Skip to main content
Help us understand how you use our websites. Take part in our 30 minute study now.

A bibliometric analysis of human strongyloidiasis research (1968 to 2017)

Abstract

Background

Strongyloidiasis is a neglected tropical disease (NTD). It is commonly associated with poverty and poor hygiene. Strongyloidiasis poses an unseen global public health problem. The aim of this study was to assess and analyze peer-reviewed literature on human strongyloidiasis to shed light on the evolution, volume, important topics, and key players in the field of human strongyloidiasis.

Methods

A validated bibliometric method was implemented using Scopus database for the study period from 1968 to 2017. The search strategy was developed based on keywords related to strongyloidiasis. Bibliometric indicators and visualization maps were presented.

Results

In total, 1947 documents were found. Retrieved documents received 32,382 citations, an average of approximately 16.6 per document, and an h-index of 76. The most frequently encountered keywords in the retrieved literature focused on hyperinfection, diagnosis, prevalence, and ivermectin. The USA led with 540 (27.7%) documents followed by Brazil (139; 7.1%) and Japan (137; 7.0%). When research output was standardized by income and population size, India ranked first (12.4 documents per GDP/capita) followed by the USA (9.1 documents per GDP/capita). The most active journal involved in publishing articles was the American Journal of Tropical Medicine and Hygiene (95; 4.8%). In terms of institutions, the University of Ryukyus (Japan) was the most active with 62 (3.2%) publications, followed by the University of Pennsylvania with 54 (2.8%) publications.

Conclusion

The volume, growth, and international research collaboration in human strongyloidiasis were inadequate given the long history of the disease, the large number of affected people, and the results obtained for other NTDs. Research in human strongyloidiasis needs to be strengthened and encouraged in endemic regions in Southeast Asia and Latin America. International research networking needs to be established to achieve the goals of Sustainable Development Goals in fighting and eradicating NTDs by 2030.

Background

Strongyloidiasis is a human parasitic infection and one type of soil-transmitted helminthiasis (STH) [1]. It is mainly caused by Strongyloides stercoralis and rarely by Strongyloides fuelleborni [2]. Strongyloidiasis is a neglected tropical disease (NTD) that is rarely recognized as a serious public health issue [3,4,5]. The history of strongyloidiasis goes back to the late nineteenth century, but interest in the condition increased in the 1940s when it was discovered that strongyloidiasis in people with impaired immune function might develop into hyperinfection syndrome and disseminated strongyloidiasis [6]. Much global efforts have been made to fight and eliminate NTDs since more than a billion people, mostly in developing countries, are infected with one or more of the NTDs [7, 8].

Strongyloidiasis is a global disease with a high prevalence in Latin America, Southeast Asia, Sub-Saharan Africa, and low prevalence in certain parts of the Southeast United States [9,10,11]. A study on the global distribution of S. stercoralis indicated that in Africa, the range of infection rates in the communities varies from 0.1% up to 91.8% while in South- and Central-America, the range varies from 1.0 to 75.3% [12]. The same study indicated that in South-East Asia, the infection rate also varies but within a small range. For example, the rate in Cambodia was 17.5%, while that in Thailand and Lao People’s Democratic Republic was 23.7 and 26.2% respectively. At the country level, the highest prevalence of strongyloidiasis was reported from Dominica, Colombia, Argentina, Bangladesh, Ecuador, and Ivory Coast [12]. The low rates reported from certain countries does not mean the absence of the infection. It could be due to lack of screening or diagnostic services particularly in countries with fragile health system and limited resources.

The main predisposing factors for S. stercoralis infection are immunosuppressive therapy, human immunodeficiency virus infection (HIV), corticosteroids, HTLV-1-co-infection, malignancies, and organ transplantation [13, 14]. Strongyloidiasis manifests in a wide range of symptoms including dermatological, respiratory (Löffler's syndrome), and digestive complaints. In hyperinfection syndrome and disseminated strongyloidiasis, symptoms may appear in several organs, including the central nervous system [1, 3, 12, 15]. In immunocompetent individuals, most infections with S. stercoralis are asymptomatic [16].

Bibliometric analysis, a well-established research method in information science, has been commonly used to shed light on research activity through quantitative description of literature in a particular disease or group of diseases [17,18,19,20]. Several bibliometric studies have been published on NTDs [21,22,23]. However, up to the author’s best knowledge, none was carried out on strongyloidiasis. Therefore, the current study aimed to assess the global research output on human strongyloidiasis published in peer-reviewed journals. The ultimate goals of the current study were to fill the knowledge gap regarding (1) quantitative analysis of national and international publications on strongyloidiasis; (2) and to compare the number of publications obtained with those for other NTDs such as leishmaniasis, Chagas disease, and Buruli ulcers.

Method

In the current study, bibliometric methodology was implemented using SciVerse Scopus database for the study period from 1968 to 2017. Scopus was used due to the advantages it has over other available databases [24]. For example, Scopus has more than 23,000 indexed journals. This is larger than the number of indexed journals in Web of Science and 100% inclusive of journals in Medline. Furthermore, Scopus has many functions that facilitate bibliometric analysis and that is why most bibliometric studies were carried out using Scopus database [25,26,27,28,29]. The study period was set to represent half a century of research. This study period has witnessed advancement in microbiological and parasitological fields. Furthermore, in the past 50 years migration from various world regions to the modern world was most evident [30].

