Skip to main content
Download PDF

Bibliometric analysis of global scientific research on carbapenem resistance (1986–2015)

Annals of Clinical Microbiology and Antimicrobials volume 15, Article number: 56 (2016) Cite this article

Abstract

Background

Antimicrobial resistance is a global public health challenge and carbapenem resistance, in particular, is considered an urgent global health threat. This study was carried out to give a bibliometric overview of literature on carbapenem resistance. In specific, number of publications, top productive countries and institutes, highly cited articles, citation analysis, co-authorships, international collaboration, top active authors, and journals publishing articles on carbapenem resistance were analyzed and discussed.

Methods

Specific keywords pertaining to carbapenem resistance were used in Scopus database. Quantitative and qualitative analysis of retrieved data were presented using appropriate bibliometric indicators and visualization maps.

Results

A total of 2617 journal articles were retrieved. The average number of citations per article was of 21.47. The growth of publications showed a dramatic increase from 2008 to 2015. Approximately 9 % of retrieved articles on carbapenem resistance were published in Antimicrobial Agents and Chemotherapy journal. Retrieved articles were published by 102 different countries. The United States of America (USA) contributed most with 437 (16.70 %) articles followed by China with 257 (9.82 %) articles. When productivity was stratified by population size, Greece ranked first followed by France. Greece also ranked first when data were stratified by gross domestic product (GDP). Asian countries have lesser international collaboration compared with other countries in the top ten list. Five of top ten productive institutes were Europeans (France, the UK, Greece, Italy, and Switzerland) and two were Asians (China and South Korea). Other active institutes included an Israeli and a Brazilian institute. Four of the top ten cited articles were published in Antimicrobial Agents and Chemotherapy journal and two were published in The Lancet Infectious Diseases.

Conclusion

There was a dramatic increase in number of publications on carbapenem resistance in the past few years. These publications were produced from different world regions including Asia, Europe, Middle East, and Latin America. International collaboration needs to be encouraged particularly for researchers in Asia. Molecular biology and epidemiology dominated the theme of the top ten cited articles on carbapenem resistance. This bibliometric study will hopefully help health policy makers in planning future research and allocating funds pertaining to carbapenem resistance.

Background

In 2014, the World Health Organization (WHO) issued a report on antimicrobial resistance (AMR) stating that AMR is becoming a global challenge that threatens the clinical benefit of many important antimicrobial agents [1]. Of a real concern in the WHO report was a warning about spread of resistance among different Gram-negative bacteria to carbapenems. This created a great deal of concern among clinicians, microbiologists and pharmacologists because carbapenems are considered antibiotics of last resort in combating serious infections [2]. Carbapenems are β-lactam antibiotics that were developed from thienamycin, which served as the parent model for other carbapenems including imipenem, ertapenem, doripenem and meropenem [3, 4]. Carbapenem resistance is a global public health challenge and efforts to minimize the spread of carbapenem resistance and risk of serious outbreaks is considered top priority [5, 6]. International health organizations, governments, healthcare providers, and researchers need to coordinate efforts and respond to this new global public health challenge by implementing programs to rationalize use of antibiotics [7–9]. As a baseline information, it is important to analyze research output published globally on carbapenem resistance. Such baseline data are needed in order to understand the current research situation and plan future research agenda accordingly.

An important and common method used to assess research activity on a certain topic is bibliometric analysis which is defined as the use of mathematical methods to analyze published articles in terms of quantity and quality [10, 11]. In bibliometric analysis, information regarding growth of publications, international collaboration, top active countries, institutes, and authors are presented. Moreover, journals publishing on the topic of interest are also presented. In some bibliometric studies, maps are presented as a method of visualization of bibliometric indicators. The retrieval of published articles on a certain topic is the first step in evaluation of literature regarding a certain problem or topic and in building evidence based clinical decisions. Retrieval of published articles on a certain topic can be achieved through the use of databases like PubMed, Google Scholar, Scopus, or Web of Science. In the past decade, a number of bibliometric studies on specific types of infections and on specific types of medical subjects like microbiology were published [12–14]. However, no bibliometric studies have been carried out on carbapenem resistance. Therefore, this study was carried out to analyze and present bibliometric indicators pertaining to literature on carbapenem resistance.

