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Originally published as JCO Early Release 10.1200/JCO.2011.35.0991 on October 24 2011

Journal of Clinical Oncology, Vol 29, No 34 (December 1), 2011: pp. 4510-4515
© 2011 American Society of Clinical Oncology.

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Urologic Oncology

Prostate Brachytherapy and Second Primary Cancer Risk: A Competitive Risk Analysis

Karel A. Hinnen, Michael Schaapveld, Marco van Vulpen, Jan. J. Battermann, Henk van der Poel, Inge M. van Oort, Joep G.H. van Roermund, Evelyn M. Monninkhof

Karel A. Hinnen, Michael Schaapveld, and Henk van der Poel, Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Amsterdam; Marco van Vulpen, Jan. J. Battermann, and Evelyn M. Monninkhof, University Medical Center Utrecht, Utrecht; Inge M. van Oort, Radboud University Nijmegen Medical Center, Nijmegen; and Joep G.H. van Roermund, Catharina Ziekenhuis, Eindhoven, the Netherlands.

Corresponding author: Karel A. Hinnen, Department of Radiation Oncology, Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital, Plesmanlaan 121, 1066 CX Amsterdam, the Netherlands; e-mail: k.hinnen{at}nki.nl.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Purpose To assess the risk of second primary cancer (SPC) after [125I]iodine prostate cancer brachytherapy compared with prostatectomy and the general population.

Patients and Methods In a cohort consisting of 1,888 patients with prostate cancer who received monotherapy with brachytherapy (n = 1,187; 63%) or prostatectomy (n = 701; 37%), SPC incidences were retrieved by linkage with the Dutch Cancer Registry. Standardized incidence rates (SIRs) and absolute excess risks (AERs) were calculated for comparison.

Results A total of 223 patients were diagnosed with SPC, 136 (11%) after brachytherapy and 87 (12%) after prostatectomy, with a median follow-up of 7.5 years. The SIR for all malignancies, bladder cancer, and rectal cancer were 0.94 (95% CI, 0.78 to 1.12), 1.69 (95% CI, 0.98 to 2.70), and 0.90 (95% CI, 0.41 to 1.72) for brachytherapy and 1.04 (95% CI, 0.83 to 2.28), 1.82 (95% CI, 0.87 to 3.35), and 1.50 (95% CI, 0.68 to 2.85) for prostatectomy, respectively. Bladder SPC risk was significantly increased after brachytherapy for patients age 60 years or younger (SIR, 5.84; 95% CI, 2.14 to 12.71; AER, 24.03) and in the first 4 years of follow-up (SIR, 2.14; 95% CI, 1.03 to 3.94; AER, 12.24). Adjusted for age, the hazard ratio (brachytherapy v prostatectomy) for all SPCs combined was 0.87 (95% CI, 0.64 to 1.18).

Conclusion Overall, we found no difference in SPC incidence between patients with prostate cancer treated with prostatectomy or brachytherapy. Furthermore, no increased tumor incidence was found compared with the general population. We observed a higher than expected incidence of bladder SPC after brachytherapy in the first 4 years of follow-up, probably resulting from lead time or screening bias. Because of power limitations, a small increased SPC risk cannot be formally excluded.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
In recent years, [125I]iodine implantation monotherapy for prostate cancer has become one of the main treatment modalities for low- to intermediate-risk, locally confined prostate cancer.1 Recent literature has reported excellent long-term clinical outcome with brachytherapy.24 Also, the combination of its specific advantages, such as single-day outpatient procedure and low postimplantation morbidity compared with surgery and external beam radiation therapy (EBRT),5,6 makes it increasingly popular.

However, because of ionizing radiation, brachytherapy may cause radiation-induced second primary cancer (SPC). For prostate cancer, most research on radiation-induced SPCs has been performed after external beam radiation therapy, with heterogeneous results and conclusions.7,8 Because of the long latency time between irradiation and radiation-induced SPC development, short follow-up for the relative recently introduced transperineal brachytherapy procedure has thus far prevented the evaluation of SPC incidences. However, recently, more sufficient follow-up has become available in patient populations treated in the early days of brachytherapy.

Therefore, in this study, we assessed SPC risk after [125I]iodine implantation brachytherapy as monotherapy for prostate cancer. We retrieved SPC incidences for our brachytherapy patients and compared SPC risk with a similar prostatectomy patient population as well as the general population.


