Original Article

An Assessment of the 100 Most Frequently Cited Articles Regarding Extracorporeal Membrane Oxygenation in the Literature

10.4274/cjms.2021.2675

  • Sibel Büyükçoban
  • Tuğra Gençpınar
  • Serdar Bayrak
  • Çağatay Bilen
  • Gökmen Akkaya
  • Volkan Hancı

Received Date: 20.08.2020 Accepted Date: 08.01.2021 Cyprus J Med Sci 2022;7(4):444-456

BACKGROUND/AIMS:

The aim of this study was to evaluate the most common 100 publications related to extra-corporeal membrane oxygenation (ECMO) in the literature.

MATERIALS AND METHODS:

Our study was conducted using the advanced mode of the Web of Science (WOS) search engine of the institute for scientific information. “TS=Extracorporeal” or “TI=Extracorporeal” terms were used for the search. The search was made on 09/09/2018 and the 100 most cited publications were identified. The total number of citations of each publication, the number of annual citations, the researchers, and the catalog data of the journals were determined using WOS and PubMed.

RESULTS:

From September 1975 to 2018, there were a total of 33,007 publications in the WOS search engine. Among the top 100 most cited studies, the highest number of citations was 1,212, and the lowest was 105. The total number of citations was 213.83±157.53. The annual average number of citations of the studies ranged between 121.20 and 3.29, and the mean number of studies was 17.60±16.20.

CONCLUSION:

Our study is the first study to evaluate and analyze the first 100 studies related to ECMO in the literature. We found an increase in the number of publications on ECMO over the last five years.

Keywords: Extracorporeal membrane oxygenation, citation, first 100, index, ECMO

INTRODUCTION

In current era, several studies have been conducted by different international or national institutes and surgical disciplines in order to determine the most cited articles for various medical areas.1-4 When a scientific paper gives a reference to another scientific paper, it is identified as “cited”. The scientific articles which have been a resource of the study or strengthen the findings of the study are accepted as cited if they are referred to in any part of another scientific paper. The impact factor of the article is evaluated according to its frequency of citation. The more cited articles and the journals with a higher impact factor accepted as more qualified.5,6

The first bibliographic study was written by Garfield et al.7 regarding the 100 citation classics from the Journal of the American Medical Association and published in the Journal of the American Medical Association (JAMA). Since then, numerous articles have been examined and presented as “the most cited articles” in specific journals.7-13

Myocardial damage may require the use of intra-aortic balloon pump or extra-corporeal membrane oxygenation (ECMO). ECMO is one of the most important and widely used auxiliary devices that provides support to the lung or heart in reversible conditions of cardiac or respiratory failure. ECMO is the preferred life saving device in cases where heart/lung machines (CPB) cannot be applied. Current articles on ECMO indications, follow-up, complications, positive contributions to transplantation or recovery are frequently encountered in the literature.

According to our research, there has been no recent study in the literature examining the number of citations of international articles related to ECMO. This study will be the first to identify the 100 most cited articles on ECMO. In this study, we aimed to examine the most cited internationally related articles about ECMO via the institute for scientific information (ISI) and the Web of Science (WOS) search engines.


MATERIALS AND METHODS

This study was conducted following Dokuz Eylül University Faculty of Medicine Non-Interventional Research Ethics Committee approval with the number 6264-GOA 2018/25-24 and then performed using the advanced mode of the WOS search engines. Consequently, there was no need for patient consent for the study information. The “SU=ECMO” word was searched for and articles published between September 1975 and 2008 were included. The search was made on 15/10/2018. Consequently, the 130 most cited articles pertaining to BAV which had been published in international journals were identified, and thus a list was created. The first authors in each article were reviewed for whether they took part in another article in the same list. The overall and annual citation count and information about the authors, articles and journals were determined via WOS and PubMed. Thereafter, letters to the editor and case reports were excluded from this study.

Statistical Analysis

Statistical analyzes were carried out using the SPSS (Statistical Package for Social Sciences, Chicago, IL, USA) 20.0 software. Categorical data were presented in absolute (n) and relative (%) frequencies. All hemodynamic data were expressed as the mean value ± standard deviation. In the comparison of the groups, Kruskal-Wallis and Mann-Whitney U tests were utilized. A p-value of <0.05 was considered as statistically significant in all statistical tests.


