Second Cancers in Classical Hodgkin Lymphoma and Diffuse Large B-Cell Lymphoma: A Systematic Review by the Fondazione Italiana Linfomi
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Identification
2.2. Eligibility Criteria
2.3. Study Selection and Data Extraction
2.4. Risk of Bias and Quality of Evidence Assessment
2.5. Data Synthesis
3. Results
3.1. What Is the Incidence of Second Cancers in cHL or DLBCL Long-Term Survivors after First- or Second-Line Treatments including ASCT?
3.2. Has the Incidence of Second Cancers in cHL or DLBCL Long-Term Survivors Who Underwent First or Second Line CHT and ASCT Changed with the Introduction of Modern RT?
3.3. Are Planned Follow-Up/Screening Schemes Effective in the Management and Early Diagnosis of Second Cancers in cHL or DLBCL Long-Term Survivors Treated, Regardless of the Type of CHT/RT (First and Second Line including ASCT)?
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Clinical Question | PICOs |
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PICO A: What is the incidence of SM in cHL or DLBCL long-term survivors after first or second line treatments? | P: population of cHL or DLBCL long-term survivors (≥5 years of disease/treatment free) aged ≥ 18 years at diagnosis I: chemotherapy (e.g., ABVD for cHL; R-CHOP for DLBCL), second-line chemotherapy and autologous transplant, radiotherapy C1: none C2: general population equal to age and sex C3: other chemotherapy/radiotherapy treatment regimens O: number of cases of second neoplasms (breast, lung, gastrointestinal, prostate, melanoma, thyroid, etc.) |
PICO B: Has the incidence of SM in cHL or DLBCL long-term survivors who underwent first or second line chemotherapy and ASCT changed with the introduction of modern radiotherapy? | P: population of cHL or DLBCL long-term survivors (≥5 years of disease/treatment free) aged ≥ 18 years at diagnosis I: new radiotherapy approaches (e.g., 3DCRT, volume reduction, dose reduction, IMRT) C: previous radiotherapy regimens (EFRT, 2DRT, RT dose) O: number of cases of second malignancies (e.g., breast, lung, gastrointestinal, prostate, melanoma, thyroid) |
PICO C: Are planned follow-up/screening schemes effective for the management and early diagnosis of second cancers in cHL or DLBCL long-term survivors treated, regardless of the type of CHT/RT (first and second line including ASCT)? | P: population of cHL or DLBCL long-term survivors (≥5 years of disease/treatment free) aged ≥18 years at diagnosis I: scheduled follow-up/monitoring schemes for second malignancies, diversified by age, gender/sex, which include laboratory and instrumental tests (e.g., breast mammography/MRI, chest CT, stool occult blood, colonoscopy, dermatoscopy, thyroid US, PSA) C1: no follow up/monitoring planned C2: follow up/monitoring schemes with different intensity (with respect to I, including different times and frequencies) O: early diagnosis of second neoplasms, problems related to overdiagnosis, QoL, mortality |
Study | Study Design and Sample Size | Intervention and Comparison | Main Outcomes |
---|---|---|---|
PICO 1 | |||
André M, 2020 [24] | Pooled analysis of randomized control trials (1227 patients with advanced stage cHL in first line | BEACOPP vs. ABVD | Incidence of SM per 1000 person-years was 6.3% in ABVD arm vs. 9.6% in BEACOPP arm. Thirteen cases of secondary MDS/AML were reported in the BEACOPP arm, compared to none in the ABVD arm. |
Torok JA, 2015 [25] | Retrospective cohort study (90 patients with early unfavourable cHL in first line) | CT (ABVD in 88%) plus RT | Seven SM were diagnosed in the cohort. The median time for diagnosis of SM was 10 years (range: 1–14 years), but all hematological SM occurred within 3 years of diagnosis. |
Engert A, 2007 [26] | Randomized control trial (627 patients with early favourable cHL in first line) | 2 ABVD plus EFRT 30 Gy vs. EFRT 30 Gy plus boost 10 Gy | Total number of SM was 39 (6.2%). Eleven of the solid SM occurred in irradiated areas, three in nonirradiated areas, and for seven cases it was unknown or unclear. There were no significant differences between treatment arms. Between years 2 and 9, the incidence remained constant (0.8% per year); numbers at risk were too small for reliable estimates beyond year 9. |