Methods

Data collection for this study was carried out using Scopus database. The methodology used was similar to that described in previously published bibliometric studies [15–21]. Keywords used for data extraction were obtained from published review articles on carbapenem resistance. Search query used for data extraction from Scopus looked like this:

(TITLE(“carbapenem resist*” OR “imipenem resist*” OR “meropenem resist*” OR “ertapenem resist*” OR “doripenem resist*” OR “carbapenemase produ*” OR “carbapenem non-susceptible” OR “carbapenem hdroly*ing”) AND PUBYEAR < 2016) OR ((TITLE-ABS-KEY(Ndm-1 OR “New Delhi metallo*” OR “carbapenemase” OR “extended-spectrum *lactamase*”) AND TITLE-ABS(“carbapenem resist*”)) OR ((TITLE (“coli” OR “enterobacter*” OR “aeruginosa” OR “baumannii” OR “klebsiella”)) AND KEY(“carbapenem resist*”)) AND PUBYEAR < 2016) AND (LIMIT-TO(SRCTYPE,”j”)) AND (EXCLUDE(DOCTYPE,”er”))

The asterisk was used for certain words to retrieve all potential correct words while the quotation marks were used to retrieve correct and exact phrases. Validity of the search query was confirmed by manual analysis of the top 100 cited articles. In this study, manual analysis of the top 100 cited articles showed no deviation from required goal of retrieving articles on carbapenem resistance. The time span for data collection was all previous years until 2015. Retrieved documents were refined and limited to journal articles. Errata and undefined documents were excluded. Bibliometric indicators were presented as top ten productive countries, institutes, authors, journals, and highly cited articles. For evaluation of quality of publications, h-index, average number of citations per article, and total number of citations were used [13, 22–25]. For quality of journals publishing articles on carbapenem resistance, impact factor (IF) and scientific journal rankings (SJR) were presented for each journal. Impact factors for journals were obtained from the latest Journal Citation Report published by Thompson Reuters [26] while SJR for journals were obtained from Scimago Journal Rank [27]. Poisson loglinear regression was carried out using the annual worldwide productivity as a dependent variable. Predictor independent variables were used as covariates in the model. The covariates were: number of publications produced annually by top three countries, number of articles with the keyword “hospital”, and number of articles produced annually in the field of molecular biology/microbiology. Author co-citation analysis (ACA) was presented as density visualization map using VOSviewer techniques [28].

Results

A total of 2617 articles were retrieved. The average number of citations per article was 21.47. The h-index of retrieved articles was 102. Most retrieved documents were original articles (2126, 81.24 %) and most of these documents were written in English language (2355, 89.99 %). Chinese language ranked second with 120 (4.59 %) articles. Growth of publications on carbapenem resistance started in 1986 and remained at an average of ten articles per year until late 1990s. Growth of publications increased slowly from 2000 to 2008 followed by a dramatic rise in the number of publications (Fig. 1). The oldest articles on carbapenem resistance were published in 1986. These old articles discussed imipenem resistance in Pseudomonas aeruginosa and Bacteroides fragilis [29–31].

Fig. 1
figure1

Temporal distribution of production of publications about carbapenem resistance (1986–2015)

Full size image

There was a linear increase in number of publications with time. However, the number of citations per article per year showed an inverse linear relationship with time indicating that older articles were being continuously cited with time (Fig. 2).

Fig. 2
figure2

Growth of publications and citations for carbapenem resistance (1986–2015)

Full size image

Relevant terms to carbapenem resistance were analyzed for number of occurrences in article titles using VOSviewer technique. Analysis showed that “pneumoniae” was the most frequent term (305 occurrences) followed by “Acinetobacter baumannii” (302 occurrences), “Pseudomonas aeruginosa” (132 occurrences), “resistant Enterobacteriaceae” (124 occurrences), and “metallo β lactamase” (21 occurrences).

Core journals that published most on carbapenem resistance were shown in Table 1. A total of 1078 (41 %) articles on carbapenem resistance were published by top ten journals listed in Table 1. Approximately 9 % (n = 232) of retrieved articles on carbapenem resistance were published in Antimicrobial Agents and Chemotherapy journal (IF of 4.476). Journals in the top ten list were in the field of antimicrobials, microbiology, infection, and antimicrobial resistance. Furthermore, all journals in the top ten list were prestigious and influential ones. The journal with the highest IF was Journal of Antimicrobial Chemotherapy (IF = 5.313).

