Arab world’s growing contribution to global leishmaniasis research (1998–2017): a bibliometric study

Background Leishmaniasis is a parasitic disease caused by a protozoan of the Leishmania genus, and is considered a neglected tropical disease. It still remains a main public health concern at global level and in Arab world mainly in low-income countries. Therefore, this study was designed to evaluate the Arab world’s growing contribution to global leishmaniasis research. Methods This study describes a bibliometric review of all leishmaniasis research publications published between January 1998 and December 2017 indexed on the Scopus database. Results The total number of publications published at global level was 17,570 papers, which achieves an average annual productivity of 878.50 papers publications. Brazil was responsible for the greatest output with the total number of publications of 3865 followed by the Unites States (n = 2729), India (n = 2119), the United Kingdom (n = 1363), and Spain (n = 1274). By limiting the analysis to the publications that have been published by Arab world, the research productivity was 993 papers, which represents 5.65% of total research output at global level in research regarding leishmaniasis. Tunisia was responsible for the greatest output from Arab world with the total number of publications of 297 followed by Sudan (n = 192), Saudi Arabia (n = 131), Morocco (n = 119) and Egypt (n = 67). Since 1998, the growth of publications on leishmaniasis fluctuates, overall showing a rising trend in both global and Arab world. There is a highly significant correlation between publication productivity related to leishmaniasis at global level and the Arab world (r = 0.936; p-value< 0.001). Leishmaniasis treatment, intracellular mechanism of infection, and lifecycle of leishmania are the major current hot topics for the research in this subject at global level and the Arab world. Conclusions The current study presents a novel review of the current Arab leishmaniasis-related research, and how these results are related to worldwide output. In comparison to the global research output, the Arab world produced less leishmaniasis research. The data presented in the current study by this innovative approach may serve relevant researchers to direct the global leishmaniasis research to Arab counties in which leishmaniasis is endemic.


Background
Leishmaniasis is a parasitic disease caused by a protozoan of the Leishmania genus, and is considered a neglected tropical disease [1]. It is transmitted by the bite of infected female phlebotomine sand flies to mammals, including human beings [2,3]. The most common types of leishmaniasis are visceral leishmaniasis, cutaneous leishmaniasis, and mucocutaneous leishmaniasis [4]. According to World Health Organization (WHO) update (2017), leishmaniasis is the main parasitic killer responsible for an estimated one million new cases of leishmaniasis and 20,000 to 30,000 deaths annually [5].
The clinical manifestations of leishmaniasis can range from subclinical (inapparent), or a self-resolving cutaneous ulcer to a disseminated infection (cutaneous, mucosal, or visceral) and even to a lethal systemic illness [6][7][8][9][10]. Leishmania infects some of the poorest people in the world, and is linked to population displacement, malnutrition lack of financial resources, and poor housing [5]. Leishmaniasis is a public health problem and it is endemic in many parts of the tropics, subtropics and the Mediterranean [11,12]. Middle Eastern countries including Arab world's countries are currently considered to be at risk from leishmaniasis because these countries are endemic for visceral and cutaneous leishmaniasis, and a huge deal of human migration from neighbouring countries is observed [13][14][15][16][17].
To encourage and strengthen research capacity in the field of neglected tropical diseases, including leishmaniasis, the WHO highlights the periodic review and development of present and national research agendas [18]. A number of global bibliometric studies exist in various infectious diseases [19][20][21][22], including tropical medicine [23][24][25][26]. In addition, several studies have evaluated the research output for leishmaniasis [25,[27][28][29][30]. Previous reports about leishmaniasis have mainly assessed the research output of international studies, and paid less interest on leishmaniasis research structure in Arab world. In other words, there is a lack of bibliometric studies regarding leishmaniasis in Arab world that evaluates the research output in a qualitative and a quantitative way, and the relationship among research hot topics was not revealed obviously. Therefore, it is essential to evaluate the scientific research output of the Arab world relative to that worldwide. In particular, the current study aimed to analyze the contribution of the Arab scientific community with regard to global contribution in (i) leishmaniasis literature during the last two decades; (ii) international collaborative patterns; (iii) productivity of the most active institutions; (iv) productivity of the most relevant journals; (v) characteristics of highly cited papers; and (vi) hot research topics. The data in this study can present a clear picture on the research growth accomplished in the field of leishmaniasis research, and it can aid researchers and practitioners in recognizing fundamental influences of this field.

