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Journal Metrics Reports 2022
Oncology & hematology, announcement of the latest impact factors from the journal citation reports.
Researchers consider a number of factors in deciding where to publish their research, such as journal reputation, readership and community, speed of publication, and citations. See how we share a whole range of information to help the research community decide which journal is the best home for their research as well as what the metrics can tell you about the performance of a journal and its articles.
Explore journal impact metrics
Journal of Gastrointestinal Cancer
Impact Factor 1.6 (2022)
5 Year Impact Factor 1.5 (2022)
Cite Score 3.3 (2022)
H5 Index 24 (2021)
Social Media Mentions 357 (2022)
Downloads 186,941 (2022)
Current Breast Cancer Reports
Impact Factor 0.9 (2022)
5 Year Impact Factor 1.2 (2022)
Cite Score 1.5 (2022)
H5 Index 14 (2021)
Social Media Mentions 159 (2022)
Downloads 57,411 (2022)
International Cancer Conference Journal
Impact Factor 0.7 (2022)
5 Year Impact Factor 0.7 (2022)
H5 Index 8 (2021)
Social Media Mentions 54 (2022)
Downloads 55,304 (2022)
Indian Journal of Gynecologic Oncology
Impact Factor 0.4 (2022)
5 Year Impact Factor 0.3 (2022)
Cite Score 0.5 (2022)
H5 Index 7 (2021)
Social Media Mentions 42 (2022)
Downloads 34,901 (2022)
Journal of the Egyptian National Cancer Institute
Impact Factor 1.8 (2022)
5 Year Impact Factor 1.7 (2022)
Cite Score 2.2 (2022)
Social Media Mentions 100 (2022)
Downloads 189,097 (2022)
Cancer Immunology, Immunotherapy
Impact Factor 5.8 (2022)
5 Year Impact Factor 6.1 (2022)
Cite Score 11.3 (2022)
H5 Index 61 (2021)
Social Media Mentions 8,073 (2022)
Downloads 1,037,346 (2022)
Journal of Cancer Research and Clinical Oncology
Impact Factor 3.6 (2022)
5 Year Impact Factor 3.8 (2022)
Cite Score 7.6 (2022)
H5 Index 51 (2021)
Social Media Mentions 3,907 (2022)
Downloads 1,066,225 (2022)
Breast Cancer Research and Treatment
Impact Factor 3.8 (2022)
5 Year Impact Factor 4.4 (2022)
Cite Score 7.5 (2022)
H5 Index 71 (2021)
Social Media Mentions 7,695 (2022)
Downloads 1,371,724 (2022)
Annals of Surgical Oncology
Impact Factor 3.7 (2022)
Cite Score 5.5 (2022)
H5 Index 70 (2021)
Social Media Mentions 14,310 (2022)
Downloads 1,994,115 (2022)
Indian Journal of Hematology and Blood Transfusion
5 Year Impact Factor 1.0 (2022)
Cite Score 1.4 (2022)
H5 Index 16 (2021)
Social Media Mentions 4,261 (2022)
Downloads 114,733 (2022)
Journal of Hematopathology
Impact Factor 0.6 (2022)
5 Year Impact Factor 0.6 (2022)
Cite Score 0.7 (2022)
H5 Index 6 (2021)
Social Media Mentions 191 (2022)
Downloads 146,240 (2022)
Current Hematologic Malignancy Reports
Impact Factor 2.9 (2022)
5 Year Impact Factor 3.0 (2022)
Cite Score 6.8 (2022)
H5 Index 31 (2021)
Social Media Mentions 2,157 (2022)
Downloads 151,698 (2022)
Journal of Mammary Gland Biology and Neoplasia
Impact Factor 2.5 (2022)
5 Year Impact Factor 2.8 (2022)
Cite Score 4.7 (2022)
H5 Index 18 (2021)
Social Media Mentions 493 (2022)
Downloads 159,286 (2022)
Supportive Care in Cancer
Impact Factor 3.1 (2022)
5 Year Impact Factor 3.5 (2022)
Cite Score 5.1 (2022)
H5 Index 63 (2021)
Social Media Mentions 9,764 (2022)
Downloads 2,059,631 (2022)
Targeted Oncology
Impact Factor 5.4 (2022)
5 Year Impact Factor 4.8 (2022)
Cite Score 8.8 (2022)
H5 Index 36 (2021)
Social Media Mentions 652 (2022)
Downloads 211,326 (2022)
Discover Oncology
Impact Factor 3.0 (2022)
5 Year Impact Factor 3.2 (2022)
Cite Score 2.6 (2022)
H5 Index 22 (2021)
Social Media Mentions 267 (2022)
Downloads 347,934 (2022)
Current Treatment Options in Oncology
Impact Factor 4.3 (2022)
Cite Score 7.8 (2022)
H5 Index 43 (2021)
Social Media Mentions 903 (2022)
Downloads 364,029 (2022)
Investigational New Drugs
Impact Factor 3.4 (2022)
H5 Index 37 (2021)
Social Media Mentions 2,195 (2022)
Downloads 400,671 (2022)
International Journal of Clinical Oncology
Impact Factor 3.3 (2022)
5 Year Impact Factor 3.3 (2022)
Cite Score 6.0 (2022)
H5 Index 39 (2021)
Social Media Mentions 2,566 (2022)
Downloads 448,702 (2022)
Medical Oncology
Cite Score 4.2 (2022)
H5 Index 42 (2021)
Social Media Mentions 1,337 (2022)
Downloads 474,847 (2022)
Current Oncology Reports
Impact Factor 4.7 (2022)
5 Year Impact Factor 5.1 (2022)
Cite Score 8.4 (2022)
H5 Index 46 (2021)
Social Media Mentions 1,602 (2022)
Downloads 496,146 (2022)
Breast Cancer
Impact Factor 4.0 (2022)
Cite Score 5.6 (2022)
Social Media Mentions 447 (2022)
Downloads 500,362 (2022)
International Journal of Hematology
Impact Factor 2.1 (2022)
5 Year Impact Factor 2.1 (2022)
Cite Score 3.7 (2022)
Social Media Mentions 5,550 (2022)
Downloads 552,571 (2022)
Clinical and Translational Oncology
5 Year Impact Factor 3.1 (2022)
Cite Score 6.2 (2022)
H5 Index 40 (2021)
Social Media Mentions 2,829 (2022)
Downloads 555,651 (2022)
Cancer Chemotherapy and Pharmacology
Social Media Mentions 3,342 (2022)
Downloads 657,709 (2022)
Gastric Cancer
Impact Factor 7.4 (2022)
5 Year Impact Factor 7.5 (2022)
Cite Score 13.9 (2022)
H5 Index 55 (2021)
Social Media Mentions 368 (2022)
Downloads 729,426 (2022)
Journal of Neuro-Oncology
Impact Factor 3.9 (2022)
5 Year Impact Factor 4.1 (2022)
Cite Score 7.3 (2022)
H5 Index 57 (2021)
Social Media Mentions 5,208 (2022)
Downloads 789,310 (2022)
Annals of Hematology
Impact Factor 3.5 (2022)
Social Media Mentions 3,689 (2022)
Downloads 825,621 (2022)
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Index and ranking
Journal of Cancer is indexed in Science Citation Index (SCI) Expanded, PubMed, PubMed Central, Essential Science Indicators, Scopus, and Google Scholar. Full texts appear in PubMed Central and Europe PMC.
Impact factor is 3.9, according to the Journal Citation Reports ® released in 2023.
Impact factor is 4.478, according to the Journal Citation Reports ® released in 2022.
Impact factor is 4.207, according to the Journal Citation Reports ® released in 2021.
Impact factor is 3.565, according to the Journal Citation Reports ® released in 2020.
Impact factor is 3.182, according to the Journal Citation Reports ® released in 2019.
©2024 Ivyspring International Publisher . Terms of use
- Journal of Clinical Oncology
Journal Abbreviation: J CLIN ONCOL Journal ISSN: 0732-183X
| Year | Impact Factor (IF) | Total Articles | Total Cites |
| 2023 (2024 update) | 42.1 | 464 | 169257 |
| 2022 | 45.3 | - | 180328 |
| 2021 | 50.717 | - | 195709 |
| 2020 | 44.544 | 339 | 189443 |
| 2019 | 32.956 | 285 | 155297 |
| 2018 | 28.245 | 356 | 154029 |
| 2017 | 26.303 | 400 | 156474 |
| 2016 | 24.008 | 478 | 149617 |
| 2015 | 20.982 | 493 | 141362 |
| 2014 | 18.428 | 466 | 133258 |
| 2013 | 17.879 | 627 | 130991 |
| 2012 | 18.038 | 597 | 128679 |
| 2011 | 18.372 | 729 | 120262 |
| 2010 | 18.970 | 784 | 114318 |
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Journal of Thoracic Oncology 2023 Impact Factor Increases Over Rating in 2022; JTO Clinical and Research Reports Off to a Strong Start
Contact: Chris Martin, IASLC Media Relations | [email protected]
(DENVER – June 27, 2024) — The International Association for the Study of Lung Cancer (IASLC) today reported that its main cancer journal, the Journal of Thoracic Oncology (JTO), improved its Impact Factor to 21.0 in 2023, up from 20.1 in 2022. The JTO , the official journal of the IASLC, now ranks second among 100 respiratory medicine journals and 13th among 322 oncology journals.
The JTO Clinical and Research Reports received its first Impact Factor of 3.0, ranking 142 out of 322 oncology journals and 37 out of 100 among respiratory journals. JTO Clinical and Research Reports (JTO CRR) is the official open-access journal of the International Association for the Study of Lung Cancer.
Impact Factors are measured by calculating the number of times journal articles in the two preceding years are cited in a current year. Thus, the 2023 Impact Factor released in 2024 is the number of times articles published in 2021 and 2022 are cited in 2023. The higher the Impact Factor, the more highly ranked the journal. Journal citation reports are issued by Clarivate Analytics.
