The Most Influential Papers in Infectious Meningitis Research: A Bibliometric Study
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.325362
Source of Support: None, Conflict of Interest: None
Keywords: Bibliometrics, infectious disease medicine, meningitis, neurology, vaccinesKey Message: The most cited articles within meningitis research are primary research studies, more frequently published in high IF journals and by North American institutions. Bacterial meningitis comprises the majority of publications, although Cryptococcus sp represented the most.discussed single agent. The articles were mainly published after the AIDS pandemic and after the implementation of the main vacci
Meningitis is an inflammation of the leptomeninges surrounding the brain and spinal cord, defined by an abnormal number of leukocytes in the cerebrospinal fluid (CSF)., Such processes have infectious or non-infectious etiologies., Non-infectious causes are uncommon and include the effects of drugs, autoimmune disorders and neoplasms. Infectious causes include viral, bacterial, fungal and parasitical agents. Viruses are by far the most prevalent infectious cause, comprising more than 50% of cases, mostly represented by enteroviruses., Even though bacterial meningitis is less common than viral, it is more life-threatening., The introduction of large-scale vaccination has transformed the epidemiology of bacterial meningitis, with Neisseria More Details meningitidis and Streptococcus. pneumoniae being the current most common agents., After the Human Immunodeficiency Virus (HIV) pandemic in the 1980s Cryptococcus sp became extremely relevant in the setting of fungal meningitis., Despite the advances in prevention, diagnosis and treatment, bacterial meningitis, for instance, still presents elevated mortality (20%) and morbidity (50%) rates., Furthermore, meningitis remains a global health issue, with over 2.8 million cases and 318,000 deaths during 2016.
Bibliometric analyses are comprehensive descriptions of publication patterns in many fields. Through citation analysis, estimation of impact and performances of scientific journals, authors, countries and research lines can be achieved. In addition, most discussed topics and types of study in the literature may be identified. Such studies may also reveal the most influential publications in any given area, which can be used to guide teaching and learning as well as the elaboration of further studies. Bibliometric analyses have been conducted within many fields, including infectious diseases,, neurology, and neurosurgery., To the authors' best knowledge, there are no bibliometric analyses regarding infectious meningitis. Given the relevance of the topic, the authors aim to perform an analysis of the 100 most cited papers within infectious meningitis research.
Search and selection strategies
The authors searched the databases Scopus and Web of Science Core Collection (WoS) during May 2019 for documents containing “(Meningitis) OR (Meningoencephalitis)” in their title. The articles were arranged from highest to lowest the number of citations and exported. Based on the articles titles and/or abstracts, two reviewers independently included those that addressed infectious meningitis, and discrepancies were resolved by consensus. When the same article was retrieved from both databases, the one with the highest number of citations was preferred. The selection process ran until reaching the 100 most cited papers.
The variables included in the analysis were journal of publication and its 2018 and 5-year Journal Citation Reports (JCR) Impact Factor (IF), year of publication, type of study, infectious agent, first and corresponding authors, and the country and institution of the corresponding author. The JCR IF of the articles were obtained from the InCites JCR website (https://jcr.clarivate.com) in July 2019. The studies were categorized in primary (i.e., original articles) and secondary research by their abstracts and/or full-texts, as needed. Primary research articles had their topic of study analyzed, which were subdivided in Treatment/Management, Clinical Features and Diagnosis/Outcomes, Pathophysiology (Laboratory), Epidemiology/Vaccines, and Miscellaneous (multiple topics). Secondary research articles were divided in narrative reviews, systematic reviews and guidelines – since these articles generally addressed multiple topics.
All variables were also assessed separately for primary research. When information regarding correspondence was not available, the first author was also considered the corresponding author. Academic institutions were preferred over hospitals and other institutions as address for correspondence. The total number of citations and the number of citations per year following publication showed asymmetric distributions (skewness of 2.55 and 3.12, respectively). Therefore, median and interquartile range (IQR) were preferred as the measure of central tendency and as the measure of dispersion, respectively. These data were retrieved from Microsoft Excel.