Schaapveld M, 2015 [27] | Retrospective cohort study (3905 patients with cHL in first line) | CT and/or RT | A total 1055 SM were observed in 908 patients; a third cancer developed in 130 patients, and a fourth developed in 17. SM risk in cHL treated patients was higher than in the general population (121.8 excess cancers per 10,000 PY). Breast cancer contributed most (24.9 cases per 10,000 PY in the whole cohort, 54.3 cases per 10,000 PY in women. SIR for any SM remained high for at least 35 years after the start of treatment for cHL, whereas the absolute excess risk increased steadily over time. A cumulative procarbazine dose of 4.3 g or more per square meter of body-surface area was associated with a higher risk of gastrointestinal cancer. |
Frontzek F, 2021 [28] | Randomize control trial (275 patients with high-risk DLBCL in first line) | R-megaCHOEP vs. R-CHOEP14 | Twenty-two SM were reported in the ITT population, 9% in the R-CHOEP14 group and 8% in the R-MegaCHOEP group. The median time to MDS/AML was 44 months; median time to solid SM was 72 months. Age older than 50 years at diagnosis was the only factor associated with significantly increased risk of secondary SM. |
Coiffier B, 2010 [29] | Randomized control trial (399 patients with DLBCL in first line, 60–80 years old) | R-CHOP21 vs. CHOP21 | Fourty-three patients (10.8%) developed a SM after entering the study, 22 in the CHOP arm and 21 in the R-CHOP arm. Three patients developed a third SM, 1 in the CHOP arm and 2 in the R-CHOP arm. There was no pattern in the type of secondary cancers that occurred. |
Castellino A, 2018 [30] | Pooled analysis of prospective trial (112 patients with DLBCL in first line) | R-CHOP21 plus lenalidomide | SM were observed in seven patients (6.3%). The median time from the end of treatment to the SM onset was 16.4 months. |
Paudel N, 2019 [31] | Retrospective cohort study (89 patients with relapsed/refractory cHL) | Total lymphoid irradiation plus carboplatin-cyclophosphamide- etoposide and ASCT | Eight of the 89 patients had developed SM at a median of 5.6 years from the time of transplant. Five patients developed hematologic SM, three were solid SM. Three of the patients with subsequent hematologic SM had received MOPP. |
Pingali SR, 2017 [32] | Retrospective cohort study (310 patients with relapsed/refractory cHL patients) | ASCT with BEAM conditioning, mobilization with ifosfamide and etoposide | Cumulative incidence of SM was 11% in the entire cohort, with 13 cases of MDS/AML, 5 non-melanoma skin cancers, 1 prostate cancer, 1 MPN, 1 sarcoma. The incidence of SM was significantly higher in pts aged >55 years at diagnosis, even after exclusion of second skin cancers. Time from initial diagnosis to transplantation and exposure to RT were not significant predictors of SM in the study population. MOPP, which was frontline CT in 20 patients, all of whom were <55 years of age, was associated with higher incidence of SM compared with ABVD. |
Sibon D, 2016 [33] | Retrospective cohort study (245 patients with relapsed/refractory cHL) | Poor risk: tandem ASCT; other patients single ASCT with BEAM conditioning | Sixteen SM occurred. The 10- and 15-year cumulative incidences of SM were 8% and 15%, respectively; the 10-year cumulative incidences of SM were 15% in intermediate-risk patients and 1.5% in poor-risk patients. Considering only patients who did not relapse after completing ASCT, the 10- and 15-year cumulative incidences of SM were 9% and 13%, respectively; the 10- and 15-year cumulative incidences of SM were 16% and 24%, respectively, for the intermediate-risk patients and 2% and 2% for the poor-risk patients. |
Minn AY, 2012 [34] | Retrospective cohort study (154 patients with relapsed/refractory cHL) | Etoposide + cyclophosmamide with TBI or carmustin or lomustin | There were 20 SM, 18 occurring more than 2 years from ASCT. The 5-, 10-, and 15-year cumulative incidence of SM was 5%, 8%, and 12%, respectively. AER was 160 per 10,000 PY of follow-up. The risk of SM compared with patients with cHL in the SEER registry was not elevated 5–10 years after ASCT, but was higher 2–5 and >10 years after ASCT. The overall risk of SM was 3.0 compared with cHL patients from SEER with an AER of 123 per 10,000 PY of follow-up. Overall risk of SM among patients receiving ASCT was not elevated compared with the non-ASCT population at Stanford. |
