CANCER RESEARCH INVESTMENT: TOP-DOWN VERSUS BIBLIOMETRIC APPROACH
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1 Rev. Med. Chir. Soc. Med. Nat., Iaşi 2015 vol. 119, no. 3 PREVENTIVE MEDICINE UPDATES CANCER RESEARCH INVESTMENT: TOP-DOWN VERSUS BIBLIOMETRIC APPROACH Mioara Calipsoana Matei 1,2,3, V.Chirica 1,2*, Doina Azoicai 1,2,3, F.D. Petrariu 1, L.Oprea 1,4 University of Medicine and Pharmacy Grigore T. Popa - Iasi Faculty of Medicine 1. Department of Preventive Medicine and Interdisciplinarity 2. Department of Oncogenetics 3. Iasi Clinical Epidemiology Unit 4. Centre for Ethics and Health Policy *Corresponding author: valeriu.chirica@yahoo.com CANCER RESEARCH INVESTMENT: TOP-DOWN VERSUS BIBLIOMETRIC AP- PROACH (Abstract): Cancer is a complex chronic disease with a real burden that goes b e- yond the individuals and their families to healthcare budgets and society. At the global level there are still many gaps in the knowledge on cancer research funding and activity. The aim of this paper is to present two approaches that can be used for the collection of data on cancer research investment. Material and methods: A scientific literature search was performed within the three databases (PubMed, Science Direct and OVID MEDICAL), using different combinations of some key words. Results: We identified 7 papers that used the top-down method and 4 that used the bibliometric approach for data collection on cancer research investment. Using the first method, usually the cancer research funding from public domain were cached, while using the second the overall expenditure (including indirect funding) could be estimated. Conclusions: The best approach for the collection of cancer research funding information is a combination of bibliometric with top-down / bottom-up methods, which allows the assessment of oncological research activity and impact, but also the evaluation of the amount of money invested on cancer research from different perspe c- tives. Keywords: CANCER, RESEARCH, FUNDING, BIBLIOMETRIC APPROACH, TOP-DOWN APPROACH. Cancer is a complex chronic disease, which change forever the life of an individual affected by it. Also, cancer is one of the leading causes of death worldwide (1). The real burden of this disease goes beyond the individuals and their families to healthcare budgets and society. With more than 14 billion euro global expenditure on oncological research (2) and an upward trend in the burden of this disease worldwide (3), cancer is one of the major global policy issues. Many financial resources were invested to study cancer initiation, etiology, diagnosis, prognosis, prevention, and treatment (4) and different methods were used to assess these expenses. But these financial resources are limited and all these methods have advantages and disadvantages. So, the correct allocation of the funds is very important. In order to help this 828
2 Cancer research investment: top-down versus bibliometric approach allocation of funds according to the burden of cancer in a specific population/ society, there is a need to obtain information on oncological research investment in different countries, regions, continents or worldwide (Europe, United States of America USA, Canada, Australia and Asia). There are some examples of studies in the literature which provide such an analysis (4, 5, 7, 19, 20), but at the global level there are still many gaps in the knowledge on cancer research funding and activity. To map the funding priorities in cancer research in order to correspond to the actual population/society needs is a major policy issue, but the collection of this data is usually hard (27). The aim of this paper is to present two approaches that can be used for the collection of data on cancer research investment. MATERIAL AND METHODS We performed a scientific literature search within the three databases (PubMed, Science Direct and OVID MEDICAL), using different combinations of some key words: cancer (or neoplasm or malignancy) AND research AND funding (or expenses or expenditure or costs). Also, another search was performed using the following combinations: cancer research funding in Europe ; cancer research funding in Asia ; cancer research funding in Australia ; cancer research funding in Canada and cancer research funding in USA. The total number of paper (including duplicates) obtained in PubMed was 20,957, in Science Direct was 87,560, and in OVID MEDICAL [Ovid MEDLINE (R) 1946 to February Week 4, 2015] was 5,617. After duplicate removal, the titles and abstracts of the remaining articles were evaluated against the following inclusion criteria: (1) published between 2005 and 2014; (2) published in English; (3) full text; (4) humans as subjects; (5) worldwide. A secondary literature search was performed using the references cited in the selected papers. A total of 22 articles were identified, for which the full-text version were obtained. From these papers 7 used the topdown method and 4 used the bibliometric approach for data collection. RESULTS The scientific papers reporting on oncological research funding were conducted in the following geographical regions: Europe (2, 5, 6, 7, 8, 9, 10, 11, 12, 13), USA (4, 14, 15, 16), Australia (17, 18, 19), Canada (20, 21, 22) and Asia (23, 24). The methods used to collect data on cancer research expenditure for the studies identified in the literature were: letters sent to the relevant Institutions/ Organizations (2, 5, 6, 7, 11, 16, 17, 18, 19) or to leading cancer researchers (2, 18, 19), interrogation of the most relevant databases regarding the data on cancer research papers (the outputs of cancer activity) (2, 5, 16, 24), information from institutional websites (where available) (2, 5, 6, 7, 11, 17, 18, 19) or interrogation of common databases regarding cancer research funding (2, 4, 11) (tab. I). From all these methods the most used was the top-down approach (25, 26). This method involves a direct survey that collects data from organizations that fund cancer-related research or from organizations that administer cancer-related projects and programs (universities and hospitals). First step is the identification of these organizations. Then letters is sent to each institution and specific data related to can- 829