    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Patient Selection
The [125I]iodine prostate brachytherapy patient cohort consisted of 1,187 patients treated between 1989 and 2005 in the Department of Radiation Oncology, University Medical Center Utrecht, or Department of Urology, the Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital. The prostatectomy patient population consisted of 983 patients treated between 1987 and 2005 in the Departments of Urology at either Radboud University Medical Center Nijmegen or the Netherlands Cancer Institute—Antoni van Leeuwenhoek Hospital. For valid comparison, only patients who had received either brachytherapy or prostatectomy as monotherapy were evaluated. Consequently, 282 patients who had received a combination of radiotherapy and prostatectomy were excluded for analysis, resulting in a final prostatectomy patient cohort of 701 patients. For all patients, data on SPC incidences during the period from 1989 to 2007 were retrieved by linkage with the Dutch Cancer Registry in May 2010. Completeness of the Dutch Cancer Registry has been reported to be between 96% and 98%.9,10

Treatment Details
[125I]Iodine brachytherapy was performed using a transrectal ultrasound–guided approach with a prescription dose of 145 Gy,11 including a 2-mm margin, constrained to the anterior rectal wall and bladder neck. Concerning the surrounding organs at risk, the aim of the brachytherapy procedure was to limit the doses to the urethra at 150% or less and anterior rectal wall at 100% or less of the prescription dose.12 More details on the brachytherapy procedure have been reported previously.2

Statistical Analysis
Time at risk started at the day of prostate cancer treatment and ended at date of SPC diagnosis, date of death, or end of follow-up. Calculation of expected numbers of SPCs was based on age-, sex-, calendar year–, and subsite-specific cancer incidence rates in the Dutch population multiplied by the corresponding number of person-years at risk. For the present analysis of SPC risk after prostate cancer, nonmelanoma skin cancers were not considered as events of primary interest. In the case of multiple SPCs, the SPC anatomically most closely related to the prostate gland was considered in all analyses. From the observed and expected numbers of events, we computed the standardized incidence ratio (SIR) of SPCs and corresponding 95% CI based on the Poisson distribution. SIRs were independently computed for two time intervals (1 to 4 and 5 to 14 years since diagnosis) and for two age groups (60 years or younger and older than 60 years of age at diagnosis). A high SIR does not necessarily imply a high disease burden, given that expected incidence of certain cancers may be low, and the SIR is measured on a multiplicative scale. The absolute excess risk, defined as the observed minus expected number of SPCs divided by the accumulated person-years and expressed per 10,000 person-years, better estimates excess disease burden, because it measures excess incidence on an additive scale. Tests for homogeneity and trend of SIRs were performed within Poisson regression models of collapsed person-time data (eg, person-time stratified by sex, time in each 5-year age interval, in each follow-up interval [1 to 4 and 5 to 14 years after diagnosis], and in each 3-year calendar period [1989 to 1991, 1992 to 1994, 1995 to 1997, and so on]).13 Tests for trend of absolute excess risks were performed within an additive Poisson model of collapsed person-time data.14 CIs were based on exact Poisson limits for the observed number of events.

Effects of the different treatments on SPC risk were quantified using multivariable regression analyses according to the method of Fine et al.15 The cumulative incidence of SPCs and their CIs were calculated in the presence of death or other SPCs, when subsites were analyzed separately, as competing risks. Interpretation of the coefficients in this model is similar to that of conventional Cox model coefficients, because this approach can be considered an extension of the Cox model. The method of Fine et al takes into account all types of events and does not assume independence between the time to each of these events, but the effect depends on the magnitude of the risk of other competing events. Treatment was entered into the model using an indicator variable (yes or no) for brachytherapy. All reported P values are two sided; the statistical significance level was set at P value less than .05.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Patients
Table 1 lists patient characteristics by treatment. Median age was 64.7 years (interquartile range [IQR], 59.9 to 69.3 years) at diagnosis. Patients treated with brachytherapy were significantly older than patients who were treated with prostatectomy (median age, 66.5 years; IQR, 61.3 to 70.9 years v 62.6 years; IQR, 58.2 to 66.3 years; P < .001). In total, 291 patients (15.4%) died during follow-up. Median follow-up for all patients combined was 7.5 years (IQR, 5.8 to 10.3 years); for brachytherapy patients, 7.1 years (IQR, 5.8 to 9.6 years); and for prostatectomy patients, 8.7 years (IQR, 6.0 to 12.3 years).


