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Salvage Cryotherapy for Recurrent Prostate Cancer After Radiotherapy: Variables Affecting Patient Outcome

From the Department of Urology, University of Texas M.D. Anderson Cancer Center, Houston, TX.

Address reprint requests to Louis L. Pisters, MD, Department of Urology, University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Box 446, Houston, TX 77030; email: lpisters{at}mail.mdanderson.org

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To determine the long-term disease-specific survival (DSS) and disease-free survival (DFS) rates after salvage cryotherapy for locally recurrent adenocarcinoma of the prostate and to identify pretreatment factors that have an impact on DSS and DFS.

PATIENTS AND METHODS: Between July 1992 and January 1995, 131 patients who had received definitive radiation therapy (XRT) underwent salvage cryotherapy for locally recurrent adenocarcinoma of the prostate. Cryotherapy failure was defined as an increasing postcryotherapy prostate-specific antigen (PSA) level of 2 ng/mL above the postcryotherapy nadir, a positive prostate biopsy, or radiographic evidence of metastatic disease. Clinical variables were studied to determine whether there was an association with the DSS and DFS.

RESULTS: The median follow-up was 4.8 years. The 5-year DSS rates were 87% for patients with a precryotherapy Gleason score 8 and 63% for those with Gleason scores of 9 and 10 (P = .012). The 5-year DFS rates were 57% for patients with a precryotherapy PSA level of 10 ng/mL and 23% for those with a PSA level greater than 10 ng/mL (P = .0004). The 5-year DSS rates for patients with a pre-XRT clinical stage of T1 to T2 and those with a clinical stage of T3 to T4 were 94% and 72%, respectively (P = .0041). The 5-year DFS rates for these groups were 90% and 69%, respectively (P = .0057).

CONCLUSION: Androgen-independent local recurrences, Gleason score, and pre-XRT clinical stage were important factors that had an impact on DSS and DFS. The subset of patients cured by salvage cryotherapy seems to be small, and patient selection is important.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
THE INCIDENCE OF locally recurrent adenocarcinoma of the prostate (PCa) after definitive radiation therapy (XRT) is significant; rates of locally recurrent PCa as determined by post-XRT biopsies have ranged from 25% to 93%.^1-4 A rising prostate-specific antigen (PSA) level after initial XRT precedes clinically detectable recurrent disease by 3 to 5 years.^5,6 In the absence of salvage therapy, at least 75% of patients will have clinical evidence of recurrent disease 5 years after a PSA elevation is detected.⁶ Furthermore, locally recurrent PCa can lead to significant morbidity, metastasis, and death.^7-10 There is no one therapy that is clearly superior in the management of locally recurrent PCa after definitive XRT.

Therapeutic options with curative intent are limited and include salvage cryotherapy,^11-15 salvage radical prostatectomy,^16-19 and salvage brachytherapy.^20-22 Age and medical comorbidities are crucial factors in determining which candidates may benefit most from these salvage procedures; generally, they have been reserved for patients with a life expectancy of at least 10 years. Hormonal therapy is another treatment option, although it is not given with curative intent.^23,24 All these therapies are associated with significant morbidity.

Because of the heterogeneous biology of PCa, only long-term clinical studies will enable us to assess whether cure can be achieved with salvage therapies. In addition, such studies will enable us to determine the clinical variables that predict long-term disease-specific survival (DSS) and disease-free survival (DFS). This knowledge will facilitate patient selection for therapies and counseling about therapeutic options. Currently, there are no long-term follow-up studies of patients who have received salvage cryotherapy for locally recurrent PCa after XRT. The purposes of this retrospective study were to determine the long-term DSS and DFS rates after salvage cryotherapy and to identify precryotherapy variables impacting outcomes.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patient Selection and Follow-Up
The patient selection and follow-up procedures have been described previously in a report with short-term follow-up.¹¹ This study evaluates the long-term outcome for these same patients. In brief, between July 1992 and January 1995, 150 patients underwent salvage cryotherapy on an institutional review board–approved protocol. Written informed consent was obtained from all patients. One hundred forty-five of the patients had received definitive XRT for their primary tumor and underwent salvage cryotherapy for biopsy-proven locally recurrent PCa without clinical evidence of metastatic disease. Staging investigations included computed tomography of the abdomen and pelvis and radionuclide bone scan. One hundred eight patients had received XRT only, and 37 patients had received various combinations of XRT, hormonal therapy (HT), and systemic chemotherapy before salvage cryotherapy. No patients were given short-term HT to improve the results of the salvage cryotherapy. Patients who received HT had evidence of clinically locally recurrent androgen-independent PCa in the form of increasing PSA level or progression of the recurrent tumor as determined by digital rectal examination. There were no exclusion criteria related to local extent of disease, PSA level, or Gleason score, provided there was a reasonable expectation that the local tumor burden could be encompassed in the freezing process. To limit our analysis to those patients treated with prior XRT or HT and XRT, we excluded 14 patients treated with prior chemotherapy along with other treatments, leaving 131 assessable patients. None of the 131 patients in this series had known metastatic disease before XRT or at the time of salvage therapy. PSA levels before XRT were not available.

