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Keywords:

  • neoplasms;
  • second primary;
  • prevalence;
  • survivors

Abstract

  1. Top of page
  2. Abstract
  3. Material and Methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

As the number of cancer survivors increases in the Netherlands, there is a concomitant increase in patients with multiple malignancies (MMs), the prevalence of which needs to be assessed to estimate care needs. This study analyzed incidence data on all malignant cancers diagnosed between 1989 and 2006 retrieved from the population-based Netherlands Cancer Registry. The point prevalence of MMs was determined on January 1, 2007. Of all cancer survivors in 2007, 30,064 (7% of the total) were patients with MMs. Their median age was 74 (interquartile range 71–76) years. Ninety two percent (i.e., 27,660) of these patients had two cancer diagnoses. The most common subsequent cancers being squamous cell skin cancer (5,468), colorectal cancer (4,634), and breast cancer (3,959). High frequency of combinations included: (i) female breast and genital cancers (any order), (ii) urinary tract and prostate cancers (any order), (iii) Hodgkin's lymphoma and subsequent female breast cancer and (iv) non-Hodgkin's lymphoma and subsequent squamous cell skin cancer. As the number of cancer survivors continues to increase and their survival improves, MMs are becoming more important in the field of cancer surveillance.

The number of cancer survivors is increasing due to improvements in early detection programs and treatment. In 2005, it was estimated that 400,000 people in the Netherlands had a previous cancer diagnosis which corresponds with 2.5% of the total population.1 By 2015, the number of cancer survivors is predicted to increase by 38% to 692,000 individuals, representing 4% of the total Dutch population.2 An additional cancer diagnosis is one of the main concerns in cancer survivors and, therefore, merits attention. In 2001, in the USA 8% of the prevalent cancer patients had multiple malignancies (MMs),3 and one of six (16%) newly diagnosed cases in 2004 had MMs.4 The International Agency of Research on Cancer (IARC) has published a series of studies assessing the relative risk of developing second malignancies after a first cancer.5–12 Similar studies have been performed in the Netherlands.13–17 These sources show that cancer patients have an increased risk of developing a second cancer compared to the general population. Furthermore, compared to patients with a single malignancy, patients with MMs often exhibit a worse 5-year relative survival following diagnosis of one or more secondary cancers.18, 19 Moreover, the six aspects of quality of life (i.e., physical functioning, pain, general health perception, energy, social functioning and role limitations due to emotional problems) have been shown to decrease significantly after a second breast cancer diagnosis.20 Data on quality of life after the diagnosis of a second cancer at another site are scarce.

Because of the increasing number of cancer survivors, MMs will become an increasingly important topic in both cancer surveillance and epidemiology. A comprehensive description of patients with MMs would help to estimate care requirements and guide future research on MMs.21, 22

This study aimed to provide a comprehensive overview of the point-prevalence of MMs in the Netherlands as of January 1, 2007.

Material and Methods

  1. Top of page
  2. Abstract
  3. Material and Methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

The population-based Netherlands Cancer Registry (NCR) provided incidence data on all malignant cancers, including MMs, diagnosed between 1989 and 2006. Information on vital status is updated through an annual linkage with the Dutch Municipality Register. This follow-up information is complete up since October 1994. Therefore, all patients diagnosed with a cancer before October 1994 who did not develop a subsequent cancer were censored at their last date of follow-up. If subsequent malignancies are diagnosed later, the follow-up of the patient can be reconstructed. Detailed description of NCR data can be found elsewhere.23 The definition of multiple primaries in the Netherlands follows guidelines proposed by the international Association of Cancer Registries (IACR) and IARC.24 According to these guidelines, a primary cancer is one that originates in a primary site or tissue and is thus neither an extension nor a recurrence or a metastasis. The recognition of the existence of two or more primary cancers does not depend on time. Only one cancer can be recognized as rising in an organ or pair of organs or tissue (as defined by the three-character category of the ICD or the topography of the ICD-O) unless the histology is different.