Table 1 Top ten journals publishing on carbapenem resistance (1986–2015)
Full size table

Retrieved articles were published by 102 different countries distributed in all world regions. However, 68.44 % (n = 1791) of retrieved articles were published by top ten ranking countries. The list of top ten productive countries included five countries in Europe, three in Asia, one in Northern America, and one in Latin America (Table 2). The United States of America (USA) had the greatest contribution with 437 (16.70 %) articles followed by China with 257 (9.82 %) articles. When productivity was stratified by population size, Greece ranked first followed by France. However, when productivity was stratified by gross domestic product (GDP), Greece ranked first followed by Spain. When quality of publications was assessed for each country by calculating the average number of citations per article, the United Kingdom (UK) ranked first followed by Greece and France. International collaboration, assessed by the number of articles with multiple country affiliations, showed that UK had the highest percentage of articles with international collaboration (82; 54.92 %) followed by France (117; 53.92 %) and Greece (40; 38.46 %). Top three countries (UK, France and Greece) engaged in international collaboration were the same top three countries which had the highest average number of citations per article.

Table 2 Top ten productive countries on carbapenem publications (1986–2015)
Full size table

Using Poisson loglinear regression, we examined variations of three factors on the annual number of publications on carbapenem resistance. The variables tested were (1) “hospital” as a keyword in the article; (2) subject area in the field of molecular biology/microbiology; and (3) annual productivity of top three countries. Variables were entered in Poisson regression model as continuous covariates. Table 3 shows that molecular biology/microbiology subject area (p < 0.01) and presence of article keyword “hospital” (p < 0.01) were significant predictors of worldwide research productivity on carbapenem resistance. The results indicated that the worldwide productivity will be 1.002 times greater for each extra article published in the field of molecular biology/microbiology. Similarly, the worldwide productivity will be 1.031 times greater for each extra article published with a keyword “hospital”. The annual productivity of the top three countries was not a significant predictor (p = 0.296) of worldwide research productivity on carbapenem resistance.

Table 3 Poisson loglinear regression model for predicting worldwide research productivity on carbapenem resistance
Full size table

Research and academic institutes involved in carbapenem resistance were presented as top ten productive institutes in Table 4. Five of top ten productive institutes were in Europe (France, Greece, UK, Italy and Switzerland) and two were in Asia (China and South Korea). Other active institutes were ones in the USA, Israel and Brazil. When ranked based on the number of published articles, Hopital de Bicetre in France ranked first followed by the University of Athens Medical School in Greece, Zhejiang University in China, VA medical center in the USA and Health Protection Agency in the UK. However, when top ten productive institutes were ranked based on quality of publications assessed by average number of citations per article, Health Protection Agency in the UK ranked first followed by Centers for Disease Prevention and Control (CDC) in the USA. At least three of top ten institutes were governmental health research institutes (VA Medical Center, CDC and Health Protection Agency).

Table 4 Top ten list of institutes publishing on carbapenem resistance (1896–2015)
Full size table

Active researchers in the field of carbapenem resistance are shown in Table 5 as top ten active authors. Professor Nordmann ranked first in number and quality of publications with 95 publications and h-index of 36. Professor Poirel ranked second in number of publications with 71 publications and h-index of 32 while Carmeli ranked third with 47 publications and h-index of 26. Both Nordman and Poirel are affiliated with the same institute (Inserm U914, Kremlin-Bicêtre, France and Département de médecine, Faculté des sciences, Université de Fribourg, Fribourg, Switzerland). Both professors have extensive research collaboration. Same applies to Professors Carmeli and Navon-Venezia who share the same affiliation and have a noticeable research collaboration. Six of top ten active authors on carbapenem resistance were in Europe, two in Israel, one in the USA and one in South Korea.

Table 5 Top ten authors publishing on carbapenem resistance (1986–2015)
Full size table

Author co-citation analysis (ACA) for top ten active authors was carried out using VOSviewer technique. The ultimate number of authors included was 28 based on a minimum number of 100 citations per author. The map produced included 28 authors distributed into three clusters (red, green, and blue) as shown in Fig. 3. Cluster number one included 13, cluster two included 11, and cluster three included four authors. Some of the authors might not be shown clearly in the map because some of the names were overlapping.

Fig. 3
figure3

Author co-citation analysis for carbapenem resistance publications (1986–2015). Minimum of 100 citations per author, 28 authors were included

Full size image

The following top active authors were present in cluster number one (red) and were commonly co-cited together: Woodford, Livermore, Tsakris and Lee. Cluster number two (green) included the following top active authors: Carmeli, Bonomo, and Navon-Venezia. Cluster number three (blue) included the following top active authors: Nordmann and Poirel.