The JTO is the primary educational publication for topics relevant to the prevention, detection, diagnosis, and treatment of all thoracic malignancies. Emphasizing a multidisciplinary approach, the JTO includes original research, review articles, and opinion pieces. The audience includes epidemiologists, medical oncologists, radiation oncologists, thoracic surgeons, pulmonologists, radiologists, pathologists, and basic scientists with a special interest in thoracic oncology.
"JTO's impact factor for 2023 has risen to 21, making it only the second respiratory journal (after Lancet Respiratory Medicine ) with an impact factor above 20," said Alex A. Adjei, MD, PhD, FACP, Editor-in-Chief of JTO . "More importantly, it is the only thoracic oncology journal with an impact factor greater than 10. This is a notable achievement since we are a sub-specialty journal dealing with only thoracic oncology. There are no other sub-specialty journals among the top 20 oncology journals, and we now rank 13th out of 322 oncology journals. This achievement is a testament to the exemplary work of our editorial board and our editorial office, as well as the support of IASLC—its executives, office staff, membership, and above all, our reviewers, readers, and authors. JTO will continue its emphasis on multidisciplinary research to serve the broad community working in thoracic oncology."
As the companion journal of the JTO , JTO CRR provides a publication hub within the IASLC for research with a more clinical focus and for article types such as case reports, phase 1 and 2 trials, high-impact retrospective studies, and database analyses. The journal offers a gold open-access publication option, which ensures immediate and permanently free access to quality lung cancer studies by everyone.
"The JTO CRR team is celebrating our first impact factor at 3.0, and we wish to thank everyone who made it possible—the authors, reviewers, editors, and the IASLC. We are thrilled to make such a terrific start, which truly reflects our commitment to excellence in science," said Emily Stone, MBBS, PhD, FRACP, and Editor-in-Chief of JTO CRR .
To submit a manuscript or to learn more about the JTO , please visit jto.org . Once there, you can peruse current in-press articles, collections of articles such as the Ninth Edition of TNM Stage Classification of Thoracic Tumors , Controversies in Thoracic Oncology , Lung Cancer Worldwide , and the freely available Editor's Choice articles. The complete contents of the JTO are free for IASLC members. Visit jtocrr.org to learn more.
About the IASLC
The International Association for the Study of Lung Cancer (IASLC) is the only global organization dedicated solely to the study of lung cancer and other thoracic malignancies. Founded in 1974, the association's membership includes more than 11,000 lung cancer specialists across all disciplines in over 100 countries, forming a global network working together to conquer lung and thoracic cancers worldwide. The association publishes the Journal of Thoracic Oncology , the primary educational and informational publication for topics relevant to the prevention, detection, diagnosis, and treatment of all thoracic malignancies. Visit www.iaslc.org for more information.
About the JTO
Journal of Thoracic Oncology ( JTO ), the official journal of the International Association for the Study of Lung Cancer, is the primary educational and informational publication for topics relevant to the prevention, detection, diagnosis, and treatment of all thoracic malignancies. JTO emphasizes a multidisciplinary approach and includes original research reviews and opinion pieces. The audience includes epidemiologists, medical oncologists, radiation oncologists, thoracic surgeons, pulmonologists, radiologists, pathologists, nuclear medicine physicians, and research scientists with a special interest in thoracic oncology.
About the JTO CRR
JTO Clinical and Research Reports is the official open-access journal of the International Association for the Study of Lung Cancer. It aims to complement the Journal of Thoracic Oncology by offering authors a gold open-access publication option and publishing the following article types in particular: phase I trials, well-performed single-arm phase II trials, subset analyses of published trials, impactful retrospective studies, database analysis, large institutional series, high-quality case reports, region-specific clinical trials, subspecialty thoracic oncology studies and selected high-quality meeting reports.
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| Title | Type | --> | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | journal | 106.094 Q1 | 211 | 49 | 124 | 4844 | 35427 | 89 | 381.89 | 98.86 | 43.95 | ||
| 2 | journal | 26.837 Q1 | 505 | 105 | 304 | 10805 | 10951 | 163 | 31.23 | 102.90 | 44.33 | ||
| 3 | journal | 21.048 Q1 | 217 | 127 | 400 | 9888 | 10807 | 183 | 28.36 | 77.86 | 38.85 | ||
| 4 | journal | 17.507 Q1 | 398 | 178 | 590 | 11546 | 12604 | 360 | 19.83 | 64.87 | 41.91 | ||
| 5 | journal | 13.942 Q1 | 294 | 144 | 670 | 5180 | 12698 | 362 | 18.81 | 35.97 | 39.02 | ||
| 6 | journal | 12.179 Q1 | 408 | 393 | 1455 | 5354 | 17873 | 634 | 11.39 | 13.62 | 42.77 | ||
| 7 | journal | 11.900 Q1 | 61 | 176 | 453 | 7513 | 5933 | 297 | 12.27 | 42.69 | 43.45 | ||
| 8 | journal | 10.639 Q1 | 624 | 783 | 1664 | 20976 | 26011 | 1205 | 13.64 | 26.79 | 41.81 | ||
| 9 | journal | 8.222 Q1 | 196 | 190 | 525 | 23895 | 14728 | 449 | 23.31 | 125.76 | 38.33 | ||
| 10 | journal | 7.879 Q1 | 178 | 266 | 803 | 6857 | 7329 | 395 | 9.53 | 25.78 | 39.88 | ||
| 11 | journal | 7.843 Q1 | 173 | 349 | 1225 | 6132 | 9916 | 523 | 7.62 | 17.57 | 39.66 | ||
| 12 | journal | 7.533 Q1 | 229 | 341 | 1297 | 8166 | 13169 | 986 | 10.13 | 23.95 | 41.52 | ||
| 13 | journal | 7.522 Q1 | 144 | 115 | 531 | 11441 | 12065 | 413 | 20.83 | 99.49 | 40.48 | ||
| 14 | journal | 6.348 Q1 | 163 | 229 | 779 | 6987 | 7925 | 489 | 11.64 | 30.51 | 45.08 | ||
| 15 | journal | 4.986 Q1 | 387 | 211 | 719 | 2601 | 4647 | 510 | 6.60 | 12.33 | 50.21 | ||
| 16 | journal | 4.955 Q1 | 44 | 226 | 490 | 6752 | 3985 | 269 | 8.13 | 29.88 | 49.94 | ||
| 17 | journal | 4.950 Q1 | 79 | 108 | 289 | 4873 | 3552 | 176 | 12.39 | 45.12 | 40.77 | ||
| 18 | journal | 4.665 Q1 | 132 | 74 | 76 | 6493 | 1477 | 75 | 17.53 | 87.74 | 34.58 | ||
| 19 | journal | 4.640 Q1 | 25 | 42 | 128 | 1802 | 959 | 125 | 8.13 | 42.90 | 35.32 | ||
| 20 | journal | 4.623 Q1 | 377 | 541 | 2035 | 19863 | 19126 | 1944 | 9.00 | 36.72 | 43.31 | ||
| 21 | journal | 4.513 Q1 | 90 | 111 | 338 | 7747 | 3828 | 324 | 9.71 | 69.79 | 40.00 | ||
| 22 | journal | 4.102 Q1 | 150 | 200 | 611 | 7359 | 6158 | 523 | 10.66 | 36.80 | 49.36 | ||
| 23 | journal | 3.974 Q1 | 76 | 186 | 488 | 5144 | 3636 | 298 | 7.48 | 27.66 | 40.68 | ||
| 24 | book series | 3.766 Q1 | 36 | 18 | 61 | 2133 | 423 | 61 | 5.00 | 118.50 | 38.18 | ||
| 25 | journal | 3.728 Q1 | 117 | 445 | 1590 | 19408 | 14743 | 1571 | 8.71 | 43.61 | 42.99 | ||
| 26 | journal | 3.667 Q1 | 164 | 87 | 305 | 7857 | 3415 | 301 | 9.74 | 90.31 | 40.97 | ||
| 27 | journal | 3.662 Q1 | 219 | 333 | 1125 | 11784 | 8477 | 975 | 7.59 | 35.39 | 43.05 | ||
| 28 | journal | 3.599 Q1 | 56 | 62 | 169 | 2562 | 1854 | 139 | 11.14 | 41.32 | 26.84 | ||
| 29 | journal | 3.468 Q1 | 498 | 331 | 1449 | 13630 | 12019 | 1431 | 8.08 | 41.18 | 42.61 | ||
| 30 | journal | 3.000 Q1 | 272 | 448 | 1331 | 22747 | 10155 | 1182 | 7.28 | 50.77 | 43.44 | ||
| 31 | journal | 2.928 Q1 | 9 | 43 | 57 | 1993 | 754 | 52 | 13.23 | 46.35 | 40.22 | ||
| 32 | journal | 2.887 Q1 | 340 | 502 | 1845 | 15437 | 8867 | 1286 | 4.35 | 30.75 | 47.18 | ||
| 33 | journal | 2.880 Q1 | 34 | 126 | 343 | 3325 | 1628 | 196 | 5.10 | 26.39 | 39.67 | ||
| 34 | journal | 2.871 Q1 | 36 | 134 | 227 | 7435 | 1667 | 224 | 6.48 | 55.49 | 38.35 | ||
| 35 | journal | 2.866 Q1 | 167 | 85 | 214 | 14862 | 1880 | 192 | 6.96 | 174.85 | 42.18 | ||
| 36 | journal | 2.838 Q1 | 159 | 155 | 390 | 26605 | 4360 | 387 | 10.09 | 171.65 | 45.66 | ||
| 37 | journal | 2.806 Q1 | 120 | 307 | 943 | 18917 | 9710 | 940 | 9.65 | 61.62 | 46.70 | ||
| 38 | journal | 2.719 Q1 | 45 | 81 | 360 | 0 | 2052 | 265 | 5.80 | 0.00 | 26.62 | ||
| 39 | journal | 2.595 Q1 | 216 | 310 | 1277 | 25474 | 11444 | 1252 | 8.55 | 82.17 | 42.85 | ||
| 40 | journal | 2.578 Q1 | 175 | 147 | 340 | 7128 | 2515 | 334 | 5.80 | 48.49 | 48.60 | ||
| 41 | journal | 2.501 Q1 | 245 | 402 | 1811 | 14117 | 9171 | 1524 | 4.66 | 35.12 | 43.56 | ||
| 42 | journal | 2.498 Q1 | 60 | 208 | 742 | 8307 | 4147 | 647 | 5.86 | 39.94 | 44.96 | ||
| 43 | journal | 2.384 Q1 | 42 | 103 | 201 | 7008 | 1426 | 145 | 6.15 | 68.04 | 44.46 | ||
| 44 | journal | 2.345 Q1 | 114 | 130 | 693 | 5642 | 4282 | 662 | 6.01 | 43.40 | 45.39 | ||
| 45 | journal | 2.275 Q1 | 46 | 95 | 346 | 4112 | 2003 | 339 | 5.65 | 43.28 | 54.50 | ||
| 46 | journal | 2.270 Q1 | 199 | 113 | 644 | 5528 | 3324 | 631 | 5.03 | 48.92 | 40.46 | ||
| 47 | journal | 2.249 Q1 | 48 | 0 | 395 | 0 | 1632 | 356 | 4.46 | 0.00 | 0.00 | ||
| 48 | journal | 2.216 Q1 | 112 | 82 | 202 | 9639 | 1470 | 201 | 7.19 | 117.55 | 37.56 | ||
| 49 | journal | 2.136 Q1 | 99 | 90 | 338 | 3391 | 2183 | 320 | 6.82 | 37.68 | 28.78 | ||
| 50 | journal | 2.131 Q1 | 260 | 429 | 1584 | 19420 | 9422 | 1500 | 6.08 | 45.27 | 45.98 |
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Circulating igg fragments for gastric cancer and esophageal cancer.