Definition of prevalence of MMs

The point prevalence of cancer is defined as the proportion of people alive with cancer at a certain point in time, disregarding the moment of disease onset. We determined the point prevalence of patients with one cancer and patients with MMs on January 1, 2007. Patients with MMs were defined as those with a primary invasive cancer followed by one or more additional cancers (invasive/in situ) between 1989 and 2006. These patients were classified as “ever diagnosed patients with MMs” and were categorized into three groups according to the vital status: alive, deceased and lost to follow-up (LFU). In this study, those alive on January 1, 2007 represent the prevalent cases of MMs. First primary invasive cancers were defined as first malignancies. Multiple primary cancers were defined according to international guidelines for multiple primary cancers.24 We chose the presented first cancers based on the SEER data in the period from 1973 till 2002.25 After a first cancer, if the 25-year cumulative incidence of the second cancers is larger than 10%, the first cancers were selected to be presented and were displayed in the following 13 anatomical sites/systems: mouth and pharynx, colorectal and anus, soft tissue, malignant melanoma of the skin, skin (squamous cell carcinoma), breast, female genital, male genital, prostate, kidney, urinary tract (renal pelvis, ureter, bladder, urethra), Hodgkin's and non-Hodgkin's lymphoma. All other first malignancies were grouped into a category “other.” Ovarian carcinomas of borderline malignancy were excluded, as were basal cell carcinomas of the skin, which were only recorded in one regional registry.26

Statistical analysis

Patients with MMs were described by gender, number, status on the last date of follow-up (alive, deceased and LFU), age on January 1, 2007 (grouped into six age categories: 0–39, 40–49, 50–59, 60–69, 70–79, 80+) and cancer types. Also calculated were: age at diagnosis of the first and subsequent cancers, and time intervals between cancer diagnoses. Age at each cancer diagnosis and time interval between diagnoses were presented as median and interquartile range (IQR). In addition, we calculated the proportion of survivors according to the number of cancer diagnoses (1, 2, 3 and 4 or more) and the period from the last diagnosis until the end of the study (<1 year, 1–2 years, 3–4 years and ≥5 years). Patients with MMs were grouped by site of first cancer. Statistical analyses were performed using SAS 9.0.

Results

  1. Top of page
  2. Abstract
  3. Material and Methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

Between 1989 and 2006, a total of 1,351,621 individuals in the Netherlands were diagnosed with cancer (data not shown); 85,676 (6%) of whom were patients with MMs. On January 1 2007, 424,340 of these patients were still alive, 7% (30,064) included patients with MMs. Ninety two percent of these patients (n = 27,660) had two cancers. Of all patients with multiple cancers diagnosed between 1989 and 2006, 58% (49,335) had died and 7% (6,277 patients) were LFU. Median age at first cancer diagnosis was 65 years (IQR: 62–67 years), and the median age on January 1, 2007 was 74 years (IQR: 71–76 years). The period between two consecutive diagnoses ranged from 0.5 to 3 years (median, 1 year). As the number of cancers diagnosed per patient increased, the time interval between the diagnoses decreased (Table 1).

Table 1. Characteristics of patients with multiple malignancies among all those diagnosed with cancer in the period 1989–2006 in the Netherlands
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On January 1, 2007 there were no surviving patients with more than five cancer diagnoses. Men were more often diagnosed with MMs than women (8% vs. 6%, respectively). Most of the prevalent patients with MMs (42%, increasing from 25 to 30% for the 2nd cancer and 51–65% for the fourth or following cancers) were diagnosed within 1 year of their last cancer diagnosis (Table 2).

Table 2. Overview of cancer survivors in the Netherlands diagnosed in the period 1989–2006 on January 1, 2007
inline image

MMs were most commonly observed among elderly patients (median 74 years), but MMs prevalence decreased among people aged 80 years or older. Less than 1% (274/30,064) of the MMs patients were younger than age 39 years (data not shown).

The youngest patients with MMs were survivors of Hodgkin's lymphoma (median age on January 1, 2007 55 years) and those with a first male genital cancer (97% testicular cancer; median age on January 1, 2007 62 years) (Table 3).

Table 3. Prevalence of multiple malignancies by sites of first cancer diagnosed in the period 1989–2006 in the Netherlands on January 1 2007
inline image

The frequency ranks of the first, second, third, fourth and higher-order cancers are shown in Figures 1a1c. The most commonly occurring second cancers were squamous cell cancer of the skin (n = 5,468), colorectal cancers (n = 4,634) and breast cancers (n = 3,959). Higher order cancers (≥3) were most frequently found for cancers of the skin (squamous cell skin cancer, n = 579), colon and rectum (n = 333) and urinary tract (n = 308).

thumbnail image

Figure 1. (a) Frequency rank of first cancers among patients with multiple malignancies, alive on January 1 2007, (b) Frequency rank of second cancers among patients with multiple malignancies, alive on January 1 2007 and (c) frequency rank of third and higher order cancers among patients with multiple malignancies, alive on January 1 2007.