In cluster number two (green), both Carmeli and Navon-Venezia are Israeli researchers, the former is in the field of molecular biology and the latter is in the field of preventive medicine. It is also noteworthy that both Nordman and Poirel (blue cluster) are affiliated with the same institute.

Top ten cited articles on carbapenem resistance were shown in Table 6 [32–41]. Four of the top ten cited articles were published in Antimicrobial Agents and Chemotherapy journal and two were published in The Lancet Infectious Diseases. The article that received the highest number of citations was “Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: A molecular, biological, and epidemiological study”. It was published in 2010 and received a total of 1212 citations. Carbapenem resistance in Klebsiella pneumoniae was mentioned in the title of five top cited articles. Professors Poirel and Nordmann had good contribution to top ten cited articles.

Table 6 Top ten cited articles on carbapenem resistance (1986–2015)
Full size table

Discussion

In this study, a bibliometric overview of worldwide publications on carbapenem resistance was presented. Extensive research review showed that few studies were published on bibliometrics of carbapenems. These studies were published in Chinese journals and in Chinese language. These Chinese studies were specific to a certain type of bacteria or specific to New-Delhi metallo β-lactamase gene responsible for carbapenem resistance [42–44]. Our study is the first bibliometric study published in English.

The steep rise in number of publications on carbapenem resistance reflects real concern of scientific and medical committees about this issue and reflects the fact that the problem is spreading across the world [37, 45–48]. The CDC considers Enterobacteriaceae carbapenem resistance as an urgent threat [49]. Despite the fact that carbapenem resistance is relatively a recent topic, the h-index of retrieved articles was 104 which indicates that carbapenem resistance is a very attractive and interesting topic to many readers in the scientific and clinical field. Furthermore, the fact that approximately 10 % of retrieved documents were written in non-English language is a proof of the clinical and research popularity of carbapenem resistance.

The core journals publishing articles on carbapenem resistance are well-known and prestigious ones in the field of microbiology and infection. The majority of core journals publishing on carbapenem resistance had an IF ≥4. It is also interesting to note that one of the core journals was in specific field of drug resistance. In fact, there are at least five international journals being specialized in antimicrobial resistance such as “Microbial Drug Resistance”, “Journal of Global Antimicrobial Resistance”, and “Infection and Drug Resistance”. The core journals were mainly those issued in the USA and the UK. This explains why the majority of retrieved articles on carbapenem resistance were written in English language. No doubt, that there was a tremendous effort of Chinese researchers to publish on carbapenem resistance. However, Chinese journals are still behind on the international arena.

Contribution of various countries to publications on carbapenem resistance showed that Asian countries (China, India and South Korea) had the lowest extent of international collaboration. This might explain the low number of citations per article published from these countries. A study showed that international collaboration increases the chances of citations [50, 51]. The result that Greece and France ranked top when results were stratified by GDP or population size was surprising. Greece had suffered serious outbreaks of infections that were resistant to carbapenems and that led to a series of publications on this topic [52, 53]. Similar situation happened in France [54–56].

List of top productive institutes included Tel Aviv Sourasky Medical Center (Israel) and Universite de Fribourg (Switzerland). However, neither Israel nor Switzerland were listed in the top ten productive countries. Several hospitals in Israel had suffered from serious outbreaks of infections resistant to carbapenems [57–59]. These outbreaks of infections that threatened many Israeli hospitals has led researchers in Israel to publish reports on carbapenem resistance. This also might explain why two of top ten active authors were affiliated with Israeli institutes.

Two articles in the top ten cited articles discussed the emergence of New Delhi metallo-β-lactamase (NDM) gene responsible for carbapenem resistance. This gene belongs to carbapenemase gene family and bacteria carrying this gene are referred to as superbugs because they are resistant to most antibiotics. The term “New Delhi” was given to the gene because the bacteria having this gene was initially isolated from a patient who was visiting India [41]. This gene made carbapenem resistance an alarming risk that could spread worldwide by travelers across different parts of the world [60]. The article that first characterized this gene became one of the top ten cited articles on carbapenem resistance field. Immediately after publication of this article, an epidemiological study with molecular and biological characterization of NDM-1 gene in Enterobacteriaceae in India, Pakistan, and the UK was published and soon became one of the top ten cited articles in the field.

