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Hodgkin Disease: Prediction of Outcome with ⁶⁷Ga Scintigraphy after One Cycle of Chemotherapy

¹ Departments of Nuclear Medicine (D.F., R.B.S., M.M., A.F., G.M.K., O.I.)
² Oncology (N.H., R.E.)
³ Radiology (D.G.), Rambam Medical Center and the Faculty of Medicine, Technion-Israel Institute of Technology, Haifa 35254, Israel.

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To investigate gallium 67 scintigraphy performed early during treatment as a means to predict outcome and thus to optimize treatment of Hodgkin disease (HD) in the future.

MATERIALS AND METHODS: Ninety-eight patients with HD were examined. Thirty-one patients underwent ⁶⁷Ga scintigraphy after one chemotherapy cycle and 83 patients after a mean 3.5 cycles (range, 2–5 cycles). Sixteen patients underwent ⁶⁷Ga scintigraphy both after one cycle and at midtreatment. Patients underwent whole-body scintigraphy and single photon emission computed tomography of the torso. Torso computed tomography (CT) was performed after a mean 3.5 cycles (range, 2–6 cycles). Failure-free survival was compared between patients with positive and patients with negative test findings (Kaplan-Meier method), and the significance of the difference was calculated. The association of failure-free survival with various prognostic clinical factors before treatment was compared (log-rank test univariate analysis).

RESULTS: Failure-free survival differed significantly (P < .002) between patients with positive and patients with negative ⁶⁷Ga scintigrams after one chemotherapy cycle but not at midtreatment. Failure-free survival was not significantly different between patients with positive and patients with negative CT scans at midtreatment. Twenty-two (92%) of 24 patients with negative ⁶⁷Ga scintigrams after one cycle and 64 (82%) of 78 patients with negative scintigrams at midtreatment remained in complete response. In four (57%) of seven patients with positive ⁶⁷Ga scintigrams after one cycle, treatment failed.

CONCLUSION: ⁶⁷Ga scintigraphy after one cycle of chemotherapy is a good early predictor of outcome of HD.

Index terms: Emission CT (ECT), 99.12962, 99.8342 • Gallium, radioactive, 99.12962, 99.12966, 99.12974, 99.8342 • Hodgkin disease, 99.8342 • Lymphatic system, neoplasms, 99.8342 • Lymphoma, radionuclide studies, 99.12966, 99.12974, 99.8342

	Introduction

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Even when chemotherapy for patients with Hodgkin disease (HD) is effective in inducing a complete response, prolonged survival, and cure, 20%–30% of the patients die of the disease; that is, they develop tumor progression or recurrence and eventually die (1). Early prediction of treatment failure and change of treatment could improve the prognosis for patients with HD who have a poor outcome. Gallium 67 scintigraphy has been considered a good technique for monitoring response after treatment of patients with lymphoma (2–7). Investigators recently reported, however, that in 101 patients with HD (8), the negative predictive value of ⁶⁷Ga scintigraphy at the end of treatment was not good enough; and ⁶⁷Ga scintigraphy after treatment, particularly in patients with stage III and IV disease, could not be used to predict which patients would develop a relapse. Those investigators (8) concluded that a negative ⁶⁷Ga scintigram after treatment has a low predictive value.

In the study presented here, we examined whether the assessment of patients with HD with ⁶⁷Ga scintigraphy at an earlier point during treatment than that routinely used (2–7) may help in separating patients in whom treatment will fail from those in whom it will not. This systematic attempt to evaluate the outcome of therapy before the end of treatment is based on preliminary anecdotal observations in three patients in whom ⁶⁷Ga scintigraphic results during treatment correlated with the outcome (9). Preliminary results indicated that outcome could be predicted with ⁶⁷Ga scintigraphy, and these results encouraged us to test ⁶⁷Ga scintigraphy after one cycle of chemotherapy. The results of early ⁶⁷Ga scintigraphy for predicting outcome were compared with those of computed tomography (CT) and with the clinical prognostic factors used before treatment.

The purpose of this study was to investigate ⁶⁷Ga scintigraphy performed early during treatment as a means to predict outcome and thus to optimize treatment of HD in the future.