Search strategy

The search strategy was based on the use of keywords relevant to S. stercoralis (Additional file 1). Examples of keywords used in the search strategy included “S* stercoralis” or “S* f*lleborni” or strongyloid* or “larva currens”. These keywords were used in the title search. Other lesser specific keywords were used in the title search but were followed with certain constraints. Examples of less specific keywords include “Hyperinf* Syndrome” or “soil-transmitted helminthiasis” followed by the presence of the keyword “strongyloid*” in the abstract of the same document. The keyword “disseminated” was not included in the search strategy because other keywords such as strongyloid* and hyperinf* will retrieve the documents about disseminated strongyloidiasis. The quotation marks were used in the search strategy to limit the search to the exact word or phrase while the asterisks were used as a wildcard. An exclusion step was used in the search strategy to eliminate false-positive results. Examples of excluded keywords include seals, dogs, horse, cat, cow, sheep, goat, or camel. This step was implemented to restrict the search to human strongyloidiasis. The current study was not limited to any language. However, only documents published in peer-reviewed journals were analyzed. Therefore, books and book chapters were excluded. The overall search strategy was developed by the author depending on systematic reviews and review articles which included the most common keywords used in the current study. A scheme showing the number of retrieved documents for each step in the search strategy was shown in the supplementary files (Additional file 2).

Validation of the search strategy

The validation of the search strategy was carried out using the same approach adopted in previously published bibliometric studies [31]. Such approach depended on the absence of false-positive results in the top 200 cited documents. The approach also depended on the absence of false-negative (missing entries) results by comparing the number of documents obtained for certain active authors with those provided by manual search using the author’s name in Scopus database. Agreement in the numbers, tested by interclass correlation coefficient using Statistical Package for Social Sciences (SPSS) [32,33,34,35,36] was used as a validity check for the absence of false-negative results.

Bibliometric indicators

The analysis included determining the volume and growth of retrieved literature, most active countries, institutions, journals, and authors being involved in publishing the retrieved documents. In Scopus, an article with all authors having the same country affiliation, is counted once for that country. However, if an article has different authors with different country affiliations, then the article is counted once for each country affiliation. Therefore, if we add up the number of publications for each country, the total might exceed the number of retrieved documents because a single article might be counted twice based on author country affiliation on that article. The same applies to counting institutions. Wherever the affiliation of an institution is mentioned in the affiliation of any article, then it was counted once for that institution. Citation analysis was used to show the mean number of citations per document as an index of readership and interest in the retrieved literature. The commonly used Hirsch index (h-index) was also used to assess the scientific impact of the retrieved literature [37]. The number of publications produced by each country was standardized by gross domestic product (GDP) per capita obtained from World Bank [38].

Data visualization

The retrieved data were also analyzed and presented as visualization maps using the free on-line program, VOSviewer [39, 40]. Visualization maps were used to show most frequent keywords in the retrieved documents. The frequency of occurrence of a particular word was directly proportional to the node size presenting the keyword in the map [39, 40]. Visualization maps were also used to shed light on the extent of international collaboration. The VOSviewer calculates the strength of collaboration between any two countries based on the thickness of connecting line and the number of publications. The link strength is given by the program and is not calculated by the author. The higher the link strength, the stronger the collaboration between two countries in terms of the number of co-authored publications relative to other countries.

Results

In the current study, the interclass Pearson correlation coefficient (r) between number of documents for active author retrieved by the two methods mentioned in the methodology section was 0.96% and the p-value was 0.002 indicative of a high degree of validity of search strategy.

Volume and growth of publications

In total, 1947 documents were obtained. The first peer-reviewed document appeared in 1908 in Southern Medical Journal and was about three cases of S. stercoralis in Tennessee, USA [41]. The total number of documents published from 1908 until 1967 was 70 documents (data not shown) and that is why the time of the study was set from 1968. The annual number of publications showed many fluctuations from the early 1970s up to 2017 and never exceeded 100 documents per year except in 2017 (Fig. 1).

Fig. 1
figure1

Growth of publications on human strongyloidiasis from 1968 to 2017

Ten most cited documents

The retrieved documents received 32,382 citations, an average of approximately 16.6 citations per document. The h-index of the retrieved documents was 76. The top ten cited documents [9, 42,43,44,45,46,47,48,49,50] were shown in Table 1. The most cited document was a review article about “Strongyloides stercoralis in the Immunocompromised Population“published in Clinical Microbiology Review in 2004 [46]. However, when the number of citations was standardized by time, an article published in PLoS Medicine received the highest number of citations per year [51] followed by an article published in PLoS Neglected Tropical Diseases [12]. The list of highly cited documents included eight review articles and two research articles; one was a clinical trial on the efficacy of ivermectin [42] while the second one was about the multiple stool sampling as a diagnostic approach to detect S. sterocralis [52]. The content of the top 10 cited articles was also evident when mapping most frequent author keywords (Fig. 2).

Table 1 Ten most cited articles in human strongyloidiasis
Fig. 2
figure2

Visualization of most frequent author keywords (minimum occurrences of 20 times)

Most active countries

Retrieved data indicated that the USA led with 540 (27.7%) documents. When data was standardized by income and population size, India ranked first followed by Brazil. Top ten active countries were listed in Table 2. Regarding citations, documents produced by researchers from Switzerland received the highest number of citations per document (50.2) while those from India received the lowest citations per document (6.3).