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Table 1. Patient Clinical Characteristics

 
Comparison of Second Cancer Incidence With General Population
The patients accumulated 14,380 person-years: 4,357 person-years for the period of 5 to 9 years after treatment and 1,193 person-years for the period of more than 10 years after treatment. During follow-up, 223 patients developed an SPC. Compared with the general population, the SIR of developing any SPC was 0.97 (95% CI, 0.85 to 1.12), with prostate cancer excluded as cause in the general population (Table 2). In our total cohort, SIRs of bladder cancer and melanoma skin cancer were significantly increased compared with the general population, whereas the SIR was significantly decreased for lung cancer. The SIR for any second malignancy did not vary by age at diagnosis of the first primary tumor (P = .40) nor by time since diagnosis (P = .25). The SIR of any SPC did not differ between patients treated with either brachytherapy or prostatectomy (SIR, 0.94; 95% CI, 0.78 to 1.12 and SIR, 1.04; 95% CI, 0.83 to 1.28, respectively). The SIR for anal cancer was significantly increased after brachytherapy (SIR, 11.5; 95% CI, 1.32 to 41.43), although based on only two patient cases occurring 11 and 14 years after treatment. Patients treated with prostatectomy showed an increased SIR of melanoma skin cancer. Both brachytherapy and prostatectomy patients showed a decreased SIR for lung cancer. After brachytherapy, there was an increased risk of bladder SPC in the first 4 years after treatment (SIR, 2.14; 95% CI, 1.03 to 3.94) and for patients age 60 years or younger (SIR, 5.84; 95% CI, 2.14 to 12.71; Tables 3, 4).


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Table 2. SIRs, AERs, and Cumulative Incidence Rates for Selected Sites According to Primary Treatment

 


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Table 3. SIRs and AERs for Selected Sites According to Primary Treatment by Follow-Up Interval

 


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Table 4. SIRs and AERs for Selected Sites According to Primary Treatment by Age at Diagnosis

 
Effect of Treatment
The 10-year cumulative incidence of any second malignancy was 13.6% (95% CI, 11.7% to 15.6%). It was 14.3% (95% CI, 11.8% to 17.0%) for patients treated with brachytherapy and 12.6% (95% CI, 9.9% to 15.6%) for patients who underwent prostatectomy. Adjusted for age, the hazard ratio for developing an SPC after brachytherapy versus prostatectomy was 0.87 (95% CI, 0.64 to 1.18). The 10-year cumulative incidence rates for cancers of the digestive tract were 5.4% (95% CI, 3.8% to 7.4%) for brachytherapy and 3.7% (95% CI 2.3% to 5.6%) for prostatectomy, with an age-adjusted hazard ratio of 0.96 (P = .92) for brachytherapy versus prostatectomy. The 10-year cumulative incidence rate for SPC of the urinary tract was 2.4% (95% CI, 1.5% to 3.8%) for brachytherapy and 2.0% (95% CI, 1.0% to 3.5%) for prostatectomy, with an age-adjusted hazard ratio of 1.13 (P = .75).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
To our knowledge, this study is the first to evaluate the risk of SPC after [125I]iodine prostate cancer brachytherapy as monotherapy compared with prostatectomy and the general population up to 20 years after treatment. Most knowledge with relation to the effect of ionizing radiation on the prostate gland and surrounding organs is based on prostate cancer treatment with EBRT. However, important differences between EBRT and brachytherapy exist, such as the much higher conformality achieved with brachytherapy and absence of a radiation beam, all resulting in a much smaller irradiated volume.

Overall, this study does not show differences in SPC incidence between patients with prostate cancer treated with prostatectomy or brachytherapy. Furthermore, no increase in tumor incidence was found compared with the general population. Whether patients received brachytherapy or prostatectomy, approximately one in eight patients would be diagnosed with any type of SPC in the 10-year period after treatment.