Scopus and WoS returned 36,242 and 23,559 documents, respectively. The number of citations of the 100 most cited articles within infectious meningitis research ranged from 220 to 1,246 (median = 287.50, IQR = 141.50). The sum of all citations was 36,231. The number of citations per year, in turn, ranged from 3.73 to 124.60 (median = 13.61, IQR = 8.53). A list with the ten most cited articles in this field is shown in [Table 1]. The most cited article is entitled ”Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS” and was published in 2009 by Park BJ et al. This was also the study with the highest number of citations per year (124.60). The 100 papers were published from 1948 to 2017 by 16 countries and 57 institutions.
Journal of publication and impact factor
The New England Journal of Medicine (NEJM) was the journal with the greatest number of articles (27, being 26 from primary research) and citations (12,266, being 10,759 from primary research), as well as the one with the greatest IF. A total of 66 articles were published in journals with a 2018 IF higher than 10. A detailed list of the most prolific journals within the top 100 is presented in [Table 2]. The relation between the 5-year IF of the journal of publication and the number of citations is shown in [Figure 1]. The journal Herpes does not publish issues anymore. Hence, its IF could not be retrieved.
Country and institutions
United States (USA) was the country with the greatest number of articles (56, being 42 from primary research) and citations (21,388, being 16,118 from primary research) in the top 100. Only nine articles were published outside North America or Europe. In two articles, information regarding country and institutions of the authors was lacking. A complete list of countries along with their number of articles and citations in top 100 is provided in [Table 3]. The institution with the greatest number of articles and citations in top 100 was Centers for Disease Control and Prevention (CDC) (six articles, all from primary research; and 3,559 citations). Following, Yale University appears with six articles (being four from primary research) and 2,286 citations (1,545 from primary research). A detailed list of the most cited institutions is shown in [Table 4].
Infectious agent and study category
The most discussed agents were bacteria, with 72 articles (48 from primary research) and 26,362 citations (being 17,492 from primary research). When analyzing a specific agent, Cryptococcus sp. comprised the highest number of articles (16, being 13 from primary research) and citations (6,617, being 5,769 from primary research). A complete list of the most discussed infectious agents is provided in [Table 5]. The majority of articles were from primary research, accounting for 70 papers and 25,754 citations. Among them, the most discussed topic was Clinical Features and Diagnosis/Outcomes, with 22 articles and 8,325 citations [Table 6]. Among the 27 articles from secondary research – which accounted for 9,730 citations - the most common type of study was Narrative Review (18 articles and 5,685 citations).
Year of publication and authors
The majority of papers were published after the late 1980s, accounting for 25,647 citations [Figure 2]. The year of 1997 had the greatest number of articles (nine, being seven from primary research) and citations (3533, being 2,822 from primary research). The author with the greatest number of publications was Quagliarello VJ, with five articles (three from primary research) whereas Van De Beek D had the highest number of citations (1,749 being 869 from primary research). The most cited authors within infectious meningitis research are shown in [Table 7].
In the present study, we conducted a bibliometric analysis of the 100 most cited articles within infectious meningitis research. These papers were published more often by North American and European institutions and in very high IF journals. The majority of publications were original articles, while the most commonly discussed topics were related to Clinical Features and Diagnosis/Outcomes and Treatment/Management. Bacteria were the most discussed agent, whereas Cryptococcus sp was the most discussed and cited single agent.
The most cited articles within infectious meningitis research were published in general medicine journals with a very high IF, with a spotlight to NEJM, The Lancet journals and the Journal of the American Medical Association (JAMA) journals [Table 2] and [Figure 1]. These journals are among the approximately 2.20% of journals indexed in the WoS database with an IF higher than 10 (data retrieved from https://jcr.clarivate.com in July 2019). This special attention dedicated to the topic is possibly due to its interdisciplinary nature, associated with its potentially life-threatening course. Indeed, meningitis is an issue that is prevalent and managed in primary, secondary and tertiary care, encompassing family physicians, pediatricians, emergency room doctors, and infectologists. Conversely, prior bibliometric analyses regarding more specialized infectologic, neurological and neurosurgical issues - such as orthopedic infections, aneurysmal subarachnoid hemorrhage, and headache disorders – showed that the most cited articles were published in more specialized journals, with a much lower IF.