Our study has the advantage of being the first to give a bibliometric overview on carbapenem resistance. We did our best to include all potential articles and to avoid false positive and false negative results. The validation method implemented by the external microbiologist did confirm accuracy of retrieved data. However, the search query itself might not be conclusive and some articles on carbapenem resistance might be missed. Furthermore, it seems that there are Chinese medical journals that not indexed in Scopus and therefore some of the Chinese articles on carbapenem resistance might be missed. Therefore, presentation of Chinese scientists in this filed might be lesser than the actual one. Some people may argue against the use of Scopus for data retrieval. However, Scopus is comprehensive, accurate, and suitable for bibliometric studies [61].

Conclusions

There was a dramatic increase in number of publications on carbapenem resistance in the last decade suggestive of serious spread of carbapenem resistance worldwide. Publications on carbapenem resistance originated from different world regions including Asia, Europe, and Latin America. The bulk of retrieved articles were published in microbiology and in journals related to infection control. These journals have high IF suggestive of clinical importance of this topic. International collaboration is important and need to be adopted by researchers in Asian countries to increase citations and readability. Molecular biology of genes responsible for carbapenem resistance and epidemiology of this problem dominated the top ten cited articles on this topic.

Abbreviations

AMR:

antimicrobial resistance

CDC:

Centers for Disease Control and Prevention

GDP:

gross domestic product

h-index:

The Hirsch Index

IF:

impact factor

NDM:

New Delhi metallo-β-lactamase

SCR:

standard competition ranking

SJR:

SCImago Journal Rank

UK:

United Kingdom

USA:

United States of America

WHO:

World health organization

References

  1. 1.

    World Health Organization. Antimicrobial resistance: global report on surveillance. 2014. http://apps.who.int/iris/bitstream/10665/112642/1/9789241564748_eng.pdf.

  2. 2.

    Nathan C, Cars O. Antibiotic resistance—problems, progress, and prospects. N Engl J Med. 2014;371(19):1761–3.

    PubMed  Article  Google Scholar 

  3. 3.

    Birnbaum J, Kahan FM, Kropp H, MacDonald JS. Carbapenems, a new class of β-lactam antibiotics. Discovery and development of imipenem/cilastatin. Am J Med. 1985;78(6A):3–21.

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Moellering RC Jr, Eliopoulos GM, Sentochnik DE. The carbapenems: new broad spectrum β-lactam antibiotics. J Antimicrob Chemother. 1989;24(Suppl A):1–7.

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA. Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother. 2007;51(10):3471–84.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Giamarellou H, Antoniadou A, Kanellakopoulou K. Acinetobacter baumannii: a universal threat to public health? Int J Antimicrob Agents. 2008;32(2):106–19.

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Carmeli Y, Akova M, Cornaglia G, Daikos GL, Garau J, Harbarth S, Rossolini GM, Souli M, Giamarellou H. Controlling the spread of carbapenemase-producing gram-negatives: therapeutic approach and infection control. Clin Microbiol Infect. 2010;16(2):102–11.

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, Vlieghe E, Hara GL, Gould IM, Goossens H, et al. Antibiotic resistance-the need for global solutions. Lancet Infect Dis. 2013;13(12):1057–98.

    PubMed  Article  Google Scholar 

  9. 9.

    Ganguly NK, Arora NK, Chandy SJ, Fairoze MN, Gill JP, Gupta U, Hossain S, Joglekar S, Joshi PC, Kakkar M, et al. Rationalizing antibiotic use to limit antibiotic resistance in India. Indian J Med Res. 2011;134:281–94.

    PubMed  Google Scholar 

  10. 10.

    Broadus R. Toward a definition of “bibliometrics”. Scientometrics. 1987;12(5–6):373–9.

    Article  Google Scholar 

  11. 11.

    Okubo Y. Bibliometric indicators and analysis of research systems: methods and examples. Paris: OCDE; 1997.

    Book  Google Scholar 

  12. 12.

    Macías-Chapula CA, Mijangos-Nolasco A. Bibliometric analysis of AIDS literature in Central Africa. Scientometrics. 2002;54(2):309–17.

    Article  Google Scholar 

  13. 13.

    Sweileh WM, Al-Jabi SW, Abuzanat A, Sawalha AF, AbuTaha AS, Ghanim MA, Zyoud SH. Assessment of research productivity of Arab countries in the field of infectious diseases using Web of Science database. Infect Dis Poverty. 2015;4(1):2.

    PubMed  PubMed Central  Article  Google Scholar 

  14. 14.

