Impact of the economic crisis on pain research: a bibliometric analysis of pain research publications from Ireland, Greece, and Portugal between 1997 and 2017

1 Introduction

Pain research is a “separate discipline in biomedicine” [1] that has increased worldwide over the last decades. Understanding pain mechanisms, pain management and pain treatment, whether in animals or humans, has been the focus for pain researchers and clinicians [2], and is the result of the development of different areas like medicine, psychology, and pharmacy [3].

The geographical and political expansion of the European Union (EU) in the last years, had a repercussion in European dominance in biomedical research [2]. This happened for several reasons, namely: the EU financial funding of research projects, the proximity between countries fostering international collaboration, and the emergence of European scientific pain associations’ journals (“The European Journal of Pain” in 1997 and “The Journal of Headache and Pain” in 2000) [2, 4]. As an example, in December 2017, a search of CORDIS (Community Research & Development Information Service) for “pain” in the tag “scientific research” retrieved 978 ongoing research projects funded by the EU [5]. There was also an increase in pan-European studies focusing mainly on chronic pain epidemiology, cancer pain, musculoskeletal diseases and pain induced disability [2].

There is an interconnection between the development of scientific research and economic funding, and in some areas of research like economics, investigation outcomes increase in crisis scenarios [6]. Usually, an economic crisis has a negative impact on research because public research and innovation budgets and scientific human resources diminish [7]. The literature demonstrates also that a country financial crisis can contaminate countries in geographic proximity, affecting large regions [8, 9].

One of the questions in the current European scenario is how the economic crises have influenced pain research outcomes in the last decade, especially in European countries like Ireland, Greece, and Portugal, where austerity has been imposed and budgets for research and for health systems have been reduced because of EU and IMF intervention [10]. Briefly, in 2008 when the USA financial crisis was obvious, the world acted as it was a restricted phenomenon; meanwhile, worldwide economies slowed, some European banks had high losses, stock markets declined, credit was more restricted and international trade dropped rising unemployment rates. Due to Euro currency and the Stability and Growth Pact, established by the Economic Monetary Union, European countries in financial debt no longer could devalue its own currency and aggravated their international credibility (difficulty to repay debts). This had a negative impact decreasing foreign direct investment especially in Greece and Portugal (with higher debt to foreign creditors). GDP of these countries grasped its lowest in 2009. In 2012, even with rescue packages, some European countries had high sovereign debt and austerity measures were not working [11].

As a result of the economic crises, Greece received a first rescue package from the EU and IMF of€110 billion in May 2010, followed by a second one of €130 billion in August 2012 (exit in June 2015), while Ireland received €67.5 billion in November 2010 (exit in December 2013) and Portugal €78 billion in April 2011 (exit in June 2014) [12]. Greek’s austerity rescue packages resulted in a deeper recession, so in August 2015 (with the end in August 2018) a new stability support program of €86 billion was launched, with IMF and European Stability Mechanism approval [11, 13, 14, 15].

Recently, the Irish economy had a strong recovery, with a GDP growth of 5.1% in 2016 and 6.5% in 2017 [16]. Official Portuguese statistics also point to an economic recovery, though at a slower pace, with a GDP increase of 1.5% in 2016 and 2.7% in 2017, which consolidates the economic recovery that began in 2014 [17]. Between 2008 and 2016, Greece had an “extreme reduction of the GDP (25%), which is equivalent to a war period” [18], but, surprisingly, the prevision of Greek economic growth in 2018 is 2.5% [19].

Returning to pain research, it must be noticed that the three referred countries have national pain societies (the Irish Pain Society, the Hellenic Society of Algology and the Portuguese Association for the Study of Pain) and a history of regular pain publications [2].

The aim of the present study was to evaluate if the economic crises affected the evolution of scientific production and performance in the field of pain research in Ireland, Greece, and Portugal. For that purpose, we performed a bibliometric analysis based on the ISI Web of Science indicators, namely the total number of published articles per country, total citations, h-index, document types, and research areas. Bibliometric analysis is a tool that facilitates monitoring and the analysis of research growth by quantitatively summarizing the activity and achievements in a given research area (productivity measures related to paper counts) and also by providing objective information on the performance (recognition and efficiency measures, that include citation counts, average citations per paper and journal’s impact factor, among others) [20, 21].