1. Introduction
2. materials and methods, 4. discussion, 5. conclusions, author contributions, institutional review board statement, informed consent statement, data availability statement, conflicts of interest.
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Click here to enlarge figure
| Cohort | Gastric Cancer | Esophageal Cancer | Control Group | |||
|---|---|---|---|---|---|---|
| Male | Femal | Male | Female | Male | Female | |
| n | 36 | 32 | 31 | 12 | 12 | 8 |
| Age, years old, min–max (median) | 20–80 (62) | 34–83 (66) | 39–82 (63) | 33–70 (63) | 48–71 (62) | 26–70 (62) |
| Adenocarcinoma | n = 31 | n = 26 | n = 4 | n = 1 | - | - |
| Signet ring cancer | n = 5 | n = 6 | - | - | - | - |
| Squamous cell carcinoma | - | - | n = 27 | n = 11 | - | - |
| Stage I–II | n = 15 | n = 12 | n = 13 | n = 6 | - | - |
| Stage III–IV | n = 21 | n = 20 | n = 18 | n = 6 | - | - |
| Tumor size T1-2 | n = 7 | n = 8 | n = 8 | n = 3 | - | - |
| Tumor size T3-4 | n = 29 | n = 24 | n = 23 | n = 9 | - | - |
| Lymph nodal spreadN0 | n = 13 | n = 13 | n = 11 | n = 6 | - | - |
| Lymph nodal spread n+ | n = 23 | n = 19 | n = 20 | n = 6 | - | - |
| Metastasis M+ | n = 9 | n = 11 | n = 4 | n = 1 | - | - |
| Group | Number of Cases | IgG-LysK | ||
|---|---|---|---|---|
| Median; Quartiles Me (Q1:Q3) | p | |||
| 20 | 0.86 (0.74; 1.00) | 1–2 | 1–3 | |
| | 43 | 1.71 (1.09; 4.03) | <0.0001 * | |
| 68 | 1.08 (0.90; 1.60) | 0.003 * | ||
| Group | Number of Cases | Median; Quartiles Me (Q1:Q3) | p | |
|---|---|---|---|---|
| 11 | 7.6 (5.6: 8.8) | IgG-LysK−/IgG-LysK+ | =0.001 * | |
| 11 | 11.1 (9.5: 12.3) | |||
| Group | Number of Cases | Median; Quartiles Me (Q1:Q3) | p | |
|---|---|---|---|---|
| 20 | 12.20 (11.7:12.9) | IgG-LysK−/IgG-LysK+ | <0.0001 * | |
| 44 | 13.75 (13.4:14.3) | |||
| Group | n | Median; Quartiles Me (Q1:Q3) | p | |
|---|---|---|---|---|
| 15 | 67.3 (53.8:78.8) | IgG-LysK−/IgG-LysK+ | <0.0001 | |
| 14 | 33.2 (23.9:43.2) | |||
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Share and Cite
Goufman, E.I.; Tikhonova, N.B.; Aleksankin, A.P.; Gershkovich, K.B.; Stepanov, A.A.; Stepanova, I.I.; Mikhaleva, L.M.; Nizyaeva, N.V.; Kovaleva, O.V.; Alferov, A.A.; et al. Circulating IgG Fragments for Gastric Cancer and Esophageal Cancer. Diagnostics 2024 , 14 , 1396. https://doi.org/10.3390/diagnostics14131396
Goufman EI, Tikhonova NB, Aleksankin AP, Gershkovich KB, Stepanov AA, Stepanova II, Mikhaleva LM, Nizyaeva NV, Kovaleva OV, Alferov AA, et al. Circulating IgG Fragments for Gastric Cancer and Esophageal Cancer. Diagnostics . 2024; 14(13):1396. https://doi.org/10.3390/diagnostics14131396
Goufman, Eugene I., Nataliia B. Tikhonova, Andrey P. Aleksankin, Karina B. Gershkovich, Alexander A. Stepanov, Irina I. Stepanova, Liudmila M. Mikhaleva, Natalia V. Nizyaeva, Olga V. Kovaleva, Alexander A. Alferov, and et al. 2024. "Circulating IgG Fragments for Gastric Cancer and Esophageal Cancer" Diagnostics 14, no. 13: 1396. https://doi.org/10.3390/diagnostics14131396
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Chemotherapy-related cardiotoxicity and its symptoms in patients with breast cancer: a scoping review
- Hyunjoo Kim 1 , 2 ,
- Bomi Hong 3 ,
- Sanghee Kim 4 ,
- Seok-Min Kang 5 &
- Jeongok Park ORCID: orcid.org/0000-0003-4978-817X 4
Systematic Reviews volume 13 , Article number: 167 ( 2024 ) Cite this article
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Chemotherapy-related cardiotoxicity is a significant concern because it is a major cause of morbidity. This study aimed to provide in-depth information on the symptoms of chemotherapy-related cardiotoxicity (CRCT) by exploring literature that concurrently reports the types and symptoms of CRCT in patients with breast cancer.
A scoping review was performed according to an a priori protocol using the Joanna Briggs Institute’s guidelines. The participants were patients with breast cancer. The concept was the literature of specifically reported symptoms directly matched with CRCT and the literature, in English, from 2010, and the context was open. The search strategy included four keywords: “breast cancer,” “chemotherapy,” “cardiotoxicity,” and “symptoms.” All types of research designs were included; however, studies involving patients with other cancer types, animal subjects, and symptoms not directly related to CRCT were excluded. Data were extracted and presented including tables and figures.
A total of 29 articles were included in the study, consisting of 23 case reports, 4 retrospective studies, and 2 prospective studies. There were no restrictions on the participants’ sex; however, all of them were women, except for one case report. The most used chemotherapy regimens were trastuzumab, capecitabine, and doxorubicin or epirubicin. The primary CRCT identified were myocardial dysfunction and heart failure, followed by coronary artery disease, pulmonary hypertension, and other conditions. Major tests used to diagnose CRCT include echocardiography, electrocardiography, serum cardiac enzymes, coronary angiography, computed tomography, and magnetic resonance imaging. In all case reports, CRCT was diagnosed through an incidental checkup according to the patient’s symptom presentation; however, only 10 of these studies showed a baseline checkup before chemotherapy. The five most common CRCT symptoms were dyspnea, chest pain, peripheral edema, fatigue, and palpitations, which were assessed by patient-reported symptom presentation rather than using a symptom assessment tool. Dyspnea with trastuzumab treatment and chest pain with capecitabine treatment were particularly characteristic. The time for first symptom onset after chemotherapy ranged from 1 hour to 300 days, with anthracycline-based regimens requiring 3–55 days, trastuzumab requiring 60–300 days, and capecitabine requiring 1–7 days.
Conclusions
This scoping review allowed data mapping according to the study design and chemotherapy regimens. Cardiac assessments for CRCT diagnosis were performed according to the patient’s symptoms. There were approximately five types of typical CRCT symptoms, and the timing of symptom occurrence varied. Therefore, developing and applying a CRCT-specific and user-friendly symptom assessment tool are expected to help healthcare providers and patients manage CRCT symptoms effectively.
Peer Review reports
Breast cancer is currently the most common cancer worldwide. Its incidence and mortality rates in East Asia in 2020 accounted for 24% and 20% of the global rates, respectively, and these rates are expected to continue increasing until 2040 [ 1 ]. In the USA, since the mid-2000s, the incidence rate of breast cancer has been increasing by 0.5% annually, while the mortality rate has been decreasing by 1% per year from 2011 to 2020 [ 2 ]. Despite the improved long-term survival rate in patients with breast cancer due to the development of chemotherapy, the literature has highlighted that cardiotoxicity, a cardiac problem caused by chemotherapy, could be a significant cause of death among these patients [ 3 ]. Chemotherapy-related cardiotoxicity (CRCT) can interfere with cancer treatment and progress to congestive heart failure during or after chemotherapy [ 4 ], potentially lowering the survival rate and quality of life of patients with cancer [ 5 ].