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Table 3 gives an overview of the distribution of subsequent cancers according to the type of the first and subsequent cancers. The shortest time interval between the first and second cancer was observed among survivors with a first urinary tract cancer (1 year); the longest time interval was found for those with Hodgkin's disease survivors (6 years). Overall, on January 1, 2007 the patients with MMs had lived with cancer (from the first diagnosis onwards) for 8 years (median), ranging from a median of 6 years for prostate cancer patients to a median of 11 years for survivors of Hodgkin's disease. The lowest proportion of subsequent cancers was found among first male genital cancers, being only 3%. The highest proportions were observed for urinary tract cancer (15%), mouth and pharynx cancer (12%), squamous cell carcinoma of the skin (10%) and colorectal cancer (9%).

In absolute terms, multiple cancers were most frequent among survivors of female breast cancer (n = 5,774), colorectal (n = 5,169) and prostate cancer (n = 3,862).The most frequent combinations between first and subsequent cancers were as follows (i) breast and female genital cancers (any order), (ii) urinary tract and prostate cancers (any order), (iii) Hodgkin's lymphoma and subsequent breast cancer, (iv) non-Hodgkin's lymphoma and subsequent squamous cell skin cancer.

Discussion

  1. Top of page
  2. Abstract
  3. Material and Methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

This study assessed the burden of MMs in terms of prevalence within the Dutch population of which the average incidence of cancer was 404 (per 100,000) from 1989 to 200623 and exhibited a 5-year crude survival of 60% in the period 2003–2007.27 The prevalence of MMs included current survivors with at least one subsequent cancer diagnosis after a first invasive cancer within the observation period from 1989 to 2006. With a median follow-up time of 8 years, 30,064 patients were diagnosed with MMs, representing 7% of all cancer survivors on January 1, 2007 in the Netherlands. A previous study in the USA reported 8% of cancer survivors had MMs in 2002.3

The most common subsequent cancers were cancers of the skin (squamous cell skin cancer), colorectal cancer and female breast cancer. The prevalence of subsequent cancers is influenced by the age at first diagnosis, incidence and survival of the first and subsequent cancers and the maximum and median length of follow-up time (e.g., history of cancer registry). The three most common subsequent cancers mentioned above are those with high incidence and a relatively good prognosis (5-year relative survival >50%) in the Netherlands.28 Although lung cancer is one of the most common cancers and shares its main risk factor (smoking) with many other cancers, it contributes little to the prevalence of MMs because of its poor prognosis (5-year survival ∼10%).29

The current population with MMs was composed mainly of elderly subjects (median age,74 years). The average age at diagnosis of first cancer was 65 years. The treatment of second or higher order cancers is complex due to old age and co-morbidity and might need to be tailored individually.30, 31 The youngest patients with MMs had Hodgkin's lymphoma (55 years) and male genital cancer (62 years) as a first primary. Their young age at first cancer diagnosis (40–50 years) combined with the good prognosis (10-year relative survival is 75–95%) led to a long life expectancy after first diagnosis.28 However, the risk of developing a subsequent cancer was 1.4 to 3.0 times higher compared to the general population.32–34 It is plausible that prevention by means of lifestyle changes (such as quitting smoking) might decrease this group's risk of a second cancer and other chronic diseases.35 However, the benefit and harm of intervention programs (for either primary or secondary prevention) remain to be investigated.17

