A bibliometric study of international scientific productivity in giardiasis covering the period 1971 – 2010

Introduction: Despite years of relative neglect, interest in Giardia infection seems to be recently growing, perhaps in part due to its inclusion into the World Health Organization’s Neglected Diseases Initiative since 2004. The purpose of this study was to provide an overview of Giardia and giardiasis research over time, as represented by the quantity of published papers. Methodology: Data for this study were collected from the electronic PubMed/Medline database of National Library of Medicine's (NLM), due to it is easily accessibility and wide use. It was accessed online between April and December 2011. Data for the period 1971–2010 were obtained and information was downloaded using the EndNote program developed by Thomson Reuters. Results: During the study period, a total of 6,964 references (articles, reviews, editorials, letter to the editor, etc.) covering different aspects of Giardia and giardiasis were located in the PubMed database after applying the search strategy reported above. Most papers were original articles and published in English. Conclusions: In this first effort to explore the development and research productivity on giardiasis over time (no previously published bibliometric studies on giardiasis exist), two interesting characteristics of the Giardia and giardiasis literature were discovered: the concentration of papers over journals disseminating the research results, and that research in this field is growing and will likely continue to grow in the coming years.


Introduction
The etiological agent of human giardiasis, Giardia lamblia (syn.G. duodenalis, G. intestinalis), is the commonest pathogenic protozoan infection of the intestinal tract.Giardia is endemic throughout the world, and its prevalence varies by age and sanitary standards [1].
Despite years of relative neglect, interest in Giardia infection seems to be recently growing, perhaps in part due to the combination of its inclusion in the World Health Organization (WHO)'s Neglected Diseases Initiative since 2004 [2] and its re-emergence in industrialized countries, where it has been increasingly recognised as an etiological agent in numerous outbreaks of diarrheal disease in day-care centers and in water-and food-associated outbreaks [3][4][5].G. lamblia is responsible for an estimated 2.8×10 8 cases per year.The prevalence of the infection is higher in developing countries, as the poor sanitary conditions favor the contamination of water and food with cysts.Approximately 200 million people have symptomatic giardiasis in Asia, Africa, and Latin America, and about 500,000 new cases are reported each year [6].
Bibliometrics, the scientific and quantitative study of publications, uses mathematical formulas to quantify productivity distribution and yield of communication output and enables predicting and studying scientific progress [6].These kinds of studies are useful tools for assessment of the social and scientific relevance of a particular discipline or subject, since they permit analysis of the growth, size, and distribution of scientific literature on the topic during a period of time.Currently, estimates of global and regional productivity of ongoing research on giardiasis may be of interest.There are international bibliometric studies in tropical medicine and/or parasitic diseases [7][8][9][10][11][12][13][14][15]; however, these have not focused exactly on the field of giardiasis.The purpose of this study was to provide an overview of Giardia and giardiasis research over time, as represented by the quantity of published papers.

Methodology
Data for this study were collected from the electronic PubMed/Medline database of the National Library of Medicine (NLM), due to its accessibility and wide use.It was accessed online between April and December 2011.Data for the period 1971-2010 were obtained and information was downloaded using EndNote version 7.0 developed by Thomson Reuters.
The search terms used to retrieve data were "Giardia" OR "giardiasis" in all fields of the database, AND the years of study  in the publication date field.The subject content of the records was analyzed according to the structure of the United States of America National Library of Medicine's Medical Subject Headings (MeSH) thesaurus; thus, check tags, main headings, and subheadings were also considered.Bibliographic data that were downloaded for analysis included author, title of article, name of journal, language of publication, date (year) of publication, and the document type.
As the period studied comprised 40 years, the evolution of the different topics analyzed in the study was possible, dividing the period in four ten-year time sub-periods: 1971-80, 1981-90, 1991-00, and 2001-10.
Two independent researchers (RA and RLV) collected the data in order to strengthen the methodological validity of the study.When there were disagreements between the two researchers, the results were discussed in meetings with the rest of the authors.