In general, USA is by far the most prolific country within medical research, having also the greatest number of citations (data retrieved from https://www.scimagojr.com/countryrank.php?area = 2700 in July 2019). Multiple bibliometric analyses also showed that USA has the greatest number of articles among the most cited within various topics.,,, Hence, at least some of the most prolific and most cited institutions in several fields are from USA. Not surprisingly, USA was responsible for the publication of 56 of the 100 most cited papers within infectious meningitis research - including the four most cited - accounting for 21,388 citations. Moreover, the country also had the three institutions with the greatest number of articles in top 100 - CDC (six articles and 3,559 citations), Yale University (six articles and 2,286 citations), and University of California (five articles and 1,396 citations) [Table 4]. The author with the greatest number of articles was Quagliarello VJ (five articles and 1,730 citations) from Yale University, whereas the most cited was Van De Beek D (three articles and 1,749 citations) from University of Amsterdam [Table 7].
Only 7 of the 100 most cited articles were published by institutions from developing countries – three from Vietnam,,, two from South Africa,, one from Panama and one from Malawi. These articles comprised 2097 citations, with all three articles from Vietnam authored by Thwaites GE. Still, while most of the high-impact research originates from Northern America and Europe, the burden of meningitis is much higher on developing countries. That discrepancy generates gaps in literature about meningitis, especially regarding its epidemiology and outcomes in such countries. In spite of that, relevant data still arise from low-resource scenarios. The Malawian article, as well as one of the South African, and one of the Vietnamese,, articles included in this analysis, for instance, reported the results of clinical trials on dexamethasone for the treatment and prevention of sequelae from infectious meningitis – a topic that has been widely discussed in the last 30 years. Even though much of the research from developing countries is not published in high-impact journals and is often available only in local databases – which were not included in this analysis –, it still provides valuable data on the subject. For instance, researchers from countries such as Brazil and India have greatly contributed to the knowledge on the epidemiology,,,, and impact of vaccination, in their countries, along many other subjects within the field of meningitis research.
The epidemiology of bacterial meningitis has changed dramatically over the last 30 years due to the implementation of mass vaccination. H. influenzae for instance, now only a minor cause of meningitis, used to represent over 50% of cases before the introduction of mass infant vaccination in 1990., Even though N. meningitidis is currently responsible for multiple large outbreaks in sub-Saharan African – a region known as the meningitis belt – mass vaccination campaigns have shown promising results in both high and low-income settings., Meanwhile, S. pneumoniae has become the main cause of sporadic cases in developed countries, and many vaccines have been developed for its multiple serotypes., In this analysis, the topics Epidemiology/Vaccines were discussed in 12 primary research publications (5,235 citations) [Table 6]. Of these, ten articles were published after the implementation of the first vaccines in the early 1990s. The agents mentioned above were frequently discussed together, being classified as “General bacteria” in this review as, comprising 36 articles and 14,794 citations. Meanwhile, 11 articles (2938 citations) exclusively discussed S. pneumoniae, 3 discussed N. meningitidis (1297 citations) and 3 discussed H. influenzae (898 citations) [Table 5].
Despite an initial understanding of the pathophysiology, clinical features and complementary exams for the diagnosis of meningitis, there were no effective treatments until the 20th century – and the disease progressed to death in 90 to 100% of cases., This understanding is evolving and is constantly getting special attention within the field. In this analysis, for example, Clinical features and Diagnosis/Outcomes were the topics with the greatest number of primary research articles (22) and citations (8,325) [Table 6]. These topics seem to be constantly the core of meningitis research interest, since these 22 articles were published regularly from 1965 to 2016. The treatment of meningitis has also been a spotlight topic in the field. Indeed, Treatment/Management were the second most addressed topics (20 articles and 7,488 citations) [Table 6] in the current study, without preference regarding year of publication – since these papers were published regularly between 1948 and 2006.