The term cardiotoxicity was first used in the 1970s to describe cardiac complications resulting from chemotherapy regimens, such as anthracyclines and 5-fluorouracil. The early definition of cardiotoxicity centered around heart failure, but the current definition is broad and still imprecise [ 6 ]. The 2022 guidelines on cardio-oncology from the European Society of Cardiology (ESC) define cardiotoxicity as including cardiac dysfunction, myocarditis, vascular toxicity, arterial hypertension, and cardiac arrhythmias. Some of these definitions reflect the symptoms. For example, cardiac dysfunction, which accounts for 48% of cardiotoxicity in patients with cancer, is divided into asymptomatic and symptomatic cardiac dysfunction. Asymptomatic cardiac dysfunction is defined based on left ventricular ejection fraction (LVEF), myocardial global longitudinal strain, and cardiac biomarkers. Symptomatic cardiac dysfunction indicates heart failure and presents with ankle swelling, breathlessness, and fatigue [ 7 ]. The ESC guidelines for heart failure present more than 20 types of symptoms [ 8 ]; however, to the best of our knowledge, few studies have been conducted to determine which heart failure symptoms and their characteristics are associated with CRCT in patients with breast cancer. Similarly, there is a lack of information related to vascular toxicity such as myocardial infarction [ 7 ].
Professional societies in cardiology and oncology have proposed guidelines for the prevention and management of cardiotoxicity in patients with cancer. According to the American Society of Clinical Oncology and the ESC, it is recommended to identify high-risk patients, comprehensively evaluate clinical signs and symptoms associated with CRCT, and conduct cardiac evaluations before, during, and after chemotherapy [ 7 , 9 , 10 ]. In addition, guidelines for patients with cancer, including those for breast cancer survivorship care, emphasize that patients should be aware of the potential risk of CRCT and report symptoms, such as fatigue or shortness of breath to their healthcare providers [ 7 , 11 , 12 ]. Although these guidelines encompass cardiac monitoring as well as symptom observation, many studies have focused solely on objective diagnostic tests, such as echocardiography, cardiac magnetic resonance, and cardiac biomarkers [ 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 ], which means that there is little interest in CRCT symptoms in patients under breast cancer care.
This lack of interest in CRCT symptoms may be related to the absence of a specific symptom assessment tool for CRCT. Symptom monitoring of CRCT in patients with breast cancer was conducted through patient interviews and reported using the appropriate terminology [ 23 ]. In terms of interviews, patients with cancer experienced the burden of expressing symptoms between cardiovascular problems and cancer treatment. Qualitative research on patients with cancer indicates that these patients experience a daily battle to distinguish the symptoms they experience during chemotherapy [ 24 ]. To reduce the burden of identifying CRCT symptoms, it is crucial to educate patients with breast cancer undergoing chemotherapy about these symptoms. To report cardiotoxicity, healthcare providers in oncology can use a dictionary of terms called the Common Terminology Criteria for Adverse Events (CTCAE) for reporting adverse events in patients with cancer [ 25 ]. Patients can also use Patient-Reported Outcome (PRO), which allows unfiltered reporting of symptoms directly to the clinical database [ 26 ]. PRO consists of 78 symptomatic adverse events out of approximately 1,000 types of CTCAE [ 27 ]. Basch et al. suggested that PRO could enable healthcare providers to identify patient symptoms before they worsen, thereby improving the overall survival rate of patients with metastatic cancer [ 28 ]. This finding implies that symptoms can provide valuable clues for enhancing the timeliness and accuracy of clinical assessments of CRCT [ 29 ]. Therefore, it is necessary to explore the scope of research focusing on CRCT symptoms for prevention and early detection of CRCT in patients with breast cancer. The detailed research questions are as follows:
What are the general characteristics of the studies related to CRCT in patients with breast cancer?
What diagnostic tools and monitoring practices are used to detect CRCT?
What are the characteristics and progression of symptoms associated with CRCT?
A scoping review is a research method for synthesizing evidence that involves mapping the scope of evidence on a particular topic [ 30 ]. It aims to clarify key concepts and definitions, identify key characteristics of factors related to a concept, and highlight gaps or areas for further research [ 30 ]. This study used a scoping review methodology based on the Joanna Briggs Institute (JBI) framework. The JBI methodology, refined from the framework initially developed by Arksey and O’Malley [ 31 ], involves developing a research question, establishing detailed inclusion and exclusion criteria, and selecting and analyzing literature accordingly [ 32 ]. In contrast to systematic reviews, scoping reviews can encompass a variety of study designs and are particularly suitable when the topic has not been extensively studied [ 33 ]; hence, the decision was made to conduct a scoping review.
Development of a scoping review protocol
To conduct this review, an a priori scoping review protocol was developed to enhance transparency and increase the usefulness and reliability of the results. The protocol included the title, objective, review questions, introduction, eligibility criteria, participants, concept, context, types of evidence source, methods, search strategy, source of evidence selection, data extraction, data analysis and presentation, and deviation from the protocol [ 34 ] (Supplementary File 1).
Eligibility criteria
A participant-concept-context (PCC) framework was constructed based on the following research criteria. The participants were patients with breast cancer. The concept was that studies that specifically reported symptoms directly matched to CRCT in patients with breast cancer and the literature, published in English since 2010, in line with the year the CRCT guidelines were announced by the Cardio-Oncology Society. The context was open. We included all types of research designs. The exclusion criteria were studies that included patients with other types of cancer, involved animal subjects, and reported symptoms not directly related to CRCT.
Search strategy
The keywords consisted of “breast cancer,” “chemotherapy,” “cardiotoxicity,” and “symptoms.” The keywords for “cardiotoxicity” were constructed according to the clinical cardiotoxicity report and ESC guidelines [ 7 , 35 ]. The keywords for “symptoms” included 40 specific symptoms of arrhythmia, heart failure, and cardiac problems [ 36 , 37 ] (Supplementary Table 1). We used PubMed, Embase, and CINAHL.
Source of evidence selection
Duplicate studies were removed using EndNote 21. The titles and abstracts were then reviewed according to the inclusion criteria, the primary literature was selected, and the final literature was selected through a full-text review. Any disagreements were resolved through discussions between the investigators.
Data extraction
The data from the literature included the general characteristics of the study, as well as information on the patients, chemotherapy, cardiotoxicity, and symptoms. The general characteristics of the study included author, publication year, country of origin, study design; patient information including sample size, sex, age, cancer type, and cancer stage; chemotherapy information including chemotherapy regimen; cardiotoxicity information including type of cardiotoxicity, diagnostic tests, and times of assessment; and symptom information including type of symptom, characteristics of symptom worsening or improvement, onset time, progression time, and time to symptom improvement. Information on whether to receive chemotherapy after the diagnosis of cardiotoxicity was explored.
Data analysis and presentation
The contents of the included studies were divided into three categories: (1) general characteristics, which encompassed study designs, patients, and medications; (2) type of CRCT and cardiac assessment for CRCT; and (3) characteristics and progression of the symptoms associated with CRCT. CRCT symptom-related data are presented in tables and figures.
In total, 487 studies were identified through database searches, and 116 duplicates were subsequently removed. After reviewing the titles and abstracts, we excluded 197 studies in which participants had cancers other than breast cancer, no symptoms, or symptom-related expressions. Of the remaining 174 studies, 146 were excluded after full-text review. Among the excluded studies, 79 were mainly clinical trials that the symptoms were not directly related to CRCT, 62 did not report specific symptoms, four were in the wrong population, and one was unavailable for full-text review. An additional study was included after a review of references, bringing the final count to 29 studies included in the analysis (Fig. 1 ).
Preferred reporting items for systematic reviews flowchart
General characteristics of studies including designs, sex and age, chemotherapy regimen, and CRCT criteria
Table 1 presents the general characteristics of the studies included in this review. The majority of these studies were published in the USA ( n =14), with Japan ( n =3), and Romania ( n =2) following. The study designs primarily consisted of case reports ( n =23), retrospective studies ( n =4), and prospective studies ( n =2).
All case reports involved female patients, except for one involving a male patient. Five quantitative studies did not specify or limit the sex of the participants, and one retrospective study included only female patients. In terms of cancer stage, the majority of studies involved patients with advanced breast cancer ( n =13), while a smaller number involved patients with early-stage breast cancer ( n =4). Twelve studies did not specify the cancer stage. Approximately 20 types of chemotherapy regimens are currently in use. Trastuzumab, which is a human epidermal growth factor receptor 2 (HER2) blocker, was mentioned in the majority of studies ( n =8), followed by capecitabine (an antimetabolite) ( n =7), and doxorubicin or epirubicin (anthracycline-based chemotherapy) ( n =6). Current chemotherapy and previous treatment methods were described together, with the exception of eight studies. Six quantitative studies defined the CRCT criteria, five of which were based on decreased LVEF and one of which was based on significant cardiac symptoms and/or electrocardiogram changes. Twenty-three case reports described the cardiovascular diagnosis as CRCT.
Diagnostic tools and monitoring practice for CRCT
Table 2 displays the types of CRCT, diagnostic tools, and times of cardiac assessment according to chemotherapy regimens. The most prevalent CRCT were myocardial dysfunction and heart failure, identified in 12 case studies, respectively. This was followed by coronary artery disease, represented in 8 case studies, pulmonary hypertension in 2 case studies, and a single case study of periaortitis. The most used test for diagnosing CRCT was echocardiography ( n =22), followed by EKG ( n =20), various types of cardiac enzymes ( n =16), coronary angiography (CAG, n =12), computed tomography ( n =6), and magnetic resonance imaging (MRI, n =4). Regarding the CRCT symptom assessment tools, the CTCAE was used in two studies, the New York Heart Association classification for heart failure in two studies, the dyspnea assessment scale in one study, and symptoms of cardiac origin, which consisted of chest pain, dyspnea, and palpitations in one study.
