Data Collection

We used the Scopus (Elsevier) database (http://www.scopus.com) to retrieve publications involving stem cell research and limited our examination to recently published papers, from 2006–2010. Scopus is an international multidisciplinary database that indexes over 17,000 peer-reviewed journals in S&T, as well as more than 500 international conference and seminar proceedings (see: http://www.info.scopus.com/scopus-in-detail/facts/, [36]. We selected Scopus for its size – it is the largest international multidisciplinary database in the world, and for its quality assurance processes – over 95% of material is peer-reviewed, and all titles are evaluated before inclusion by an external Content Selection and Advisory Board [37]. Additionally, Scopus has wider coverage of journals from developing countries and emerging economies, including China, compared to another frequently used database, the Web of Science (see: http://thomsonreuters.com/products_services/science/science_products/a-z/web_of_science/). Scopus also has better coverage from many countries where English is not the first language, and includes peer-reviewed, and evaluated non-English titles [36] (and see: http://www.info.sciverse.com/UserFiles/sciverse_scopus_content_coverage_0.pdf). Thus, analyzing data from the Scopus database should generate a relatively accurate, and the most comprehensive picture of China’s participation in the field of stem cell research.

A caveat is that some collaboration will not result in co-authored papers, while other co-authored papers may have involved only limited collaboration. Nevertheless, this methodology has been widely used [23], [27]–[30], and provides the opportunity to compare collaboration between countries, and to examine changes over time.

We used ‘stem cell’ as the search term, limiting this term to occurrence in ‘article titles, abstracts or keywords’. We solely included papers published between 2006–2010, and the search was conducted within three of the four broad subject areas offered by Scopus: life sciences (including >4,300 titles); health sciences (including >6,800 titles (100% medline coverage)); and physical sciences (including >7,200 titles). For this study, we limited our collection to three key document types that are cited by and include references to other academic publications – namely articles, conference papers and reviews – together referred to in this study as ‘papers’.

We tested various search strings before arriving at the term ‘stem cell’, which in Scopus also captures the hyphenated and plural forms (stem-cell and stem cells, respectively). To begin, we obtained a comprehensive list of vocabulary commonly used to describe stem cell research by consulting the National Library of Science’s Medical Subject Headings (MeSH). This list included: adult stem cells, embryonic stem cells, fetal stem cells, hematopoietic stem cells, mesenchymal stem cells, multipotent stem cells, myoblasts, neoplastic stem cells, neural stem cells, pluripotent stem cells, side-population cells and totipotent stem cells. We note that the term ‘stem cell’ captures all these permutations, except myoblasts and side population cells – which in some cases are not considered to be stem cells. We note that a query for ‘keywords’ in Scopus includes both author assigned keywords and index terms. The latter are assigned by Scopus indexers from standard controlled vocabularies (see: http://www.jisc-adat.com/adat/adat_db_details.pl?ns_ADAT:DB=Scopus). Author assigned keywords tend to be more specific, while index terms allow a document to be searchable in more broadly recognized and relative terms. Thus, papers mentioning more specific terms such as ‘myoblasts’ or ‘side-population cells’ in cases where they are indeed stem cells, would be likely to qualify this relationship in either the author keywords or index terms using the broadly recognizable term ‘stem cell’. Accordingly, we noted articles in our dataset captured using ‘stem cell’ such as “Side population cells isolated from hepatic carcinoma cell lines escape being killed by NK cells from NOD/SCID mice” [38], where the term ‘stem cell’ appears in both author keywords and index terms, but not in the title or abstract. Likewise, we considered a number of more and less-specific terms such as ‘progenitor cells’ before arriving at ‘stem cell’ as our search term.