3 Mioara Calipsoana Matei et al. cer research expenditure are required (such as the name of funding organization, the name of the project, the name of the chief investigator, type of funding organizations, collaborators, source of funding, the amount of money spent by Common Scientific Outline CSO categories, and by cancer site) (7, 19). Besides, the researchers involved in the assessment of oncological research investments evaluate the amount of money spent by political group, by countries/territories, and by Gross Domestic Product (GDP)/ per capita. Where the information is incomplete or it is not provided, the chief investigators are contacted and asked for this data. Also, the websites are checked were available. Follow up letters are sent to the organizations which do not respond to the first request. Many attempts (letters, s, and phone calls) are used to contact these institutions. The information has to be cross checked. If there are data provided in other currencies than the official currency used in the survey, they are converted within maximum two days of receipt of the information. Other type of currency conversion could be the usage of an average conversion rate over the calendar year. This approach avoids the involvement of variations in currency conversion rates as a confounder (4). A final verification letter could be sent to all organizations providing them with the figures for their institution as well as for the other institutions in the country and ask them for updates (7, 19). The response rate for top-down method is high (62-96%) compared with bottom-up approach, which means to directly contact the leading cancer researchers (27-42%) (2, 17, 19). No TABLE I Methods used in the literature to collect data on cancer research investment Methods used in different studies to collect data on cancer research investment [authors / year of publication (reference)] Common Top-down Bibliometric Bottom-up Web sites databases approach approach approach interrogation interrogation Cancer Australia / 2014 (17) / 2007 (5) Eckhouse S, Sullivan R / 2006 (6) / 2005 (7) Gillum LA et al. / 2011 (16) Kanavos P / 2010 (11) / 2011 (18) / 2011 (19) / 2007 (5) Gillum LA et al. / 2011 (16) Hong W, Dong E / 2014 (24) / 2008 (2) / 2011 (18) / 2011 (19) Cancer Australia / 2014 (17) / 2007 (5) Eckhouse S, Sullivan R / 2006 (6) / 2005 (7) / 2011 (18) / 2011 (19) International Cancer Research Partnership / 2012 (4) Kanavos P / 2010 (11) 830
4 Cancer research investment: top-down versus bibliometric approach Using the top-down approach, Eckhouse et al. showed that in 2004 the noncommercial funding organizations spent 1.97 billion (on direct funding of cancer research) in Europe and 5.15 billion in USA. Besides, there were 1.36 billion in Europe and 0.10 billion in USA from national healthcare systems and universities ( hidden expenses or indirect funding). Also, there were 3.09 billion from Pharmaceutical Industry (direct spending) worldwide contributing to public domain (not all companies). So, in 2004 a total of billion were invested from public domain on cancer research (2, 5). The bibliometric method for the assessment of cancer research investment was taken into account for the evaluation of direct (2, 5, 16, 24) or indirect costs (2, 5). There are many ways of using the bibliometric approach. First, it could be evaluated the total number of scientific articles on cancer, over a specific period. The relevant databases are searched (ISI Thomson Web of Science, PubMed, Google scholar etc.) using specific filters / queries (2, 5, 24, 27). There is the possibility to select the topic, the language, the type of documents, the timespan and other settings (eg. Citation Indexes in the case of ISI Thomson Web of Science). There are Boolean operators, parentheses, field tags, and query sets available to help the researcher with the creation of his own query. When the final results were obtained, an Excel database could be used to store the bibliometrical details of each scientific article. The number of papers related to a country / region / organization could be evaluated using two methods of counting: the integer counting (which means that a paper is counted as unity for each country / institution appeared among the addresses) or fractional counting (which means that the researcher have to divided the number of addresses for a particular country / institution by the total number of addresses identified in the article) (28). The analysis could provide data on the type of research (basic/ clinical), the type of funding organization, the type of collaboration (national/ international) and regarding the values by CSO or by cancer site. Second, the quality of cancer research