We observed four pairs of cancers that frequently occur together. It should be noted that this observed association on prevalence should not be simply interpreted as a result of shared risk factors, which is normally interpreted in the incidence data. Cancer prevalence is an interaction of various factors such as risk of getting cancer (incidence), risk of dying from cancer (mortality) and duration of time lived with cancer (survival) and many more. Therefore, the etiological link between the first and subsequent merits attention, but should be considered only one of the multitude of factors which determine the prevalence of MMs and, more particularly, the prevalence of specific combinations of multiple cancers. There are etiological theories concerning the development of subsequent cancers: (i) specific treatment effects6, 9; (ii) shared risk factors between first and subsequent cancers (lifestyle or environmental factors12, 36); (iii) shared genetic predisposition and (iv) combinations of the above three.5, 10, 37 Adverse effects of treatment (i.e., radiotherapy) may explain the high prevalence of breast cancer among Hodgkin's lymphoma survivors.38–40 Although second lung cancer is also associated with radiotherapy,35 the poor prognosis of lung cancer contributed to its low proportion of multiple cancers in this cancer type. Shared risk factors, e.g., hormonal risk factors such as nulliparity, obesity, and hormone-replacement therapy, probably relates breast cancer to female genital cancers.41, 42 Moreover, carriers of BRCA1/2 may contribute 2–5% in developing breast and ovarian cancers, especially among younger patients.43 As to the last theory, the combination of the previous three factors has hardly been studied and is difficult to explain with our data. In addition to the above general theories, disease or treatment-induced immunosuppression may explain the high frequency of squamous cell skin cancer after non-Hodgkin's lymphoma.44

Finally and importantly, enhanced early detection programs (e.g., clinical follow-up and screening programs) may explain some of the high frequency cancer pairs, especially when the time interval between the first and the second cancer diagnosis is short; for instance, in case of prostate and urinary tract (usually bladder) cancer, the short interval between the first and the second cancer diagnosis (≈1 year) may reflect the common diagnostic process of these two cancers.45

Recent Dutch studies of long-term survivors of breast, Hodgkin's and non-Hodgkin's lymphoma, prostate and endometrial cancer showed that disease progression (recurrence, metastasis and detection of other primary cancers) negatively affects health status and quality of life.20, 46 As data on quality of life among MMs patients are scarce, more studies are needed before designing interventions to improve the quality of life in this population.

To our knowledge, this is the first population-based, nation-wide report on the prevalence of MMs that includes all cancer types (excluding basal cell carcinomas of the skin). This ensures the representativeness and validity of the prevalence estimates.

Concerning the accuracy and completeness of cancer diagnoses in the NCR, most cases were histologically confirmed cancers retrieved from the nation-wide pathology network (PALGA), and therefore, a high accuracy of cancer diagnosis may be expected. Furthermore, the National Registry of Hospital Discharge Diagnosis system collected data on patients who were only diagnosed clinically, which increases the completeness of the NCR data. Finally, the application of IARC/IACR rules for multiple primary cancers24 facilitates external comparison of the study results, as long as the same coding rules are applied.

The main limitation of the current prevalence data is the probable underestimation of MMs cases. First, 18 years of follow-up does not yield the lifetime prevalence but represents about 90% of the full estimate.47 Second, 7% of ever diagnosed multiple cancer patients were LFU, which may have led to an underestimate of prevalence. Third, we were unable to include the most common cancer: basal cell carcinoma. Although this is the case in most registries, if this cancer had been taken into account, higher MMs prevalence values would have emerged. Finally, the coding rules that were used to record multiple primaries should be taken into consideration when making cross-countries comparisons. For example, in USA, the Surveillance, Epidemiology, and End Results (SEER) use different rules than those defined by IACR/IARC.48 Differences between the coding guidelines include: the existence of two or more primary cancers do not depend on time in the IACR/IARC guidelines, however, only metachronous cancers (occurring 2 or more months after initial diagnosis) are recorded as separate primaries in the SEER guidelines; furthermore, regarding cancers originating from paired organs (e.g., ovary, Wilm's cancer, Retinoblasma), SEER guidelines treat them as independent, whereas, the IACR/IARC guidelines regard them as one single cancer unless a histological difference exists. In general, the IACR/IARC guidelines are more restrictive than those applied by SEER. Moreover, there are unresolved debates regarding coding of multiple primaries.49 However, it is yet to be investigated how such coding differences affect differences in recorded prevalence.

In conclusion, on January 1 2007, 30,064 patients were alive with MMs, representing 7% of all cancer survivors and 0.2% of the total Dutch population. The estimate is subject to a possible 10–15% of underestimation. As the number of cancer survivors continues to increase by 3–5% annually and prognosis improves with each year survived,50 MMs are becoming more important in the field of cancer surveillance.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Material and Methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References

The authors would like to thank Dr. J.A. (Jan Anne) Roukema for his valuable comments and advice.