Scopus search and analysis tools were used to limit the collection to papers authored by researchers affiliated to institutions in China and/or Canada. We note that throughout this work China refers to mainland China. Additionally, Scopus reports data for Taiwan and Hong Kong separately from mainland China, and we have reported their data separately likewise. By placing a limit of affiliation ‘in China’, all papers without a China-based author were excluded. Placing an additional limit of affiliation ‘in Canada’, all papers without an author affiliated in either country were excluded. These papers constituted China-Canada international collaborations. Finally, excluding affiliations in all other countries yielded papers with only Canadian and Chinese addresses. These papers constituted bilateral China-Canada collaborations, or domestic papers when all but China or Canada-authored papers were excluded. Corresponding authors were determined from the reprint address.

Scientometric Indicators

Statistics were generated based on the following indicators using Scopus data analysis tools.

Participation of Countries in Stem Cell Research

In Figure 1 we present number of papers published worldwide in stem cell research between 2006–2010. Our search string generated 79,076 unique stem cell papers; 75% of these were articles, 21% were reviews and 4% were conference papers. The number of stem cell papers published globally increased from 12,700 in 2006, to 18,657 in 2010, an increase of almost 48%. Thus, our data indicate that the stem cell research field is growing rapidly. For comparison, a similar study showed a global doubling of stem cell publication numbers between 1991 and 2002 [22].

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Figure 1. Total worldwide stem cell papers by year.

Shown is the total number of papers published worldwide in stem cell research by year, 2006–2010.

https://doi.org/10.1371/journal.pone.0057176.g001

The top ten countries ranked by stem cell research paper output, and two additional emerging economies, India and Brazil, for comparison are shown in Table 1. The US dominates stem cell research over 2006–2010, with 27,378 papers published, more than three times the total published by China (8,546), the second most prolific producer over this time. Germany was the third largest producer (6,938), closely followed by Japan (6,771) and the UK (5,647). Canada was the 8^th largest producer (2,977). These rankings closely reiterate global rankings in overall science and engineering publications [23]. They list the top three as the US, China and Japan, with the next five countries being the same as our data, though in slightly different order. Thus, publication volume rankings in stem cell science are largely consistent with global science publication patterns. Notably, our analysis shows that in 2006, China ranked fourth, closely clustered with Germany and Japan. However, from 2007 to 2010 China’s research output rapidly pulled ahead. The other emerging economies studied here, Brazil (844–19^th) and India (742–21^st), did not show a particularly strong publication performance. China also out performs South Korea (2143–9^th), another major player on the Asian stem cell scene, by almost a factor of four. Other members of SNAP – Australia (1,859), Taiwan (863), Singapore (775), and Thailand (125) – were 12^th, 16^th, 20^th and 37^th respectively in terms of numbers of publication volume. SNAP’s other members are China, South Korea, Japan, and India.

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Table 1. Output of stem cell papers by top producing countries of stem cell research.

https://doi.org/10.1371/journal.pone.0057176.t001

Publication growth rates over the five-year study period per country are shown in Table 1. While all countries monitored show a steady increase in paper output over the years examined, China’s increase in publication rate of 156% is more than three times that of other large producers, the US (47%), Germany and the UK (54%), France (40%), Canada (46%). This is especially striking in light of China’s relatively recent entry into the stem cell research arena, and the large number of papers it now produces. Also striking were increases in publication from South Korea (141%), and from India (161%) and Brazil – which showed the largest increase over time (209%) – though in the case of the latter two countries, absolute publication output was comparatively low.

Our results reflect national policy and investment towards stem cell research over recent years. The US is the world’s largest investor in overall R&D, and so it is not surprising that it remains the world’s largest producer of stem cell research. In 2008, the US’ gross domestic expenditure on R&D (GERD) represented 42.5% of OECD countries’ total, or almost US$400B. At the same time the US accounted for 16% of the world’s scientific publishing [43]. While federal funding for human embryonic stem cell research was restricted from 2001–2008, federal funding for stem cell research in general continued to be substantial [34]. Thus, comparatively massive funding continued to push this field forward in the US.

