Abstract
Purpose
To evaluate the cancer research effort of some major countries over two 5‐year periods (2010–2014 and 2015–2019) on the basis of scientific publications and interventional clinical trial metrics and to analyze the relationship between research effort and cancer burden (incidence and mortality).
Materials and Methods
Clinical trials were extracted from ClinicalTrials.gov using a specific query. Publications were identified in Web of Science (WoS) using a query based on keywords and were then analyzed using InCites, a bibliometric tool. Bibliometric indicators were computed per country and per period.
Results
During 2010–2019, 1 120 821 cancer‐related publications were identified in WoS, with 447 900 and 672 921 (+50%) articles respectively published in 2010–2014 and 2015–2019. Meanwhile, 38% and 7% of the articles were published in oncology and cell biology journals, respectively. Exactly 30% of the published articles were contributed by the USA. In the study period, China strongly increased its production and overspecialization. Apart from China, which had a low normalized citation impact (NCI), almost all countries increased their NCIs; in particular, France's NCI increased from 1.69 to 2.44. As for clinical trials, over 36 856 were opened worldwide during that period. Over 17 000 (46.5%) opened in the USA, which remained the leader during the study period. China ranked second worldwide in terms of the number of open trials in 2015–2019. Results revealed that the 17 cancer localizations versus cancer burden and research effort showed no evident relationship.
Conclusion
The results may provide a scientific basis for decision making for continued research. Based on bibliometric data, this type of study will aid public health policymaking and lead to a more transparent public fund allocation.
Keywords: bibliometrics, cancer, clinical trials, publications, research assessment
1. BACKGROUND
Cancer is a major public health problem throughout the world. In fact, reports from the World Health Organization showed approximately 9.6 million cancer‐related deaths in 2018, or about one in six deaths, thus making cancer the second leading cause of mortality worldwide. 1 In the same year, the number of new cases was estimated at 18.1 million. 2 , 3 Cancer is also a pathology that affects many organs. In this regard, there are many types of mortality depending on the affected organs, gender, socioeconomic factors, and geographic area. The economic impacts of cancer are also substantial, with global costs estimated at 1.2 billion dollars in 2010. 4
Individual nations have established unique structures dedicated to the care of cancer patients. These structures have also resulted in numerous research programs targeted at cancer diagnosis and management. While many data are available on the prevalence, incidence, and mortality rate of cancer, 3 , 5 , 6 there is a lack of information concerning the research activities carried out in oncology. In 2019, approximately 60 000 articles were published in oncology journals across the world, thus putting oncology in eighth place among all disciplines and first among the medical disciplines (Web of Science (WoS)/Incites data). In this regard, many robust databases are available for finding and retrieving scientific publications, with notable resources including PubMed, WoS (Clarivate Analytics), Scopus (Elsevier), and CrossRef. These databases are further reinforced by analytical tools such as InCites (Clarivate Analytics) and SciVal (Elsevier), which enable researchers to conduct bibliometric analyses on the basis of factors such as the specific discipline (e.g., oncology, neurology), country of origin, and affiliated institution. However, from 1995 to 2019, only about 250 bibliometric studies related to cancer are shown in PubMed. These include studies describing the 50 or 100 most cited articles in a given cancer site or articles describing the evolution of the number of publications about a given cancer type. These studies are generally limited to a single cancer 7 , 8 , 9 or to a single country of origin. 10 In fact, none of the available studies measured scientific output at the global level, by country of origin, or for all cancers combined. Addressing this gap is the objective of the current work.
In order to guarantee the transparency of results, the International Committee of Medical Journal Editors requires that all clinical studies be declared in an international registry prior to initiation. 11 Here, researchers may use the ClinicalTrials.gov database, which was established in 2000, 12 specifically to declare the main parts of all relevant studies. As such, the database provides access to information on clinical trials initiated around the world, thus making it possible to measure research efforts in a given pathology based on the country of origin. In this study, the main objective of gathering information on scientific publications and interventional clinical trials was to measure the cancer research efforts (quantitative and qualitative data) of different countries over two separate five‐year periods, namely, 2010–2014 and 2015–2019. A five‐year period is used in many bibliometric indicators and academic and research‐related institution ranking, such as Shanghai Ranking 13 or SCImago. 14
We searched the two following databases:
The WoS database and InCites platform, which provide volumes of publications per country and individual article impacts in terms of the number of received citations;
The ClinicalTrials database, which provides information related to clinical trial involvement.
Analyses were first performed for all cancers combined and then by individual location while distinguishing between hematologic and solid tumors. This essentially constituted an analysis of all cancers combined.
