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Open Access

Stage migration of testicular germ cell tumours in Alberta, Canada, during the COVID-19 pandemic: a retrospective cohort study

Richard Lee-Ying, Dylan E. O’Sullivan, Richard Gagnon, Nicholas Bosma, Rebecca N. Stewart, Cindy Railton, Derek Tilley, Nimira Alimohamed, Naveen Basappa, Tina Cheng, Michael Kolinsky, Safiya Karim, Dean Ruether, Scott North, Steven Yip, Brita Danielson, Daniel Heng and Darren Brenner
July 05, 2022 10 (3) E633-E642; DOI: https://doi.org/10.9778/cmajo.20210285
Richard Lee-Ying
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Dylan E. O’Sullivan
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Richard Gagnon
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Nicholas Bosma
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Rebecca N. Stewart
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Cindy Railton
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Derek Tilley
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Nimira Alimohamed
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Naveen Basappa
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Tina Cheng
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Michael Kolinsky
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Safiya Karim
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Dean Ruether
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Scott North
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Steven Yip
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Brita Danielson
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Daniel Heng
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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Darren Brenner
Department of Oncology (Lee-Ying, O’Sullivan, Gagnon, Stewart, Railton, Tilley, Alimohamed, Cheng, Karim, Ruether, Yip, Heng, Brenner), University of Calgary, Tom Baker Cancer Centre, Calgary, Alta.; BC Cancer Agency–Victoria (Bosma), Victoria, BC; Department of Oncology (Basappa, Kolinsky, North, Danielson), University of Alberta, Cross Cancer Institute, Edmonton, Alta.
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  • Figure 1:
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    Figure 1:

    Changes in 3-month incidence of testicular cancer overall, by stage and for stage III before and during the COVID-19 pandemic in Alberta. The black dotted line represents the first 3-month period of the COVID-19 pandemic in our study. (A) Incidence of testicular cancer overall and by stage for each 3-month time period. (B) Proportion of stage III testicular cancers diagnosed for each 3-month period. Note: the first and last periods have been standardized to a 3-month incidence.

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    Figure 2:

    Changes in 3-month incidence of pure seminoma and nonseminoma testicular cancers by stage and for stage III, before and during the COVID-19 pandemic in Alberta. The first black dotted line represents the first 3-month period of the COVID-19 pandemic in our study. The second black dotted line indicates the period with the 6-month lag time for seminomas. (A) Incidence of pure seminoma testicular cancer by stage for each 3-month period. (B) Proportion of stage III pure seminoma testicular cancers diagnosed for each 3-month period. (C) Incidence of nonseminoma testicular cancer by stage for each 3-month period. (D) Proportion of stage III nonseminoma testicular cancers diagnosed for each 3-month period. Note: the first and last periods have been standardized to a 3-month incidence.

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    Figure 3:

    Monthly proportion of testicular germ cell tumours by stage. (A) All cases; time 0 (solid line) represents Apr. 1, 2020, the beginning of the pandemic in Alberta in our study; the dashed line represents the 3-month lag time for nonseminomas and the dotted line represents the 6-month lag time for seminomas. (B) Seminomas; time 0 (solid line) incorporates a 6-month lag time (Oct. 1, 2020). (C) Nonseminomas; time 0 (solid line) incorporates a 3-month lag time (July 1, 2020).

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    Table 1:

    Baseline patient and presentation characteristics stratified by histology

    CharacteristicNo. (%)*
    Seminoma
    n = 192
    Nonseminoma
    n = 143
    Age, yr, mean ± SD38.5 ± 14.532.5 ± 11.9
    Histology
     Seminoma192 (100.0)55 (38.5)
     Embryonal–102 (71.3)
     Yolk sac–69 (48.3)
     Choriocarcinoma–20 (14.0)
     Teratoma–74 (51.7)
     Other–20 (14.0)
    pT stage
     1122 (63.5)70 (48.9)
     2+66 (34.4)52 (36.4)
     0 or unknown4 (2.1)21 (14.7)
    cN stage
     0159 (82.8)92 (64.3)
     111 (5.7)11 (7.7)
     211 (5.7)19 (13.3)
     311 (5.7)21 (14.7)
    M stage
     0185 (96.4)120 (83.9)
     17 (3.6)23 (16.1)
    Cancer stage
     I159 (82.8)88 (61.5)
     II26 (13.5)28 (19.6)
     III7 (3.7)27 (18.9)
    Treatment location
     Tom Baker Cancer Centre68 (35.4)53 (37.1)
     Cross Cancer Institute80 (41.7)60 (41.9)
     Other44 (22.9)30 (21.0)
    Orchiectomy188 (97.9)130 (90.9)
    Radiation therapy10 (5.2)1 (0.7)
    Systemic therapy22 (11.5)51 (35.7)
    • Note: cN = node (clinical), M = metastasis, pT = tumour (pathological), SD = standard deviation, TGCT = testicular germ cell tumour.