Methods
All leishmaniasis research publications published between January 1998 and December 2017 indexed on the Scopus database were analysed while the ones published in 2018 were excluded because Scopus as a secondary source has not yet archived all the publications from the primary sources for this year. The Scopus was used because it is the most widely accepted and frequently used database for analysis of scientific publications in different fields [22,[31][32][33][34]. The search was completed in November 2018. A bibliometric filter to capture leishmaniasis related publications from the Scopus database was created by using the key words 'leishmaniosis, or 'Leishmaniasis' or 'leishmania' or 'kala-azar' in the 'title' selection mode.
All documents referring to leishmaniasis research during the last two decades were assessed with the following aspects: document types, languages, yearly publications, countries and collaboration patterns, institutions, journals, h-index, citations, and research hotspots. The analysis focused on providing outputs for the top ten prolific of the following: countries, journals with their impact factors (IF), cited articles, and institutions as in the most previous bibliometric studies [19,33,[35][36][37]. In the current study, IF for the most prolific journals were extracted according to the 2017 journal citation report (JCR) at the time of study. Based on downloaded publications from Scopus database, bibliometric maps were created to determine the hot topics using the VOSviewer software version 1.6.9 (freely available at www. vosviewer.com). The collected data from the Scopus were limited to all 22 Arab countries, including "Algeria, Bahrain, Comoros, Djibouti, Egypt, Iraq, Jordan, Kuwait, Lebanon, Libyan Arab Jamahiriya, Morocco, Mauritania, Oman, Palestine, Qatar, Syrian Arab Republic, Saudi Arabia, Sudan, Somalia, Tunisia, United Arab Emirates, and Yemen" [38].

Statistical analysis
The Statistical Package for Social Sciences (SPSS) software version 16 was applied for analysis, while graphical research output was also conducted in Microsoft Excel. Pearson correlation coefficient was used to analyze trends in publication between publication productivity related to leishmaniasis at global level and productivity related to leishmaniasis from Arab world.
papers. The global research output consists of 15,021 articles (85.49%), followed by reviews (1175 papers, 6.69%), letters to the editor (615 papers, 3.50%). The remainders were other types (759 papers, 4.32%). Retrieved publications were written in 30 different languages, mainly English (n = 16,002; 91.08%) followed by Portuguese (n = 545; 3.10%), Spanish (n = 443; 2.52%), and French (n = 362; 2.06%). By limiting the analysis to the publications that have been published by Arab world, the research productivity was 993 papers during 1998-2017, which represents 5.65% of total scientific research output at global level in research related to leishmaniasis. The Arab world research output consists of 881 articles (88.72%), followed by reviews (51 papers, 5.14%), and letters to the editor (37 papers, 3.73%). The remainders were other types (24 papers, 2.42%). Retrieved publications from Arab world were written in 6 different languages, mainly English (n = 882; 88.82%). Since 1998, the growth of publications on leishmaniasis fluctuates, overall showing a rising trend in both global and Arab world ( Fig. 1). There is a highly significant correlation between publication productivity related to leishmaniasis at global level and the Arab world (r = 0.936; p-value < 0.001).
A total of 135 countries worldwide contributed to the literature on leishmaniasis over the study period. The publications share of the top 10 most productive countries in leishmaniasis research ranges from 22.00% for Brazil to 3.35% for Canada during 1998-2017. Table 1 shows the top 10 top-ranking countries at global level in terms of relative contribution of each country to the total number of publications. Brazil was responsible for the greatest output with the total number of publications of 3865 followed by the Unites States (n = 2729), India (n = 2119), the United Kingdom (n = 1363) and Spain (n = 1274); ( Table 1). The highest h-index value was 119 for the USA, followed by 102 for the UK, 83 for Brazil, 83 for India, and 82 for Germany. The USA, with the largest number of international collaboration publications (n = 1633), led this productivity rank followed by the UK (n = 937). Table 2 shows the ranking of Arab countries with relative contribution of each country to the total number of publications from Arab world. Tunisia was responsible for the greatest output with the total number of publications of 297 followed by Sudan (n = 192), Saudi Arabia (n = 131), Morocco (n = 119) and Egypt (n = 67); ( Table  2). The highest h-index value for Arab countries was achieved by Sudan (43) followed by Tunisia (31), Morocco (21), Saudi Arabia (20), and Palestine (18). The Arab countries have collaborated with 52 countries/ territories in leishmaniasis research (Table 3).