Postcryotherapy follow-up consisted of a history, physical examination with digital rectal examination, and PSA determination every 3 months. Computed tomography and bone scans were obtained at the discretion of the physician who assessed the patient during follow-up. Telephone calls to patients or their local physicians were conducted to maximize and confirm our follow-up data on PSA, bone scans, and computed tomography scans for patients who received their follow-up medical care at other institutions. A PSA level of less than 0.1 ng/mL was considered undetectable (< 0.3 ng/mL early in the series). An increase in PSA of 2 ng/mL above the nadir value was considered a treatment failure. One hundred ten patients underwent transrectal ultrasound-guided standardized sextant biopsies of the prostate 6 months after salvage cryotherapy or earlier if they had increasing PSA levels. A biopsy was considered positive and indicative of a treatment failure if any cancer cells were identified in any of the cores. Any postcryotherapy computed tomography scans or bone scans demonstrating radiologic evidence of metastatic disease were considered evidence of treatment failure.

Cryotherapy Procedure
The cryotherapy equipment and technique have been previously described.¹¹ The number of cryoprobes varied depending on the estimated volume of the prostate gland. A commercially manufactured urethral warming catheter was used in most cryotherapy procedures. One or two freeze-thaw cycles were performed.

Statistical Analysis
The DSS and DFS were analyzed using Kaplan-Meier actuarial methodology. The DSS and DFS were calculated for the entire group and for patients stratified by precryotherapy PSA, Gleason score of the pre-XRT and recurrent tumor, pre-XRT clinical stage, and type of initial therapy to determine any associations between the variables studied and the outcome. The log-rank test was used to evaluate the significance of differences between the actuarial curves. A value of P < .05 was considered statistically significant.

	RESULTS

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Salvage Cryotherapy Treatment Failures
There were 125 patients for whom pre-XRT clinical stage data were available. There were 70 patients for whom pre-XRT Gleason score data were available. The median follow-up for the 131 patients was 4.8 years (range, 1.5 to 6.3 years). Information on the Gleason score and PSA of the recurrent tumor before cryotherapy was available for 125 patients. Information on the clinical stage of recurrence before cryotherapy was available for 131 patients. One hundred eight and 23 patients received XRT or XRT and HT, respectively, before salvage cryotherapy. Table 1 summarizes the pretreatment clinical factors in these patients. The most common manifestation of a cryotherapy failure was a rising PSA level, which occurred in 82 (63%) of 131 patients (Table 2).

View larger version (10K): [in this window] [in a new window]   Fig 1. Overall survival for all 131 patients.

View larger version (11K): [in this window] [in a new window]   Fig 2. Overall DSS for all 131 patients.

View larger version (11K): [in this window] [in a new window]   Fig 3. Overall DFS for all 131 patients.

View larger version (13K): [in this window] [in a new window]   Fig 4. DSS for all 131 patients stratified by presalvage cryotherapy treatments with definitive XRT or a combination of XRT and HT.

View larger version (14K): [in this window] [in a new window]   Fig 5. DFS for all 131 patients stratified by presalvage cryotherapy treatments with definitive XRT or a combination of XRT and HT.

View larger version (15K): [in this window] [in a new window]   Fig 6. DSS for all 95 patients with a presalvage cryotherapy PSA level of 10 ng/mL stratified by presalvage cryotherapy treatment with definitive XRT (n = 76) or a combination of XRT and HT (n = 19).