Since, in general, the economic crisis started around 2008 and possibly had a higher impact in pain research in the following years, we have extended our analysis from 1997 to 2017, in order to compare the evolution before and after the onset of the crisis.

2 Methods

3 Results

3.1 Analysis of publication outputs

3.1.1 Productivity – the number of publications

Between 1997 and 2017, 2,368 articles were published by an author with Irish, Greek or Portuguese affiliation. Only 17 of those articles were a result of international cooperation between the mentioned countries (11 signed by Greek and Irish authors and 6 by Greek and Portuguese authors).

In 1997, 26 articles were published about pain or nociception altogether and in 2017 there were 230 (Table 1). The year with the highest number of publications was 2015 (n=239), followed by 2017 (n=230) and 2016 (n=223).

Table 1:

Number of publications per year and country.

Year	Ireland	Greece	Portugal	World
1997	17	7	2	3,171
1998	23	11	6	3,550
1999	19	20	2	3,574
2000	30	12	0	3,916
2001	35	14	9	3,750
2002	20	17	6	4,146
2003	29	19	10	4,483
2004	33	25a	14a	4,948
2005	24	25	8	5,290
2006	40b	29b	15	5,598
2007	34	41	6	6,009
2008	48c	46c	18	6,779
2009	50c	38c	32	6,918
2010	62b	30b	38	7,465
2011	70b	48a,b	42a	7,890
2012	85	37	47	8,453
2013	84b	43a,b	67a	9,465
2014	88	39d	79d	9,773
2015	120	44	75	11,324
2016	109b	40	74	12,001
2017	123	39a	68a	10,739
Total	1143	624	618	139,242

1. ^aOne article with Greek and Portuguese cooperation; ^bone article with Irish and Greek cooperation; ^cthree articles with Irish and Greek cooperation; ^dtwo articles with Greek and Portuguese cooperation.

Of the three countries analyzed in the present study, Ireland had the highest number of publications (1,143), and its publication growth was steady during the studied period and similar to what happened worldwide. On the contrary, the number of Greek publications increased slowly until 2008 and then remained stable until 2017. Regarding Portuguese publications, there were a small number of published studies until 2007, a rapid growth from then until 2014 and a slight decline thereafter (Fig. 1).

Fig. 1:

Publication growth per country.

Each of the mentioned countries has a unique reality of population growth, real gross domestic product (GDP) per capita and percentage of GDP invested in research and development (Table 2 and Fig. 2). GDP measures the value of the total final output of goods and services produced by an economy within a certain period of time, while real GDP is adjusted for inflation. The percentage of Gross Domestic Expenditures on Research and Development (GERD) is a measure of governmental and private effort to generate and transfer knowledge and is used for international comparisons [24].

Table 2:

Population, real GDP^a and research expenditure indicators evolution.