2. METHODS
Data on publications were extracted from the WoS, 15 which is marketed by Clarivate Analytics. The WoS categorizes journals based on their stated disciplines (e.g., neuroscience, surgery, or immunology) 16 ; the oncology category therefore consists of specific oncology journals. Previous internal analyses conducted on these WoS categories have revealed that only one‐third of all cancer publications have been published in oncology journals, as oncology is a very transversal discipline, while the remaining two‐thirds have been published in specialty journals (e.g., neurology, pneumology, or urology). In order to count all publications, we used the following criteria for our search query:
Published in a cancer journal;
Contains cancer‐generic keywords in the title (Title field in the WoS) or author keywords (Author Keywords field in the WoS); examples include “cancer,” “tumor,” and “neoplasms”;
Contains specific localization cancer keywords in the title or author keywords; examples include “glioma,” “glioblastoma,” and “mesothelioma.”
We identified appropriate keywords for our searches by using terms available in the “Medical Subject Headings,” a controlled vocabulary thesaurus used in Medline for indexing articles, 17 and by selecting those found in a sample of articles published in oncology journals. The resulting list was subsequently validated by two oncology experts, Pr. X. Troussard from CHU Caen Normandie 18 , 19 and Pr. JP Metges from CHU de Brest. 20 , 21 We then examined the contributions from major countries with reference to the global output, as determined based on the number of articles with authors from each country. We also compared the production of different countries with reference to their overall production in biomedical research (Medical & Health Science in the WoS database) and citation impact. The following two bibliometric indicators were also computed:
The specialization index (SI), which is the ratio of the percentage of articles from a given country related to specific areas of disease to the percentage of articles concerning the same areas of disease worldwide. Index values >1 indicate that the given country has an overspecialization in that disease area while index values <1 indicate underspecialization. The SI is a robust indicator with which we can observe the general changes in the research profile of a country over time. 22
The category normalized citation impact (CNCI or NCI); for a given article, the CNCI is the ratio of the observed number of citations to the expected number of citations (defined as the mean number of citations for all articles published in the same year in the same WoS category). Here, a normalized bibliometric indicator compensates for the fact that the number of citations a given article receives is partly influenced by the year of publication (i.e., older articles have more opportunities for citation) and size of the scientific field. 23 The CNCI of a given country is the mean CNCI of all articles co‐authored by that country; the benchmark value is 1, with higher CNCI values reflecting higher impacts in terms of citation numbers.
Next, we conducted our bibliometric analysis using the InCites analytical tool, 24 which was developed by Clarivate Analytics based on data indexed in the WoS. In this study, we only analyzed documents that were categorized as “Article” or “Review” in the WoS. We then extracted clinical trial data from ClinicalTrials.gov, specifically considering all interventional studies in cancer (Condition = Cancer) that were initiated from 2010 to 2019 across the world. The field “Country” identified the different countries participating in each study while the “Conditions” field made it possible to reclassify studies according to the different types of investigated cancer. Finally, the “Funder” field was used to determine whether studies were promoted by an academic institution or industry.
3. RESULTS
3.1. Scientific publications
For the period of 2010–2019, we found a total of 1 120 821 cancer‐related publications in the WoS, including 447 900 from 2010–2014 and 672 921 from 2015–2019, reflecting an increase of just over 50%. Table 1 shows the number of publications by discipline (WoS categories). From 2015 to 2019, only 38.2% of publications were found in oncology journals. Excluding cell biology (+2.1%), experimental medicine (+2.2%), and hematology (−1.3%), the distributions changed slightly between the two periods in terms of discipline.
TABLE 1.