Top 10 journals with the most publications at global level are presented in Table 4, representing 3505 publications accounting for 19.95% of the total publications. The most prolific journals in the field of leishmaniasis were Plos Neglected Tropical Diseases (n = 523, I.F. = 4.367), American Journal of Tropical Medicine and Hygiene (n = 492, I.F = 2.564), and Experimental Parasitology (n = 364, I.F. = 1.821). While Table 5 shows the top  Figure 2 illustrates the term map of the global hot topics of leishmaniasis research over the period of 1998-2017 as extracted from titles and abstracts of publications. The term map was set up based on 952 terms encompass 4 main clusters in four colors: red, green, yellow, and blue. The red cluster included terms that were mainly related to the leishmaniasis causes and epidemiology research topics. The yellow cluster included terms closely related to treatment research topics. The green cluster included terms mainly related to the intracellular mechanism of infection. Blue cluster included terms roughly related to the lifecycle of leishmania. Whereas Fig. 3 illustrates the term map of the Arab world hot topics of leishmaniasis research over the period of 1998-2017 as extracted from titles and     [6,[39][40][41][42][43][44][45][46][47] at global level on leishmaniasis are presented in Table 6. From 1998 to 2017, the most frequently cited publication "Leishmaniasis: Current situation and new perspectives" published by Comparative Immunology, Microbiology and Infectious Diseases was from Switzerland by Desjeux [43] in 2004. The top 10 most cited publications [10,[48][49][50][51][52][53][54][55][56] from Arab world on leishmaniasis are presented in Table 7. From 1998 to 2017, the most frequently cited publication "Cutaneous leishmaniasis" published by Lancet Infectious Diseases was from Tunisia with international collaboration by Reithinger et al. [10] in 2007. Table 8 presents the performances of the top 10 most prolific institutes in the field of leishmaniasis between 1998 and 2017 at global level, representing 5498     Table 9 presents the performances of the top 10 most productive institutes in the field of leishmaniasis between 1998 and 2017 from Arab world or from international collaboration, representing 640 publications accounting for 64.45% of the total publications. The Institut Pasteur de Tunis is the largest contributor publishing 178 publications on leishmaniasis. The

Discussion
This study has made a comprehensive research on scientific research output of the Arab world relative to that worldwide in the field of leishmaniasis. The research findings have indicated that leishmaniasis has attracted more and more attention from Arab and worldwide scholars over the past decade. However, despite a significant growth of leishmaniasis publications in Arab world and at global level, the distributions are highly unbalanced at some regional levels. As a result of the current bibliometric analysis, researchers can get basic information on leishmaniasis research such as hot research topics in a historic perspective. However, from the Arab world only the top five countries -Tunisia, Sudan, Saudi Arabia, Morocco and Egypt -ranked well at global level as regards the number of publications related to leishmaniasis research: 17th, 24th, 32nd, 34th, and 40th, respectively. The current study shows that Arab countries are lagging behind most developed and developing countries in the number of publications related to leishmaniasis in contrast with high prevalence rate leishmaniasis in Arab countries. The WHO Eastern Mediterranean Region reported a very high proportion (82%) of countries endemic for cutaneous and visceral leishmaniasis [4]. The status of the health-research system in the Arab world has been described previously in numerous areas of health such as dengue research [21], pharmaceutical wastewater research [57], integrative and complementary medicine research [58], toxicology research [59], tobacco smoking research [60], breast cancer research [61], and infectious disease research [62]. Health-research systems in the Arab world are perceived as being non-productive system due to low priority in national research funding levels and development planning [63][64][65]. Despite the health services have improved in some Arab countries especially those with oil-based economies, the performance and development of their health-research system are lower than expected [66]. Generally, the amount of research related to medical field conducted in Arab world has grown considerably during the last decades and is still relatively small when compared with other world regions [61,[67][68][69].