Concerning a radiation-induced SPC, most radiation will end up in the directly surrounding organs, the urinary bladder, and rectum, resulting in the highest likelihood of inducing SPC in these organs. We found that regardless of treatment, the observed number of bladder SPCs was higher than expected, with an excess of eight extra bladder SPC incidences diagnosed per 10,000 person-years in both the prostatectomy and brachytherapy cohorts. In subanalysis, the increased bladder SPC risk proved only significant for brachytherapy patients age 60 years or younger and 1 to 4 years after brachytherapy. However, it is unlikely that this increase in bladder cancer incidence was caused by ionizing radiation, because the latency period between brachytherapy and bladder cancer development is expected to be longer. On the basis of data derived from studies of survivors of Hiroshima,16,17 Chernobyl,18 and pediatric oncology, the latency period for SPC development is typically at least 5 to 10 years and may well exceed more than 15 years.19,20 Also, the fact that incidences of bladder cancer were higher than expected in prostatectomy patients suggests the effect of a lead-time or screening bias. The explanation for this bias is that patients with prostate cancer receive regular follow-up and are, therefore, at increased risk of being diagnosed with an SPC or are diagnosed in an earlier phase of SPC development. Nonetheless, from a clinical point of view, it is important for clinicians to be aware of this increased incidence of bladder cancer so soon after treatment. A recent study that analyzed 44 patients with bladder cancer who had previously undergone prostate cancer radiotherapy also reported an average latency period of only 5.5 years.21

In literature, a majority of the large SEER (Surveillance, Epidemiology, and End Results) registry studies on the risk of SPC after prostate cancer EBRT treatment show a small but significantly increased risk of bladder SPC,2226 although studies using different registries do not uniformly agree on such an increased risk.2729 Furthermore, the combination of EBRT and a history of smoking, a well-recognized independent contributor to bladder cancer, has been reported to result in an additional doubling of the bladder cancer SPC risk.30 In accordance with most literature on prostate cancer irradiation and SPC of the bladder, we found a small increased risk in early follow-up. However, it is unlikely to have been brachytherapy induced.

There was no increased risk of rectal SPC in our study population, with an observed incidence of one in 100 patients during the 10-year period after prostate cancer treatment in either treatment cohort. Literature on the risk of rectal SPC after prostate cancer irradiation is inconsistent. Some studies have reported an increased risk of rectal SPC after EBRT,24,31 whereas other studies have not found any increase.22,32,33 One explanation may be that the latency period for development of radiation-induced rectal SPC exceeds reported follow-up, and additional follow-up is required. Nonetheless, with current evidence, there is no cause for immediate concern regarding brachytherapy-induced rectal SPC.

With regard to organs well outside the brachytherapy irradiation field, we found that the SPC incidence of lung cancer was significantly lower than expected in both the brachytherapy and prostatectomy populations. This may indicate selection, with a lower than average frequency of smokers in both treatment cohorts. One explanation for this decreased lung cancer incidence is that the high morbidity in patients with a history of smoking presents as a contraindication for definitive prostate cancer treatment. Furthermore, we found a higher than expected incidence of melanoma skin cancer in both treatment cohorts, most apparent (and significant) in the prostatectomy cohort. Again, this is probably the result of a screening bias. Although additional explanations for the decreased lung cancer and increased melanoma skin cancer incidences may be possible, most important is that a relation seems to exist with the prostate cancer population, but an association with brachytherapy treatment itself is unlikely.

Some methodologic limitations of this study should be discussed. First, the relatively small number of patient-years is a main shortcoming of this study. As mentioned before,19,20 the latency period between radiation treatment and SPC development may well exceed 15 or more years, and therefore, follow-up needs to be extended to exclude any potential risk of radiation-induced SPC without doubt. However, for transperineal prostate cancer brachytherapy, follow-up is limited because of its relative short history.34 Consequently, the exact extent of a brachytherapy-induced SPC risk in the second decade after brachytherapy needs confirmation.

Nonetheless, it is arguable whether latency periods are equally long, regardless of patient age or specific organs at risk.21,35 Several studies have found an increased risk of bladder SPC at only 5 years after radiotherapy.22,24,29 Also, considering the older age of most patients treated with brachytherapy, death resulting from intercurrent diseases would interfere with follow-up longer than 15 years. For these patients, life expectancy would only be influenced if a radiation-induced SPC were to occur in the first 10 to 15 years after treatment. On the basis of the data presented in this study, it is improbable that life expectancy is influenced by radiation-induced SPC in these patients. In contrast, for younger patients, confirmation of the presented results with additional follow-up is required.