    Ramos JM, Padilla S, Masia M, Gutierrez F. A bibliometric analysis of tuberculosis research indexed in PubMed, 1997–2006. Int J Tuberc Lung Dis. 2008;12(12):1461–8.

    CAS  PubMed  Google Scholar 

  15. 15.

    Sweileh WM, Al-Jabi SW, Zyoud SH, Sawalha AF. Bronchial asthma and chronic obstructive pulmonary disease: research activity in Arab countries. Multidiscip Respir Med. 2014;9(1):38.

    PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Zyoud SH, Al-Jabi SW, Sweileh WM, Awang R. Contribution of Arab countries to pharmaceutical wastewater literature: a bibliometric and comparative analysis of research output. Ann Occup Environ Med. 2016;28:28.

    PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

    Zyoud SH, Waring WS, Al-Jabi SW, Sweileh WM, Rahhal B, Awang R. Intravenous lipid emulsion as an antidote for the treatment of acute poisoning: a bibliometric analysis of human and animal studies. Basic Clin Pharmacol Toxicol. 2016. doi:10.1111/bcpt.12609.

    PubMed  Google Scholar 

  18. 18.

    Zyoud SH. Global research trends of Middle East respiratory syndrome coronavirus: a bibliometric analysis. BMC Infect Dis. 2016;16(1):255.

    PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

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

    PubMed  PubMed Central  Article  Google Scholar 

  20. 20.

    Zyoud SH, Al-Jabi SW, Sweileh WM, Al-Khalil S, Alqub M, Awang R. Global methaemoglobinaemia research output (1940–2013): a bibliometric analysis. Springerplus. 2015;4:626.

    PubMed  PubMed Central  Article  Google Scholar 

  21. 21.

    Zyoud SH, Al-Jabi SW, Sweileh WM, Awang R, Waring WS. Bibliometric profile of the global scientific research on methanol poisoning (1902–2012). J Occup Med Toxicol. 2015;10:17.

    PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Sweileh WM, Al-Jabi SW, Sawalha AF, Zyoud SH. Bibliometric analysis of nutrition and dietetics research activity in Arab countries using ISI Web of Science database. Springerplus. 2014;3:718.

    PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Sweileh WM, Al-Jabi SW, Shanti YI, Sawalha AF, Zyoud SH. Contribution of Arab researchers to ophthalmology: a bibliometric and comparative analysis. Springerplus. 2015;4:42.

    PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Sweileh WM, Zyoud SH, Al-Jabi SW, Sawalha AF. Contribution of Arab countries to breast cancer research: comparison with non-Arab Middle Eastern countries. BMC Womens Health. 2015;15:25.

    PubMed  PubMed Central  Article  Google Scholar 

  25. 25.

    Sweileh WM, Zyoud SH, Al-Jabi SW, Sawalha AF. Public, environmental, and occupational health research activity in Arab countries: bibliometric, citation, and collaboration analysis. Arch Public Health. 2015;73(1):1.

    PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Reuters T. Journal citation reports. 2015. https://jcr.incites.thomsonreuters.com/.

  27. 27.

    SCImago. Scimago journal and country rank. 2015. http://www.scimagojr.com/journalrank.php.

  28. 28.

    van Eck NJ, Waltman L. Software survey: VOSviewer, a computer program for bibliometric mapping. Scientometrics. 2010;84(2):523–38.

    PubMed  Article  Google Scholar 

  29. 29.

    Bauernfeind A, Hörl G. Imipenem resistance in Pseudomonas aeruginosa. Immun Infekt. 1986;14(6):221–4.

    CAS  PubMed  Google Scholar 

  30. 30.

    Cuchural GJ Jr, Malamy MH, Tally FP. β-Lactamase-mediated imipenem resistance in Bacteroides fragilis. Antimicrob Agents Chemother. 1986;30(5):645–8.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Cullmann W, Büscher KH, Opferkuch W. Characterization of imipenem resistance in Pseudomonas aeruginosa: decreased phenotypic expression of outer membrane proteins D1 and D2. Immun Infekt. 1986;14(6):227–9.

    CAS  PubMed  Google Scholar 

  32. 32.