First 25 Web of Science categories of cancer articles from 2010 to 2019
| 2010–2014 | 2015–2019 | ||||
|---|---|---|---|---|---|
| Web of Science Category | Total | Number of Publications | Number of Publications | ||
| All articles | 1 120 821 | 447 900 | Part (%) | 672 921 | Part (%) |
| Oncology | 425 926 | 169 130 | 37.8 | 256 796 | 38.2 |
| Cell Biology | 80 100 | 26 328 | 5.9 | 53 772 | 8.0 |
| Surgery | 76 285 | 34 591 | 7.7 | 41 694 | 6.2 |
| Medicine, Research, & Experimental | 67 585 | 21 024 | 4.7 | 46 561 | 6.9 |
| Biochemistry & Molecular Biology | 67 146 | 28 591 | 6.4 | 38 555 | 5.7 |
| Radiology, Nuclear Medicine, & Medical Imaging | 61 237 | 26 428 | 5.9 | 34 809 | 5.2 |
| Pharmacology & Pharmacy | 57 152 | 22 554 | 5.0 | 34 598 | 5.1 |
| Hematology | 51 872 | 24 347 | 5.4 | 27 525 | 4.1 |
| Pathology | 47 811 | 20 917 | 4.7 | 26 894 | 4.0 |
| General & Internal Medicine | 43 815 | 13 276 | 3.0 | 30 539 | 4.5 |
| Gastroenterology & Hepatology | 39 489 | 17 673 | 3.9 | 21 816 | 3.2 |
| Multidisciplinary Sciences | 38 782 | 15 612 | 3.5 | 23 170 | 3.4 |
| Immunology | 36 822 | 16 212 | 3.6 | 20 610 | 3.1 |
| Genetics & Heredity | 27 840 | 12 580 | 2.8 | 15 260 | 2.3 |
| Clinical Neurology | 27 310 | 12 124 | 2.7 | 15 186 | 2.3 |
| Urology & Nephrology | 27 258 | 11 857 | 2.6 | 15 401 | 2.3 |
| Obstetrics & Gynecology | 25 017 | 11 224 | 2.5 | 13 793 | 2.0 |
| Biotechnology & Applied Microbiology | 23 214 | 9167 | 2.0 | 14 047 | 2.1 |
| Public, Environmental, & Occupational Health | 22 711 | 10 143 | 2.3 | 12 568 | 1.9 |
| Chemistry, Multidisciplinary | 21 080 | 6168 | 1.4 | 14 912 | 2.2 |
| Endocrinology & Metabolism | 18 376 | 8239 | 1.8 | 10 137 | 1.5 |
| Chemistry, Medicinal | 18 354 | 7819 | 1.7 | 10 535 | 1.6 |
| Respiratory System | 16 943 | 7139 | 1.6 | 9804 | 1.5 |
| Pediatrics | 15 267 | 7194 | 1.6 | 8073 | 1.2 |
| Biophysics | 14 536 | 6417 | 1.4 | 8119 | 1.2 |
Note: List of the first 25 Web of Science categories in which cancer articles have been published.
Table 2 shows the number of publications and ranks for both investigated periods, specifically concerning the 20 countries with the highest scientific production rates in the area of cancer from 2010 to 2019 (WoS documents retrieved through the query). These data were compared with all medical research (Medical & Health Sciences) and documents published in oncology journals. As such, we found that the largest contribution was provided by the United States for both periods while China's contribution increased from fourth to second for all medical disciplines and remained stable in the second position for cancer during both periods. Japan and South Korea were also better positioned in oncology than in medical research at large. Conversely, the United Kingdom was better positioned for medical research at large than for cancer research. This suggests the existence of overspecialization in China, Japan, and South Korea and underspecialization in the United Kingdom. The percentage of articles published by each country in oncology journals is mostly close to the world average of 43.2% (484 298/1 120 821), except a few countries with lower rates, including Brazil with 28.9% (5806/20096), India with 34.0% (11 695/34402), and Turkey with 34.9% (7435/21278); and a few countries with higher rates, including Sweden with 48.5% (9449/19493), Canada with 48.5% (21 806/44954), the Netherlands with 48.9% (15 815/32365), and Belgium with 50.4% (7681/15229).
TABLE 2.