Table 2 Most active countries in research about human strongyloidiasis

International research collaboration

Countries with a minimum research output of 20 documents and had research collaboration with other countries were mapped (Fig. 3). The collaboration map showed four clusters of countries. In the collaboration map, all connecting lines were relatively thin indicative of the absence of strong research collaboration among active countries. However, the strongest research collaboration was between the USA and countries in Latin America, particularly Peru (link strength = 14), Brazil (link strength = 10), and Argentina (link strength = 10).

Fig. 3
figure3

Research collaboration among countries with minimum research output of 20 documents in human strongyloidiasis (1968–2017)

Ten most active institutions, journals, and authors

The ten most active institutions were shown in Table 3. The University of Ryukus (Japan) led with 62 (3.2%) documents. The University of Pennsylvania (54; 2.8%) ranked second while the National Institutes of Health (Bethesda, USA) ranked third with (46; 2.4%). The list also included active institutions in Switzerland, Brazil, Peru, and Thailand.

Table 3 Ten most active institutions in human strongyloidiasis

The ten most active journals were shown in Table 4. The American Journal of Tropical Medicine and Hygiene led with 93 (4.8%) documents followed by Transactions of The Royal Society of Tropical Medicine and Hygiene (53; 2.7%) and Plos Neglected Tropical Diseases (41; 2.1%). The list of active journals included ones affiliated with the USA, UK, Thailand, the Netherlands, and Poland. The most active journals were mainly in the field of parasitology or tropical medicine.

Table 4 Ten most active journals in publishing documents on human strongyloidiasis

Analysis of the retrieved documents showed that 7178 author names were involved in publishing the retrieved documents, giving a mean of 3.6 authors per document taking into consideration that there were 1656 (82.8%) documents as research articles and the remaining 343 (17.2%) documents were as letters, reviews, notes, editorials, conference papers, and short surveys. The list of most active authors (Table 5) included six from the USA, one from Brazil, two from Italy, and one from Japan.

Table 5 Ten most active authors in human strongyloidiasis

Research themes of the retrieved documents

The main research themes in the retrieved documents were investigated by visualizing terms used by authors in titles and abstracts with a minimum occurrence of 20 times. The map showed that the most frequent terms in titles/abstracts created four clusters (Fig. 4). The first cluster (red) focused on immunosuppression and corticosteroids (512 documents) as risk factors for hyperinfection and disseminated strongyloidiasis. The second cluster (green) was mainly about epidemiology/prevalence (241 documents) of the disease. The third cluster (blue) focused mainly on treatment using ivermectin and other medications (546 documents). The fourth cluster (light green) focused on diagnosis and new techniques such as PCR and ELISA (347 documents).

Fig. 4
figure4

Visualization map of most frequent terms in titles/abstracts of the retrieved documents

Discussion

The current study aimed to assess global research output on human strongyloidiasis hoping to (1) attract the attention of researchers and health policy makers to this NTD, (2) add information to the existing literature on strongyloidiasis, and (3) give credit to key players in strongyloidiasis research.

Volume of the retrieved literature

The current study indicated that the volume of the retrieved literature was relatively low given that 30–100 million individuals or more might be infected with S. stercoralis and given the number of publications on other neglected tropical diseases [1, 53, 54]. For example, a bibliometric study on leishmaniasis using Scopus for the study period from 1998 to 2017 yielded 17,570 publications [55]. Another study on dengue found that the number of publications reached 1000 publications in one year [56]. A third study showed that contribution of countries in Latin America to Chagas diseases was approximately 3000 articles [57]. There are several reasons behind the relatively low volume of literature on strongyloidiasis compared to other NTDs. The number of experts and those specifically interested in S. stercoralis maybe limited. Even if the number of experts and researchers in this field were high, the limited international research collaboration might have played a negative role in global research output [58, 59]. Research networking and collaboration is an essential aspect to make scientific progress, particularly in the biomedical field. This was evident in the co-authorship as well as the multidisciplinary nature of recent science [60, 61]. Establishing research networks increases research output, creates new research opportunities, facilitates technology transfer, increase citations of research manuscripts, especially if there is an international team of authors involved [62,63,64,65]. Building research networks is extremely important for developing countries where research community is fragmented and research grants are scarce [62]. The finding that the h-index of the retrieved literature on strongyloidiasis was 76 which is relatively lower than that reported for dengue [66] and leishmaniasis [55].

The wrong belief that strongyloidiasis does not pose a global health threat might also have played a negative role in this regard [67]. Research interest in emerging serious infections such as Zika and Ebola and other endemic infections such as malaria and tuberculosis might have overshadowed research in infections such as soil-transmitted helminthiasis (STH) [68].

Annual growth of publications

The current study also showed that more than half of the retrieved documents were published in the past two decades. Opportunistic infections in certain categories of people such as patients with hematological malignancies, transplant recipients, and patients on corticosteroids or other immunosuppressive drugs [69,70,71,72] positively affected the growth of publications in this field in the past two decades. The advancement in techniques implemented in the diagnosis and detection of S. stercoralis was also an indirect potential reason behind the increasing number of publications seen in the past two decades [73,74,75]. Several international programs such as the World Health Organization’s Global NTD Programs, the Centers for Disease Control and Prevention’s Global NTD Program, the United States Global Health Initiative, the United States Agency for International Development’s NTD Program, and others were implemented to focus on NTDs, and fighting to control or eliminate them [76,77,78]. It is hoped that these programs will stimulate researchers and increase the volume and growth of publications in strongyloidiasis and other NTDs. The starting of several peer-reviewed journals in the field of neglected diseases as well as diseases of poverty helped in the growth and visibility of strongyloidiasis research in recent years. Examples of such journals include PLOS Neglected Tropical Diseases and Infectious Diseases of Poverty. Furthermore, the emergence of ivermectin as an effective drug of choice for acute and chronic strongyloidiasis in intestinal stages, hyperinfection syndrome, and disseminated strongyloidiasis positively affected the number of publications in the past two decades [42].