Year	Ireland			Greece			Portugal			European Union (28 countries)
	Population	Real GDP per capita1	R&D expenditure2	Population	Real GDP per capita1	R&D expenditure2	Population	Real GDP per capita1	R&D expenditure2	Population	Real GDP per capita1	R&D expenditure2
1997	3,654,955	25,600	1.24e	10,629,267	16,000	0.43	10,084,196	14,600	0.56	483,512,803	21,000	NA
1998	3,693,386	27,400	1.21	10,693,250	16,500	NA	10,133,758	15,300	0.62	485,877,558b	21,600	NA
1999	3,732,006	30,000	1.15e	10,747,768	17,000	0.57	10,186,634	15,800	0.68	486,577,953	22,200	NA
2000	3,777,565	32,400	1.09	10,775,627	17,600	NA	10,249,022	16,200	0.72e	487,259,080b	22,900	NA
2001	3,832,783	33,800	1.05	10,835,980	18,200	0.56	10,330,774	16,400	0.76	488,240,527b	23,400	NA
2002	3,899,702	35,300	1.06	10,888,274	18,900	NA	10,394,669	16,500	0.72e	488,962,706	23,700	NA
2003	3,964,191	35,800	1.12	10,915,770	19,900	0.55	10,444,592	16,300	0.7	490,691,578	23,900	NA
2004	4,028,851	37,500	1.18	10,940,369	20,900	0.53e	10,473,050	16,500	0.73e	492,555,798	24,400	NA
2005	4,111,672	38,900	1.19	10,969,912	20,900	0.58	10,494,672	16,600	0.76	494,598,322	24,800	1.74
2006	4,208,156	40,000	1.2	11,004,716	22,000	0.56e	10,511,988	16,800	0.95e	496,436,597	25,500	1.76
2007	4,340,118	40,800	1.23	11,036,008	22,700	0.58e	10,532,588	17,200	1.12	498,300,775	26,200	1.77
2008	4,457,765	38,400	1.39	11,060,937	22,600	0.66b,e	10,553,339	17,200	1.45b	500,297,033b	26,200	1.84
2009	4,521,322	36,300	1.61e	11,094,745	21,500	0.63e	10,563,014	16,700	1.58	502,090,235	25,000	1.93
2010	4,549,428	36,800	1.59e	11,119,289	20,300	0.6e	10,573,479	17,000	1.53	503,170,618b	25,500	1.93
2011	4,570,881	37,700	1.55e	11,123,392	18,500p	0.67	10,572,721	16,700	1.46	502,964,837b	25,800	1.97
2012	4,582,707	37,600	1.56e	11,086,406	17,200p	1.56e	10,542,398	16,100	1.38	504,047,964b	25,700	2.01
2013	4,591,087	38,100	1.56e	11,003,615	16,800p	1.56e	10,487,289	16,000	1.33	505,163,008	25,700	2.02
2014	4,605,501p	41,200	1.5e	10,926,807	17,000p	1.5e	10,427,301	16,300	1.29	507,011,330e	26,100	2.03
2015	4,628,949p	51,400	1.2	10,858,018	17,100p	1.2	10,374,822	16,600	1.24	508,540,103b,e	26,600	2.03
2016	4,724,720b,e	53,600	1.18e	10,783,748	17,100p	1.18e	10,341,330	16,900p	1.27p	510,277,177e,p	27,100	2.03p
2017	4,774,833e	56,300b	NA	10,757,293e,p	17,400p	NA	10,309,573e	17,400e	NA	511,522,671b,p	27,600	NA

1. ^aGDP measures the value of total final output of goods and services produced by an economy within a certain period of time, while real GDP is adjusted for inflation. ¹Euro per capita; ²percentage of GDP; ^bbreak in time series; ^eestimated; ^pprovisional; NA=not available; Data from Eurostat.

Fig. 2:

Real GDP per capita (euro per capita) evolution.

Irish population and GDP per capita has grown in the last two decades (in fact GDP per capita has duplicated), although the percentage of research investment has slightly decreased, the real investment in research as also increased.

In Greece and Portugal, the population has grown until 2010/2011 and then decreased (although the population in 2017 is higher than in 1997); also the GDP per capita in these countries has grown until 2007/2008 and then decreased; but the percentage of research expenditure has increased, especially in Portugal in the last 10 years.

From the observed countries, Ireland has a GDP that is about twice higher than the European (considering the 28 countries) average, while Greek and Portuguese GDP are lower than the European average, and the three countries have a percentage of GDP expenditure in research lower than the European average.

When we consider the number of pain publications per capita (Table 3), Ireland is the most productive country (with 7 times more papers per capita than Greece and 4 times more than Portugal in 2017, in 1997 the ratio was identical to Greece (6.7) but much higher comparing to Portugal (24 times more productive). The lowest cost of paper production, as measured by the real GDP per capita per publication, has changed through the years: first, it was Ireland (1997–2001), then Greece (2002–2008) and finally Portugal (2009–2017). Portugal had the most expensive cost per paper from 1997 till 2008 and then, in the last decade, the lowest cost.