Regarding the times of cardiac evaluation, two studies performed regular cardiac checkups including before, during, and after chemotherapy. There were 10 case studies and six quantitative studies describing cardiac function testing before chemotherapy, of which seven studies performed regular cardiac screening tests and two studies mentioned cardiac screening even after the completion of chemotherapy. The frequency of regular checkups varied from every 3 months to every two to four cycles. In all case reports ( n =23), CRCT were diagnosed through incidental checkups based on patients’ symptom presentation, and in most cases, several tests were performed subsequentially for CRCT diagnosis. In one case study, cardiac evaluation was conducted 3 days after the patient’s initial symptom presentation, when the symptoms became more severe.
Characteristics and progression of symptoms associated with CRCT
Table 3 shows the descriptive scope of the CRCT-related symptoms according to the chemotherapy regimens used in the included studies. The mapping factors included initial symptoms, symptom onset or severity, symptom progression, medical management, and CRCT results. One of the most frequent symptoms associated with CRCT was dyspnea, which was discussed in 19 studies and described as difficulty in breathing, shortness of breath, or New York Heart Association (NYHA) class II or III. When dyspnea appeared as the initial symptom of CRCT, the symptom progression was worsening in eight case studies and persistent in two cases. Chest pain was described in 12 studies as a symptom characterized by a squeezing, tingling, burning, tightened, or atypical feeling that was relieved by rest and exacerbated by exertion. Other symptoms included peripheral edema ( n =6), fatigue ( n =5), and palpitation ( n =2). The symptoms were assessed by patient-reported symptom presentation rather than using a symptom assessment tool.
The symptoms could be categorized based on the type of chemotherapy regimens used. In the case studies involving anthracycline-based regimen and HER2 blockers, dyspnea was the most frequently observed symptom ( n =7), followed by peripheral edema ( n =2), and chest pain or discomfort ( n =2). In case studies where antimetabolites were used, specifically capecitabine, chest pain was a common and prominent symptom. This chest pain typically manifested between 1 and 7 days after drug administration and persisted until treatment. Notably, four out of seven patients reported this symptom on the first day of chemotherapy, according to the case reports. The time for first symptom onset after chemotherapy ranged from 1 hour to 300 days, with anthracycline-based regimens requiring 3–55 days, trastuzumab requiring 60–300 days, and capecitabine requiring 1–7 days. Figure 2 shows the progression of symptoms in case studies, detailing the time of symptom onset, the date of symptom reporting, and the date of treatment completion following the use of chemotherapy. The studies that did not specify any of the dates of symptom onset, reporting, and completion of treatment were excluded from the figure.
Figure 3 shows symptoms according to the main types of chemotherapy regimens reported in case studies. Dyspnea with trastuzumab and chest pain with capecitabine are particularly characteristic. A retrospective study included in this scoping review reported that chest pain was the most common symptom associated with capecitabine, followed by dyspnea and palpitation [ 40 ]. Furthermore, peripheral edema was primarily observed with anthracycline, alkylating, and HER2 blockers, while fatigue was noted with various anticancer drugs, irrespective of the type of chemotherapy regimen.
Ongoing chemotherapy was discontinued after CRCT was detected in 20 case studies. When patients presented symptoms indicative of CRCT, the majority were promptly hospitalized for further evaluation, medication, or interventional treatment. The majority of studies indicated the initiation of cardiac medication ( n =21), with three case studies involving coronary intervention and two involving treatment with wearable devices. Most management procedures were conducted in a general ward or an intensive care unit.
In most case studies, symptoms improved following cardiac treatment, with either complete or partial recovery of LVEF observed in 19 instances. However, a few studies reported a poor prognosis, including two instances of death. LVEF recovered in most patients within 6 months when treated with an anthracycline-based regimen and HER2 blockers (Fig. 2 ). A retrospective study reported that the rates of complete or partial recovery of CRCT following treatment with doxorubicin-based chemotherapy and trastuzumab were 42.9% and 86.1%, respectively [ 39 ]. Another retrospective study noted that the recovery time of CRCT when treated with HER2 blockers increased in correlation with the severity of the NYHA class, ranging from 8 to 80 weeks [ 38 ]. In the case of the antimetabolite capecitabine, all patients recovered within a day to a week, except one patient who did not recover.
This scoping review was conducted to explore the scope of studies focusing on CRCT symptoms, including the general characteristics of the studies, diagnostic tools, monitoring practices related to detecting CRCT, and the characteristics and progression of symptoms associated with CRCT. The primary findings of this review were as follows: (1) common symptoms related to CRCT and differences in symptoms according to the chemotherapy regimens used were identified; (2) the symptoms reported by the patient served as clues to suspect a specific type of CRCT; and (3) regular monitoring practices for CRCT prevention and detection were insufficient.
First, the current study identified common symptoms such as dyspnea, chest pain, peripheral edema, fatigue, and palpitation associated with CRCT, as well as variations in symptoms depending on the chemotherapy regimen used in patients with breast cancer. Among these symptoms, dyspnea, edema, and chest pain were frequently observed in patients receiving anthracycline-based and/or HER2 blocker drugs. These symptoms, which are associated with heart failure, appeared later compared to those observed with capecitabine, as depicted in Fig. 2 . This may be due to the known impact of anthracycline-based and/or HER2 blocker regimens on cardiomyocytes and other cells, leading to myocardial damage [ 42 ]. Therefore, the symptoms are related to heart failure, potentially resulting from the impairment of ventricular filling or ejection in patients undergoing treatment with these regimens [ 43 ].
In a similar vein, Attin et al. (2022) documented the occurrence of symptoms such as lower extremity edema, chest pain, difficulty breathing, and fatigue before the diagnosis of CRCT in women undergoing breast cancer treatment. They conducted a retrospective and longitudinal investigation of the symptoms, signs, and cardiac tests of 15 patients who experienced CRCT, using their electronic medical records. In their study, cardiotoxicity was defined by an echocardiogram or MRI showing a decrease in LVEF of 5 to 10%, with a specialist’s confirmation note. They compared the number of symptom occurrences during the first half of the year with those during the second half of the year prior to the diagnosis of cardiotoxicity. Specifically, the frequency of lower-extremity edema significantly increased from three occurrences in the first half of the year to 17 occurrences in the second half of the year. The frequency of symptoms for dyspnea and chest pain also increased from 10 and 8 times, respectively, to 16 and 14 times in the second half of the year. While there was limited information on the doses or timing of chemotherapy, 87% of the patients received the same chemotherapy regimens, namely anthracyclines and/or HER2 blockers [ 44 ]. This suggests that the increase in symptom occurrence over time may be related to the accumulation of anthracycline and the duration of anti-HER2 therapy [ 45 ].
Salyer et al. (2019) conducted a study on the prevalent symptoms of heart failure and their clustering. They identified three symptom clusters: sickness behavior, gastrointestinal disturbance, and discomfort of illness. Notably, dyspnea, edema, and pain were grouped into the discomfort of illness cluster, which aligns with the symptoms we observed in patients treated with anthracyclines and/or HER2 blockers [ 46 ]. Therefore, it is crucial for patients undergoing treatment with anthracyclines and/or HER2 blockers to be vigilant for symptoms such as dyspnea, edema, or chest pain, as these are indicative of heart failure.
Chest pain caused by vasospasm was a predominant symptom in patients taking antimetabolite regimens such as oral capecitabine, and it manifested as the following types of cardiotoxicities: vasospasm-related arrhythmia, myocardial disease, and ischemia [ 47 ]. Vasospasm can be triggered by endothelial dysfunction, hypersensitive vascular smooth muscle, reactive oxidative stress, or chemotherapy regimens [ 48 , 49 ]. According to previous studies, in patients using antimetabolite drugs such as 5-fluorouracil or capecitabine, chest pain was usually reported to occur from several hours to 72 hours after the first administration [ 47 , 50 , 51 , 52 , 53 ]. To detect chemotherapy-related coronary vasospasm in the early stage, it is recommended to carefully monitor typical or atypical symptoms of chest pain and EKG monitoring during drug infusion [ 54 ]. Muco et al. (2022) reported severe outcomes resulting from delayed management of vasospastic angina symptoms. The patient’s cardiac evaluation was performed 3 days after the onset of symptoms, and unfortunately, she did not recover from brain damage caused by coronary vasospastic sequelae. The authors stressed the importance of medical teams recognizing the symptoms of CRCT through vigilant monitoring and patient education [ 55 ].
As seen in the symptoms of CRCT caused by heart failure and vasospasm, careful observation of symptoms and conducting appropriate tests are crucial to prevent cardiotoxicity and minimize damage. These characteristics of CRCT and the associated symptoms related to chemotherapy regimens can provide crucial educational content for healthcare providers and patients preparing for chemotherapy. In addition, CRCT and symptom progression according to chemotherapy regimens could be used to formulate research questions for future systematic reviews.
Second, the preventive management of CRCT necessitates adherence to recommended guidelines. The 2022 ESC guidelines on cardio-oncology have updated the classification of CRCT and the monitoring protocols based on the chemotherapy regimens used [ 7 ]. The CRCT identified in the current study aligns with the drug toxicity outlined in the 2022 ESC guidelines. These guidelines advocate for regular cardiac monitoring before, during, and after chemotherapy to prevent and manage CRCT induced by anthracycline and HER2 blockers [ 7 , 12 ]. In this scoping review, two of 23 records described cardiac monitoring before, during, and after chemotherapy. An Australian multicenter study revealed that 59% of patients were referred to a cardiologist before CRCT occurred, but only 15% of patients diagnosed with CRCT had consulted a cardiologist before chemotherapy [ 41 ]. Given the declining mortality rates among cancer patients, managing CRCT requires a collaborative approach between oncology and cardiology to minimize mortality and morbidity in patients with breast cancer undergoing chemotherapy [ 7 ]. Therefore, it remains crucial to emphasize adherence to cardiac monitoring guidelines and foster cooperation between oncology and cardiology.