The movement of large numbers of migrants from low- to high-income countries [79] and the presence of large numbers of patients with an immune problem who are at high risk of strongyloidiasis changed the attitude of developed countries toward this infection and positively affected the growth of publications in this field [15, 80].

Highly cited documents

The current study showed that highly cited documents in strongyloidiasis focused on hyperinfection syndrome, prevalence, diagnosis, and treatment. The fatal consequences of disseminated strongyloidiasis and hyperinfection syndrome were the main reason behind the increasing emphasis on strongyloidiasis literature. Detailed data on the epidemiology of S. stercoralis are also needed and constitute a real challenge to international health bodies [1]. Such epidemiological data are needed not only in endemic areas but also in developed countries in Europe and Northern America. It is strongly believed that human strongyloidiasis is underdiagnosed because many cases are asymptomatic and the available diagnostic methods lack sensitivity [1]. For example, in many developed countries, immigrants and refugees particularly those migrating from tropical and subtropical countries need to be screened for strongyloidiasis [81,82,83]. Furthermore, the large numbers of people with HIV/AIDS, HLTV-1, and people on immunosuppressants due to organ transplant requires more accurate and detailed screening [84,85,86,87,88,89,90,91]. The number of positive cases, and consequently the number of publications, could be partly due to implementing serological and molecular methods in immune-compromised patients or high-risk groups [75].

Most active countries

The current study indicated that the USA led in terms of number of publications, number of active institutions, journals, and authors. Several reasons could be cited for this leadership. First, the relatively high number of researchers, academic and research institutions, technology and funding. Second, strongyloidiasis have been detected in the USA in certain rural areas of the southeastern states and the Appalachian region [17]. Third, the large numbers of Asian and Latino migrants and refugees in the USA [79] increased the interest of USA researchers in this infection. Fourth, the presence of immunocompromised people in the USA and the high risk of this category to develop hyperinfection syndrome increased the interest of USA researchers in this disease. The list of active countries also included several European countries and Australia. The argument made about the role of USA in research in human strongyloidiasis applies to active European countries and Australia. The list of active countries included one country in Latin America, Brazil. A systematic review of the prevalence of strongyloidiasis in Latin America reported that high rates of strongyloidiasis are present in Argentina, Ecuador, Venezuela, Peru and Brazil [92]. The authors of the systematic review concluded that for most studied countries it was not possible to define reliable prevalence data because of paucity and/or inadequacy of studies and the need for specific diagnostic methods for detection of S. stercoralis [92]. The list of active countries included Japan and India. The most active institution was also based in Japan. A recent study that reviewed studies of the last 20 years on S. stercoralis’s global prevalence found that in South-East Asia and the Western Pacific region, 40 investigations were conducted in Thailand, 15 in Australia, 14 in Japan, and 14 in India [12]. In Japan, studies have shown that S. stercoralis was only endemic in Okinawa prefecture mostly due to high prevalence of HTLV-1 infections [93, 94].

Limitations

The current study has a few limitations that are inherent to bibliometric methodology. Scopus is not inclusive of all parasitology and infectious-related journals, particularly those published from developing countries in Southeast Asia, Latin America, Eastern Europe, and Africa. Most countries with a high prevalence of the infection have lesser number of indexed journals than high-income countries where prevalence is supposed to be low or absent. Furthermore, the number of non-English journals indexed in Scopus is relatively low which creates a bias toward countries publishing English journals. The search strategy implemented in the current study was meant to be comprehensive and valid. However, the presence of false-positive or false-negative documents remains a possibility because search strategy showed more than 95% validity (agreement) and not 100% agreement between results for active authors and results obtained by searching authors individually. Finally, the method of counting documents by Scopus allows the same document to be counted several times if authors have different country affiliations. The same applies when counting the number of documents for authors and institutions. This means that there is an overlap in the results pertaining to top ten active countries, authors and institutions. Therefore, the results might have overestimated the real research productivity of certain countries, authors, or institutions.

Conclusion

The current study showed that the volume and growth of literature in strongyloidiasis were relatively poor given the large number of affected people worldwide. The current study also showed limited international research collaboration in this field. Certain world regions in Africa, the Middle East, and Eastern Europe showed a negligible contribution to this field. To support and strengthen the fight against NTDs including strongyloidiasis and to implement the paradigm of universal health coverage (SDG target 3.8), international bodies need to stimulate researchers to conduct research activities in all aspects of NTDs [54]. The current study supplies the World Health Organization and other national and international health bodies with data needed to plan future activities that will help eliminate this neglected infection. Furthermore, the findings of the current study help create a forum that brings together all those interested in the subject to unify efforts and recruit funding needed to win the fight against strongyloidiasis.

Availability of data and materials

Data pertaining to this study could be retrieved using Scopus and the search strategy is outlined in Additional file 1.

Abbreviations

NTDs:

Neglected tropical diseases

STH:

Soil-transmitted helminthiasis

References

  1. 1.

    Intestinal worms (Strongyloidiasis, Key Facts) [http://www.who.int/intestinal_worms/epidemiology/strongyloidiasis/en/].