View larger version (16K): [in this window] [in a new window]   Fig 7. DFS for all 95 patients with a presalvage cryotherapy PSA level of 10 ng/mL stratified by presalvage cryotherapy treatment with definitive XRT (n = 76) or a combination of XRT and HT (n = 19).

View larger version (14K): [in this window] [in a new window]   Fig 8. DSS for all 125 patients stratified by presalvage cryotherapy PSA 10 ng/mL (n = 95) or greater than 10 ng/mL (n = 30).

View larger version (15K): [in this window] [in a new window]   Fig 9. DFS for all 125 patients stratified by presalvage cryotherapy PSA level of 10 ng/mL (n = 95) or greater than 10 ng/mL (n = 30).

View larger version (15K): [in this window] [in a new window]   Fig 10. DSS for all 125 patients with assessable Gleason scores in the recurrent tumor before salvage cryotherapy stratified by Gleason scores of less than 9 (n = 95) or 9 and 10 (n = 30).

View larger version (16K): [in this window] [in a new window]   Fig 11. DFS for all 125 patients with assessable Gleason scores in the recurrent tumor before salvage cryotherapy stratified by Gleason scores of less than 9 (n = 95) or 9 and 10 (n = 30).

View larger version (16K): [in this window] [in a new window]   Fig 12. DSS for all 125 patients with assessable pre-XRT clinical staging in the pre-XRT tumor stratified by clinical stage T1 to T2 (n = 50) or T3 to T4 (n = 75).

View larger version (13K): [in this window] [in a new window]   Fig 14. DSS for all 92 patients with assessable pre-XRT Gleason scores in the pre-XRT tumor stratified by Gleason scores of less than 7 (n = 47) or 7 to 10 (n = 23).

View larger version (16K): [in this window] [in a new window]   Fig 13. DFS for all 125 patients with assessable pre-XRT clinical staging in the pre-XRT tumor stratified by clinical stage T1 to T2 (n = 50) or T3 to T4 (n = 75).

View larger version (13K): [in this window] [in a new window]   Fig 15. DSS for all 92 patients with assessable pre-XRT Gleason scores in the pre-XRT tumor stratified by Gleason scores of less than 7 (n = 47) or 7 to 10 (n = 23).

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

One important finding in our study was the significant differences in DSS and DFS after local recurrence of androgen-dependent versus androgen-independent tumors. Men with locally recurrent PCa after XRT and HT had lower DSS and DFS rates after salvage cryotherapy. The local PCa recurrences that occurred in patients after XRT and HT suggest that the clonal population of PCa cells in these recurrences was androgen-independent. The prognostic importance of androgen independence in a locally recurrent PCa has not been previously reported. Since androgen independence of the recurrent tumors had a significant impact on the DSS and DFS of patients receiving salvage cryotherapy, this factor should be considered in determining therapeutic options. Androgen independence denotes a significantly worse prognosis after salvage cryotherapy.

Precryotherapy PSA did not impact DSS but did impact DFS. PSA levels may not have been associated with DSS for two reasons. First, the follow-up, although long, may not have been long enough; with further follow-up, more patients with higher precryotherapy PSA values might have died of PCa. Second, many patients with androgen-independent locally recurrent PCa eventually died of disease despite having a low PSA level at the time of recurrence. PSA levels were associated with DFS in an expected manner. Patients with a precryotherapy PSA value greater than 10 ng/mL were more likely to have cryotherapy failure. This is consistent with biochemical failure patterns after primary radical prostatectomy and XRT.

Another factor affecting DSS was the Gleason score of the recurrent tumor. Although the pathologists had difficulty in grading all irradiated biopsy specimens, the identification of high-grade PCa was not visually difficult. The DSS was significantly improved for patients who had a Gleason score of less than 9. This finding is consistent with tumor grade being a significant prognostic factor after definitive primary therapies for PCa.^28,29 However, the Gleason score did not significantly impact on the 5-year DFS. This observation may have been caused by the lower-grade tumors failing later than the high-grade tumors, which seemed to have an early failure rate as indicated by the early decline in the Kaplan-Meier curve for patients with Gleason 9 and 10 PCa (Fig 11).