World ranking for cancer‐related biomedical research and cancer‐related articles in oncology journals
| Cancer | Medical & health sciences | Cancer documents in the Web of Science | Oncology journals | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 2010–2019 | 2010–2014 | 2015–2019 | 2010–2014 | 2015–2019 | 2010–2014 | 2015–2019 | |||||||
| Country | Nb docs | Nb docs | Rank | Nb docs | Rank | Nb docs | Rank | Nb docs | Rank | Nb docs | Rank | Nb docs | Rank |
| World | 1 120 821 | 2 599 256 | 3 206 267 | 447 900 | 672 921 | 200 810 | 283 488 | ||||||
| USA | 334 212 | 856 893 | 1 | 997 732 | 1 | 145 541 | 1 | 188 671 | 1 | 71 278 | 1 | 86 687 | 1 |
| China | 233 415 | 182 821 | 4 | 398 470 | 2 | 66 373 | 2 | 167 042 | 2 | 29 595 | 2 | 81 117 | 2 |
| Japan | 82 898 | 147 206 | 5 | 169 870 | 5 | 36 144 | 3 | 46 754 | 3 | 15 969 | 3 | 20 007 | 3 |
| Germany | 75 024 | 183 806 | 3 | 208 346 | 4 | 33 595 | 4 | 41 429 | 4 | 14 400 | 4 | 17 743 | 4 |
| Italy | 68 160 | 133 040 | 6 | 162 590 | 6 | 28 583 | 6 | 39 577 | 5 | 12 569 | 6 | 16 764 | 5 |
| UK | 67 289 | 222 553 | 2 | 269 254 | 3 | 29 073 | 5 | 38 216 | 6 | 13 356 | 5 | 16 100 | 6 |
| France | 51 652 | 112 053 | 8 | 128 922 | 9 | 22 905 | 7 | 28 747 | 7 | 10 596 | 7 | 13 177 | 7 |
| South Korea | 48 028 | 81 807 | 13 | 105 690 | 13 | 19 717 | 8 | 28 311 | 8 | 7622 | 9 | 11 003 | 9 |
| Canada | 44 954 | 130 399 | 7 | 161 455 | 7 | 19 061 | 9 | 25 893 | 9 | 9696 | 8 | 12 110 | 8 |
| India | 34 402 | 86 077 | 11 | 117 868 | 10 | 10 442 | 13 | 23 960 | 10 | 4545 | 13 | 7150 | 13 |
| Spain | 33 567 | 85 991 | 12 | 108 092 | 11 | 14 012 | 10 | 19 555 | 12 | 5727 | 12 | 8045 | 12 |
| Australia | 32 910 | 105 142 | 9 | 147 331 | 8 | 13 085 | 12 | 19 825 | 11 | 6209 | 11 | 8571 | 11 |
| Netherlands | 32 365 | 87 212 | 10 | 106 754 | 12 | 13 889 | 11 | 18 476 | 13 | 6947 | 10 | 8868 | 10 |
| Taiwan | 22 711 | 39 323 | 19 | 44 639 | 20 | 9993 | 14 | 12 718 | 15 | 3709 | 16 | 5535 | 14 |
| Turkey | 21 278 | 64 793 | 15 | 79 798 | 15 | 7980 | 16 | 13 298 | 14 | 3675 | 17 | 3760 | 18 |
| Brazil | 20 096 | 81 597 | 14 | 100 636 | 14 | 7730 | 18 | 12 366 | 16 | 2230 | 20 | 3576 | 20 |
| Sweden | 19 493 | 51 175 | 17 | 65 025 | 17 | 8437 | 15 | 11 056 | 18 | 4314 | 14 | 5135 | 16 |
| Switzerland | 19 179 | 54 771 | 16 | 71 512 | 16 | 7848 | 17 | 11 331 | 17 | 3765 | 15 | 5217 | 15 |
| Poland | 16 582 | 34 704 | 20 | 46 585 | 19 | 6530 | 19 | 10 052 | 19 | 2621 | 19 | 3690 | 19 |
| Belgium | 15 229 | 40 300 | 18 | 50 776 | 18 | 6339 | 20 | 8890 | 20 | 3252 | 18 | 4429 | 17 |
Abbreviations: Nb docs, number of documents (articles and reviews) published; Rank, world ranking for cancer‐related biomedical research (medical & health sciences) and cancer‐related articles in oncology journals (20 main countries).
Notice that the number of publications in oncology journals is not exactly the same between Tables 1 and 2. This is due to the fact that publications from multidisciplinary journals may be reclassified into specific subject areas in Incites.
Figure 1 shows the 10 countries with the highest outputs in oncology journals over the entire investigated period as well as the evolution of their specialization indices (national over‐ and underspecializations shown for given fields) and normalized impact indices (citation impacts) between the subdivided periods. First, China clearly showed a strong overspecialization (which increased again between the two periods), along with somewhat lesser overspecializations in Japan, Italy, South Korea, and France. There was also a notable underspecialization in the United Kingdom. Apart from China, which currently shows a low CNCI, almost all countries increased their CNCIs. This was particularly evident in France, which showed an increase from 1.69 to 2.44.
FIGURE 1.