  2. 2.

    Ashford R. Strongyloides fuelleborni and similar parasites in animals and man. Strongyloidiasis Major Roundworm Infect Man. 1989:271–86.

  3. 3.

    World Health Organization. Neglected tropical diseases. [http://www.who.int/neglected_diseases/diseases/en/].

  4. 4.

    Beknazarova M, Whiley H, Ross K. Strongyloidiasis: A disease of socioeconomic disadvantage. Int J Environ Res Public Health. 2016;13(5).

  5. 5.

    Nutman TB. Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitol. 2017;144(3):263–73.

    Article  Google Scholar 

  6. 6.

    Cox FE. History of human parasitology. Clin Microbiol Rev. 2002;15(4):595–612.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Mitra AK, Mawson AR. Neglected tropical diseases: epidemiology and global burden. Trop Med Infect Dis. 2017;2(3):36.

    PubMed Central  Article  PubMed  Google Scholar 

  8. 8.

    Kappagoda S, Ioannidis JP. Prevention and control of neglected tropical diseases: overview of randomized trials, systematic reviews and meta-analyses. Bull World Health Organ. 2014;92(5):356–366C.

    PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Genta RM. Global prevalence of strongyloidiasis: critical review with epidemiologic insights into the prevention of disseminated disease. Rev Infect Dis. 1989;11(5):755–67.

    CAS  PubMed  Article  Google Scholar 

  10. 10.

    Puthiyakunnon S, Boddu S, Li Y, Zhou X, Wang C, Li J, Chen X. Strongyloidiasis--an insight into its global prevalence and management. PLoS Negl Trop Dis. 2014;8(8):e3018.

    PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Centers for Disease Control and Prevention. Parasites, Strongyloidiosis. [https://www.cdc.gov/parasites/strongyloides/epi.html].

  12. 12.

    Schar F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, Vounatsou P, Odermatt P. Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis. 2013;7(7):e2288.

    PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Schar F, Giardina F, Khieu V, Muth S, Vounatsou P, Marti H, Odermatt P. Occurrence of and risk factors for Strongyloides stercoralis infection in South-East Asia. Acta Trop. 2016;159:227–38.

    PubMed  Article  Google Scholar 

  14. 14.

    Terefe Y, Ross K, Whiley H. Strongyloidiasis in Ethiopia: systematic review on risk factors, diagnosis, prevalence and clinical outcomes. Infectious Diseases of Poverty. 2019;8(1):53.

  15. 15.

    Montes M, Sawhney C, Barros N. Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis. 2010;23(5):500–4.

    PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Schär F, Odermatt P, Khieu V, Panning M, Duong S, Muth S, Marti H, Kramme S. Evaluation of real-time PCR for Strongyloides stercoralis and hookworm as diagnostic tool in asymptomatic schoolchildren in Cambodia. Acta Trop. 2013;126(2):89–92.

    PubMed  Article  CAS  Google Scholar 

  17. 17.

    Sweileh WM. Global research trends of World Health Organization's top eight emerging pathogens. Glob Health. 2017;13(1):9.

    Article  Google Scholar 

  18. 18.

    Sweileh WM, Sawalha AF, Al-Jabi S, Zyoud SH. Bibliometric analysis of literature on antifungal triazole resistance: 1980–2015. GERMS. 2017;7(1):19–27.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    Sweileh WM, AbuTaha AS, Sawalha AF, Al-Khalil S, Al-Jabi SW, Zyoud SH. Bibliometric analysis of worldwide publications on multi-, extensively, and totally drug - resistant tuberculosis (2006-2015). Multidisciplinary Respir Med. 2016;11:45.

    Article  Google Scholar 

  20. 20.

    Sweileh WM, Sawalha AF, Al-Jabi SW, Zyoud SH, Shraim NY, Abu-Taha AS. A bibliometric analysis of literature on malaria vector resistance: (1996 - 2015). Glob Health. 2016;12(1):76.

    Article  Google Scholar 

  21. 21.

    Bai J, Li W, Huang YM, Guo Y. Bibliometric study of research and development for neglected diseases in the BRICS. Infect Dis Poverty. 2016;5(1):89.

    PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Poulin R. Qualitative and quantitative aspects of recent research on helminth parasites. J Helminthol. 2002;76(4):373–6.

    PubMed  Article  Google Scholar 

  23. 23.

    Ram S. A bibliometric profile of lymphatic filariasis research in India. J Vector Borne Dis. 2015;52(1):73–8.

    PubMed  Google Scholar 

  24. 24.

    Falagas ME, Pitsouni EI, Malietzis GA, Pappas G. Comparison of PubMed, Scopus, web of science, and Google scholar: strengths and weaknesses. FASEB J. 2008;22(2):338–42.

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Sweileh WM. A bibliometric analysis of global research output on health and human rights (1900-2017). Glob Health Res Policy. 2018;3:30.

    PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Sweileh WM. Bibliometric analysis of literature in AIDS-related stigma and discrimination. Transl Behav Med. 2018.

  27. 27.

    Sweileh WM. Global output of research on the health of international migrant workers from 2000 to 2017. Glob Health. 2018;14(1):105.

    Article  Google Scholar 

  28. 28.

    Sweileh WM. Global research output on HIV/AIDS-related medication adherence from 1980 to 2017. BMC Health Serv Res. 2018;18(1):765.

    PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Sweileh WM. Research trends on human trafficking: a bibliometric analysis using Scopus database. Glob Health. 2018;14(1):106.