China’s rapid rise in the stem cell arena reflects its increasing overall R&D investments, and its subsequent emergence as one of the world’s main producers of scientific knowledge. Over the decade from 2000–2010, China increased its R&D spending six-fold [8], and now represents the world’s second largest gross domestic expenditure on R&D (GERD) after the US. In parallel, between 1998 and 2008 China’s overall output of scientific papers increased by about twenty-fold [43], now ranking China third after the US and Japan in total papers published [8]. China has had a large emphasis on health research and ranks, for instance in second place globally in health biotechnology publications, just after the United States [44] Burgeoning funding and facilities, and policy to increase the number of local science trainees, retain local talent, and recruit foreign-trained China-born scientists back to China, as well as the absence of stem cell-related political and ethical controversies in China, have all contributed to its growth in the stem cell field [1],[2]. Interest seems not to be waning. This year, the national government’s funding commitment for stem cell research for the next five years was estimated at close to US$500M, a sum which does not include local government funding, industry support and other funding initiatives [1].

International Collaboration in Stem Cell Research

To examine the emphasis on international collaboration in general in stem cell research, we calculated the collaboration rates in stem cell research for the leading countries that publish in the field from 2006–2010 (Table 2). We also included rates for the emerging economies Brazil and India, and for Hong Kong for comparison. Our data show a relatively large variance in collaboration rates between countries. Papers published in collaboration as a percent of total papers (average collaboration rate over time) ranged from 19% percent (China) at the lowest end of the scale to 51% (Canada, Hong Kong) at the highest. Rates of collaboration generally increased over the time period examined (Fig. 2). Of note, our data show that while China is the second most prolific producer of stem cell research in the world, it has the lowest international collaboration rate of the countries we examined.

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Figure 2. Collaboration rates of top producers of stem cell research, and Canada, Brazil and India.

Shown are the collaboration rates of the top five global producers of stem cell research; the USA, China, Germany, Japan, and the UK, and for comparison - Canada, and emerging economies Brazil and India, 2006–2010.

https://doi.org/10.1371/journal.pone.0057176.g002

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Table 2. Select countries’ international collaboration rates, 2006–2010.

https://doi.org/10.1371/journal.pone.0057176.t002

Commentators have underscored the importance of international collaboration in advancing stem cell science. For example, international collaboration has been a key strategy in diversifying and progressing research by the California Institute of Regenerative Medicine [45]. Canadian analysts have pointed to the role of international partnerships for Canada’s advance on the global stem cell scene [22]. International collaboration with China-born western-trained scientists has been instrumental in some of China’s key stem cell accomplishments [1]. Smaller or less scientifically productive nations have been noted to seek higher rates of international collaboration [46],[47]. Nevertheless, our data show that in the stem cell field, relatively large countries with strong stem cell research programs (Germany, UK, France, Canada) published about 50% of their research in collaboration.

The US has been shown to be a preferred partner in overall scientific collaboration with most nations [23],[23],[47]. We also show it is the top collaboration partner for both China and Canada in stem cell research. With ample infrastructure, funding and human resources of its own, the US has more modest collaboration rates (30%). Nevertheless, others have shown it also benefits in terms of citation rate by engaging in international stem cell research collaborations [30]. Research indicates that China’s relative international collaboration in science is decreasing as its scientific capacity and output increase [42],[48]. Our data show that in the stem cell field, its relative collaboration rate is low and stable.

China and Canada’s Key International Collaborators in Stem Cell Research

We examined the top collaboration partners of Canada and China by examining more closely their co-authored papers produced between 2006–2010 (see Figures 3A, 3B and 4A, 4B). The results showed that the US was by far the top partner for both countries, showing 885 co-affiliated papers with Canada, and 901 with China over this period. For Canada, the top collaborators in terms of papers are Germany (204), the UK (191), Japan (126), France (117), China (96) and Australia (90). For China, we also examined collaboration with SNAP member countries, and with Hong Kong because of their historical, cultural and political ties. China’s top collaborators in terms of numbers of papers after the US were Japan (164), the UK (128), Hong Kong (123), Germany (100), Canada (96) and Singapore (80). Thus, Canada ranked as 6^th key partner for China, and vise versa for China’s collaboration with Canada, demonstrating a relative symmetry in the emphasis the two countries place on collaboration with each other in terms of numbers of papers published. Our rankings for stem cell research papers very closely reflect China’s international collaboration partners for overall scientific publication [42]. Examining Canada’s numbers over time (Figure 4A) shows overall increased numbers of collaborative papers with most countries, notably Germany, Japan, China and the UK. Increases in the number of collaborations with these countries were 153%, 150%, 125% and 112% respectively. China (Fig. 4B) also showed increased numbers of co-affiliated papers over time with almost all countries examined, in particular with Australia (600%), Germany (363%), the US (309%), Singapore (225%), the UK (179%), and Canada (125%).