CNCI and SI evolution of the top 10 countries with the highest numbers of cancer‐related publications. Evolution between 2010–2014 and 2015–2019 regarding the normalized citation impact (CNCI) and specialization index (SI) for the 10 countries with the highest numbers of cancer‐related publications. Bubble sizes are correlated with the number of publications
3.2. Clinical trials
A total of 175 309 interventional studies were initiated worldwide from 2010 to 2019, and these include 36 856 cancer‐related studies; a comparison of the years 2010 and 2019 showed 2848 and 4571 articles, respectively. This overall percentage of around 20% remained stable over the 10‐year investigated period. Of the 36 856 total studies, 1% received US federal funding, 11% received funding from the National Institute of Health, 38% received industrial funding, and 75% received “other funding” (a single study could also receive co‐funding). The “other” category mainly referred to studies that were promoted by academic institutions (e.g., hospitals, universities) or research groups (e.g., the European Organization for Research and Treatment of Cancer, Brussels, Belgium). Table 3 shows the 20 countries with the highest number of interventional cancer studies initiated over the investigated period while Figure 2 shows the global rankings. With more than 17 000 studies, the United States participated in 46.5% of all such studies initiated worldwide and remained the leader over the entire period. It was followed by China, which showed a strong increase, specifically rising from ninth place in the world in 2010 to second place in 2019, thus surpassing France, which nevertheless moved up to third place. We also observed a strong progression in Spain, which exceeded Canada in 2019. Conversely, Germany dropped from fourth to ninth. Further, the national rankings differed significantly when categorized based on funding; for example, Spain sharply increased its rank in industrial studies while China and France sharply increased their ranks in academic studies. 25
TABLE 3.
Top 20 most prominent countries in terms of cancer‐related clinical trials
| Country | TOTAL | 2010 | 2011 | 2012 | 2013 | 2014 | 2015 | 2016 | 2017 | 2018 | 2019 | Part (%) | % Evol 2010/2019 a |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| GLOBAL | 36 856 | 2848 | 2961 | 3033 | 3129 | 3468 | 3887 | 4131 | 4327 | 4501 | 4571 | +60 | |
| USA | 17 148 | 1536 | 1487 | 1495 | 1535 | 1643 | 1776 | 1753 | 2003 | 2016 | 1904 | 46.5 | +24 |
| China | 4759 | 154 | 214 | 260 | 302 | 348 | 503 | 661 | 676 | 764 | 877 | 12.9 | +469 |
| France | 3730 | 284 | 322 | 344 | 364 | 374 | 415 | 404 | 401 | 422 | 400 | 10.1 | +41 |
| Canada | 2857 | 259 | 248 | 275 | 274 | 304 | 291 | 328 | 326 | 302 | 250 | 7.8 | −3 |
| Spain | 2501 | 154 | 208 | 224 | 249 | 260 | 272 | 280 | 314 | 285 | 255 | 6.8 | +66 |
| Germany | 2444 | 214 | 272 | 246 | 241 | 261 | 288 | 252 | 253 | 242 | 175 | 6.6 | −18 |
| UK | 2403 | 176 | 214 | 216 | 241 | 266 | 272 | 255 | 324 | 244 | 195 | 6.5 | +11 |
| Italy | 2392 | 184 | 202 | 232 | 256 | 266 | 265 | 235 | 283 | 262 | 207 | 6.5 | +13 |
| South Korea | 2169 | 187 | 186 | 192 | 211 | 233 | 258 | 211 | 263 | 253 | 175 | 5.9 | −6 |
| Belgium | 1614 | 129 | 141 | 154 | 192 | 170 | 170 | 147 | 187 | 185 | 139 | 4.4 | +8 |
| Netherlands | 1505 | 116 | 124 | 126 | 156 | 183 | 188 | 158 | 164 | 158 | 132 | 4.1 | +14 |
| Australia | 1467 | 98 | 108 | 115 | 138 | 149 | 165 | 133 | 207 | 192 | 162 | 4.0 | +65 |
| Japan | 1153 | 92 | 94 | 97 | 107 | 114 | 138 | 117 | 151 | 128 | 115 | 3.1 | +25 |
| Taiwan | 1073 | 69 | 70 | 81 | 91 | 135 | 127 | 110 | 140 | 142 | 108 | 2.9 | +57 |
| Poland | 1047 | 82 | 98 | 93 | 107 | 110 | 118 | 102 | 128 | 109 | 100 | 2.8 | +22 |
| Denmark | 927 | 59 | 79 | 62 | 102 | 104 | 113 | 98 | 116 | 108 | 86 | 2.5 | +46 |
| Israel | 877 | 65 | 71 | 69 | 103 | 92 | 95 | 94 | 105 | 98 | 85 | 2.4 | +31 |
| Russia | 844 | 71 | 102 | 75 | 84 | 70 | 91 | 74 | 103 | 90 | 84 | 2.3 | +18 |
| Brazil | 735 | 57 | 77 | 65 | 59 | 70 | 80 | 60 | 101 | 86 | 80 | 2.0 | +40 |
| Austria | 688 | 66 | 66 | 71 | 77 | 73 | 79 | 64 | 71 | 63 | 58 | 1.9 | −12 |
Note: List of the 20 most prominent countries classified on the basis of the number of cancer‐related clinical trials initiated from 2010 to 2019.