    Bradford PA, Urban C, Mariano N, Projan SJ, Rahal JJ, Bush K. Imipenem resistance in Klebsiella pneumoniae is associated with the combination of ACT-1, a plasmid-mediated AmpC β-lactamase, and the foss of an outer membrane protein. Antimicrob Agents Chemother. 1997;41(3):563–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Bratu S, Landman D, Haag R, Recco R, Eramo A, Alam M, Quale J. Rapid spread of carbapenem-resistant Klebsiella pneumoniae in New York City: a new threat to our antibiotic armamentarium. Arch Intern Med. 2005;165(12):1430–5.

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S, et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis. 2010;10(9):597–602.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    Lauretti L, Riccio ML, Mazzariol A, Cornaglia G, Amicosante G, Fontana R, Rossolini GM. Cloning and characterization of blaVIM, a new integron-borne metallo-β-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob Agents Chemother. 1999;43(7):1584–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Nordmann P, Cuzon G, Naas T. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis. 2009;9(4):228–36.

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Nordmann P, Naas T, Poirel L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis. 2011;17(10):1791–8.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. 38.

    Poirel L, Nordmann P. Carbapenem resistance in Acinetobacter baumannii: mechanisms and epidemiology. Clin Microbiol Infect. 2006;12(9):826–36.

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME, Brown S, Amyes SG, Livermore DM. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents. 2006;27(4):351–3.

    CAS  PubMed  Article  Google Scholar 

  40. 40.

    Yigit H, Queenan AM, Anderson GJ, Domenech-Sanchez A, Biddle JW, Steward CD, Alberti S, Bush K, Tenover FC. Novel carbapenem-hydrolyzing β-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob Agents Chemother. 2001;45(4):1151–61.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. 41.

    Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, Walsh TR. Characterization of a new metallo-β-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 2009;53(12):5046–54.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Yang J, Cai Y, Liu Z-Y, Liang B-B, Bai N, Wang R. Bibliometric analysis of publications about New Delhi metallo-β-lactamase 1-positive drug-resistance bacteria. Chin J Clin Pharmacol. 2011;8:022.

    Google Scholar 

  43. 43.

    Xiu-Zhen D, Bei-Bei L, Yue L, Jing Z, Rui W, Jin W. Bibliometric analysis of research papers about the resistance mechanisms of Pseudomonas aeruginosa. Chin J Clin Pharmacol. 2014;30(1):40–2.

    Google Scholar 

  44. 44.

    Yue L, Bei-bei L, Hui N, Jin W, Rui W. Bibliometric analysis of publications about Klebsiella pneumoniae carbapenemases (KPC)-producing Klebsiella pneumoniae. Chin J Clin Pharmacol. 2014;7:635–8.

    Google Scholar 

  45. 45.

    Higgins PG, Dammhayn C, Hackel M, Seifert H. Global spread of carbapenem-resistant Acinetobacter baumannii. J Antimicrob Chemother. 2010;65(2):233–8.

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Schwaber MJ, Carmeli Y. Carbapenem-resistant Enterobacteriaceae: a potential threat. JAMA. 2008;300(24):2911–3.

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Nemec A, Krizova L, Maixnerova M, Diancourt L, van der Reijden TJ, Brisse S, van den Broek P, Dijkshoorn L. Emergence of carbapenem resistance in Acinetobacter baumannii in the Czech Republic is associated with the spread of multidrug-resistant strains of European clone II. J Antimicrob Chemother. 2008;62(3):484–9.

    CAS  PubMed  Article  Google Scholar 

  48. 48.

    Nordmann P, Dortet L, Poirel L. Carbapenem resistance in Enterobacteriaceae: here is the storm! Trends Mol Med. 2012;18(5):263–72.

    CAS  PubMed  Article  Google Scholar 

  49. 49.

    Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States, 2013. 2014. http://www.cdc.gov/drugresistance/threat-report-2013/.

  50. 50.

    Figg WD, Dunn L, Liewehr DJ, Steinberg SM, Thurman PW, Barrett JC, Birkinshaw J. Scientific collaboration results in higher citation rates of published articles. Pharmacotherapy. 2006;26(6):759–67.

    PubMed  Article  Google Scholar 

  51. 51.

    Huamani C, Rey de Castro J, Gonzalez-Alcaide G, Polesel DN, Tufik S, Andersen ML. Scientific research in obstructive sleep apnea syndrome: bibliometric analysis in SCOPUS, 1991–2012. Sleep Breath. 2015;19(1):109–14.

    PubMed  Article  Google Scholar 

  52. 52.

    Poirel L, Lebessi E, Heritier C, Patsoura A, Foustoukou M, Nordmann P. Nosocomial spread of OXA-58-positive carbapenem-resistant Acinetobacter baumannii isolates in a paediatric hospital in Greece. Clin Microbiol Infect. 2006;12(11):1138–41.