Tarella C, 2011 [35] | Retrospective cohort study (234 patients with relapsed/refractory cHL; 569 patients with high-risk DLBCL in first line or relapsed/refractory DLBCL) | High-dose sequential chemotherapy | The cumulative incidence of MDS/AML in cHL at 5-, 10, and 15-years was 4.1%, 5%, and 15%, respectively, while the cumulative incidence of solid SM was 1.8, 5.5, and 6.9%, respectively. Risk analyses for MDS/AML and solid SM were performed for the whole populations and not for cHL patients only. The overall SIR for MDS/AML was 2.6, with a significantly higher risk for patients aged younger than 45 years (SIR 7.2) and 45 to 65 years of age (SIR 2.1) compared to the age-matched Italian population. Overall, the SIR for solid SM was 3.2; again, increased risk compared to the Italian population was documented for patients aged younger than 45 years (SIR 7.6) and 45 to 65 years of age (SIR 2.7). |
Franklin J, 2017 [36] | Systematic review (9498 patients with cHL in first line) | Different therapies including CT and RT | In patients treated with CT the omission of additional RT probably reduces SM incidence, corresponding to an estimated reduction of 8-year SM risk from 8% to 4%. The authors observed that the decrease would be particularly true for AML. The authors investigated the role of the number of CT courses, which probably has little or no effect on SM risk, and the role of intensified CT in patients with advanced stage disease, with insufficient evidence to determine the effect on SM. In patients who received intensified CT, the rate of secondary AML (and for younger patients, all SM) was probably higher than in patients treated with standard-dose ABVD-like protocols. |
PICO 2 | |||
Patel CG, 2018 [37] | Retrospective cohort study (1541 patients with early stage cHL in first line) | IFRT or EFRT | A trend of lower risk of death from SM in more recently-treated patients (smaller fields) was observed, though this did not reach statistical significance, likely due to the small number of events within each treatment era. |
LeMieux MH, 2015 [38] | Retrospective cohort study (8807 patients with early stage cHL in first line) | IFRT or EFRT | The authors suggests that patients treated with RT prior to 2000 (larger fields) had a slightly higher risk of SM compared to treatment in 2000 and later. |
Schaapveld M, 2015 [27] | Retrospective cohort study (3905 patients with cHL in first line) | CT and/or RT | Patients who received supradiaphragmatic RT not including the axilla had a lower risk of a solid SM than those who received complete mantle-field RT, largely due to a lower risk of breast cancer. |
De Bruin ML, 2009 [39] | Retrospective cohort study (1022 female patients with cHL in first line) | Mantle field RT or smaller field RT | Mantle field RT (involving the axillary, mediastinal, and neck nodes) was associated with a 2.7-fold increased risk compared with similarly dosed (36 to 44 Gy) mediastinal RT alone. |
Conway JL, 2017 [40] | Retrospective cohort study (734 patients with cHL in first line) | Mantle field RT or smaller field RT | The 20-year cumulative incidences for secondary breast cancer, after accounting for death and loss to follow-up as competing risks, were 7.5% in mantle field and 3.1% in smaller field RT, compared to 2% in CT only. |
Franklin J, 2017 [36] | Systematic review (9498 patients with cHL in first line) | Different therapies including CT and RT | There is insufficient evidence to determine whether smaller radiation field reduces SM risk and the impact on OS and PFS, with the bias of a too short follow-up of the included studies to record the occurrence of solid tumors. |
Franklin J, 2005 [41] | Systematic review (9312 patients with cHL in first line) | Different therapies including CT and RT | No difference in second tumor incidence between EFRT and IFRT. |
PICO 3 | |||
Diller L, 2002 [42] | Prospective cohort study (90 partecipating out of 167 patients with cHL treated with RT) | Mx | Ten out of 90 women had a breast cancer, 8 unilateral and 2 bilateral cancer. All cancers were detectable with Mx. Most of the tumors were small and without evidence of nodal involvement. Nine non-breast cancers have developed in members of this cohort during the follow-up period. Screening by Mx can detect small, node-negative breast cancers in these patients. Multivariate analysis revealed that older patients who understood that they were at high risk and received risk information from an oncologist were seven times more likely than patients without this profile to have had a mammogram in the previous 2 years |