“% Evol 2010/2019” = [(Number of publications in 2019/Number of publications in 2010) − 1] × 100.
FIGURE 2.
Top 10 country rankings in terms of the number of cancer‐related interventional clinical trials. Evolution of top 10 countries' yearly rankings in terms of the number of cancer‐related interventional clinical trials from 2010 to 2019
3.3. Relationship between the burden of cancer localization and research production
Table 4 shows the number of new cases and deaths in 2018 for the main cancers at the global level as well as the numbers of clinical trials and publications from 2015 to 2019. There are some immediately noticeable differences in the rankings for epidemiological data (incidence and mortality) and research efforts (clinical trials and publications). For one, breast cancer showed the highest incidence rate, with intermediate mortality (sixth rank) and high research efforts, while hematology ranked first in terms of research but substantially lower in terms of incidence (sixth) and mortality (fifth). In addition, esophageal and gastric cancers ranked fourth and second in terms of incidence and mortality but ranked eighth and tenth in terms of research, respectively.
TABLE 4.
Incidence versus mortality versus opened trials versus publications
| Incidence | Mortality | Trials | Publications | |||||
|---|---|---|---|---|---|---|---|---|
| 2018 | 2018 | 2015–2019 | 2015–2019 | |||||
| Cancer localization | Nb cases | Rank | Nb cases | Rank | Nb | Rank | Nb | Rank |
| Breast | 2 261 419 | 1 | 684 996 | 6 | 2595 | 2 | 64 046 | 2 |
| Lung | 2 237 641 | 2 | 1 822 422 | 1 | 2227 | 3 | 50 522 | 3 |
| Colorectal | 1 931 590 | 3 | 935 173 | 3 | 1510 | 4 | 38 229 | 4 |
| Esophagus & Stomach | 1 693 203 | 4 | 1 312 869 | 2 | 976 | 8 | 27 339 | 10 |
| Prostate | 1 414 259 | 5 | 375 304 | 10 | 1209 | 5 | 27 909 | 8 |
| Hematology | 1 278 362 | 6 | 711 840 | 5 | 3490 | 1 | 103 772 | 1 |
| Uterus | 1 021 494 | 7 | 439 201 | 9 | 618 | 13 | 8672 | 16 |
| Head & Neck | 931 931 | 8 | 467 125 | 7 | 947 | 9 | 27 534 | 9 |
| Liver | 905 677 | 9 | 830 180 | 4 | 768 | 11 | 28 566 | 7 |
| Thyroid | 586 202 | 10 | 43 646 | 16 | 208 | 16 | 10 531 | 14 |
| Bladder | 573 278 | 11 | 212 536 | 12 | 419 | 14 | 9931 | 15 |
| Pancreas | 495 773 | 12 | 466 003 | 8 | 772 | 10 | 15 694 | 12 |
| Kidney | 431 288 | 13 | 179 368 | 14 | 403 | 15 | 11 127 | 13 |
| Skin | 324 635 | 14 | 57 043 | 15 | 1116 | 6 | 37 884 | 5 |
| Ovary | 313 959 | 15 | 207 252 | 13 | 679 | 12 | 15 779 | 11 |
| Brain | 308 102 | 16 | 251 329 | 11 | 1009 | 7 | 37 596 | 6 |
| Testis | 74 458 | 17 | 9334 | 17 | 32 | 17 | 2147 | 17 |
Note: Incidence (number of cases in 2018), mortality (number of cases in 2018), number of opened trials (2015 to 2019), number of publications (2015 to 2019) and ranks of 17 cancer localizations.
4. DISCUSSION
By finding both the number of publications and number of registered clinical trials, this study explored the breadth of cancer research at the global level and based on the different types of cancer. At the global level, we found discrepancies between the burdens of cancer by incidence and mortality rates as well as in research production. Although Miao, 7 Akmal, 8 and Andersen 9 used similar methodologies, their investigations were restricted to scientific production rates for esophagogastric cancer, glioblastoma, and hematology. As our searches were based on specific keyword queries, the number of returned publications might not have been exhaustive. However, our objective was to compare different countries over two unique periods, in which case any potential bias should not imply a significant difference in rankings. In fact, the proportion of publications found in oncology journals (nearly 38%) confirmed that our decision to conduct a keyword analysis was appropriate. By querying the ClinicalTrials.gov database, we were also able to observe a rapid increase for China and Spain regarding their participation in cancer‐related clinical trials. Unfortunately, inclusion data are not available through ClinicalTrials.gov; the figures also presented centers without inclusion. Further, only interventional studies were included as many other types of studies (e.g., registries or population‐based studies) may be conducted without registration.