References

  1. Top of page
  2. Abstract
  3. Material and Methods
  4. Results
  5. Discussion
  6. Acknowledgements
  7. References
  • 1
    Dutch Comprehensive Cancer Centres. Available at: http://www.ikcnet.nl/page.php?id=1525&nav_id=97. Accessed on July 14, 2009.
  • 2
    Kanker in Netherland. Trends, prognoses, en implicatie voor zorgvraag. 2004. 2004.
  • 3
    Mariotto AB, Rowland JH, Ries LA, Scoppa S, Feuer EJ. Multiple cancer prevalence: a growing challenge in long-term survivorship. Cancer Epidemiol Biomarkers Prev 2007; 16: 56671.
  • 4
    Ries LAGMD, KrapchoM, StinchcombDG, HowladerN, HornerMJ, MariottoA, MillerBA, FeuerEJ, AltekruseSF, LewisDR, CleggL, EisnerMP, et al., eds. SEER cancer statistics review, 1975–2005. Bethesda, MD: National Cancer Institute, 2007.
  • 5
    Brennan P, Scelo G, Hemminki K, Mellemkjaer L, Tracey E, Andersen A, Brewster DH, Pukkala E, McBride ML, Kliewer EV, Tonita JM, Seow A, et al. Second primary cancers among 109 000 cases of non-Hodgkin's lymphoma. Br J Cancer 2005; 93: 15966.
  • 6
    Hashibe M, Ritz B, Le AD, Li G, Sankaranarayanan R, Zhang ZF. Radiotherapy for oral cancer as a risk factor for second primary cancers. Cancer Lett 2005; 220: 18595.
  • 7
    Mellemkjaer L, Friis S, Olsen JH, Scelo G, Hemminki K, Tracey E, Andersen A, Brewster DH, Pukkala E, McBride ML, Kliewer EV, Tonita JM, et al. Risk of second cancer among women with breast cancer. Int J Cancer 2006; 118: 228592.
  • 8
    Scelo G, Boffetta P, Hemminki K, Pukkala E, Olsen JH, Andersen A, Tracey E, Brewster DH, McBride ML, Kliewer EV, Tonita JM, Pompe-Kirn V, et al. Associations between small intestine cancer and other primary cancers: an international population-based study. Int J Cancer 2006; 118: 18996.
  • 9
    Richiardi L, Scelo G, Boffetta P, Hemminki K, Pukkala E, Olsen JH, Weiderpass E, Tracey E, Brewster DH, McBride ML, Kliewer EV, Tonita JM, et al. Second malignancies among survivors of germ-cell testicular cancer: a pooled analysis between 13 cancer registries. Int J Cancer 2007; 120: 62331.
  • 10
    Riska A, Pukkala E, Scelo G, Mellemkjaer L, Hemminki K, Weiderpass E, McBride ML, Pompe-Kirn V, Tracey E, Brewster DH, Kliewer EV, Tonita JM, et al. Second primary malignancies in females with primary fallopian tube cancer. Int J Cancer 2007; 120: 204751.
  • 11
    Scelo G, Boffetta P, Autier P, Hemminki K, Pukkala E, Olsen JH, Weiderpass E, Tracey E, Brewster DH, McBride ML, Kliewer EV, Tonita JM, et al. Associations between ocular melanoma and other primary cancers: an international population-based study. Int J Cancer 2007; 120: 1529.
  • 12
    Chuang SC, Scelo G, Tonita JM, Tamaro S, Jonasson JG, Kliewer EV, Hemminki K, Weiderpass E, Pukkala E, Tracey E, Friis S, Pompe-Kirn V, et al. Risk of second primary cancer among patients with head and neck cancers: a pooled analysis of 13 cancer registries. Int J Cancer 2008; 123: 23906.
  • 13
    de Vries E, Soerjomataram I, Houterman S, Louwman MW, Coebergh JW. Decreased risk of prostate cancer after skin cancer diagnosis: a protective role of ultraviolet radiation? Am J Epidemiol 2007; 165: 96672.
  • 14
    Soerjomataram I, Louwman WJ, de Vries E, Lemmens VE, Klokman WJ, Coebergh JW. Primary malignancy after primary female breast cancer in the South of the Netherlands, 1972–2001. Breast Cancer Res Treat 2005; 93: 915.
  • 15