    Article  Google Scholar 

  30. 30.

    Nations U. International migration report 2017-highlights: UN; 2018.

    Google Scholar 

  31. 31.

    Sweileh WM. Bibliometric analysis of peer-reviewed literature in transgender health (1900 - 2017). BMC Int Health Hum Rights. 2018;18(1):16.

    PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    Gearing RE, Mian IA, Barber J, Ickowicz A. A methodology for conducting retrospective chart review research in child and adolescent psychiatry. J Cana Acad Child Adolesc Psychiatry. 2006;15(3):126–34.

    Google Scholar 

  33. 33.

    Kimberlin CL, Winterstein AG. Validity and reliability of measurement instruments used in research. Am J Health Syst Pharm. 2008;65(23):2276–84.

    PubMed  Article  PubMed Central  Google Scholar 

  34. 34.

    Banks NJ. Designing medical record abstraction forms. Int J Qual Health Care. 1998;10(2):163–7.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. 35.

    Allison JJ, Wall TC, Spettell CM, Calhoun J, Fargason CA Jr, Kobylinski RW, Farmer R, Kiefe C. The art and science of chart review. Jt Comm J Qual Improv. 2000;26(3):115–36.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Hallgren K. Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol. 2003;8(1):23–34.

    Article  Google Scholar 

  37. 37.

    Ellegaard O, Wallin JA. The bibliometric analysis of scholarly production: how great is the impact? Scientometrics. 2015;105(3):1809–31.

    PubMed  PubMed Central  Article  Google Scholar 

  38. 38.

    The World Bank Data. GDP Per Capita. [https://data.worldbank.org/].

  39. 39.

    VOSviewer. Text mining and visualization using VOSviewer. [https://arxiv.org/abs/1109.2058].

  40. 40.

    Manual for VOSviewer version 1 .6.8. Leiden University. [http://www.vosviewer.com/documentation/Manual_VOSviewer_1.5.4.pdf].

  41. 41.

    Brush CE. Strongyloides Stercoralis, with report of three cases from Tennessee. South Med J. 1908;1(4):248–52.

    Article  Google Scholar 

  42. 42.

    Marti H, Haji HJ, Savioli L, Chwaya HM, Mgeni AF, Ameir JS, Hatz C. A comparative trial of a single-dose ivermectin versus three days of albendazole for treatment of Strongyloides stercoralis and other soil- transmitted helminth infections in children. Am J Trop Med Hyg. 1996;55(5):477–81.

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, Marti H, Utzinger J. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: Effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis. 2008:2(11).

    PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    Siddiqui AA, Berk SL. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis. 2001;33(7):1040–7.

    CAS  PubMed  Article  Google Scholar 

  45. 45.

    Scowden EB, Schaffner W, Stone WJ. Overwhelming strongyloidiasis: an unappreciated opportunistic infection. Med (United States). 1978;57(6):527–44.

    CAS  Google Scholar 

  46. 46.

    Keiser PB, Nutman TB. Strongyloides stercoralis in the Immunocompromised population. Clin Microbiol Rev. 2004;17(1):208–17.

    PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, Vounatsou P, Odermatt P. Strongyloides stercoralis: Global Distribution and Risk Factors. PLoS Negl Trop Dis. 2013:7(7).

    PubMed  PubMed Central  Article  Google Scholar 

  48. 48.

    Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo S, Verweij JJ, Magnussen P. Strongyloidiasis - the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg. 2009;103(10):967–72.

    PubMed  Article  Google Scholar 

  49. 49.

    Igra-Siegman Y, Kapila R, Sen P, Kaminski ZC, Louria DB. Syndrome of hyperinfection with Strongyloides stercoralis. Rev Infect Dis. 1981;3(3):397–407.

    CAS  PubMed  Article  Google Scholar 

  50. 50.

    Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, Sanitation, Hygiene, and Soil-Transmitted Helminth Infection: A Systematic Review and Meta-Analysis. PLoS Med. 2014;11(3).

    PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014;11(3):e1001620.

    PubMed  PubMed Central  Article  Google Scholar 

  52. 52.

    Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, Marti H, Utzinger J. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis. 2008;2(11):e331.

    PubMed  PubMed Central  Article  Google Scholar 

  53. 53.

    Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367(9521):1521–32.

    PubMed  Article  Google Scholar 

  54. 54.

    Bisoffi Z, Buonfrate D, Montresor A, Requena-Mendez A, Munoz J, Krolewiecki AJ, Gotuzzo E, Mena MA, Chiodini PL, Anselmi M, et al. Strongyloides stercoralis: a plea for action. PLoS Negl Trop Dis. 2013;7(5):e2214.

    PubMed  PubMed Central  Article  Google Scholar 

  55. 55.

    Al-Jabi SW. Arab world’s growing contribution to global leishmaniasis research (1998–2017): a bibliometric study. BMC Public Health. 2019;19(1):625.

    PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    Mota FB, Galina AC, RMd S. Mapping the dengue scientific landscape worldwide: a bibliometric and network analysis. Mem Inst Oswaldo Cruz. 2017;112(5):354–63.

    PubMed  PubMed Central  Article  Google Scholar 

  57. 57.

    Delgado-Osorio N, Vera-Polanía F, Lopez-Isaza A F, Martinez-Pulgarin D F, Murillo-Abadia J, Muñoz-Urbano M, Cardona-Ospina J A, Bello R, Lagos-Grisales G J, Villegas-Rojas S. Bibliometric assessment of the contributions of literature on Chagas disease in Latin America and the Caribbean. Recent Pat Antiinfect Drug Discov. 2014;9(3):202–8.