Additionally, symptom assessment is important for the early detection of patients with CRCT. The studies included in the current scoping review assessed whether patients’ symptoms could detect CRCT using interviews with patients, the New York Heart Association classification, a dyspnea assessment scale, and CTCAE tools. The United States National Cancer Institute recommends that healthcare providers use CTCAE and patients with cancer use PRO to report adverse events, including symptoms. CTCAE is a broad and comprehensive terminology that encompasses adverse events related to cancer treatment, has been used since the 1980s [ 25 ], and is not specialized in cardiotoxicity. Additionally, a discrepancy between CTCAE and PRO discovered that healthcare providers often underestimate both the incidence and duration of symptoms compared to the patients [ 56 , 57 , 58 ]. Specifically, healthcare providers tend to report symptom severity as lower than that reported by patients. For instance, there are notable discrepancies between healthcare providers and patients when reporting severe or very severe symptoms of fatigue, dyspnea, and limb edema in patients with early-stage breast cancer undergoing chemotherapy. The reported rates were 8% and 22% for fatigue, 0% and 4% for dyspnea, and 0% and 5% for limb edema, from healthcare providers and patients, respectively. Therefore, it is necessary to develop a user-friendly questionnaire to assess the various symptoms of CRCT.
Finally, we found that once CRCT was confirmed, cardiac treatment was promptly initiated and chemotherapy was frequently halted until CRCT resolution. A Delphi study on the use of anthracycline and trastuzumab proposed altering the treatment schedule or discontinuing treatment until there was an improvement in LVEF [ 59 ]. However, the professional societies did not provide definitive recommendations regarding continuing or ceasing ongoing chemotherapy. Instead, they suggested that the decision to continue or discontinue ongoing chemotherapy should be made based on the patient’s potential risks and benefits [ 60 ]. For example, Polk et al. (2016) reported that out of 22 patients with CRCT resulting from capecitabine, six continued medications with or without cardiac treatment; some of these patients experienced the same symptoms, while others did not exhibit significant symptoms [ 40 ]. Further research is required to explore the continuation or discontinuation of chemotherapy when CRCT is confirmed.
This study has some limitations. First, although we did not restrict the patients’ sex when reviewing the literature, most patients, except for one, were female. This may be related to the lower incidence of breast cancer in men. Second, although this scoping review mapped CRCT symptoms according to chemotherapy regimens, including anthracycline-based drugs, HER2 blockers, and antimetabolites, it did not cover cardiotoxicity related to other types of chemotherapy regimens. Thus, exploring the symptoms by focusing on expanded chemotherapy regimens and cardiovascular toxic diseases will assist in overcoming this limitation. Third, of the 29 studies, 23 were case reports with some grey literature, which may be justified by the nature of scoping reviews that allow for inclusion irrespective of the data source [ 61 ] and the study type. Experimental or observational clinical studies use objective criteria, such as diagnostic tests to generate primary evidence. However, case reports have led to new medical discoveries regarding the prevention and treatment of diseases [ 62 ]. Given the nature of case reports, specific symptoms that could provide clues for evaluating CRCT in patients with breast cancer are most often found in these reports. We incorporated grey literature to gather more comprehensive information on CRCT-related symptoms. However, to mitigate the potential issue of unverified quality in grey literature, we initially organized 16 studies from peer-reviewed literature and subsequently incorporated the grey literature into our findings. This approach helped to clarify the results of the peer-reviewed literature, particularly the types of chemotherapy regimens [ 63 ]. Finally, regarding the literature selection criteria, we examined articles written in English and published since 2010, the year the cardio-oncology guidelines were announced, thereby excluding articles published before 2010.
This scoping review allowed data mapping according to the study design and chemotherapy regimens. The key messages included a type of CRCT, cardiac assessment, and in-depth information regarding the CRCT symptoms. There were approximately five typical CRCT symptoms, including dyspnea, chest pain, peripheral edema, fatigue, and palpitations, and the timing of symptom occurrence varied. The symptoms were assessed by patient-reported symptom presentation rather than using a symptom assessment tool. Therefore, developing and applying a CRCT-specific and user-friendly symptom assessment tool are expected to help healthcare providers and patients manage CRCT symptoms effectively.
Availability of data and materials
The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.
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The authors thank Nawon Kim, a librarian at the Yonsei University Medical Library, for building search terms and guiding the database searches.
This research is supported by the Brain Korea 21 FOUR Project founded by the National Research Foundation (NRF) of Korea, Yonsei University College of Nursing.
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Kim, H., Hong, B., Kim, S. et al. Chemotherapy-related cardiotoxicity and its symptoms in patients with breast cancer: a scoping review. Syst Rev 13 , 167 (2024). https://doi.org/10.1186/s13643-024-02588-z
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The experıance of tertıary center for adult granulosa cell tumor: whıch factors predıct survival?
- Mustafa Şahin 1 ,
- Tufan Arslanca 1 ,
- Yeşim Özkaya Uçar 1 ,
- Gülşah Tiryaki Güner 1 ,
- İlker Selçuk 1 &
- Hakan Raşit Yalçın 1
Journal of Ovarian Research volume 17 , Article number: 127 ( 2024 ) Cite this article
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This retrospective study aims to evaluate the clinical course and long-term outcomes of patients diagnosed with adult granulosa cell tumors (AGCT).
The study analyzed a cohort of 112 AGCT patients with a median follow-up of 87 months. Data regarding disease-free survival (DFS), overall survival (OS), recurrence rates, and prognostic factors were collected and analyzed. Surgical interventions, including lymphadenectomy and cytoreductive surgery, were assessed for their impact on outcomes.
The study revealed favorable long-term outcomes, with a 5-year DFS of 85% and a 10-year DFS of 83%. Additionally, a 5-year OS of 100% and a 10-year OS of 96% were observed. Recurrence occurred in 13.4% of cases, with advanced stage and positive peritoneal cytology identified as independent poor prognostic factors for DFS. Lymph node involvement was rare, and routine lymphadenectomy did not improve outcomes. Conservative surgery showed comparable DFS rates to definitive surgery in early-stage disease. However, cytoreductive surgery was crucial for advanced and recurrent tumors, with complete tumor resection enhancing survival outcomes.
The study underscores the importance of vigilant follow-up and individualized treatment strategies for AGCT patients. Despite the retrospective nature of the analysis, the substantial patient cohort and meticulous surgical interventions contribute valuable insights into AGCT management. Prospective multicenter studies are warranted to further elucidate prognostic factors and optimize treatment approaches for this rare malignancy.
Granulosa cell tumors are the most common malignant sex cord stromal tumors (SCST), accounting for approximately 2–5% of all ovarian malignancies with an incidence rate of approximately 0.4–1.7/100.000 [ 1 ]. Granulosa cell tumors are divided into two histological types; adult granulosa cell tumors (AGCT) and juvenile granulosa cell tumors. Approximately 95% of all patiens possess the adult variant. Although, AGCT is usually diagnosed in the premenopausal or early postmenopausal period, it can be seen at younger ages as well. AGCT has a favorable prognosis and shows a slow clinical course. The 5-year overall survival rate is 75–95% in stage I, 55–75% in stage II, and 22–50% in stage III/IV. The tumor stage is the most significant factor associated with oncologic outcome [ 1 , 2 ]. Recurrences in AGCT are mostly multifocal and the most common site of recurrence is the pelvis. Recurrence rates range from 6 to 48% and 50–80% of patients who have a mortal course. Recurrences are most common within 5 years following surgery, while late recurrences can be observed after 30–40 years [ 3 , 4 ]. Due to the slow growth of the tumor and hormonal symptoms, most patients are diagnosed in the early stages [ 5 ].
The primary treatment for AGCT is surgery, which can be curative in the early stages. In the postmenopausal period, the standard treatment is a hysterectomy and a bilateral salpingo-oophorectomy. In early-stage patients who wish to preserve their fertility, conservative surgery that preserves the other ovary and uterus can be performed [ 6 ]. The role of surgical staging in the treatment of AGCT is still unclear. The benefit of lymphadenectomy is controversial and only the removal of suspicious lymph nodes is recommended [ 7 ].
The National Comprehensive Cancer Network (NCCN) guideline recommends adjuvant chemotherapy in advanced stages. However, there is no evident consensus on adjuvant treatment in stage 1C [ 8 ]. The role of adjuvant chemotherapy in the treatment of primary or recurrent disease in AGCT is still unclear [ 2 ].
The rarity of AGCT makes it difficult to recognize the prognostic factors, predict the oncologic outcomes and determine the appropriate treatment. In this study, we aimed to investigate the clinicopathologic prognostic factors affecting the recurrence and survival in AGCT patients.
Materials and methods
The data of 112 patients who have been diagnosed and treated for AGCT between the years of January 2004 and August 2019 in the gynecologic oncology clinic were retrospectively evaluated. Data was obtained from the electronic database system, patient files, pathology reports and operative notes. Ethics committee approval has been obtained for the study (decision number 14 dated April 27, 2021).
The International Federation of Gynecology and Obstetrics (FIGO) 2014 staging system was used for staging [ 9 ]. Those operated on before 2014 were re-staged according to 2014 FIGO criteria, by re-evaluating the pathology reports. The extent of the first operation was evaluated according to the extent of the disease and the desire for fertility. The surgical procedure, in which at least part of the one ovary and uterus were preserved, was defined as “conservative surgery”. In our center, conservative treatment is applied to patients with stage IA, 1B and stage IC1 according to the 2014 FIGO staging system, and to patients with fertility potential and close follow-up opportunity. Patients with fertility desires underwent unilateral salpingo-oophorectomy without hysterectomy. “Definitive surgery” was defined as hysterectomy and bilateral salpingo-oophorectomy. The inclusion of lymphadenectomy and omentectomy in the surgical procedure was determined by the senior surgeon. The upper limit of para-aortic lymphadenectomy was the left renal vein. When evidence of a more extensive disease existed, cytoreductive surgical techniques were used, as well as, staging surgery.