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Figure 3. Canada’s and China’s total collaboration papers with key producers of stem cell research. A:

Canada’s collaboration papers, 2006–2010. Shown are Canada’s total numbers of collaboration papers with the other top nine global producers of stem cell research, and for comparison - emerging economies Brazil and India, and Australia. B: China’s collaboration papers, 2006–2010. Shown are China’s total number of collaboration papers with the other top nine global producers of stem cell research, and for comparison - emerging economies Brazil and India, Stem Cell Network Asia Pacific (SNAP) members, and Hong Kong.

https://doi.org/10.1371/journal.pone.0057176.g003

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Figure 4. Canada’s and China’s collaboration with their top five collaboration partners, and select others. A:

Top Canada’s collaboration (collaboration with US not shown). Shown is the number of stem cell papers co-authored by Canada per year, together with its top five collaboration partners after the US (its top collaborator – data not shown); Germany, the UK, Japan, France and China, as well as for comparison - the number of co-authored papers with Australia, and emerging economies Brazil and India. B: Top China’s collaboration (collaboration with US not shown). Shown is the number of stem cell papers co-authored by China per year, in collaboration with its top five collaboration partners after the US (its top collaborator – data not shown); Japan, the UK, Hong Kong, Germany, and Canada, as well as for comparison - the number of co-authored papers with Stem Cell Network Asia Pacific (SNAP) members, Hong Kong, and emerging economies Brazil and India.

https://doi.org/10.1371/journal.pone.0057176.g004

We next examined the collaboration preferences of countries, while controlling for the bias arising from the varying numbers of papers published by different countries using Salton’s measure. Salton’s is a representation of the mutual strength of collaboration between the two countries – the larger the value of Salton’s measure, the stronger is the collaboration preference. To examine the strength of collaboration in stem cell science for China and Canada, and their collaboration partners we calculated Salton’s measures over 2006–2010 (Table 3, Table 4). For Canada, these clearly indicate the strongest mutual preference for collaboration of the countries we examined is with the US (0.097), followed by the UK (0.045), Germany (0.044), Australia (0.037) and France (0.037). China ranked 10^th in Canada’s preference for partners in stem cell research collaboration of the countries we examined (0.019). On China’s side, Salton’s measure for Hong Kong was highest (0.069), followed by the US (0.056), Japan (0.030), Singapore (0.029), and then Canada (0.019) in 5^th position of our selected countries. These results reflect an effect on collaboration preference of geographical proximity, and also – particularly in the case of Hong Kong and China, and for Canada with the UK, Australia and France – historical, cultural and linguistic ties. Clearly for both China and Canada, there is much to be gained from taking advantage of US strengths in stem cell science. Thus far, China’s collaboration with India and Brazil has been limited, indicated both by numbers of co-affiliated paper numbers and Salton’s measure respectively; with India (7 papers 2006–2010, Salton’s measure 0.002) and Brazil (2 papers, 0.0004). This situation may shift in the future as these countries recently committed to collaboration in R&D, innovation and technology transfer toward improving public health (BRICS Health Ministers’ Meeting- Beijing Declaration, 2011, see: http://keionline.org/node/1183). Nevertheless, while China’s stem cell program is still relatively young, there may be greater advantage in accessing scientific knowledge and building international reputation through collaboration with established players, rather than partnering with other newcomers to the field.