Table 3:

Temporal evolution of the publications’ ratio per country.

Year	Ireland			Greece			Portugal
	Publications	Publications per capitaa	Real GDP/publication	Publications	Publications per capitaa	Real GDP/publication	Publications	Publications per capitaa	Real GDP/publication
1997	17	4.7	1,505.9	7	0.7	2,285.7	2	0.2	73,000.0
1998	23	6.2	1,191.3	11	1.0	1,500.0	6	0.6	25,500.0
1999	19	5.1	1,578.9	20	1.9	850.0	2	0.2	79,000.0
2000	30	7.9	1,080.0	12	1.1	1,466.7	0	0.0	0.0
2001	35	9.1	965.7	14	12.9	1,300.0	9	0.9	1,822.2
2002	20	5.1	1,765.0	17	1.6	1,111.8	6	0.6	2,750.0
2003	29	7.3	1,234.5	19	1.7	1,047.4	10	1.0	1,630.0
2004	33	8.2	1,136.4	25	2.3	836.0	14	1.3	1,178.6
2005	24	5.8	1,620.8	25	2.3	836.0	8	0.8	2,075.0
2006	40	9.5	1,000.0	29	2.6	758.6	15	1.4	1,120.0
2007	34	7.8	1,200.0	41	3.7	553.7	6	0.6	2,866.7
2008	48	10.8	800.0	46	4.2	491.3	18	1.7	955.6
2009	50	11.1	726.0	38	3.4	565.8	32	3.0	521.9
2010	62	13.6	593.5	30	2.7	676.7	38	3.6	447.4
2011	70	15.3	538.6	48	4.3	385.4	42	4.0	397.6
2012	85	18.5	442.4	37	3.3	464.9	47	4.5	342.6
2013	84	18.3	453.6	43	3.9	390.7	67	6.4	238.8
2014	88	19.1	468.2	39	3.6	435.9	79	7.6	206.3
2015	120	25.9	428.3	44	4.1	388.6	75	7.2	221.3
2016	109	23.1	491.7	40	3.7	427.5	74	7.2	228.4
2017	123	25.8	457.7	39	3.6	446.2	68	6.6	255.9

1. ^aPer million inhabitants.

3.1.2 Articles citation profile

The 2,368 articles were cited 26,112 times. Irish articles are cited more often, and have an h-index (a measure of publications productivity and citation impact) of 52, while Greek publications h-index is 45 and Portuguese is 36 (Table 4).

Table 4:

Citation profile per country.^a

	Ireland	Greece	Portugal
Sum of citation	13,045	6,977	6,090
Without self-citations	12,333	6,751	5,704
Mean citation per item	11.41	11.18	9.85
h-index	52	45	36
Uncited articles	462	227	292

1. ^aThese data are the result of a country-specific query search in ISI Web of Science.

Forty-one percent of the articles have no citations (n=981), but, as expected, a large proportion (30%) of all uncited articles were published in the last 2 years (2016 and 2017). Of these, 55 were from Greece, 88 from Portugal, and 153 from Ireland, representing 70%, 62% and 66% of the publications per country in those years, respectively.

There were nine highly cited articles, i.e. with more than 100 citations (Table 5). Concerning the document type, articles represent 56% (n=1,314) of all published work. The most common language used was English (98%, n=2,315), 1.7% of the articles were published in Portuguese (n=40), and very few articles in other languages such as Greek, Spanish and Russian.

Table 5:

Top 10 highly cited articles by an Irish, Greek or Portuguese representative author.