The adjuvant treatment decision was made by the gynecologic oncology council. In our hospital, bleomycin, etoposide and cisplatin (BEP; 3 or 4 cycles) are most commonly preferred in the adjuvant treatment of AGCT, and platinum-based chemotherapy regimens such as carboplatin/ paclitaxel (CP; 6 cycles) or etoposide/cisplatin (EP; 6 cycles) are also used. Chemotherapy response in patients was evaluated according to RECIST 1.1 criteria [ 10 ]. Clinical responses were defined as follows: (a) Complete clinical response (CCR): Complete disappearance of lesions and absence of new lesions; (b) Partial clinical response (PCR): A reduction in the size of lesions by at least 30%; (c) Progressive disease (PD): A ≥ 20% increase in the maximum diameter of the lesion, the appearance of a new lesion ≥ 1 cm, or progression of a non-target lesion; (d) Stable disease (SD): Lesions that were neither in the partial clinical response group, nor in the progressive disease group, based on the smallest overall diameters at the time of the study. The clinical response of patients was evaluated 1 month after the first treatment (surgery + adjuvant treatment) using clinical, laboratory parameters and imaging methods.
After treatment, patients were followed up every 3 months for the first 2 years, every 6 months until the fifth year and annually thereafter. We defined recurrences distal to the pelvic inlet as pelvic recurrence, recurrences between the pelvic inlet and diaphragm as upper-abdominal recurrence, and other recurrences as extra-abdominal recurrence. Cytologically defined ascites and peritonitis carcinomatosa were considered as upper-abdominal recurrence, and recurrence in the liver parenchyma was evaluated as extra-abdominal recurrence.
Statistical analysis
Statistical analysis was performed using SPSS version 22 (IBM, Chicago, USA). Disease-free survival (DFS) was defined as the time from operation until recurrence/progression of disease or last contact in those who did not develop recurrence. Overal survival (OS), was defined as the time from disease to death or last contact. The Kaplan–Meier method was used for survival analysis and differences were analyzed by the log-rank test. Factors with a p value less than 0.05 in the univariate analysis were included in the multivariate analysis. The Cox regression model was used in the multivariate analysis. The cut-off point for statistical significance was set as p value less than 0.05.
Clinical, surgical, and pathological features
The mean age of the 112 patients that constituted the study group was 50.3 ± 12.57 years and ranged between 17 and 81 years of age. The mean age of the 13 patients (11.6%) that underwent conservative surgery was 30.6 ± 7.6 years and ranged between 17 and 43 years of age.
Abdominal or pelvic pain (24.1%) and palpable adnexal mass (21.4%) were the most frequently reported presenting symptoms, followed by abdominal distention (18.8%) and vaginal bleeding (17.9%). Other less common symptoms accounted for 7.1% of cases. Only 12 patients (10.7%) were asymptomatic and were diagnosed incidentally during investigations conducted for non-gynecologic reasons. The mean tumor size was 89.6 ± 55.76 mm and ranged between 10 and 300 mm. Lymphadenectomy was performed in 94 of the patients (83.9%). Pelvic and para-aortic pelvic lymph node dissection was performed in 91 patients (81.3%), and only pelvic lymph node dissection was performed in 3 patients (2.6%). The mean number of lymph nodes removed in these patients was 51 ± 26.27 and ranged between 7 and 132. Three (3.2%) of the patients who underwent lymphadenectomy had positive lymph node metastasis and the metastases were in the pelvic lymph nodes. One hundred-four (92.8%) patients were stage I, 3 (2.7%) were stage II, 4 (3.6%) were stage III, and 1 (0.9%) was stage IV. Preoperative cyst rupture was detected in 2 (1.8%) patients, and 17 (15.2%) patients had intraoperative cyst rupture. Peritoneal cytology revealed malignancy in 12 (10.7%) of the patients and 4 (4%) had metastases in the omentum. The average time from the diagnosis of the disease to the first surgery of 112 patients was 15.2 ± 10.3 days and ranged from 1 to 54 days. Complementary surgery was performed in 35 (31.2%) patients after the first surgery. The average time from diagnosis of the disease to completion surgery is 45.7 ± 11.5 days and varies between 23 and 67 days. No residue tumor was observed in all patients during initial surgery (Table 1. ).
Adjuvant treatment and survival analysis
Adjuvant chemotherapy was administered to 30 patients. Of these, 22 were stage IC and 8 were stage 2–4. Of these, 17 patients (64.9%) received BEP, and 13 (35.3%) received others as adjuvant therapy (12 patients CP and 1 patient EP). While the 5-year DFS was 68% in the group receiving BEP, it was 59% in the other group ( p = 0.773). It was observed that adjuvant treatment types did not determine DFS. Thirty patients received adjuvant therapy, with a 5-year disease-free survival (DFS) rate of 64%. Conversely, 82 patients did not receive adjuvant therapy, and their 5-year DFS rate was 94%. The 5-year DFS rate significantly decreased in patients receiving adjuvant therapy compared to those who did not (64% vs. 94%; p < 0.001) (Table 2 ).
The median follow-up period of the patients was 87 months and ranged between 4 and 215 months. During this period, it was observed that 15 (13.4%) patients developed recurrence and 3 (2.7%) died becouse of the disease. Of the patients included in the study, the 5-year DFS was 85%, 10-year DFS was 83%. 5-year OS was 100% and the 10-year OS was 96%.
In the univariate analysis, positive peritoneal cytology, advanced stage and receiving of adjuvant treatment were associated with poor DFS. The 5-year DFS decreased from 93 to 56% in patients with positive peritoneal cytology ( p = 0.001) (Fig. 1 ). The 5-year DFS which was 91% in stage 1, was 13% in stages 2–4 ( p < 0.001) (Fig. 2 ). 5-year DFS significantly reduced in those receiving adjuvant therapy (respectively, 64% vs . 94%; p < 0.001) (Table 2. ). However, this relationship was thought to be related to the stage of the disease, as treatment was mostly given to those experiencing stage IC-IV disease. In stage 1, 73.3% ( n = 22/104) of patients received adjuvant treatment and all of them were in stage IC, whereas this rate was 100% ( n = 8/8) in stages 2–4 ( p < 0.001). Statistical analysis could not be performed for OS, as death due to disease occurred in only 3 patients.
Cancer-specific survival of patients with granulosa cell tumors by peritoneal cytology
Cancer-specific survival of patients with granulosa cell tumors by FIGO stage
Since adjuvant treatment was significantly correlated with stage, a model was created using peritoneal cytology and stage for multivariate analysis. Accordingly, stage 2–4 and positive peritoneal cytology were found to be independently poor prognostic factors for recurrence (respectively, odds ratio (OR) = 114.042, 95% confidence interval (CI) = 19.415–669.883, p < 0.001 and OR = 4.251, 95% CI = 1.125–16.072, p = 0.033) (Table 2. ).
Recurrence pattern
Of the 15 patients with recurrence, 7 (46.7%) had recurrence only in the pelvic region, 3 (20%) only in the upper abdominal region, 4 (26.6%) in the pelvic and upper abdominal region, and 1 (6.6%) in the upper abdominal and extra-abdominal region. Recurrences were observed as focal in 10 (66.6%) and as multifocal in 5 (33.3%) patients. The mean time for recurrence was 29 months and ranged between 9 and 86 months. Eight of the patients were in stage 1 and 7 were in stages 2–4.
Conservative surgery was applied in 1 patient (patient no: 1) at initial surgery. In addition adjuvant chemotherapy was given to 11 patients after initial surgery. Lymph node metastasis was present in 3 patients, omental metastasis in 4 patients and peritoneal cytology showed malignancy in 5 patients. Tumor-cyst rupture was present in 3 of the patients (Table 3 ).
It has been determined that after the first recurrence, 14 (93.3%) of these patients underwent secondary cytoreductive surgery, followed by salvage chemotherapy. No residue tumor was observed in these patients after secondary cytoreduction. CCR was obtained with salvage treatment in all of these 14 patients. One patient, who developed extra-abdominal recurrence, received salvage chemotherapy and external radiotherapy ( patient no: 9 ). After 18 months of follow-up, no recurrence has been observed yet in this patient. In finally, all patients with first recurrence CCR was achieved with salvage treatments after the first recurrence (Table 3 ).
It has been determined, that 6 of the patients developed a second recurrence and 5 patients with the secondary recurrence underwent tertiary cytoreductive surgery, followed by salvage chemotherapy (Table 4 ). No residue tumor was observed in these 5 patients after tertiary cytoreduction. One patient with extra-abdominal recurrence received salvage chemotherapy and external radiotherapy ( patient no 10 ). CCR was achieved in 4 patients following salvage treatment after the second recurrence. Two patients with omental and extra-abdominal recurrence died due to progressive disease; the follow-up periods of these patients were 52 and 154 months after initial surgery, respectively ( patient no 2, and 10, respectively ).
Furthermore, 3 of the 4 patients, with whom CCR was obtained after the second recurrence, developed a third recurrence and 2 of the patients underwent quaternary cytoreductive surgery, followed by salvage chemotherapy. No residue tumor was observed in these patients after quartenary cytoreduction. CCR was achieved in these two patients. The patient who were given salvage chemotherapy and external radiotherapy for extra-abdominal recurrence died due to progressive disease ( patient no 7 ) (Table 4 ).
The clinical course of AGCT progresses slowly and the prognosis is good. Mangili et al. have reported 5-year DFS as 91.5%, 10-year DFS as 71.6% and 5-year OS as 97%, 10-year OS as 95% [ 11 ]. In our study with a median follow-up period of 87 months, 5-year DFS was 85%, 10-year DFS was 83% and 5-year OS was 100%, 10-year OS was 96%. Recurrence was observed in 13.4% of the patients. In multivariate analysis, advanced stage and positive peritoneal cytology were independent poor prognostic factors for DFS. Recurrence was 114 times higher in patients with stage 2–4 compared to stage I and 4.2 times higher in patients with positive peritoneal cytology compared to those with negative peritoneal cytology.