Kwong A, 2008 [43] | Randomized trial (167 responding out of 297 patients with cHL treated with RT) | Early vs. late telephone counseling | Completion of Mx during the period of the study was reported by 115 of the 167 subjects: 99 Mx were reviewed, 17 recalled; 7 of the 17 women with abnormal Mx were recommended for biopsy. Four out of 115 (3.5%) women who reported completion of Mx (3.5%) were diagnosed with DCIS and two of these had, at least, microscopic evidence for invasive cancer. Three of these patients were diagnosed solely because of calcifications observed on mammography. In the fourth, mammography confirmed suspicious findings noted on self-examination and professional clinical examination. |
Lee L, 2008 [44] | Prospective cohort study (100 responding out of 360 patients with cHL treated with RT) | Clinical exam and Mx | Twelve of the 100 participating women (12%) were diagnosed with breast cancer after a median of 5 years of surveillance. Seven cancers presented as palpable masses (six invasive, one DCIS), five were detected by Mx (one invasive, four DCIS). Screening Mx may be effective at detecting DCIS, but may be inadequate for early invasive BC detection in this high-risk population. Evaluation of more intensive screening and the contribution of MRI for earlier detection is warranted. |
Howell SJ, 2009 [45] | Report of screening (243 screening reports in patients with cHL treated with RT) | No imaging or breast MRI/US or Mx/US or Mx | Of 417 women, 23 (5.5%) have been diagnosed with breast cancer. Five of them were diagnosed within the screening program, none of them involved axillary lymph nodes compared with 7 of 13 (54%) diagnosed outside the program. |
Elkin EB, 2011 [46] | Observational case-control study (253 patients with cHL treated with RT matched 741 breast cancer patients with no history of cHL) | Various surveillance methods | cHL survivors were more likely to have breast cancer detected by screening Mx (40% vs. 33%), were more likely to be diagnosed at an earlier stage (61% vs. 42%), were less likely to have axillary lymphnode involvement (25% vs. 39%), and were more likely to present with bilateral disease (6% vs. 2%). |
Mariscotti G, 2013 [47] | Retrospective cohort trial (54 patients with cHL treated with RT) | Clinical exam/US or clinical exam/US/Mx | The authors concluded that patients treated with RT have a higher risk of developing breast cancer and that they need to undergo adequate breast surveillance protocols. They suggested to use of MRI in patients ≤30 years of age and as a complementary method to US/Mx in patients >30, as suggested for women with BRCA mutations. |
Ng AK, 2013 [48] | Prospective cohort study (148 patients with cHL treated with RT) | MRI and Mx surveillance | The overall sensitivity of Mx for breast cancer detection was 68%, as compared with 67% for breast MRI. The use of both screening modalities increased the sensitivity to 94% |
Monitoring strategies should be individualized, depending on RT dose, type of CT regimen, age at therapy, and predisposing factors (family history, sex, behavioral risk factors). |
No evidence of screening programs for DLBCL survivors, |
Breast cancer: for patients treated with >10 Gy RT on the chest: start at age 40 or 8 years after RT, whichever comes first, by annual Mx, add annual breast MRI for women who received chest RT between ages 10–30 years. |
Lung cancer: annual chest LDCT scan for smokers treated with alkylators/RT. |
Skin cancer: annual skin evaluation of the irradiated skin areas. |
Thyroid cancer: neck ultra-sound for pts treated with neck RT. |
Colorectal cancer: annual FOB and colonoscopy every 10 years (based on findings) for pts treated with abdominal RT (≥20 Gy), starting from the age of 30 years or 5 years after RT. |
MDS/AML: annual blood cell count evaluation. |
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Nassi, L.; De Sanctis, V.; Loseto, G.; Gerardi, C.; Allocati, E.; Ciavarella, S.; Minoia, C.; Guarini, A.; Bari, A. Second Cancers in Classical Hodgkin Lymphoma and Diffuse Large B-Cell Lymphoma: A Systematic Review by the Fondazione Italiana Linfomi. Cancers 2022, 14, 519. https://doi.org/10.3390/cancers14030519
Nassi L, De Sanctis V, Loseto G, Gerardi C, Allocati E, Ciavarella S, Minoia C, Guarini A, Bari A. Second Cancers in Classical Hodgkin Lymphoma and Diffuse Large B-Cell Lymphoma: A Systematic Review by the Fondazione Italiana Linfomi. Cancers. 2022; 14(3):519. https://doi.org/10.3390/cancers14030519
Chicago/Turabian StyleNassi, Luca, Vitaliana De Sanctis, Giacomo Loseto, Chiara Gerardi, Eleonora Allocati, Sabino Ciavarella, Carla Minoia, Attilio Guarini, and Alessia Bari. 2022. "Second Cancers in Classical Hodgkin Lymphoma and Diffuse Large B-Cell Lymphoma: A Systematic Review by the Fondazione Italiana Linfomi" Cancers 14, no. 3: 519. https://doi.org/10.3390/cancers14030519