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Table 3. Canada’s strength of collaboration with other top producers of stem cell research, 2006–2010.

https://doi.org/10.1371/journal.pone.0057176.t003

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Table 4. China’s strength of collaboration with other top producers of stem cell research, 2006–2010.

https://doi.org/10.1371/journal.pone.0057176.t004

China-Canada Collaboration

We focus on yearly trends in China-Canada co-publications in stem cell research in Figure 5. We see that collaboration between the two countries is on a steady rise. Canada-China collaborations in stem cell research have increased from year to year, more than doubling between 2006–2010 for a total of 95 papers; 84% articles, 14% reviews, and 2% conference papers. Of these, 62% were bilateral collaborations involving only China and Canada. Bilateral collaborations also increased over time, for a total of 59 papers; 86% articles, 12% reviews, and 0.2% conference papers.

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Figure 5. Total China-Canada collaboration papers written per year.

Shown is the total number of stem cell papers co-authored by China and Canada, 2006–2010. The number of bilateral collaboration papers between the two countries is shown in red, while the number of multilateral collaboration papers, involving other countries in addition to China and Canada, is shown in blue.

https://doi.org/10.1371/journal.pone.0057176.g005

China and Canada have had over 130 years of interaction, including commerce, immigration and missionary ventures [49]. One example of amicable relations between the countries is the story of Canadian physician Norman Bethune, a figure of historical importance in China for contributions made to the field of health care delivery. In 2009, the Canadian Institutes of Health Research (CIHR) and the China Scholarship Council (CSC) initiated a Canada-China Norman Bethune Health Research Scholarship Program, offering Chinese doctorate students the opportunity for health-related training in Canadian institutions (see: http://www.cihr-irsc.gc.ca/e/39515.html). Such programs aim to facilitate engagement between scientists from the two countries, allowing them to build relationships and embark on collaborative ventures.

Politically, Canada and China have witnessed fluctuations in the tone of their bilateral relationship [49]. However, both countries seem to recognize the mutual political and economic advantages of further partnership, and the Chinese and Canadian scientific communities seem to be increasing their joint output in stem cell publications.

Of the 95 international China-Canada collaborations, 50% listed an author-based at a Chinese institution as the corresponding author, 31% at a Canadian institution, and 14% were US-based. Of the 59 bilateral China-Canada collaborations, 66% listed China-based corresponding authors, and 34% were Canada-based. These results suggest that China-based researchers are driving these bilateral and international collaborations.

Impact of Collaboration

We examined the impact collaboration is having on the scientific community by calculating the average number of CPP for stem cell research papers published between 2006–2010. The CPP for domestic Chinese papers (listing China-affiliated researchers only) was 4.22. In contrast, the CPP for domestic Canadian papers was 16.99, a highly significant difference (P<0.001). For papers listing both Chinese and Canadian authors (international or multilateral China-Canada collaborations) the CPP was 15.11. Thus, collaboration with Canada dramatically increases the average citation rate for China-based researchers (P>0.001). The decrease in average citation rates for Canada-based authors in collaboration with Chinese authors was small and not significant. Papers authored in bilateral collaboration between China and Canada showed a lower CPP (11.7) compared to multilateral China-Canada collaborations (20.2), however this difference was not statistically significant. Some research has shown that a publication’s ‘citedness’ almost solely depends on the number of affiliations or authors involved [27],[39]–[41]. To discern the effect of internationalization and cooperation on impact, as opposed to the number of authors or affiliations, we calculated the Pearson correlation coefficients for the relationship between the number of citations received by a paper and the number of authors, affiliations and number of countries listed on the papers. For both bilateral and multilateral China-Canada collaboration, there was very low correlation between number of authors (R = 0.07), number of affiliations (R = −0.06), or number of countries (R = 0.08) and the number of citations a paper received. Thus, our analysis indicates that the increase in impact observed in China-Canada collaboration is due to internationalization or cooperation, rather than the number or authors, affiliations or countries involved on a paper.