    Soerjomataram I, Louwman WJ, Lemmens VE, Coebergh JW, de Vries E. Are patients with skin cancer at lower risk of developing colorectal or breast cancer?. Am J Epidemiol 2008; 167: 14219.
  • 16
    Soerjomataram I, Louwman WJ, Lemmens VE, de Vries E, Klokman WJ, Coebergh JW. Risks of second primary breast and urogenital cancer following female breast cancer in the south of The Netherlands, 1972–2001. Eur J Cancer 2005; 41: 23317.
  • 17
    Soerjomataram I, Louwman WJ, van der Sangen MJ, Roumen RM, Coebergh JW. Increased risk of second malignancies after in situ breast carcinoma in a population-based registry. Br J Cancer 2006; 95: 3937.
  • 18
    Soerjomataram I, Vries Ed. Correspondence: Author reply: a further caveat in interpreting cancer survival. Nat Rev Clin Oncol 2010; 7.
  • 19
    Rosso S, De Angelis R, Ciccolallo L, Carrani E, Soerjomataram I, Grande E, Zigon G, Brenner H. Multiple tumours in survival estimates. Eur J Cancer 2009; 2: 2.
  • 20
    Thornton AA, Madlensky L, Flatt SW, Kaplan RM, Pierce JP. The impact of a second breast cancer diagnosis on health related quality of life. Breast Cancer Res Treat 2005; 92: 2533.
  • 21
    Giles G. How important are estimates of cancer prevalence?. Ann Oncol 2002; 13: 8156.
  • 22
    Zanetti R, Micheli A, Rosso S, Sant M. The prevalence of cancer: a review of the available data. Tumori 1999; 85: 40813.
  • 23
    Dutch Comprehensive Cancer Centres, Available at: http://www.ikcnet.nl/page.php?id=96, Accessed on July 14, 2009
  • 24
    International Association of Cancer Registries (IACR). International rules for multiple primary cancers. Asian Pac J Cancer Prev 2005; 6: 1046.
  • 25
    Curtis RE FD, Ron E, Ries LAG, Hacker DG, Edwards BK, Tucker MA, Fraumeni JF, Jr. New malignancies among cancer survivors: SEER cancer registries, 1973–2000. Bethesda, MD: National Cancer Institute, 2006.
  • 26
    de Vries E, Louwman M, Bastiaens M, de Gruijl F, Coebergh JW. Rapid and continuous increases in incidence rates of basal cell carcinoma in the southeast Netherlands since 1973. J Invest Dermatol 2004; 123: 6348.
  • 27
  • 28
    Available at: http://www.ikcnet.nl/page.php?id=96, Accessed on July 14th 2009.
  • 29
    Janssen-Heijnen ML, Coebergh JW. The changing epidemiology of lung cancer in Europe. Lung Cancer 2003; 41: 24558.
  • 30
    Janssen-Heijnen ML, Houterman S, Lemmens VE, Louwman MW, Maas HA, Coebergh JW. Prognostic impact of increasing age and co-morbidity in cancer patients: a population-based approach. Crit Rev Oncol Hematol 2005; 55: 23140.
  • 31
    Janssen-Heijnen ML, Maas HA, Houterman S, Lemmens VE, Rutten HJ, Coebergh JW. Comorbidity in older surgical cancer patients: influence on patient care and outcome. Eur J Cancer 2007; 43: 217993.
  • 32
    Dores GM, Metayer C, Curtis RE, Lynch CF, Clarke EA, Glimelius B, Storm H, Pukkala E, van Leeuwen FE, Holowaty EJ, Andersson M, Wiklund T, et al. Second malignant neoplasms among long-term survivors of Hodgkin's disease: a population-based evaluation over 25 years. J Clin Oncol 2002; 20: 348494.
  • 33
    Travis LB, Curtis RE, Storm H, Hall P, Holowaty E, Van Leeuwen FE, Kohler BA, Pukkala E, Lynch CF, Andersson M, Bergfeldt K, Clarke EA, et al. Risk of second malignant neoplasms among long-term survivors of testicular cancer. J Natl Cancer Inst 1997; 89: 142939.
  • 34
    van Leeuwen FE, Stiggelbout AM, van den Belt-Dusebout AW, Noyon R, Eliel MR, van Kerkhoff EH, Delemarre JF, Somers R. Second cancer risk following testicular cancer: a follow-up study of 1,909 patients. J Clin Oncol 1993; 11: 41524.