	MATERIALS AND METHODS

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One hundred thirty-eight patients with histologically confirmed HD were enrolled in the study between 1986 and 1995. Ninety-eight consecutive patients with ⁶⁷Ga-avid lymphoma whose files contained the necessary information were included in the study. The study was approved by the Institutional Review Board for Studies in Humans (Helsinki Committee), and informed consent was obtained from each patient. Patients were excluded from the study because of the absence of clinical or diagnostic information, because they did not follow the protocol, or because they were lost to follow-up.

Of the 98 patients included in the study, 31 patients underwent ⁶⁷Ga scintigraphy after one cycle of chemotherapy, and 83 patients underwent ⁶⁷Ga scintigraphy after a mean of 3.5 cycles (range, 2–5 cycles). Sixteen patients underwent ⁶⁷Ga scintigraphy both after one cycle of chemotherapy and at midtreatment (Table 1). One hundred fourteen ⁶⁷Ga studies were performed in 50 male patients and 48 female patients with a median age of 27 years (range, 5–76 years). Thirty-three patients were younger than 20 years old. Eight of them underwent ⁶⁷Ga scintigraphy after one cycle of treatment and 25 at midtreatment.

Twenty-one patients were treated with MOPP-ABVD (mechlorethamine hydrochloride, Oncovin [vincristine sulfate; Eli Lilly, Indianapolis, Ind], procarbazine hydrochloride, and prednisone; Adriamycin [doxorubicin hydrochloride; Pharmacia & Upjohn, Kalamazoo, Mich], bleomycin sulfate, vinblastine sulfate, and dacarbazine), 59 with MOPP-ABV (Adriamycin [doxorubicin hydrochloride; Pharmacia & Upjohn], bleomycin sulfate, and vinblastine sulfate), six with ABVD, five with MOPP, and seven with other chemotherapeutic combinations.

Imaging
Before treatment, ⁶⁷Ga scintigraphy in all patients had yielded a positive baseline ⁶⁷Ga study that demonstrated sites of ⁶⁷Ga-avid lymphoma. The original reading of the scintigram as it appears in the patient's file was used to determine whether ⁶⁷Ga scintigrams were positive or negative during treatment.

The ⁶⁷Ga study was considered positive for the presence of disease when uptake of ⁶⁷Ga persisted in a site of disease that was known before treatment; the study was considered positive even when there was some decrease in the intensity of uptake. Any new abnormal uptake of ⁶⁷Ga clearly separated from normal structures and unexplained by other causes was considered positive. Vague nonfocal uptake was not considered to indicate the presence of cancer, and the study was read as negative. Diffuse lung uptake (10), parahilar uptake (11), focal uptake in fractured ribs, and uptake in the colon were not considered to indicate the presence of lymphoma.

⁶⁷Ga scintigrams and CT scans were each evaluated independently by the same physicians. The ⁶⁷Ga scintigram was read by one or more of the authors (D.F., R.B.S., O.I.), and the CT scan was read by another author (D.G.).

⁶⁷Ga scintigraphy was performed as previously described (2–4,9,10). Adult patients received 8 mCi (296 MBq) of ⁶⁷Ga 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 obtained 7–14 days after injection when abdominal activity interfered with the interpretation of ⁶⁷Ga scintigraphy or when it was not clear that uptake of ⁶⁷Ga was really present in the early study.

Scintigraphy was performed either with a single-head digital SPECT camera with a large rectangular field of view (SP-6; Elscint, Haifa, Israel) or with a dual-head digital camera (Helix or Varicam; Elscint). Three energy peaks of ⁶⁷Ga at 93, 184, and 300 keV were used. A parallel-hole medium-energy collimator was used with the camera with the very large rectangular field of view, and a special collimator for ⁶⁷Ga (HPC-5; Elscint) was used with the dual-head cameras. Planar anterior and posterior views were obtained with 0.5–1.0 x 10⁶ counts per view. Whole-body scanning with the dual-head camera was performed for 20 minutes at 48 hours after injection and for 26 minutes for the delayed studies.