All 95 China-Canada collaboration papers were written in the English language. In contrast, of domestic papers out of China (6948), 53% were in English, 48% were in Chinese, and 0.13% in Japanese, with the remaining few published in French. A total of 99.6% of domestic Canadian papers (1467) were in English. English is the primary language of global science, and publication in English greatly increases the number of researchers able to access, and thus cite, a paper. Thus, we examined the effect of publication language on ‘citedness’ for domestic Chinese papers. The CPP for papers published in Chinese was 0.47. In contrast, for those published in English the CPP was 7.64 (P>0.001), suggesting a significant effect of publication language on impact. We also compared the CPP of domestic Chinese papers published in English with China-Canada collaboration papers. The highly significant effect on impact of collaboration with Canada-based researchers for China-based researchers remained even when the effect of language was taken into account (P = >0.001). Alongside accessing complementary or novel expertise, an ancillary benefit Chinese researchers may gain in working with Canadian counterparts is the production of high quality manuscripts in English; publication in English is an important route by which non-English speaking nations can bring their research into the mainstream.

Publication Journals

To further examine the characteristics of the 95 China-Canada collaboration papers, we looked at the journals in which researchers are choosing to publish their research (Table S1). The 95 papers were published in 76 different journals. The greatest number was published in PLoS One, reflecting a preference for open access and a journal focusing on a wide spectrum of scientific disciplines. Publication in such a journal may optimize the dissemination of research findings to other scientists in the field, making it freely available to stakeholders in both high and low income settings. This too may be a strategy by which Chinese scientists are facilitating greater international recognition for their work.

Funding on China-Canada Collaboration Papers

We investigated the funding sources credited in the 95 China-Canada collaboration papers. The National Natural Science Foundation of China (NSFC) was the top funder credited, appearing on more than 25% of the papers, followed by the Canadian Institutes of Health Research (CIHR), which was listed on almost 17%. Just over 80% percent of papers for which funding information was available were supported at least in part by the NSFC, China’s MOST through their National ‘863’ applied research or their ‘973’ basic research funding programs, National State Key labs program – laboratories sanctioned by the Chinese government to pursue areas of particular national interest – or local Chinese city or provincial S&T bureaus. Likewise, more than forty percent of papers acknowledged support from federal or provincial Canadian S&T programs including the CIHR, National Sciences and Engineering Council (NSERC), Canadian Foundation for Innovation (CFI), the Canada Research Chairs program, the Fonds de la Recherche en Santé du Québec (FRSQ), and the Canadian National Research Council (CNRC). Several studies were also partially funded by more targeted research funding bodies, such as the Canadian Stem Cell Network and by national or provincial disease specific groups such as the Heart and Stroke Foundation of Canada, the American Cancer Society, and the Leukemia & Lymphoma Society of Canada. Many of these bodies specifically mention nurturing international collaboration as being an important value or goal (for examples see: Internationalization of CIHR funding policy and program tools at http://www.cihr-irsc.gc.ca/e/40953.html; National Sciences and Engineering Research Council of Canada, International Opportunities at http://www.nserc-crsng.gc.ca/International-Internationale/Index_eng.asp; MOST, International Cooperation at http://www.most.gov.cn/eng/cooperation/200610/t20061008_36195.htm; Shanghai Municipal Science and Technology Commission at http://www.shanghai.gov.cn/shanghai/node17256/node17679/node17681/userobject22ai12991.html; NSFC, International Cooperation and Exchange at http://www.nsfc.gov.cn/e_nsfc/desktop/zn/0110.htm). Among these agencies, for example, the NSFC and CIHR established the China-Canada Joint Health Research Initiative grants program in 2005 to foster research collaboration between China and Canada. The CIHR and NFSC contribute US$1,138,000 and US$800,000 respectively per year for this program (see: Research Net, Funding Opportunity Details at http://www.researchnet-recherchenet.ca/rnr16/vwOpprtntyDtls.do?prog=1520&view=&type=AND&resultCount=25). Joint dedicated funding is an important incentive for encouraging international collaboration between research communities. This initiative is planning to support projects in multiple areas. Stem cell science is not highlighted, although such projects could fit under some of the six focus areas. Thus, accessible funding for China-Canada stem cell research collaboration exists. Such collaboration may be further enhanced by dedicated stem cell-targeted initiatives.