  • 35
    Travis LB, Gospodarowicz M, Curtis RE, Clarke EA, Andersson M, Glimelius B, Joensuu T, Lynch CF, van Leeuwen FE, Holowaty E, Storm H, Glimelius I, et al. Lung cancer following chemotherapy and radiotherapy for Hodgkin's disease. J Natl Cancer Inst 2002; 94: 18292.
  • 36
    Chuang SC, Hashibe M, Scelo G, Brewster DH, Pukkala E, Friis S, Tracey E, Weiderpass E, Hemminki K, Tamaro S, Chia KS, Pompe-Kirn V, et al. Risk of second primary cancer among esophageal cancer patients: a pooled analysis of 13 cancer registries. Cancer Epidemiol Biomarkers Prev 2008; 17: 15439.
  • 37
    Hemminki K, Scelo G, Boffetta P, Mellemkjaer L, Tracey E, Andersen A, Brewster DH, Pukkala E, McBride M, Kliewer EV, Chia KS, Pompe-Kirn V, et al. Second primary malignancies in patients with male breast cancer. Br J Cancer 2005; 92: 128892.
  • 38
    Travis LB, Hill D, Dores GM, Gospodarowicz M, van Leeuwen FE, Holowaty E, Glimelius B, Andersson M, Pukkala E, Lynch CF, Pee D, Smith SA, et al. Cumulative absolute breast cancer risk for young women treated for Hodgkin lymphoma. J Natl Cancer Inst 2005; 97: 142837.
  • 39
    Hill DA, Gilbert E, Dores GM, Gospodarowicz M, van Leeuwen FE, Holowaty E, Glimelius B, Andersson M, Wiklund T, Lynch CF, Van't Veer M, Storm H, et al. Breast cancer risk following radiotherapy for Hodgkin lymphoma: modification by other risk factors. Blood 2005; 106: 335865.
  • 40
    Travis LB, Hill DA, Dores GM, Gospodarowicz M, van Leeuwen FE, Holowaty E, Glimelius B, Andersson M, Wiklund T, Lynch CF, Van't Veer MB, Glimelius I, et al. Breast cancer following radiotherapy and chemotherapy among young women with Hodgkin disease. JAMA 2003; 290: 46575.
  • 41
    Brinton LA LJJ, Devesa SS. Epidemiology of breast cancer In: DoneganWL SJe, ed. Cancer of the breast, 5th edn. Philadelphia: Saunders, 2002. 11132.
  • 42
    Brinton LA LJJ, Sherman ME. Epidemiology of gynecologic cancers. In: HoskinsWJ PCYRe, ed. Principles and practice of gynecologic oncology, 4th edn. Philadelphia: Lippincott Williams & Wiklkins, 2005. 332.
  • 43
    Nelson HD, Huffman LH, Fu R, Harris EL. Genetic risk assessment and BRCA mutation testing for breast and ovarian cancer susceptibility: systematic evidence review for the U.S. Preventive Services Task Force. Ann Intern Med 2005; 143: 36279.
  • 44
    Hemminki K, Jiang Y, Steineck G. Skin cancer and non-Hodgkin's lymphoma as second malignancies. markers of impaired immune function? Eur J Cancer 2003; 39: 2239.
  • 45
    Travis LB. Therapy-associated solid tumors. Acta Oncol 2002; 41: 32333.
  • 46
    Thong MS, Mols F, Coebergh JW, Roukema JA, van de Poll-Franse LV. The impact of disease progression on perceived health status and quality of life of long-term cancer survivors. J Cancer Surviv 2009; 3: 16473.
  • 47
    Capocaccia R, De Angelis R. Estimating the completeness of prevalence based on cancer registry data. Stat Med 1997; 16: 42540.
  • 48
    NCI. 2006b. SEER Program Coding and Staging Available at: Manual:http://seer.cancer.gov/tools/codingmanuals/, Assessed on July 14th, 2009.
  • 49
    Percy-Laurry AL, Johnson CH, Reichman ME, Adamo M, Lewis DR, Peace S. Revising the multiple primary and histology coding rules. J Regist Manag 2007; 34: 816.
  • 50
    Janssen-Heijnen ML, Houterman S, Lemmens VE, Brenner H, Steyerberg EW, Coebergh JW. Prognosis for long-term survivors of cancer. Ann Oncol 2007; 18: 140813.