Total citations	Title	Representative author	Year	Country
282	Validity of four pain intensity rating scales	Ferreira-Valente, MA	2011	Portugal
236	Different pain scores in single transumbilical incision laparoscopic cholecystectomy versus classic laparoscopic cholecystectomy: a randomized controlled trial	Tsimogiannis, KE	2010	Greece
168	Trunk muscle stabilization training plus general exercise versus general exercise only: Randomized controlled trial of patients with recurrent low back pain	Koumantakis, GA	2005	Greece
140	Multimodal analgesia with gabapentin and local anesthetics prevents acute and chronic pain after breast surgery for cancer	Fassoulaki, A	2005	Greece
132	Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis	Cruz, F	2004	Portugal
128	Synaptobrevin I mediates exocytosis of CGRP from sensory neurons and inhibition by botulinum toxins reflects their anti-nociceptive potential	Dolly, JO	2007	Ireland
124	Gabapentin in postamputation phantom limb pain: A randomized, double-blind, placebo-controlled, cross-over study	Buggy, DJ	2002	Ireland
104	Effect of bisphosphonates on pain and quality of life in patients with bone metastases	Costa, L	2009	Portugal
103	Carotid artery disease as a marker for the presence of severe coronary artery disease in patients evaluated for chest pain	Kallikazaros, I	1999	Greece

3.1.3 Institutions, research areas, and authors

The affiliation institutions are mostly universities or universities hospitals (Table 6). The ten institutions with more articles published in this sample represent 60% (n=1,424) of all articles. University of Porto (n=206), University College Dublin (n=195) and University of Athens (n=194) are the Portuguese, Irish and Greek institutions with more publications respectively, representing 33%, 17% and 31% of the articles published about pain in those countries between 1997 and 2017.

Table 6:

Top five institutions according to the number of publications by country.

Ireland			Greece			Portugal
Institution	Numbera	%b	Institution	Numbera	%b	Institution	Numbera	%b
University College Dublin	195	17.1	University of Athens	194	17.0	University of Porto	206	18.0
Trinity College Dublin	158	13.8	Athens Medical School	87	7.6	University of Lisboa	112	9.8
National University of Ireland Nui Galway	142	12.4	Aristotle University of Thessaloniki	80	7.0	University of Coimbra	80	7.0
Ulster University	130	11.4	University of Patras	44	3.8	Sao Joao Hospital	67	5.9
University of Limerick	120	10.5	University of Crete	42	3.7	University of Minho	51	4.5
Total	745	65.2	Total	447	71.6	Total	516	83.5

1. ^aNumber of publications; ^bpercentage of publications by country.

The three major pain research fields are neurosciences/neurology (19%, n=454), general internal medicine (16%, n=370) and anaesthesiology (13%, n=296). Irish main fields are general and internal medicine, neurosciences/neurology and anaesthesiology (Table 7). Neurosciences/neurology, anaesthesiology and orthopedics, and are the main Greek pain research fields. Portuguese authors main pain research fields are neurosciences/neurology, anaesthesiology, and rheumatology.

Table 7:

Top five research fields, number of publications and percentage by country.

Ireland			Greece			Portugal
Research area	Numbera	%b	Research area	Numbera	%b	Research area	Numbera	%b
General internal medicine	267	23.4	Neurosciences/neurology	170	27.2	Neurosciences/neurology	91	14.7
Neurosciences/neurology	193	16.9	Anaesthesiology	80	12.8	Anaesthesiology	74	12.0
Anaesthesiology	142	12.4	Rheumatology	73	11.7	Orthopedics	65	10.5
Rehabilitation	99	8.7	Psychology	62	9.9	Surgery	65	10.5
Rheumatology	66	5.8	General internal medicine	48	7.7	General internal medicine	55	8.9
Total	767	67.1	Total	433	69.4	Total	350	56.6

1. ^aNumber of publications; ^bpercentage of publications by country.

The five authors with more publications in pain research in each country are depicted in Table 8.

Table 8:

Top five authors per country.

Ireland			Greece			Portugal
Author	Numbera	%b	Author	Numbera	%b	Author	Numbera	%b
Finn DP	53	4.6	Mystakidou K	21	3.4	Tavares I	40	6.5
Baxter GD	45	3.9	Fassoulaki A	16	2.6	Lima D	37	6.0
Hurley DA	43	3.8	Vlahos L	16	2.6	Almeida A	33	5.3
McGuire BE	40	3.5	Melemeni A	13	2.1	Cruz F	21	3.4
Harmon D	39	3.4	Tsilika E	13	2.1	Castro-Lopes JM	17	2.8
Total	220	19.2	Total	79	12.7	Total	148	23.9

1. ^aNumber of publications; ^bpercentage of publications by country.