SPECT scans of the head, neck, thorax, abdomen, and pelvis were obtained in all patients at 48 hours after injection. SPECT was performed with a 360° rotation, 60 projections 6° apart, accumulating 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 with SP-1 or XP computers (Elscint). Tomograms were obtained in the transaxial, sagittal, and coronal planes.

Chemotherapy may suppress uptake of ⁶⁷Ga by tumors of active lymphoma for a few days after administration. ⁶⁷Ga was therefore injected 2 weeks after the end of the cycle of chemotherapy. At this time, chemotherapy does not affect ⁶⁷Ga uptake (9,12).

Eighty-six patients underwent CT after a mean of 3.5 cycles of treatment (range, 2–6 cycles). For each patient, a CT scan of the chest, abdomen, and pelvis was obtained. When necessary, scans of the head and neck and of the extremities were obtained. The section thickness for the neck was 2.5–3.0 mm and 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 was used for the lungs and mediastinum. Patients received 80 mL of the contrast medium, iopamidol (Iopamiro; Bracco, Milan, Italy), as a bolus intravenous injection. A test that did not show any mass in the place of a previous tumor or a test that showed a decrease of 90% or more in tumor mass compared with pretreatment size was read as negative for the presence of disease at CT; otherwise the test results were considered abnormal.

Statistical Analysis
Treatment failure was considered to occur (a) when the patient did not achieve a complete response after treatment and developed tumor progression or (b) when a recurrence of disease was seen after complete response. Failure-free survival was defined as the duration of survival without progression of disease from the start of treatment.

The statistical significance of the duration of failure-free survival was calculated with the Kaplan-Meier method. A P value of less than .05 was considered to represent a statistically significant difference. Failure-free survival was compared for patients with negative and patients with positive ⁶⁷Ga scintigrams and CT scans. The log-rank test was used to evaluate with univariate analysis the association between failure-free survival and the clinical factors considered to be prognostic (13–15).

When information about prognostic factors was missing in a patient, that patient was excluded from the analysis of that factor. ⁶⁷Ga scintigraphic results after one cycle and at midtreatment and the age, performance status, stage, bulk, B-symptoms, lactic hydrogenase level, and CT scan at midtreatment were evaluated for association with failure-free survival (13–15).

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
The results of ⁶⁷Ga scintigraphy and CT during treatment are shown in Table 2. Failure-free survival was significantly different between patients with HD who had positive and those who had negative ⁶⁷Ga scintigrams after one cycle of treatment (P < .002) (Fig 1). No significant difference in failure-free survival was seen between patients with positive and patients with negative ⁶⁷Ga scintigrams at midtreatment (Fig 2).

View larger version (12K): [in this window] [in a new window]   Figure 1. Failure-free survival curves of patients with HD who had positive and those who had negative 67Ga scintigrams after one cycle of chemotherapy.

View larger version (14K): [in this window] [in a new window]   Figure 2. Failure-free survival curves of patients with HD who had positive and those who had negative 67Ga scintigrams at midtreatment (difference between groups is not significant [NS]).

With univariate analysis, none of the clinical risk factors—age, stage, performance status, bulk, B-symptoms, and lactic dehydrogenase level—were significantly associated with failure-free survival. Failure-free survival was not significantly different between patients with positive and patients with negative CT scans at midtreatment (Fig 3). In nine (20%) of 44 patients with HD and with a positive CT scan during treatment, treatment failed; and of 42 patients with negative CT scans, 34 (81%) remained in complete response. Adding relevant CT results to ⁶⁷Ga scintigraphic results did not change the statistical significance of the difference between patients with positive and patients with negative ⁶⁷Ga scintigrams after one cycle or at midtreatment.

View larger version (14K): [in this window] [in a new window]   Figure 3. Failure-free survival curves of patients with HD who had positive and those who had negative CT scans at midtreatment (difference between groups is not significant [NS]).

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

Failure-free survival was significantly different (P < .002) between patients with HD who had positive and those who had negative ⁶⁷Ga scintigrams after one cycle of treatment. Twenty-two (92%) of 24 patients who had negative ⁶⁷Ga scintigrams after one cycle remained in complete response, and in four (57%) of seven with positive ⁶⁷Ga scintigrams, treatment failed (Table 3). The results at midtreatment were not as good. These data show that ⁶⁷Ga scintigraphy in patients with HD should optimally be performed after one cycle of treatment. The ability to predict the outcome in patients early during treatment, as compared with later ⁶⁷Ga studies, may be due to the high sensitivity of HD to chemotherapy.