The rise of HIV has not only increased the incidence of meningitis, but also directed attention to specific infectious agents among infected individuals, such as Cryptococcus sp., which changed meningitis epidemiology., Indeed, in the 1950s there were less than 300 cases reported in the world, which increased dramatically during the AIDS pandemic and reached, in the early 1990s, an annual incidence of 17-66 per 1,000 for HIV-infected individuals., CM has also been on the rise due to the spread of immunosuppressive treatments for organ transplantation and autoimmune disease, as well as for complications of cancer and its treatment., In our study, Cryptococcus sp was specifically discussed in 16 articles (6,617 citations), being the single most common as well the most cited discussed pathogen among the top 100. Among these papers, 14 were published in the late 1980s and thereafter – including the most cited article of the entire analysis and the two with the greatest number of citations per year. This pattern is probably a result of the massive increase in its incidence after the AIDS pandemic. Besides, [Figure 2] shows that the majority of articles and citations within infectious meningitis correspond to the period after the late 1980s – after the AIDS pandemic and after the implementation of the main vaccines for meningitis.
Mycobacterium tuberculosis used to be the most common cause of meningitis at the turn of the 20th century, decreasing significantly after the improvement of socioeconomic conditions and implementation of primitive health policies., However, it has recently been on the rise in both low and high-income settings. The spiking incidence of tuberculous meningitis appears to be linked to the recent AIDS pandemic, as well as to immigrations, growth of prisons and homeless populations and decline in TB control funding. The appalling increase in incidence has led to renewed interest in tuberculous meningitis in recent years, as demonstrated by the large number of articles published on the subject after 1990 included in this review.
Strengths and limitations
Among the strengths of the present study, the authors highlight the use of two complementary databases (Scopus and WoS). Scopus encompasses over 36,000 titles and presents superior coverage regarding biomedical research publications, it only includes references of studies articles published from 1970 and onwards (data retrieved from https://www.elsevier.com/solutions/scopus/how-scopus-works/content in July 2019). WoS, in turn, has an arguably inferior coverage with 21,000 titles, although it includes articles published as early as 1900 (data retrieved from https://clarivate.libguides.com/webofscienceplatform/coverage in July 2019). Even though Google Scholar (GS) has a wider coverage than both Scopus and WoS, the impact of GS exclusive citations is much lower than that of publications also found in the latter two databases., For these reasons, the authors chose WoS and Scopus for this review.
This study presents some limitations. It is important to consider that the citation count may be influenced by factors not necessarily related to the impact and quality of a study, such as the addressed topic and the study design., For instance, clinical interventional research articles may be severely underestimated when compared to basic and diagnostic research within the same field. Also, although the absolute number of citations provides an overview of landmark articles, it is one among many methods to evaluate the most relevant publications. Thus, it is possible that some relevant studies were not captured by this analysis. Data regarding country, institution and department were obtained using the corresponding author's information, which may differ from that of the first author or other co-authors. Also, some researchers have multiple affiliations, which could compromise the identification of the most cited institutions. Furthermore, since the absolute number of citations for any given paper tends to increase over time, this review may have favored earlier over later publications. One clear example is the 97th most cited article, which was published in 2017 and has the second highest citation density (110.50 citations per year).
To the authors' best knowledge, this is the first bibliometric analysis to evaluate the most cited studies on infectious meningitis. Similarly to other areas, research on meningitis is largely centralized in Northern America and Europe, especially in the United States. Since infectious meningitis is a multidisciplinary field, the most cited articles were published in very high IF general journals. Bacteria were the most studied agents of infectious meningitis, whereas Cryptococcus sp was the most discussed single agent – probably due to its relation with AIDS. Primary research more frequently addressed topics such as clinical features and management while secondary research consisted mostly of narrative reviews. Meningitis research boomed after the AIDS pandemic and after the introduction of new vaccines, as demonstrated by the increase in publications in the late 1980s. Infectious meningitis is a widely studied subject in many fields of medicine and, given its impact on public health in both high and low-income settings and it's still daunting morbimortality, future research must be encouraged.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]