A second limitation is the relative small size of our study population. A priori power analyses showed that our study had only sufficient power to detect rather large effects when comparing patients treated with brachytherapy with patients treated with prostatectomy for most of the sites of primary interest (ie, 80% power to detect 2.0-fold increased hazard ratio for bladder and rectal cancers combined, 2.6-fold increased hazard ratio for bladder cancer, 2.5-fold increased hazard ratio for rectal cancer). A null finding in our study would have made these rather large effects unlikely. Our study now shows in essence no increased risk associated with brachytherapy, with subhazard ratios of 0.9 to 1.1; as stated, this at least means that no strong effects of brachytherapy are to be expected. We cannot formally exclude hazard ratios in the order of 1.5 to 2.0, but these are not likely and would still result in a relatively small excess number of patient cases.

A third limitation is that details about additional SPC risk factors, such as smoking status, were unavailable. Because of the strong association between smoking and bladder cancer risk,30 an unequal distribution of smokers between brachytherapy and prostatectomy cohorts could have biased results. However, with almost equal lung cancer rates for brachytherapy and prostatectomy patients, large differences in smoking status seem unlikely.

Additional carcinogenic factors that are known in literature, such as hereditary nonpolyposis colorectal cancer, familial adenomatous polyposis, and professional health hazards like aromatic amines exposure,36 may also contribute to SPC incidence in organs at risk. However, the exact interplay of these different carcinogenic factors and cancer development remains elusive.

Strengths of this study include the following. Until now, a majority of studies on SPC after prostate cancer have been based on the SEER registries. This European study differs with regard to smaller ethnic variety and general access to public health. For instance, because of the large percentage of black population in the United States, who have a higher prostate cancer risk profile,37 the corresponding SPC risk may also be different. The public health system in the Netherlands provides equal access to health resources and, therefore, may influence both prostate cancer treatment rates as well as diagnostic rates of SPC differently than in the United States. This results in larger homogeneity of our patient population and also provides cancer incidence rates more suitable for European populations.

Comparison was conducted not only with the general population but also with a prostatectomy patient population, acting as a reference group of more comparable counterparts. Brachytherapy patients are not a random selection of the general populations, and differences may exist with regard to higher genetic or acquired susceptibility to cancer in general. Also, the aforementioned screening and lead-time bias influence SPC rates for brachytherapy patients, stressing the importance of an adequate reference group, such as postatectomy patients. The common decrease in lung cancer and increase in melanoma skin cancer incidence rates in both our treatment cohorts when compared with the general population seem to confirm this.

In contrast to EBRT for prostate cancer, evidence for brachytherapy and risk of radiation-induced SPCs is lacking. Several studies have suggested a higher SPC risk after EBRT compared with brachytherapy,24,25,38,39 although this may have been an effect of selection bias between treatments.40 Some EBRT studies have also reported on a brachytherapy subpopulation. However, in many cases, these brachytherapy patients received additional EBRT to some extent, thus obscuring the independent effect of brachytherapy on potential SPC development. To our knowledge, this is the first large study specifically designed to analyze the relation between brachytherapy as monotherapy and SPC incidences. Because brachytherapy is becoming increasingly popular as an alternative to EBRT and prostatectomy, knowledge of potential SPC risk is important.


    AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Although all authors completed the disclosure declaration, the following author(s) indicated a financial or other interest that is relevant to the subject matter under consideration in this article. Certain relationships marked with a "U" are those for which no compensation was received; those relationships marked with a "C" were compensated. For a detailed description of the disclosure categories, or for more information about ASCO's conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors.

Employment or Leadership Position: None Consultant or Advisory Role: None Stock Ownership: None Honoraria: Karel A. Hinnen, sanofi-aventis Research Funding: None Expert Testimony: None Other Remuneration: None


    AUTHOR CONTRIBUTIONS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
Conception and design: Karel A. Hinnen, Marco van Vulpen, Jan J. Battermann, Joep G.H. van Roermund, Evelyn M. Monninkhof

Provision of study materials or patients: Jan J. Battermann, Henk van der Poel, Inge M. van Oort

Collection and assembly of data: Karel A. Hinnen, Michael Schaapveld, Henk van der Poel, Inge M. van Oort, Joep G.H. van Roermund

Data analysis and interpretation: Karel A. Hinnen, Michael Schaapveld, Evelyn M. Monninkhof

Manuscript writing: All authors

Final approval of manuscript: All authors


    NOTES
 
Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 AUTHORS' DISCLOSURES OF...
 AUTHOR CONTRIBUTIONS
 REFERENCES
 
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Submitted January 31, 2011; accepted August 17, 2011.


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