    CAS  PubMed  Article  Google Scholar 

  58. 58.

    He Z-L, Geng X-S, Campbell-Hunt C. Research collaboration and research output: a longitudinal study of 65 biomedical scientists in a New Zealand university. Res Policy. 2009;38(2):306–17.

    Article  Google Scholar 

  59. 59.

    Miramontes JR, González-Brambila CN. The effects of external collaboration on research output in engineering. Scientometrics. 2016;109(2):661–75.

    Article  Google Scholar 

  60. 60.

    Zerhouni E, Medicine. The NIH Roadmap. Sci (New York, NY). 2003;302(5642):63–72.

    CAS  Article  Google Scholar 

  61. 61.

    Rhoten D. The dawn of networked science. Chron High Educ. 2007;54(2):B12.

    Google Scholar 

  62. 62.

    Puljak L, Vari SG. Significance of research networking for enhancing collaboration and research productivity. Croat Med J. 2014;55(3):181–3.

    PubMed  PubMed Central  Article  Google Scholar 

  63. 63.

    Liu X, Jiang S, Chen H, Larson CA, Roco MC. Nanotechnology knowledge diffusion: Measuring the impact of the research networking and a strategy for improvement. J Nanopart Res. 2014;16(9).

  64. 64.

    Shaw IF. Research networking and collaboration: a case study. Qual Inq. 2018.

  65. 65.

    Protogerou A, Caloghirou Y, Siokas E. Research networking and technology fusion through EU-funded collaborative projects. Sci Public Policy. 2013;40(5):576–90.

    Article  Google Scholar 

  66. 66.

    Sa’ed HZ. Dengue research: a bibliometric analysis of worldwide and Arab publications during 1872–2015. Virol J. 2016;13(1):78.

    Article  Google Scholar 

  67. 67.

    Montes M, Sawhney C, Barros N. Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis. 2010;23(5):500.

    PubMed  PubMed Central  Article  Google Scholar 

  68. 68.

    Krolewiecki AJ, Lammie P, Jacobson J, Gabrielli AF, Levecke B, Socias E, Arias LM, Sosa N, Abraham D, Cimino R, et al. A public health response against Strongyloides stercoralis: time to look at soil-transmitted helminthiasis in full. PLoS Negl Trop Dis. 2013;7(5):e2165.

    PubMed  PubMed Central  Article  Google Scholar 

  69. 69.

    Gedle D, Kumera G, Eshete T, Ketema K, Adugna H, Feyera F. Intestinal parasitic infections and its association with undernutrition and CD4 T cell levels among HIV/AIDS patients on HAART in Butajira, Ethiopia. J Health Popul Nutr. 2017;36(1):15.

    PubMed  PubMed Central  Article  Google Scholar 

  70. 70.

    Mahmud MA, Bezabih AM, Gebru RB. Risk factors for intestinal parasitosis among antiretroviral-treated HIV/AIDS patients in Ethiopia. Int J STD AIDS. 2014;25(11):778–84.

    PubMed  Article  Google Scholar 

  71. 71.

    Mariam ZT, Abebe G, Mulu A. Opportunistic and other intestinal parasitic infections in AIDS patients, HIV seropositive healthy carriers and HIV seronegative individuals in Southwest Ethiopia. East Afr J Public Health. 2008;5(3):169–73.

    PubMed  Google Scholar 

  72. 72.

    Nkenfou CN, Nana CT, Payne VK. Intestinal parasitic infections in HIV infected and non-infected patients in a low HIV prevalence region, West-Cameroon. PloS One. 2013;8(2):e57914.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. 73.

    Taniuchi M, Verweij JJ, Noor Z, Sobuz SU, Lieshout L, Petri WA Jr, Haque R, Houpt ER. High throughput multiplex PCR and probe-based detection with Luminex beads for seven intestinal parasites. Am J Trop Med Hyg. 2011;84(2):332–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. 74.

    Kishimoto K, Hokama A, Hirata T, Ihama Y, Nakamoto M, Kinjo N, Kinjo F, Fujita J. Endoscopic and histopathological study on the duodenum of Strongyloides stercoralis hyperinfection. World J Gastroenterol. 2008;14(11):1768–73.

    PubMed  PubMed Central  Article  Google Scholar 

  75. 75.

    Krolewiecki AJ, Ramanathan R, Fink V, McAuliffe I, Cajal SP, Won K, Juarez M, Di Paolo A, Tapia L, Acosta N, et al. Improved diagnosis of Strongyloides stercoralis using recombinant antigen-based serologies in a community-wide study in northern Argentina. Clin Vaccin Immunol. 2010;17(10):1624–30.

    CAS  Article  Google Scholar 

  76. 76.

    Hotez P, Aksoy S. PLOS Neglected Tropical Diseases: Ten years of progress in neglected tropical disease control and elimination ... More or less. PLoS Negl Trop Dis. 2017;11(4):e0005355.

    PubMed  PubMed Central  Article  Google Scholar 

  77. 77.

    Njim T, Aminde LN. An appraisal of the neglected tropical diseases control program in Cameroon: the case of the national program against onchocerciasis. BMC Public Health. 2017;17(1):103.

    PubMed  PubMed Central  Article  Google Scholar 

  78. 78.