Compared the current findings with the findings from developed countries, the Arab world produced less leishmaniasis research. This may be related to a relatively indigent economy in most Arab countries as reported in the online database of the World Bank [70]. In addition to a high poverty-growth elasticity for most Arab countries [71] according to population size and gross domestic product (GDP) per capita [70], which may lead to inadequate funding to support leishmaniasis research. For that reason, governments in the Arab world should give more attention to leishmaniasis research by offering more manpower and materials to support it. Also, the developed world should be persuaded to grant more collaborative plans with Arab world, and to attract more funding for leishmaniasis research and disease control.
Brazil is by far the most prolific country and is responsible for the greatest of number of publications in the field of leishmaniasis. A possible explanation for this finding may be due to high prevalence of leishmaniasis in this country which was exposed to many outbreaks [4,[72][73][74][75]. Additionally, other developing countries, such as India, and Iran, accounted in the most prolific countries in the field of the leishmaniasis research activity at global level, which may have been connected to a high prevalence of leishmaniasis in these countries [76][77][78].
In this study, Tunisia and Sudan had the highest research productivity in the field leishmaniasis. Previous  [20][21][22]35]. A possible explanation for these findings may be referring to leishmaniasis prevalence rates which are higher in Tunisia and Sudan. According to WHO report, zoonotic cutaneous leishmaniasis in Tunisia is endemic and considered a major public health problem and the annual incidence is approximately 30 per 100,000 people [82]. In Sudan, visceral leishmaniasis has been among the most important health problems [83]. Nearly 90% of global cases of visceral leishmaniasis occurred in the following countries: Brazil, Bangladesh, Ethiopia, India, and Sudan [4,6]. Additionally, Afghanistan, Algeria, Brazil, Colombia, the Islamic Republic of Iran, Iraq, Morocco, Peru, Sudan, the Syrian Arab Republic, Tunisia and Yemen represent 90% of cutaneous leishmaniasis cases that are reported worldwide [4]. Leishmaniasis treatment, intracellular mechanism of infection, and lifecycle of leishmania are the major current hot topics for the research in this subject at global level and the Arab world. Furthermore, the major current hot topics in the current study are presented by the research highlighted in the most highly-cited publications [6,10,[39][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54][55][56], which gives an important and valuable insight into which publications and topics are motivating the research growth in this field over the time.
Similar to other studies [19,33,[35][36][37], some limitations of this bibliometric study should be addressed. Although Scopus is one of the most largest global database [84], it might contain most publications in the field of leishmaniasis research. The main limitation relays to the citation and publications count applied for journals indexed by the Scopus. The citation and publication counts in these journals do not include citations and publications published in non-Scopus-indexed journals.

Conclusions
The current study presents a novel review of the current Arab leishmaniasis-related research, and how these results are related to worldwide output. In summary, this study evaluated almost the last two decades of leishmaniasis literature output at the global level as well as the Arab world level. The findings of the current study indicated that Brazil was responsible for the greatest output in term of total number of publications in the field of leishmaniasis as indexed by Scopus during the period studied followed by the Unites States, India, the United Kingdom, and Spain. Additionally, Tunisia was responsible for the greatest output from Arab world followed by Sudan, Saudi Arabia, Morocco, and Egypt. In comparison to the global research output, the Arab world produced less leishmaniasis research. It can be concluded that research in the topics related to "leishmaniasis treatment", "intracellular mechanism of infection", and "lifecycle of leishmania" will undoubtedly continue to be the hotspots of leishmaniasis research at global level and the Arab world. In conclusion, the data presented in the current study by this innovative approach presents a clear picture on the research growth accomplished in the field of leishmania research, and may serve relevant researchers to direct the global leishmaniasis research as to Arab countries in which Leishmaniasis is endemic.