D.F.; study concepts, D.F., R.B.S., O.I., N.H., R.E.; study design, D.F., R.B.S., O.I.; definition of intellectual content, D.F., R.B.S., N.H., R.E., G.M.K., O.I.; literature research, R.B.S., M.M.; clinical studies, R.B.S., M.M., D.G.; data acquisition, M.M., R.B.S.; data analysis, D.F., R.B.S., M.M., O.I.; statistical analysis, R.B.S., A.F.; manuscript preparation, D.F., R.B.S., N.H., R.E., G.M.K., O.I.; manuscript editing, D.F., O.I.; manuscript review, D.F., R.B.S., N.H., R.E., D.G., G.M.K., O.I.

	References

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Front, D. Articles by Israel, O. Search for Related Content PubMed PubMed Citation Articles by Front, D. Articles by Israel, O.