    Qian MB. Neglected tropical diseases and global burden of disease in China. Infect Dis Poverty. 2017;6(1):25.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. 79.

    International Migration Report 2017 [http://www.un.org/en/development/desa/population/migration/publications/migrationreport/docs/MigrationReport2017_Highlights.pdf].

  80. 80.

    Mazigo HD. Strongyloidiasis and schistosomiasis: lessons from migrants' data. Lancet Glob Health. 2019;7(2):e171–2.

    PubMed  Article  Google Scholar 

  81. 81.

    Lim S, Katz K, Krajden S, Fuksa M, Keystone JS, Kain KC. Complicated and fatal Strongyloides infection in Canadians: risk factors, diagnosis and management. CMAJ. 2004;171(5):479–84.

    PubMed  PubMed Central  Article  Google Scholar 

  82. 82.

    Nuesch R, Zimmerli L, Stockli R, Gyr N, Christoph Hatz FR. Imported strongyloidosis: a longitudinal analysis of 31 cases. J Travel Med. 2005;12(2):80–4.

    PubMed  Article  Google Scholar 

  83. 83.

    Dawson-Hahn EE, Greenberg SLM, Domachowske JB, Olson BG. Eosinophilia and the seroprevalence of schistosomiasis and strongyloidiasis in newly arrived pediatric refugees: an examination of Centers for Disease Control and Prevention screening guidelines. J Pediatr. 2010;156(6):1016–8 e1011.

    PubMed  Article  Google Scholar 

  84. 84.

    Stewart DM, Ramanathan R, Mahanty S, Fedorko DP, Janik JE, Morris JC. Disseminated Strongyloides stercoralis infection in HTLV-1-associated adult T-cell leukemia/lymphoma. Acta Haematol. 2011;126(2):63–7.

    PubMed  PubMed Central  Article  Google Scholar 

  85. 85.

    Evering T, Weiss LM. The immunology of parasite infections in immunocompromised hosts. Parasite Immunol. 2006;28(11):549–65.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Montero A, Mazzolini G, Rojas SP, Brarda G, Conde H, Munoz M. Hyperinfection by Strongyloides stercoralis as first manifestation of AIDS. Med. 1996;56(3):319–20.

    CAS  Google Scholar 

  87. 87.

    Sarangarajan R, Ranganathan A, Belmonte AH, Tchertkoff V. Strongyloides stercoralis infection in AIDS. AIDS Patient Care STDs. 1997;11(6):407–14.

    CAS  PubMed  Article  Google Scholar 

  88. 88.

    Satyanarayana S, Nema S, Kalghatgi AT, Mehta SR, Rai R, Duggal R, Bhardwaj JR. Disseminated Strongyloides stercoralis in AIDS: a report from India. Indian J Pathol Microbiol. 2005;48(4):472–4.

    PubMed  Google Scholar 

  89. 89.

    Sauca Subias G, Barrufet Barque P, Besa Beringues A, Rodriguez Ramos E. Strongyloides stercoralis hyperinfection in a patient with acquired immunodeficiency syndrome. An Med Interna. 2005;22(3):139–41.

    CAS  PubMed  Google Scholar 

  90. 90.

    Siegel MO, Simon GL. Is human immunodeficiency virus infection a risk factor for Strongyloides stercoralis hyperinfection and dissemination. PLoS Negl Trop Dis. 2012;6(7):e1581.

    PubMed  PubMed Central  Article  Google Scholar 

  91. 91.

    Trione N, Corti M, Castello T, Abuin JC, Bellegarde E. Disseminated infection due to strongyloides stercoralis in AIDS patients. A report of 2 cases. Acta Gastroenterol Latinoam. 2001;31(5):399–402.

    CAS  PubMed  Google Scholar 

  92. 92.

    Buonfrate D, Mena MA, Angheben A, Requena-Mendez A, Munoz J, Gobbi F, Albonico M, Gotuzzo E, Bisoffi Z, Group CPS. Prevalence of strongyloidiasis in Latin America: a systematic review of the literature. Epidemiol Infect. 2015;143(3):452–60.

    CAS  PubMed  Article  Google Scholar 

  93. 93.

    Arakaki T, Iwanaga M, Asato R, Ikeshiro T. Age-related prevalence of Strongyloides stercoralis infection in Okinawa, Japan. Trop Geogr Med. 1992;44(4):299–303.

    CAS  PubMed  Google Scholar 

  94. 94.

    Hayashi J, Kishihara Y, Yoshimura E, Furusyo N, Yamaji K, Kawakami Y, Murakami H, Kashiwagi S. Correlation between human T cell lymphotropic virus type-1 and Strongyloides stercoralis infections and serum immunoglobulin E responses in residents of Okinawa, Japan. Am J Trop Med Hyg. 1997;56(1):71–5.

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

The author would like to thank An-Najah National University for facilitating this study by providing the necessary software and technical support.

Funding

None.

Author information

Affiliations

Authors

Contributions

This was a single-authored publication. The author read and approved the final manuscript.

Corresponding author

Correspondence to Waleed M. Sweileh.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The author declares that he has no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sweileh, W.M. A bibliometric analysis of human strongyloidiasis research (1968 to 2017). Trop Dis Travel Med Vaccines 5, 24 (2019). https://doi.org/10.1186/s40794-019-0100-1

Download citation

Keywords

  • Human strongyloidiasis
  • Bibliometric analysis
  • Keyword mapping
  • Geographical distribution
  • Scopus