RESULTS

In the literature analysis from September 1975 to 2018, there were 33,007 publications in the WOS search engine with the search keywords “TS=Extracorporeal” or “TI=Extracorporeal”. The highest number of citations in the first 100 most cited studies was 1,212, while the lowest was 105. The mean total number of citations of the 100 most cited studies was 213.83±157.53. The annual mean number of citations of the studies ranged between 121.20 and 3.29 and the mean number of studies was 17.60±16.20.

The most cited study was conducted by Peek et al.14 Lancet trial, published in 2009, titled “Efficacy and economic assessment of conventional ventilatory support versus extracorporeal membrane oxygenation for severe adult respiratory failure (CESAR): A multicentre randomised controlled trial”. The first three topics of the 100 most referenced studies in the area of ECMO were acute respiratory distress syndrome (ARDS) (25%), CPR (17%) and neonatal respiratory distress syndrome (YD-RDS) with peritoneopericardial diaphragmatic hernia (YD PPDH) (13%). The study with the highest number of citations was published in the Annals of Thoracic Surgery (9%), followed by Critical Care Medicine (9%), the Journal of Thoracic and Cardiovascular Surgery (7%), Pediatrics (7%), the Lancet (7%), and JAMA (7%).

All of the 100 most cited articles in the field of ECMO were in the SCI index. When the distribution of the studies by country was examined, the first three countries were determined to be the United States (57%), Germany (7%) and France (7%). It was determined that 28% of the studies were from the European countries and 72% from countries outside the European continent. No significant relationship was found between the continent of the author and the total and annual citations or between the continent of the journal and the number of total and annual citations (p>0.05) (Table 1, 2).

When the 100 most cited studies were evaluated, it was found that the mean number of annual citations of the studies published between 2005-2009 and after 2010 was significantly higher than the other periods (p<0.001). In the evaluation made according to the authors’ country, there was no significant difference in terms of the total number of citations and the mean number of annual citations (Table 3, 4).

When evaluated according to the types of the most cited 100 study, the total number of citations of and prospective clinical studies and case series was higher than other studies (p<0.001). In addition, meta-analyses, prospective studies and compilations were found to be higher than the other studies (p=0.019) In our study, it was determined that the annual mean number of citations of ECMO applications in adults was higher than the study of pediatric and adult ECMO subjects (p=0.001).

There was a significant difference between the mean and total number of citations in the evaluation made by the department. It was found that the total number of citations (p=0.010) was higher in those studies which were evaluated as pediatrics, anesthesia and other branches in the other branches. It was determined that the mean number of annual citations of the studies (p=0.001) involving intensive care and cardiology branches were higher than those of other branches.

According to the journals, the mean number of citations (p=0.002) and the number of annual citations average of the studies (p=0.011) published in the Lancet, NEJM and JAMA journals were significantly higher than other journals. It was determined that the total number of citations of ARDS and YD PPHT studies were higher and the number of annual mean citations was higher in ARDS-related studies.


DISCUSSION

The aim of this study was to investigate the most cited articles of ECMO through the WOS search engine of the ISI. The mean number of annual citations of the 100 most cited studies was significantly higher than the other studies and the number of citation articles was higher than prospective clinical studies. In addition, the total number of cited cases, and the average number of annual citations of prospective studies and review studies were higher than other studies. The mean number of annual citations was higher in those studies related to practices. Also, there was a significant difference between the mean and total number of citations in the evaluation made according to the department and results of the studies. It was determined that the mean number of annual citations was higher in those articles related with ARDS and YD PPHT.

The use of ECMO is being tried in more and more extensive indications with the spread of the ECMO team. The current guidelines include bridging treatments under ECMO support. Original research articles on ECMO have been increasing in number with experience. In this study, reviewing the most cited internationally cited articles related to ECMO through the ISI and the WOS search engine provided an up-to-date perspective to see the differences between these articles according to their authors, countries and institutions.