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Tsakris A, Pournaras S, Woodford N, Palepou MF, Babini GS, Douboyas J, Livermore DM. Outbreak of infections caused by Pseudomonas aeruginosa producing VIM-1 carbapenemase in Greece. J Clin Microbiol. 2000;38(3):1290–2.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Cuzon G, Ouanich J, Gondret R, Naas T, Nordmann P. Outbreak of OXA-48-positive carbapenem-resistant Klebsiella pneumoniae isolates in France. Antimicrob Agents Chemother. 2011;55(5):2420–3.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  55. 55.

    Poirel L, Menuteau O, Agoli N, Cattoen C, Nordmann P. Outbreak of extended-spectrum β-lactamase VEB-1-producing isolates of Acinetobacter baumannii in a French hospital. J Clin Microbiol. 2003;41(8):3542–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    Carbonne A, Thiolet JM, Fournier S, Fortineau N, Kassis-Chikhani N, Boytchev I, Aggoune M, Seguier JC, Senechal H, Tavolacci MP, et al. Control of a multi-hospital outbreak of KPC-producing Klebsiella pneumoniae type 2 in France, September to October 2009. Euro Surveill. 2010;15(48):19734.

    PubMed  Google Scholar 

  57. 57.

    Schwaber MJ, Lev B, Israeli A, Solter E, Smollan G, Rubinovitch B, Shalit I, Carmeli Y. Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention. Clin Infect Dis. 2011;52(7):848–55.

    PubMed  Article  Google Scholar 

  58. 58.

    Samra Z, Ofir O, Lishtzinsky Y, Madar-Shapiro L, Bishara J. Outbreak of carbapenem-resistant Klebsiella pneumoniae producing KPC-3 in a tertiary medical centre in Israel. Int J Antimicrob Agents. 2007;30(6):525–9.

    CAS  PubMed  Article  Google Scholar 

  59. 59.

    Leavitt A, Navon-Venezia S, Chmelnitsky I, Schwaber MJ, Carmeli Y. Emergence of KPC-2 and KPC-3 in carbapenem-resistant Klebsiella pneumoniae strains in an Israeli hospital. Antimicrob Agents Chemother. 2007;51(8):3026–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. 60.

    Rolain JM, Parola P, Cornaglia G. New Delhi metallo-β-lactamase (NDM-1): towards a new pandemia? Clin Microbiol Infect. 2010;16(12):1699–701.

    CAS  PubMed  Article  Google Scholar 

  61. 61.

    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 

Download references

Authors’ contributions

WS concept and idea; and manuscript preparation and submission. NS and SZ data analysis and result section. SA, AS and AA literature review, critical thinking, data interpretation and manuscript preparation. All authors read and approved the final manuscript.

Acknowledgements

The authors would like to acknowledge Shatha, T (An-Najah National University) for her language and professional editing of the manuscript.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

All data present in this article can be retrieved from Scopus using keywords listed in the methodology.

Author information

Affiliations

  1. Department of Physiology, Pharmacology and Toxicology, College of Medicine and Health Sciences, An-Najah National University, Nablus, 44839, State of Palestine

    Waleed M. Sweileh, Ansam F. Sawalha & Adham S. AbuTaha

  2. Department of Pharmaceutical Chemistry and Technology, College of Medicine and Health Sciences, An-Najah National University, Nablus, 44839, State of Palestine

    Naser Y. Shraim

  3. Department of Clinical and Community Pharmacy, College of Medicine and Health Sciences, An-Najah National University, Nablus, 44839, State of Palestine

    Samah W. Al-Jabi & Sa’ed H. Zyoud

Authors
  1. Waleed M. Sweileh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naser Y. Shraim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samah W. Al-Jabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ansam F. Sawalha
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Adham S. AbuTaha
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sa’ed H. Zyoud
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Waleed M. Sweileh.

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., Shraim, N.Y., Al-Jabi, S.W. et al. Bibliometric analysis of global scientific research on carbapenem resistance (1986–2015). Ann Clin Microbiol Antimicrob 15, 56 (2016). https://doi.org/10.1186/s12941-016-0169-6

Download citation

Keywords

  • Carbapenem
  • Resistance
  • Bibliometric analysis

Annals of Clinical Microbiology and Antimicrobials

ISSN: 1476-0711

Contact us