outputs could be evaluated using the impact factor of the journals which published the scientific paper (24) (the scientific value of the journal in which were published the outputs) or the actual citation impact, defined as the number of citations received by a specific article in the next 5 years after its publication (28) (the scientific value of the papers itself). Also, the potential citation impact could be used in this respect. The last indicator is calculated as the number of citations expected to be received by an individual paper, considering that is cited with the average frequency for papers of that journal in that year (28). Some authors evaluated the number of research papers on cancer over a specific period (usually a 10-year period) in a specific country / region (2, 5, 24), others provided a deeper analysis and calculated the impact of the outputs on cancer research or estimated the amount of money spent on oncological research (using the number of research outputs identified for a specific country / region / institution and the mean cost per paper (2, 5, 27). Using the bibliometric approach was shown that the Global Public Sector cancer research expenditure was around billion, from which: USA = 5.27 billion, Europe = 3.33 billion, Japan = 1.00 billion, Canada = 0.27 billion, Australia = 831
5 Mioara Calipsoana Matei et al billion and the Rest of the World = 0.98 billion. The major funder for oncological research were the Government ( 4,712 million), followed by Charity ( 456 million) and healthcare systems and universities ( 109 million) in the USA, whilst the universities and healthcare systems ( 1,364 million), followed by Government ( 992 million), and, Charity ( 872 million) were the relevant funders in EU (5). Although, the USA invested a higher amount of money in cancer research compared to Europe (5), these regions were comparable when analyzed their overall oncological research productivity as a volume of publications (2). In China, the scientific papers resulting from breast cancer research followed an upward trend over the period of Although, the number of articles from China rose from 267 in 2004 to 3,414 in 2013, was still far behind the USA (with more than 7,000 papers), but well in advance compared with other countries such as Japan (1,030), England (1,157) or Germany (1,196) (24). DISCUSSION The bibliometric method is a relatively new tool used for the assessment of cancer research funding priorities (2, 27, 28). The expenditure evaluated using the bibliometric approach was 41% greater in Europe than the amount of money found using the top-down method (directly reported funds) combined with other methods, except the bibliometric one, and 2% greater in the USA (5). Over a 10-year period, from 1994 to 2003, when the assessment was done in absolute terms (% of total number of publications), European cancer research activity was dominated by Germany (9.6%), UK (9.1%), Italy (7.3%), and France (6.79%), followed by Netherlands (3.6%) and Sweden (2.5%), but when the analysis taken into consideration the number of papers / billion euro GDP, Sweden (2.2), Greece and Netherlands (2.1 each) had the greatest outputs (2, 5). The difference between data collected using the bibliometric approach (national estimation) and top-down methods (directly reported investments) in Europe resulted from the funds added by the universities and healthcare services (money spent for infrastructure), so called indirect costs (5). The top-down approach is a widely used method for the data collection on cancer research funding, with the advantage of providing directly reported information, usually with high accuracy. Generally, this method catches data on public domain. But, there are some aspects that could be considered as disadvantages. First, in some cases there is a need for many follow-up letters, phones, and s to get the expected percentage of answers. So, sometimes the rate response could be too low. Second, the rate response from private organizations could be even lower. The number of articles published is considered as a good measure of oncological research efforts. Vanderelst D et al. showed that the volume of publications represents a valid estimate of the magnitude of research funding (27). So, the bibliometric approach is a reliable way to collect information on cancer research investment. Even more, some authors found that the number of published articles was correlated with the burden of a disease on the population / society (Swingler G et al., 2003, cited by Vanderelst D et al.) (27). Cancer research scientific papers are one of the major outputs of investment and an 832
6 Cancer research investment: top-down versus bibliometric approach objective surrogate of the global cancer research activity and impact (2, 28). Besides, the scientific productivity in specific areas of research (including cancer) could stimulate further interest from researchers and the funding organizations and could support some the targeted investments (16). This method is useful when there is a short period of time available for the estimation of oncological research expenditure. However, the analysis of cancer research investment in Far East (especially China and India), but also in Latin America and Russia, is difficult because the names of many authors are the same and an important percent of these papers are published in other languages and national journals that do not appear in the most relevant databases such as ISI Thomson Web of Science, PubMed, Google Scholar and so on, which are English-databases (2). Also, the bibliometric approach provides estimated values. CONCLUSIONS 1. There are many different methods that could be taken into account for data collection on oncological research investment, with advantages, but also with disadvantages. 