Of the clinical parameters available before XRT, only clinical stage predicted survival by having a significant impact on the DSS and DFS. It would seem that local control continues to be a problem and affects survival with salvage cryotherapy in tumors that were locally advanced at the outset of the initial XRT. The pre-XRT Gleason scores did not have a significant impact on the DSS or DFS after salvage cryotherapy. Gleason score is usually a potent predictor of survival. Our observations may be explained by the fact that the patients in this series had their initial prostate biopsy specimens evaluated by various pathologists in the United States and there was no central pathologic review. A significant number of these specimens may have been undergraded. In contrast, the grade of the recurrent tumors were determined by M.D. Anderson pathologists, and this likely resulted in more consistent evaluations. Initial pre-XRT tumor grade for many patients was not available for review; therefore, sample size is likely also a factor affecting the lack of impact the pre-XRT Gleason score had on survival.

The DFS rates observed in this long-term study characterize the postcryotherapy natural history of clinically locally recurrent PCa after XRT. Patients may live many years with evidence of persistent locally recurrent or newly diagnosed metastatic disease as determined by PSA, prostate biopsy, or radiographic studies. It is noteworthy that the definitions of treatment failure in this study had an impact on the time of diagnosing clinical failure. The rapid declines in the Kaplan-Meier curves for DFS are likely related to the sextant biopsy specimens obtained at 6 months; when positive, they were considered evidence of treatment failure.

Contemporary studies of salvage cryotherapy with similar patient selection and with short follow-up have reported 2-year biochemical recurrence-free survival of 74%.³⁰ Our data would suggest that the biochemical recurrence-free survival rate will decline with longer follow-up, as our 5-year DFS was 40%. Contemporary series also report lower complication rates, such as urinary incontinence rates of 6.7% to 7.9%.^30,31 However, the morbidity from salvage cryotherapy can be significant, with prior studies demonstrating urinary incontinence rates of 73%, erectile dysfunction rates of 72%, and more severe complications requiring major operative intervention.^11,32 Although less frequent with improvements in technique, serious complications of salvage cryotherapy still occur, and the procedure should be offered to those patients most likely to benefit. To attempt to determine selection criteria, a contemporary study with short-term follow-up has identified factors that seem to predict a worse outcome with salvage cryotherapy.³¹ These factors included PSA greater than 10 ng/mL before cryotherapy, Gleason score 8 to 10 before XRT, clinical stage T3 or T4 disease, and patients with increasing PSA despite HT.³¹

We believe that cryotherapy is not an optimal therapeutic option for all patients with locally recurrent PCa after XRT. On the basis of our current study, salvage cryotherapy is more likely to fail in patients who have locally recurrent androgen-independent PCa, a PSA level of greater than 10 ng/mL, a Gleason score of 9 and 10 for the recurrent PCa, or a pre-XRT clinical stage greater than T2. What is not known is whether these patients would receive a significantly greater benefit from another therapy with curative intent, namely, salvage prostatectomy, or other noncurative approaches such as early or late androgen-deprivation therapy. Patients who demonstrated better survival are those who had locally recurrent androgen-dependent disease, a PSA level of less than 10 ng/mL, Gleason scores of less than 9, and pre-XRT clinical stages of T1 to T2, and these patients may be optimal candidates for salvage cryotherapy.

In conclusion, not all locally recurrent PCas have the same natural history. There are differences in the tumor biology and life expectancy for patients with local failures after XRT for PCa. Disease-specific death rates are higher for patients with locally recurrent androgen-independent tumors, those who have a Gleason score of 9 or 10 in the local recurrence, or those with a pre-XRT clinical stage of T3 to T4. The subset of patients cured by salvage cryotherapy seems small, and therefore patient selection is important.

	ACKNOWLEDGMENTS

 
Supported in part by the R. Samuel McLaughlin Foundation Fellowship (to J.I.I.) and Core grant no. CA16672 from the National Cancer Institute.

	REFERENCES

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Submitted June 15, 2001; accepted March 12, 2002.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Izawa, J. I. Articles by Pisters, L. L. Search for Related Content PubMed PubMed Citation Articles by Izawa, J. I. Articles by Pisters, L. L. Social Bookmarking                            What's this?