    • ↵* Unless otherwise indicated.

    • View popup
    Table 2:

    Differences in staging, systemic therapy setting, largest tumour dimension and pre-orchiectomy markers before and during the COVID-19 pandemic

    VariableNo. (%)*p value
    Before pandemic†
    n = 231
    During pandemic
    n = 104
    Cancer stage0.002¶
     I166 (71.9)81 (77.9)
     II47 (20.3)7 (6.7)
     III18 (7.8)16 (15.4)
    IGCCC risk category‡0.07**
     Good52 (80.0)13 (56.5)
     Intermediate6 (9.2)5 (21.7)
     Poor7 (10.7)5 (21.7)
    Systemic therapy setting§0.1**
     Outpatient44 (78.5)13 (61.9)
     Inpatient or ICU12 (21.4)8 (38.1)
    Largest tumour dimension, cm0.06††
     Mean ± SD4.5 ± 3.65.1 ± 4.1
     Median (IQR)3.6 (2.4–5.5)4.2 (3.1–6)
     No. missing records1 (0.4)0 (0)
    Pre-orchiectomy LDH, U/L0.1††
     Mean ± SD288 ± 358278 ± 476
     Median (25th–75th percentiles)198 (170–279)192 (167–237)
     No. missing records49 (21.2)20 (19.2)
    Pre-orchiectomy β-HCG, IU/L0.4††
     Median (25th–75th percentiles)5 (1.0–13.8)5 (0.5–20.0)
     No. missing records17 (7.4)9 (8.7)
    Pre-orchiectomy AFP, ng/mL0.1††
     Median (25th–75th percentiles)3.6 (2.0–6.4)3 (2.0–6.0)
     No. missing records18 (7.8)7 (6.7)
    • Note: AFP = α fetoprotein, HCG = human chorionic gonadotropin, ICU = intensive care unit, IGCCC = International Germ Cell Consensus Classification, IQR = interquartile range, LDH = lactate dehydrogenase, SD = standard deviation, TGCT = testicular germ cell tumour.

    • ↵* Unless otherwise indicated.

    • ↵† Includes a 6-month lag period for seminomas and a 3-month lag period for nonseminomas.

    • ↵‡ IGCCC risk category was applicable only to stage II and stage III patients before (n = 65) and during (n = 23) the pandemic.

    • ↵§ Systemic therapy setting was applicable only to patients who received systemic treatment before (n = 56) and during (n = 21) the pandemic.

    • ↵¶ χ2 test.

    • ↵** Fisher exact test.

    • ↵†† Wilcoxon rank sum test.

    • View popup
    Table 3:

    Monthly incidence of TGCTs before and during the pandemic*

    VariableMonthly incidenceRate ratio (95% CI)
    Before pandemicDuring pandemic
    Overall11.6910.430.89 (0.72–1.11)
     Stage I8.138.211.01 (0.79–1.30)
     Stage II2.51.000.40 (0.21–0.72)
     Stage III1.061.211.14 (0.58–2.26)
    Nonseminoma5.563.790.68 (0.48–0.95)
     Stage I3.252.500.77 (0.50–1.18)
     Stage II1.380.430.32 (0.12–0.74)
     Stage III0.940.860.92 (0.52–1.97)
    Seminoma6.136.641.08 (0.82–1.44)
     Stage I4.885.711.17 (0.86–1.60)
     Stage II1.130.570.51 (0.21–1.15)
     Stage III0.130.362.74 (0.56–21.26)
    • Note: CI = confidence interval, TGCT = testicular germ cell tumour.

    • ↵* Using Apr. 1, 2020, as the pandemic cut-off (without lag time).

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Stage migration of testicular germ cell tumours in Alberta, Canada, during the COVID-19 pandemic: a retrospective cohort study
Richard Lee-Ying, Dylan E. O’Sullivan, Richard Gagnon, Nicholas Bosma, Rebecca N. Stewart, Cindy Railton, Derek Tilley, Nimira Alimohamed, Naveen Basappa, Tina Cheng, Michael Kolinsky, Safiya Karim, Dean Ruether, Scott North, Steven Yip, Brita Danielson, Daniel Heng, Darren Brenner
Jul 2022, 10 (3) E633-E642; DOI: 10.9778/cmajo.20210285

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Stage migration of testicular germ cell tumours in Alberta, Canada, during the COVID-19 pandemic: a retrospective cohort study
Richard Lee-Ying, Dylan E. O’Sullivan, Richard Gagnon, Nicholas Bosma, Rebecca N. Stewart, Cindy Railton, Derek Tilley, Nimira Alimohamed, Naveen Basappa, Tina Cheng, Michael Kolinsky, Safiya Karim, Dean Ruether, Scott North, Steven Yip, Brita Danielson, Daniel Heng, Darren Brenner
Jul 2022, 10 (3) E633-E642; DOI: 10.9778/cmajo.20210285
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