Stage is a well-defined prognostic factor associated with recurrence and survival in ACGT. Schumer et al. have reported 5-year OS to be 75–95% in stage I, 55–75% in stage II, 50% in stage III and 22% in stage IV [ 1 ]. Karalok et al. have reported that 5-year DFS was 96% in stage I, 70% in stage III and 50% in stage IV [ 6 ]. In our study, the 5-year DFS, which was 91% in stage 1, decreased to 13% in stages 2–4.
Guidelines from ESGO, SIOPE, and ESMO currently recommend the BEP regimen as the most commonly used regimen for advanced and recurrent AGCTs [ 12 ]. However, response rates for the conventional combination of bleomycin in recent studies are only between 22 and 35% [ 13 ]. The carboplatin/paclitaxel combination is emerging as a less toxic alternative to BEP.
Adjuvant chemotherapy is advocated especially in advanced stages and macroscopic residual disease [ 2 , 10 , 11 ]. Adjuvant chemotherapy may also be considered for extensive inoperable disease or recurrent disease. However, despite the high survival rate in AGCT, the role of adjuvant chemotherapy in the early stages is unclear. According to a recent meta-analysis, the administration of adjuvant chemotherapy did not improve the oncological and prognostic outcomes of AGCT , regardless of whether the patients had early or advanced/recurrent disease [ 13 ].
The development of new targeted drugs in conjunction with molecular studies in adjuvant treatment may increase the survival rates. Among the targeted drugs investigated for AGCT, antiangiogenic drugs have garnered attention. In a study by Tsoi et al., Bevacizumab (a monoclonal anti-VEGF-A antibody) treatment demonstrated reduced tumor growth and prolonged survival in AGCT [ 14 ]. But, in an randomized clinical trial of patients with relapsed SCST, adding bevacizumab to paclitaxel did not benefit [ 15 ]. New targeted approaches, such as tumor necrosis factor-related apoptosis-inducing ligand, FOXL2'nin (Forkhead box L2), nuclear factor kappa B (NF-kB), phosphatidyl inositol-3-kinase serine/threonine kinase pathway, and mammalian target of rapamycin (mTOR), may prove effective in treating AGCT [ 16 ].
Another adjuvant treatment option is radiotherapy. Evans et al.'s study found that radiotherapy had no significant effect on the relapse rate, with relapse occurring in 20% of patients receiving radiotherapy [ 17 ]. Similarly, Ohel et al. were unable to demonstrate any advantage in the use of radiotherapy for AGCT [ 18 ]. However, contrasting these findings, more recent and comprehensive studies have indicated that adjuvant radiotherapy (RT) can prolong survival in patients with advanced or recurrent AGCT disease. In the study by Hauspy et al., adjuvant RT resulted in a significantly longer disease-free survival (DFS) [ 19 ]. Moreover, in a recent comprehensive review by Barcellini et al., RT has shown promise and feasibility for unresectable AGCT and recurrent diseases [ 20 ]. The efficacy of radiotherapy in AGCT is not well defined due to limited data.
Positive peritoneal cytology is a controversial prognostic factor in AGCT. Especially in stage I (IC), it makes receiving adjuvant chemotherapy controversial. Lee et al. have found the positive peritoneal cytology rate of 11.8% in AGCT [ 21 ]. This rate was 10.7% in our study. In the studies presented by Lee et al. and Björkholm et al. peritoneal cytology positivity was found to be significant in terms of recurrence [ 9 , 22 ]. In our study, the probability of recurrence was increased 4.2-fold in patients with positive peritoneal cytology and 5-year DFS decreased from 93 to 56%. On the contrary, in the studies of Park et al. and Ertas et al. no correlation has been demonstrated between peritoneal cytology positivity and recurrence [ 2 , 23 ].
The incidence of lymph node metastasis at primary surgery in AGCT is low. Wang et al. have reported the incidence of lymph node metastasis as a 3.9% [ 24 ]. In our study, the rate of lymph node involvement was 3.2%. The addition of lymphadenectomy to the surgical procedure did not improve oncological outcomes. Similarly, Erkılınç et al. have also reported that lymphadenectomy did not lead to improvement in DFS and OS and, on the contrary, increased postoperative morbidity [ 25 ]. Abu-Rustum et al. have reported an isolated nodal recurrence rate of 5.9% and suggested that recurrences may be due to occult nodal metastases that were not detected at the time of the initial diagnosis [ 26 ]. Nevertheless, in the study presented by ourselves, no lymphatic recurrence was detected in any of the 15 patients with recurrence. In conclusion, removal of only suspicious lymph nodes rather than routine lymphadenectomy is the preferred surgical approach in AGCT.
Surgery is the primary treatment option for newly diagnosed or recurrent AGCT. However, the limits of primary surgery are not clear. Definitive surgery for early-stage primary tumors has been demonstrated to provide no survival or recurrence advantage compared with conservative surgery. The indications and the prognosis of the conservative approach are controversial [ 27 ]. In our study, conservative surgery did not worsen DFS rates when compared to definitive surgery. As for the advanced stage and recurrent tumors on the other hand, cytoreductive surgery is the most effective treatment method [ 8 ]. Sun et al. have stated that 85% of the patients with residual tumors developed recurrence [ 27 ]. In both primary and recurrent disease surgery, cytoreduction, having the goal of leaving no residual tumor, is important in terms of recurrence and DFS.
Due to the rarity of the disease, surgical experience data for AGCT recurrence is limited and there exists no consensus on how to choose the treatment. In the study by Lee et al. and Abu Rustum et al. most of the recurrences were intraperitoneal and 70% were pelvic [ 19 , 21 ]. In our study, 93.3% of the primary recurrences were pelvic and intraabdominal and 6.6% were extra-abdominal. Recurrences in AGCT are usually focal and localized in one region [ 16 ]. In the study we presented, 66.6% of recurrences were focal and 33.3% were multifocal. This facilitates to avoid leaving residual tumor in salvage cytoreduction. Mangili et al. have reported that optimal debulking surgery is an effective treatment in case of recurrence [ 11 ]. However, recurring recurrences may develop during follow-up. In our study, surgeries have been performed on 14 out of 15 patients with recurrence, 4 out of 6 patients with second recurrence and 2 out of 3 patients with third recurrence without leaving residual tumor and complete clinical response has been obtained in all patients with the treatments offered. Whereas, 2 patients who could not undergo surgery due to extensive widespread disease died due to progressive disease in the second and third recurrence. In recurrent AGCTs, complete resection of the tumor determines survival outcomes [ 13 ]. If complete resection of the tumor can be achieved with salvage cytoreductions in recurrences, complete clinical response can be obtained in such patients.
Maximal cytoreductive surgery forms the cornerstone of treatment for primary and recurrent GCT. In cases of suboptimal surgical outcomes or unresectable metastatic disease, chemotherapy is commonly employed. However, there is limited data available on the use of adjuvant chemotherapy following complete cytoreductive surgery at recurrence [ 28 , 29 ]. Surgery is recommended for patients with relapse according to ESGO guidelines. If the patient who has undergone complete debulking has not received chemotherapy afterward, follow-up or chemotherapy may be recommended. If one has received chemotherapy, the first option after surgery is follow-up, and the second is chemotherapy [ 30 ]. Yumru-Celiksoy et al. found that no benefit was derived from adjuvant systemic treatment, of any type, following complete cytoreductive surgery in patients with GCT-relapse [ 31 ]. A study by Memorial Sloan Kettering showed that chemotherapy did not improve the recurrence-free interval of patients with GCTs, even though also non-tumor-free operated patients were included [ 32 ]. In the multicenter retrospective MITO-9 study, further relapses were observed in 33% of patients who underwent surgery alone versus 37.5% of patients who underwent secondary cytoreductive surgery followed by chemotherapy. Mangili et al. noted that postoperative residual tumor was the only risk factor for decreased survival [ 11 ]. If surgery is performed without a tumor with repeated cytoreductive surgeries, the toxicity of unnecessary subsequent chemotherapy should be avoided [ 33 ].
İnhibin is secreted by granulosa cell tumors and is a useful tumor marker that falls after tumor removal and is also a marker for tumor recurrence. CA125 is not increased in GCTs, but sometimes it is useful in detecting relapse in those with values of Alfa-fetoprotein (AFP) / Beta-Human Chorionic Gonadotropin (β-hCG) within the normal range [ 25 ]. The production of estradiol by AGCT varies widely, and its value as a tumor marker is limited [ 34 ]. In the study by Haltia et al., HE4 and CA125 levels in AGCT patients were generally found to be below normal reference limits [ 35 ]. Rey et al. demonstrated that serum AMH can be considered as a marker for the diagnosis of ovarian AGCT [ 36 ]. Robertson et al. showed that inhibin levels were not elevated in all patients with AGCT and that serum inhibin was not specific for the diagnosis of AGCT [ 37 ]. Although the hormonal activity of ovarian AGCT suggests that the synthesized hormones may serve as tumor markers, the use of these tumor markers they have limited use in diagnosis and follow-up.
The retrospective nature of the study is the most important disadvantage. The relative high number of patients, a follow-up period of approximately 90 months, lymphadenectomy in 83.9% of the patients and the fact that the surgeries were performed without leaving residual tumors constitute the strengths of the study. In the present study, all the procedures have been performed by gynecooncologists and the pathology specimens have been evaluated by gynecopathologists as well.
Advanced stage and peritoneal cytology are factors associated with survival and recurrence in AGCT. For appropriate eligible patients, offering of fertility-sparing approach at an early stage is a safe choice. Removal of suspicious lymph nodes should be preferred over systematic lymph node dissection. Most recurrences are curable with surgery and completion of surgery without leaving any residuals is the most important factor for survival. Since AGCT is rare and recurrence can occur at any stage; prospective, randomized, well-controlled and multicenter studies are required to clarify the prognostic factors.
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Şahin, M., Arslanca, T., Uçar, Y.Ö. et al. The experıance of tertıary center for adult granulosa cell tumor: whıch factors predıct survival?. J Ovarian Res 17 , 127 (2024). https://doi.org/10.1186/s13048-024-01453-w
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