The United States played a leading role in cancer research in the 10‐year investigated period, accounting for around 30% of all related publications and 46% of clinical trials. However, major developments are evident in other countries over the same period. For example, China made significant progress, as shown by its SI (>2). In Japan, an intense and persistent overspecialization might have been catalyzed due to the fallout from Hiroshima and Nagasaki, with sustaining factors, including a voluntary policy targeted at esophageal cancer screening, which has been implemented for more than 20 years, and a generally high incidence of cancer (more than one million new cases in 2018). Meanwhile, the United Kingdom showed underspecialization (decreasing over the second period of investigation) and increasing NCI, both of which are surprising in view of its cancer incidence rate (similar to those found in Japan, France, and Italy) and high level of scientific production in biomedical research. The results are similar when looking at clinical trials. Finally, it should be noted that France is well‐positioned in terms of the citation impact of scientific publications (NCI rose from 1.69 to 2.44) and clinical trials (third in the world). These advancements may partly be explained based on the implementation of three successive cancer plans (from 2003 to 2019) and substantial provisions of dedicated resources.
We also found a strong correlation between the number of registered trials and number of publications. There was only a weak correlation between epidemiological data (incidence and mortality) and research efforts (trials and publications). This may partly be explained by the different prevalence rates for certain cancers between countries (e.g., high rates of breast cancer in the United States, colorectal cancer in Japan, and prostate cancer in the United Kingdom). Further, cancer research is not coordinated at the global level, meaning that individual countries tend to focus on different cancers. Carter 26 and Coronado 27 evaluated the relationship between research funding and societal burdens at several cancer sites in the United Kingdom and Canada and showed various rates of over‐ and underfunding after adjusting for mortality and life expectancy.
5. CONCLUSIONS
The data herein could offer general value and constitute a scientific basis for deciding which areas of focus are most appropriate in continued research at the continental, national, and regional levels, specifically in locations with high rates of mortality. Based on bibliometric data, this type of study should also contribute to the formation of public health policies while encouraging the more transparent allocation of public and associated types of funding.
AUTHOR CONTRIBUTIONS
Vincent Akiki: Data curation (equal); formal analysis (equal); methodology (equal); visualization (equal); writing – review and editing (equal). Xavier Troussard: Validation (equal); writing – review and editing (equal). Jean‐Philippe Metges: Validation (equal); writing – review and editing (equal). Patrick Devos: Conceptualization (equal); formal analysis (equal); methodology (equal); project administration (equal); supervision (lead); visualization (equal); writing – original draft (equal); writing – review and editing (equal).
FUNDING INFORMATION
This research did not receive any specific grant from funding agencies in the public, commercial, or not‐for‐profit sectors.
CONFLICT OF INTEREST
The authors have stated explicitly that there are no conflicts of interest in connection with this article.
ETHICS STATEMENT
This study is a review of data from ClinicalTrials.gov and Web of Science. It does not require ethics approval.
ACKNOWLEDGMENTS
We would like to thank Joel Menard for his valuable advice concerning this research and Editage (www.editage.com) for the English language editing service.
Akiki V, Troussard X, Metges J‐P, Devos P. Global trends in oncology research: A mixed‐methods study of publications and clinical trials from 2010 to 2019. Cancer Reports. 2023;6(1):e1650. doi: 10.1002/cnr2.1650
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
REFERENCES
- 1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394‐424. doi: 10.3322/caac.21492 [DOI] [PubMed] [Google Scholar]
- 2. World Health Organization, International Agency for Research on Cancer – Cancer Today. Accessed May 9, 2022. https://gco.iarc.fr/today
- 3. Ferlay J, Colombet M, Soerjomataram I, et al. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 2019;144(8):1941‐1953. doi: 10.1002/ijc.31937 [DOI] [PubMed] [Google Scholar]