After only one cycle, patients with a good outcome have negative ⁶⁷Ga scintigrams. Patients who respond later and still have positive scintigrams have a higher chance for treatment failure. That the chance to achieve a complete response and long survival is higher in those who respond rapidly has been shown in patients with aggressive non-Hodgkin lymphoma (16,17). For patients with HD, ⁶⁷Ga scintigraphy after one cycle appears to be a good technique to separate those who respond rapidly from those who respond slowly. At midtreatment, however, only small amounts of the nonsensitive cells remain in the tumors of patients who experience a relapse, and these amounts cannot be detected with ⁶⁷Ga scintigraphy.

Therefore, ⁶⁷Ga scintigraphy after completion of chemotherapy or even at midtreatment may not always be sensitive enough to be used to predict the outcome for patients with HD. Negative ⁶⁷Ga scintigrams after one cycle of treatment appear to indicate patients with HD who will respond to treatment and to separate them from those in whom treatment will fail and who will therefore need to change therapy.

The ability to use ⁶⁷Ga scintigraphy to separate patients with good and poor outcomes at an early stage of treatment may be useful particularly in the pediatric age group, in which chemotherapy can cause long-term damage. The dose of chemotherapy could be reduced for children in whom a good outcome could be expected on the basis of ⁶⁷Ga scintigraphic findings (18,19). In the present study, however, only eight young patients underwent ⁶⁷Ga scintigraphy after one cycle.

The value of scintigraphy for assessing tumor response to therapy has been described in detail (2–5,9). No technique, however, can determine whether disease has been completely eradicated for lymphoma or for other tumors. With the present state of technology, it is impossible to detect the existence of a small cluster of cancer cells remaining after treatment that will cause a recurrence of disease in the future. The number of cells necessary to cause a relapse is unknown but is probably small because sometimes it may take months or years to develop masses large enough to manifest a detectable relapse. The present results, however, indicate that early ⁶⁷Ga scintigraphy may help to detect cancer cells that can later cause treatment failure. In the future, patients with negative ⁶⁷Ga scintigrams after one cycle of treatment may be selected for reduction of the dose of chemotherapy without affecting survival.

The present results also show that CT during treatment is not a good technique to determine tumor response to treatment. This is, of course, reasonable because CT shows a residual mass even at the end of treatment, which does not necessarily indicate the presence of cancer (2–7). While such patients with a residual fibrotic and necrotic mass at the end of treatment may achieve a prolonged complete response, they are even more likely to have an abnormal CT scan early in treatment and still have a good outcome. The determination of tumor response with CT is based on the change in size of the tumor. At each point during treatment, tumor size is the result of the equilibrium between (a) the clearing of necrotic and fibrotic tissue from the tumor after the death of sensitive cells due to treatment and (b) the growth of resistant cells. CT does not necessarily show the decrease of viable cancer cells in patients with lymphoma (3,9,12).

In conclusion, the data of this study show that performing ⁶⁷Ga scintigraphy after one cycle of chemotherapy is a good technique to separate patients with HD in whom treatment will not fail from those in whom it will. ⁶⁷Ga scintigraphy has the potential to be used to identify patients who may benefit from an early change in treatment before a nontreatable increase of the cancer cells occurs.

	Footnotes

 
Address reprint requests to D.F.

Abbreviations: ABV = Adriamycin (doxorubicin hydrochloride), bleomycin sulfate, and vinblastine sulfate ABVD = Adriamycin (doxorubicin hydrochloride), bleomycin sulfate, vinblastine sulfate, and dacarbazine HD = Hodgkin disease MOPP = mechlorethamine hydrochloride, Oncovin (vincristine sulfate), procarbazine hydrochloride, and prednisone

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

Received January 23, 1998; revision requested April 6, 1998; revision received May 6, 1998; accepted September 23, 1998.

	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.