4 Discussion and conclusions

Pain scientific research has increased in the three countries analyzed during the period under study. That is consistent with the data from a bibliometric analysis of the “Pain” journal publications, one of the reference journals in the pain field, between 1975 and 2007, describing the growth of pain research [1].

Although the studied countries have a common European background and endured an economic crisis in recent years, the results of the present study demonstrate that the growth of the number of Irish, Greek and Portuguese publications over the analyzed time had a different profile.

Ireland is the country with a higher number of publications (more than 100 in the last 3 years), a higher number of citations and the number of publications per year rose at a constant pace. Irish population and GDP also increased over the last 20 years despite the recent economic crisis, in fact, the Irish economy was the first to recover in 2013 [16]. The University College Dublin is the institution with more publications and the three most productive authors of the three countries analyzed are Irish (Finn, Baxter, and Hurley).

Greek performance was very different in the last two decades: in the beginning, there was a publication growth, but from 2008 onwards the number of publications per year remained stable. There are four Greek highly cited papers and the University of Athens is the Greek institution with more publications. Greek population and GDP has oscillated in the studied years, but there was an increment in research expenditure in the last years (Greece has the lowest percentage of research investment of the three countries, but is the only one that has always increased that investment). In leading European countries (like Sweden, Austria, Germany, Denmark, and Finland), GERD value is around 3% of GDP, but the reported rate for the three studied countries is around 1%. An effort to reduce Greek National Health expenditure was also observed [25], which may also have consequences for Greek pain research.

Portugal is the country with fewer pain publications, with only two papers published in 1997, and fewer citations, but with the fastest growth from 2007 to 2014. Looking at Portuguese statistics, in the last decade population growth, GDP and research expenditure has reached a peak and then decreased (although to a slightly higher level than in 1997). In the last decade, Portugal had the lowest cost of paper production (measured by the GDP per capita per publication) while in 1997 it had the highest of the three compared countries. This could be the result of the Investment and Employment Initiative approved in 2008 by the Portuguese Council of Ministers to face the economic crisis. Portugal also has the most cited article included, a paper about pain scales validation by Ferreira-Valente in 2011. It is important to highlight that citations counts do not necessarily reflect article quality, only its impact on scientific research [6]. The University of Porto is the main promoter of pain research in Portugal.

This data corroborates, as in other studies, that scientific development is conditioned by the socio-economic context [24]. Probably, of the three analyzed countries, Greek financial crises and uncertainty had extended to scientific research, since there is always a time delay between research funding and publishing the article.

To our knowledge, this is the first bibliometric analysis in pain research to consider the economic crisis scenario in three European countries over 20 years, but this bibliometric study has some limitations. The first one is that only one electronic database was searched to retrieve the published articles. On the other hand, the main advantage of using ISI Web of Science was the standardization of the collected article’s information, especially about article’s citation profiles.

Secondly, by using only the terms “pain and nocicep*” in the title, a considerable number of publications on the subject of pain may be missed. However, this is likely to affect equally the publications arising from the three countries, and the main purpose of the present study was to analyse the evolution over the years and not the absolute numbers. In fact, bibliometric comparisons between countries or research fields should be interpreted with caution [26].

Also, the criteria of the author’s country affiliation institution defining the country of publication may not always reflect the country where the scientific work was conducted and/or funded, since authors from one country may work in institutions from different countries.

We also recognize that analysing the number of citations of the articles published in the last years is premature since the peak of articles citations usually occurs 2–3 years after the publication [26].

Finally, one must consider the time lag that encompasses scientific production from the start of a research project until the publication of the results [24], so possibly only in a few more years, we will be able to fully understand the economic crisis impact in scientific research.