2. The top-down approach is a widely used method for the assessment of cancer research expenses, especially from public domain, which provides directly reported data, but sometimes at a lower response rate. 3. The bibliometric approach is a relatively new tool for the evaluation of cancer research funding, but also on the impact of this activity. This method helps the setting of cancer research funding priorities and the appropriate financial resources allocation, according to the actual population/society needs. 4. The best approach for the collection of cancer research funding information is a combination of bibliometric with topdown / bottom-up methods, which allows the assessment of oncological research productivity and scientific impact, but also the evaluation of the amount of money invested on cancer research from different perspectives. ACKNOWLEDGEMENTS This work received financial support through the "Programme of Excellence in Multidisciplinary Doctoral and Postdoctoral research of Chronic Diseases", contract no. POSDRU/159/1.5/S/133377, beneficiary Grigore T. Popa University of Medicine and Pharmacy - Iasi, co-financed from the European Social Fund through Sectoral Operational Programme Human Resources Development This paper does not represent the official view of the Romania Government or European Union. REFERENCES 1. World Health Organization (2015). Global Health Observatory (GHO) data. ( 2. Eckhouse S, Lewison G, Sullivan R. Trends in the global funding and activity of cancer research. Molec Oncol 2008; 2(1): Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase, 2013; No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer. ( 833
7 Mioara Calipsoana Matei et al. 4. International Cancer Research Partnership (2012). Cancer Research Funding from an International Perspective: Report from the International Cancer Research Partnership. ( 5. Eckhouse S, Lewison G, Sullivan R. Investment and outputs of Cancer Research: from the public sector to industry. The second Cancer Research Funding Survey. European Cancer Research Managers Forum; ( Sector_to_Industry). 6. Eckhouse S, Sullivan R. A Survey of Public Funding of Cancer Research in the European Union. PLOS Medicine 2006; 3 (7) : e Eckhouse S, Castanas E, Chieco-Bianchi L, Cinca S, Meunier F, Moulton B et all. European Cancer Research Funding Survey. European Cancer Research Managers Forum; ( 8. Fricker J. Cancer research funding in Europe. Molecular Oncology 2007; 1(2): Illman J. Cancer Research Funding in Europe low compared with US, survey finds. Journal of National Cancer Institute 2005; 97(10): Institut National du Cancer (2010). French National Cancer Institute Scientific Report ( 11. Kanavos P, Sullivan R, Lewison G, Schurer W, Eckhouse S, Vlachopioti Z. The role of funding and policies on innovation in cancer drug development. ecancer 2014; 4 : Torjesen I. Cancer Research UK will increase its research spending by 50% over the next five to 10 years. BMJ 2014; 348 : g3012. doi: /bmj.g Watson R. Europe is second class continent for cancer research. BMJ 2005; 330: Brown H. Cancer research funding in USA. Molecular Oncolology 2007; 1(2): Chow DS, Itagaki MW. Interventional Oncology Research in the United States: slowing growth, limited focus, and a low level of funding. Radiology 2010; 257(2): Gillum LA, Gouveia C, Dorsey ER, Pletcher M, Mathers CD, McCulloch CE, Johnston SC. NIH Disease Funding Levels and Burden of Disease. PLoS One 2011; 6(2): e Cancer Australia. Cancer research in Australia: an overview of cancer research projects and research programs in Australia 2006 to Cancer Australia, Surry Hills, NSW; Shirazee N, Musiello T, Saunders C, Johnson C. Cancer research and funding in Western Australia. An overview from 2008 to Cancer Forum 2011; 35 (3) : Shirazee N, Musiello T, Saunders C, Johnson C. Cancer research and funding in Western Australia. An overview from 2008 to Cancer and Palliative Care Research and Evaluation Unit; ( Australia.pdf). 20. Canadian Cancer Research Alliance (2014). Cancer Research Investment in Canada, ( 21. Canadian Cancer Research Alliance (2012). Cancer Research Investment in Canada, : The Canadian Cancer Research Alliance s Survey of Government and Voluntary Sector Investment in Cancer Research in Toronto: CCRA. 22. Gotay C (2013). Trend in cancer research funding in Canada. ( cancerprevent.ca/files/ documents/gotay,carolyn-trends Cancer Research Funds_2013.pdf). 23. Cheng MH. Cancer research funding in Asia. Molecular Oncology 2007; 1(2): Hong W, Dong E. The past, present and future in breast cancer research in China. Cancer Letters 2014; 351: Inmon, W.H. Building the Data Warehouse, 4th ed. Wiley Publishing, Indianapolis, Kimball, R., Ross, M. The Data Warehouse Toolkit: The Complete Guide to Dimensional Modeling. Wiley, New York, Vanderelst D, Speybroeck N. Scientometrics reveals funding priorities in medical research policy. J Informatics 2013; 7: Lewison G, Purushotham A, Mason M, McVie G, Sullivan R. Understanding the impact of public health policy on cancer research: a bibliometric approach. Eur J Cancer 2010; 46(5):
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