Results
During the study period, a total of 6,964 references (articles, reviews, editorials, letter to the editor, etc.) covering different aspects of Giardia and giardiasis were located in the PubMed database after applying the search strategy reported above.Figure 1 shows the growth of Giardia and giardiasis literature over the years studied.
There was an increase in publication output, mainly in the last decade, where the scientific output reached values of more than 200 articles per year (Figure 1).Despite the lack of research observed during the first three decades, the advances in proteomics, the study of domestic animals as reservoirs of potentially zoonotic agents, the effect of climate change on the incidence of infectious diseases, the analysis of environmental risk factors, among other aspects, allowed the study on Giardia and giardiasis to experience growth during the last period.
The most common type of documents on Giardia and giardiasis were original articles, accounting for 78.49% of the total (5,466) studies.Reviews were the second most common type of document (n = 601; 8.63%), followed by case reports (6.81%) and letters to the editors (3.60%).The rest were < 1%, corresponding to other types of studies (Table 1).A significant pattern observed, especially during the last decade, was the increase of clinical research.Comparative studies, clinical trials, and evaluation studies of different therapeutic strategies against giardiasis were the main type of clinical research identified.

Language of publication
The articles identified were published in 27 languages (Table 2).Over the entire period, the main language was English (Figure 2), which increased from 66.67% to 88.40% over the years.The other languages (i.e., Russian, Polish and German, which were the most common non-English languages during the period 1971-1980) were replaced in the next decades by Spanish and French.Spanish was the second most important language since the 1980s.A surprising position during the last decade was occupied by Turkish (the third position, 1.93% of articles published).

Journals of publication
A total of 1,224 scientific journals published the 6,964 articles on Giardia and giardiasis during the period of 1971-2010.Only 30 (2.4%) journals published 2,234 (32.1%) articles of the whole scientific output, while the rest was spread over 1,194 journals (Table 3).4).The third most productive journal, Veterinary Parasitology, the Netherlands, was also the most productive during the first 10 years of this century.

Research topics
The analysis of MeSH terms used by indexers in PubMed completed the current view of the Giardia and giardiasis research.The description of articles through MeSH terms is less complete and accurate in articles published before the 1990s.Regardless, it is an important approach to be taken into account in bibliometric analysis.
Humans (66.33%) and animals (58.36%) have been studied in similar proportions by the international scientific community (Table 5).Both terms were used together in 2,063 articles (29.6%), which is related, on the one hand, to the analysis of prevalence and clinical manifestations of the disease, and to the zoonotic significance of this infection on the other hand.The research on Giardia and giardiasis in animals was very strong during the 2001-2010 period.
A different view offers the descriptors related to gender.Despite both terms being used in similar proportions (male, 31.81%;female, 30.869%), the coincidence of terms is significantly high (a total of 2,150 articles using both terms).This clearly indicates that there were no identified gender differences in clinical research on Giardia and giardiasis during this period.
Infants were the most studied age group in the scientific literature on Giardia and giardiasis, according to the keywords used to describe this aspect (child; child, preschool; infant; infant, newborn).Infants were studied specifically in 2,000 articles (28.7%), which demonstrates the importance of this age group in clinical research.In Giardia and giardiasis research, the most studied animal models were mice (5.76%), dogs (3.81%), cattle (2.86%), cats (2.10%), and rats (1.57%).Mice and rats are classical biological models used in pre-clinical studies, and their use in articles during the first two decades is significant.However, domestic animals, especially dogs and cats, were intensively studied during the last ten years.
In general, the most frequently used keywords revealed the most important research trends in the field (Table 6).Major descriptors relating to "parasitology", "isolation and purification" or "epidemiology" aspects of Giardia and giardiasis research were present during the whole study period.However, these research fronts changed during the different periods studied."Drug therapy", "therapeutic use" and "complications"; and "parasitology", "epidemiology" and "feces" were the three major descriptors during the periods 1971-1980 and 1981-1990, respectively."Isolation and purification" and "epidemiology" were the three major descriptors for the last two periods studied.