No paper credited the International Science and Technology Partnerships Canada (ISTP) initiative, which has been given the task of delivering the Canadian government’s commitment to promote science and technology collaboration with China. Accordingly, projects in stem cell research are not yet among those seventeen projects funded through ISTP (see: ISTP Canada, China-Canada R&D projects at http://www.istpcanada.ca/international_programs/China/current_projects/index.php). Also none of the 95 China-Canada collaboration papers cited any international collaboration-specific funding by name.

Collaborating Institutions

To begin to understand more about the groups and institutions in Canada and China who chose to collaborate, we examined the affiliations of authors on collaborative stem cell science papers (data not shown). According to Scopus results, the top five Canadian institutions from which this research is produced are the University of British Columbia (Vancouver), the University of Calgary (Calgary), the University of Toronto (Toronto), the Universities of Manitoba and the University of Alberta (Edmonton). The top 4 Chinese institutions were Tsinghua University (Beijing), Shanghai Jiaotong University (Shanghai), Harbin Medical University (Harbin), and Third Military Medical University (Chongqing). We also examined the top authors producing co-affiliated papers (data not shown). These data suggest that China’s international collaborations may often be established through colleagues based in Canada or the US, who may have been educated in, or have national ties to, China. For example, B. Zhou and M-C Poon were the two top authors in terms of numbers of papers published. Both authors are affiliated at the National Research Center for Stem Cell Engineering and Technology in Tianjin, while Poon is also affiliated at the University of Calgary. Examination of their publications reveals they have published together multiple times between 2006–2010. Both Zhou and Poon have published with multiple colleagues at the National Research Center for Stem Cell Engineering and Technology, as well as others affiliated at other Chinese institutions. On several papers Zhou is also affiliated at Harvard Medical School, and has published with colleagues there on several papers. These data begin to suggest how collaborative relationships may be sparked and propagated through groups and institutions, and could be explored and verified through further in depth study.

Areas of Mutual Research Interest

Finally, to ascertain areas of China-Canada mutual stem cell research interest and to gain deeper insight on the type of projects being under-taken by collaborating researchers, we analyzed the author key words, index terms, the abstracts, and if required the body text, of the 95 co-affiliated papers. We also examined the country of affiliation of the corresponding author on these papers to begin to gain some perspective on the country driving the research in question (Table S2).

There were 70 basic research papers. Canada-China basic research collaborations covered a range of disciplines with the greatest number of papers focused in oncology, studies of basic stem cell biology, neuroscience, cardiology, and mechanisms of bone development/osteogenesis. The majority of the basic research papers utilized adult cell types (40), followed by mouse embryonic stem cells. Only three studies focused on manipulations with human embryonic stem cells (hESCs), with the corresponding author for these papers based in Canada. The relatively low number of studies on hESCs was perhaps unexpected given that regulatory guidelines on these cell-types are less restrictive in China, and it has been suggested that international collaborators may target hESC research in seeking collaborations in Asia [30]. Conversely, it may be beneficial for Chinese researchers to collaborate on such research with countries with tighter regulation, such as Canada, in order to build public trust – particularly international trust – in their work.

There were nine papers reporting clinical trial or case reports featuring allogenic or autologous stem cell transfers. The corresponding author for five of these was China-based, while three were US-based. Six of these studies were carried out in China, one reported worldwide multi-centre data, and there was no information on where the trial took place for two. Analysts have noted that the availability of enormous patient populations in China allowing for faster and less costly clinical trials may be another attraction for international stem cell research collaborators [3],[50]. However, robust regulatory mechanisms that can deal with the rising international interest in collaboration are needed [3].