- 4. World Health Organization, International Agency for Research on Cancer – World Cancer Report 2014. Accessed May 9, 2022. https://publications.iarc.fr/Non-Series-Publications/World-Cancer-Reports/World-Cancer-Report-2014
- 5. IHME – Global Burden of Disease (GBD). Accessed May 9, 2022. http://www.healthdata.org/gbd/2019
- 6. Allemani C, Matsuda T, Di Carlo V, et al. Global surveillance of trends in cancer survival 2000‐14 (CONCORD‐3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population‐based registries in 71 countries. Lancet. 2018;391(10125):1023‐1075. doi: 10.1016/S0140-6736(17)33326-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Miao Y, Liu R, Pu Y, Yin L. Trends in esophageal and esophagogastric junction cancer research from 2007 to 2016: a bibliometric analysis. Medicine (Baltimore). 2017;96(20):e6924. doi: 10.1097/MD.0000000000006924 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Akmal M, Hasnain N, Rehan A, et al. Glioblastome multiforme: a bibliometric analysis. World Neurosurg. 2020;136:270‐282. doi: 10.1016/j.wneu.2020.01.027 [DOI] [PubMed] [Google Scholar]
- 9. Andersen JP, Bogsted M, Dybkaer K, et al. Global myeloma research clusters, output, and citations: a bibliometric mapping and clustering analysis. PLoS One. 2015;10(1):e0116966. doi: 10.1371/journal.pone.0116966 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Chua TC, Crowe PJ, Morris DL. Trends in surgical oncology research in Australia during the period 1998–2009—a bibliometric review. J Surg Oncol. 2011;104(2):216‐219. doi: 10.1002/jso.21942 [DOI] [PubMed] [Google Scholar]
- 11. ICMJE Recommendations – Clinical Trials. Accessed May 9, 2022. http://www.icmje.org/recommendations/browse/publishing-and-editorial-issues/clinical-trial-registration.html
- 12. ClinicalTrials.gov. Accessed May 9, 2022. https://clinicaltrials.gov/
- 13. ShanghaiRanking's Academic Ranking of World Universities Methodology. Accessed May 9, 2022. https://www.shanghairanking.com/methodology/arwu/2021
- 14. SCIMAGO – Ranking Methodology. Accessed May 2, 2022. www.scimagoir.com/methodology.php
- 15. Web of Science Core Collection. Accessed March 16, 2021. clarivate.com/webofsciencegroup/solutions/web-of-science-core-collection/
- 16. Web of Science Research Areas. Accessed May 9, 2022. incites.help.clarivate.com/Content/Research-Areas/wos-research-areas.htm
- 17. MESH browser – Neoplasms MeSH Descriptor. Accessed May 9, 2022. https://meshb.nlm.nih.gov/record/ui?ui=D009369
- 18. Hermine O, Lefrere F, Bronowicki JP, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med. 2002;347(2):89‐94. doi: 10.1056/NEJMoa013376 [DOI] [PubMed] [Google Scholar]
- 19. Troussard X, Grever MR. The revised guidelines for the diagnosis and management of hairy cell leukaemia and the hairy cell leukaemia variant. Br J Haematol. 2021;193(1):11‐14. doi: 10.1111/bjh.17201 [DOI] [PubMed] [Google Scholar]
- 20. Kojima T, Shah MA, Muro K, et al. Randomized phase III KEYNOTE−181 study of pembrolizumab versus chemotherapy in advanced esophageal cancer. J Clin Oncol. 2020;38(35):4138‐4148. doi: 10.1200/JCO.20.01888 [DOI] [PubMed] [Google Scholar]
- 21. Vidal O, Soriano‐Izquierdo A, Pera M, et al. Positive VEGF immunostaining independently predicts poor prognosis in curatively resected gastric cancer patients: results of a study assessing a panel of angiogenic markers. J Gastrointest Surg. 2008. June;12(6):1005‐1014. doi: 10.1007/s11605-007-0336-3 [DOI] [PubMed] [Google Scholar]
- 22. Aksnes DW, van Leeuwen TN, Sivertsen G. The effect of booming countries on changes in the relative specialization index (RSI) on country level. Scientometrics. 2014;101(2):1391‐1401. doi: 10.1007/s11192-014-1245-3 [DOI] [Google Scholar]
- 23. Waltman L. A review of the literature on citation impact indicators. J Informet. 2016;10(2):365‐391. doi: 10.1016/j.joi.2016.02.007 [DOI] [Google Scholar]
- 24. InCites Analytics. Accessed November 14, 2020. https://clarivate.com/products/incites/
- 25. CNCR – What is France's Place in Terms of Cancer Research? Global Report. Accessed May 2, 2022. https://www.cncr.fr/wp-content/uploads/2022/01/CNCR-LaRechercheEnCancerologie_v1-EN.pdf
- 26. Carter AJR, Delarosa B, Hur H. An analysis of discrepancies between United Kingdom cancer research funding and societal burden and a comparison to previous and United States values. Health Res Policy Syst. 2015;13:62. doi: 10.1186/s12961-015-0050-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Coronado AC, Finley C, Badovinac K, Han J, Niu J, Rahal R. Discrepancies between Canadian cancer research funding and site‐specific cancer burden: a spotlight on ten disease sites. Curr Oncol. 2018;25(5):338‐341. doi: 10.3747/co.25.4230 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.