Main authors
A total of 16,864 authors were involved in the scientific research on Giardia and giardiasis during the 40-year period.Taking into account the activity of authors (27,244 entries of authors in 6,964 articles), the average number of authors per article was 3.91.Only 26 of these authors published more than 30 articles during the whole period, and 11 of them had an average higher than one article per year (Table 7).
The top 26 authors were led by the Americans F. D. Gillin and T. E. Nash and the Australian R. C. Thompson, all of them highly productive during the three last decades.The United States of America included 10 authors in the ranking, followed by Australia (5), India (3), and Canada (3).Europe was represented by three authors, one each from the United Kingdom, Sweden, and Norway.Latin America included two authors, one each from Argentina and Mexico.

Discussion
Systematic monitoring and evaluation of research on parasitic infections -in this case, Giardia and giardiasis, currently part of the WHO's Neglected Diseases Initiative -is becoming essential to help public health policies, decision makers, and related research workers.Bibliometric studies, despite their methodological limitations, are useful tools for assessing the social and scientific relevance of a particular discipline or subject, since they allow the analysis of the growth, size, and distribution of scientific literature on the topic in question during a given time period.According to Boreham et al. [17], research on Giardia and giardiasis has evolved through three phases: the observational and descriptive approach, the use of quantitative experimental and survey methods, and the use of molecular tools.This study was a purely descriptive analysis of the publications related to Giardia and giardiasis indexed in the PubMed database over four decades, as well as their evolution during this period [1][2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17].According to the present study, there has been a steady growth of literature dedicated to Giardia and giardiasis throughout the 40-year period analyzed.Part of this could related to the progressive improvement in sanitation and the fading of the role of fatal epidemic infections and other public health problems that seemed to be more pressing as overwhelming everyday health concerns.Additionally, it should be mentioned that the extension of giardiasis to industrialized countries, the expansion of its range of symptoms, the search for better diagnostic procedures, and the increase in therapeutic failures with the drugs currently in use, may also have renewed the interest in this protozoan disease, as well as the increase in research on its molecular aspects and the incorporation of new journals in PubMed devoted to the study of parasitic and tropical diseases in recent years, including a wide diversity of geographical regions.
One of the important consequences of giardiasis is the potential persistence of symptoms after treatment, probably due to this parasitic infection triggering postinfectious syndromes such as celiac disease, lactose intolerance, food intolerance/allergies, or others.Some cases may be reinfection or relapse.Recognition of those consequences could be another possible reason behind the increasing number of publications on Giardia and giardiasis [18].
Another reason behind the increased number of publications may be the recent and increasing occurrence of outbreaks in more developed settings, such as Norway, with important long-term sequelae [19]; thus more research may be driven by its occurrence in these settings [20].
As expected, original articles were the most common type of document retrieved.This increased number of published original articles is mainly attributed to the research on molecular and basic aspects, as well as to the extension to the area of veterinary medicine, and the search of new diagnostic tools, which seems to be a continuous stimulus for the development of research in this field.
The introduction, in the last decades, of new journals (particularly non-English journals) in PubMed could also have had an impact on this.The core of journals with high productivity usually contains more relevant articles in the area.Parasitology Research, a journal that is devoted to parasites, published the highest number of articles, while the Transactions of the Royal Society of Tropical Medicine and Hygiene, the American Journal of Tropical Medicine and Hygiene -which were in the top ten of the most productive journals on Giardia and giardiasis during the four decades studied -the Southeast Asian Journal of Tropical Medicine and Public Health, Med Parazitol, and Wiad Parazytol had frequent publications on Giardia and giardiasis during the four decades analyzed.It is interesting to observe the importance that is conferred to veterinary giardiasis; Veterinary Parasitology was the third most productive journal, and also the most productive during the first 10 years of this century.The steady increase in the literature on Giardia and giardiasis and its diffusion in some of the most prestigious scientific journals suggest that giardiasis is a disease whose development is in full swing, from clinical and basic research perspectives.
The fact that a high number of articles was written in English language is not surprising; as stated by Meneghini and Packer [18], English has become the modern lingua franca of scientific activities in a world that is economically, scientifically, and culturally largely dominated by Anglo-American countries.However, it is well known that the PubMed database is biased in favor of English-language journals; thus, our survey may have penalized those researchers and countries that have a tradition of publishing their work in journals of their own language.This could be the case for non-English-speaking researchers from Eastern Europe and Japan, who tend to publish their findings in regional journals in their mother tongue, which leads to the risk that results might be ignored simply because they are not readily accessible to the international scientific community.Surprisingly, Spanish and German are taking a relevant place, perhaps as a reflection of some initiatives created to overcome this dilemma, the main aim of which is to strengthen the impact and quality of national journals with the goal of gaining greater international visibility for articles published in languages other than English [17].
A further consideration regarding a problem that affects many biomedical topics should be noted; the analysis of keywords revealed a high heterogeneity of terms.Perhaps if all keywords were re-elaborated in order to group together concepts expressed with similar terms, a more synthetic picture of current research trends within Giardia and giardiasis could have been found.On the other hand, the ranking of the most productive authors involves some of the most influential and prestigious researchers devoted to the study of the disease, including classics such as Nash, Thompson, Farthing, and Faubert.
Potential limitations of the study are related to the database used to retrieve articles.Further studies should include other databases such as the Science Citation Index and Scopus, as well regional databases such as Latin American Literature in Health Sciences (LILACS) and the Scientific Electronic Library Online (SciELO).The PubMed database does not represent all scientific and biomedical journals published; in fact, many articles of importance may appear in journals other than those indexed in the PubMed database or may not be indexed, as in the cases of contributions made to scientific conferences and meetings.However, the recognized quality of the publications included in these databases and their coverage means that the documents selected constitute a more than representative sample of the international research on Giardia and giardiasis.
Despite its methodological limitations, this study represents the first effort to explore the development and research productivity of Giardia and giardiasis over time and has pointed out two interesting characteristics of the Giardia and giardiasis literature: the concentration of papers over journals disseminating the research results, and that research in this field growing and will likely continue to grow in the future.

Figure 1 .
Figure 1.Scientific output per year during four decades on Giardia and giardiasis in PubMed, 1971-2010* This journal's core was headed by Parasitology Research (Germany), which covered a high number of research on Giardia and giardiasis during the entire period.Five journals (Transactions of the Royal Society of Tropical Medicine and Hygiene, United Kingdom; the American Journal of Tropical Medicine and Hygiene, the United States (USA); the Southeast Asian Journal of Tropical Medicine and Public Health, Thailand; Med Parazitol (Moscow), Russia; and Wiad Parazytol, Poland) were found to have frequent publications on Giardia and giardiasis during the four decades analyzed.The rest of journals, with some exceptions (Lancet, United Kingdom; Journal of Infectious Diseases, USA; Annals of Tropical Medicine and Parasitology, United Kingdom; Gut, United Kingdom; and Gastroenterology, USA) had the most publications on Giardia and giardiasis during the last decade.Only the American Journal of Tropical Medicine and Hygiene, USA was in the top ten of the most productive journals on Giardia and giardiasis during the four decades studied (Table

Figure 2 .
Figure 2. Total number of giardiasis research publications in PubMed in any language (black circles), in English (squares), and in non-English languages (black triangles) between 1971 and 2010

Table 1 .
Characterization of the scientific output on giardiasis covered by PubMed 1971-2010 (type of articles and clinical research)

Table 2 .
Evolution per decade of the different languages involved in the scientific output on giardiasis covered by PubMed, 1971-2010

Table 3 .
The top 30 journals with a large coverage on giardiasis research during the period 1971-2010

Table 4 .
The top ten of most productive journals on giardiasis by decade, 1971-2010

Table 5 .
Samples, gender, age groups, and animal models most frequently studied in articles on giardiasis covered byPubMed, 1971PubMed,  -2010

Table 6 .
List of the keywords (MeSH terms) most frequently used in articles on giardiasis covered byPubMed, 1971PubMed,  -2010

Table 7 .
Authors with 30 or more papers on Giardia or giardiasis during the period 1971-2010