The first oxygenator-like device was developed by Von Frey and Gruber in 1885, while Gibbon developed the first film/bubble oxygenation heart-lung machine and Clowes et al. continued to develop membrane oxygenators.15-17 The first successful neonatal ECMO was performed in 1975. A large number of scientific research articles have been published in order to increase the success rate of ECMO applications and to reduce morbidity. In study based on 827 ECMO cases in newborns, it was observed that leukocyte reduced blood use, and decreased complications related to transfusion in ECMO.17 In neonatal ECMO cases, complications related to transfusion were found to be reduced by 41% with concentrated platelet replacement.18 In a study with newborns, it was found that high prime volume was a significant risk factor in postoperative ECMO support in 64 cases with low birth weight (below 2.5 kg).19

It is important to evaluate the scientific effectiveness of articles with the number of citations and annual mean citations of scientific articles on ECMO. We aimed to capture a scientific point of view by reviewing and interpreting the first 100 publications on ECMO. As a result of the increase in interventional procedures in the cardiovascular field with technology, the number of bibliographic publications has increased in the current literature.

Kolkailah et al.20 published a bibliographic study on human heart transplantations with half a century of experience. In that study, it was found that 85% of the researchers were male, and they could not find a significant relationship between the journal’s primary index and the number of annual journal editions. Usman et al.21 examined the first 100 publications on heart valve diseases and found an increase in the number of publications with catheter-based methods in recent years. We found that interventional procedures made with the support of ECMO in recent years have also increased in terms of their publication and citation index over the last 5 years. Researchers can carry out more work on this issue.

Lai et al.22 performed bibliographic research on aortic dissection and reported results on the development of aortic dissection surgical techniques. Liao et al.23 pointed out an increase in treatment with preventive measures by looking at the first 100 citationed research studies on coronary heart disease. In recent years, Shuaib et al.24 reported a decrease in the number of publications in the field of cardiology, because there has been a shift to the cardiovascular field and the guidelines support this. In our publication, we made a similar comment by looking at the publication citation number increase in recent years in interventional procedures, and we linked this to the team’s work together with the heart team and pointed out an increase in hybrid operations.

Pennell et al.25 found an increase in the number of studies performed in the last 5 years when they examined cardiovascular magnetic resonance. They attributed this to an increase in the number of patients in the cardiovascular field and the widespread use of imaging methods. Oh and Galis26 reported bibliographic studies on hypertension and emphasized that there has been an increase in the number of citations in parallel with developments in technology. Friedmacher et al.27 found that the scientometric analysis of congenital diaphragmatic hernias has increased in recent years with technological developments. ECMO shows the positive effect of congenital diaphragmatic hernia treatment on bridging support on surveillance. In order to develop renewable multidisciplinary therapies, citation index evaluation studies have been emphasized as they have global value.

For the expansion of ECMO cost effectiveness and cardiopulmonary resuscitation with ECMO support, Kilchemmann et al.28 suggested that bibliometric evaluation should be performed at repeated times in ECMO. Eldredge et al.29 and Bautista-Rodriguez et al.30 stated in their studies that further research is needed especially for the success of pediatric ECMO applications. Senst and Diaz31 reported that the use of ECMO has become widespread after looking at recent publications.

Bacon et al.32 reviewed current publications on ECMO and presented a review of the positive results of ECMO support in stage II bidirectional Glenn and stage III Fontan procedures in single ventricular patients. Iantorno et al.33 performed a review of the current literature on the emergency valve-in-valve transcatheter aortic valve replacement of acute aortic regurgitation and cardiogenic shock in the use of preoperative veno-arterial ECMO. They emphasized that case series have been introduced in recent years.

Patroniti et al.34 reported that the best strategy for mechanical ventilation and respiratory monitoring in ECMO patient monitoring has not been defined by the current literature review. They also presented a compilation of ARDS-ECMO and the conclusion that more publications on ECMO are needed. Cohen et al.35 evaluated the invasive procedures of emergency treatment in 6 countries up to 2006. They pointed out the importance of digital recordings and the storage of data. They also stated that publications should be evaluated bibliographically with PubMed and other search engines at certain intervals. Loomba and Anderson36 compiled bibliometric studies and demonstrated the weakness or strength of publications in pediatric cardiology.

The most cited study was conducted by Peek et al.14 (CESAR-2009): A multi-center randomized controlled trial, published in the journal Lancet. They recommended the transfer of adult patients with severe but potentially reversible respiratory failure with a Murray score of 3.0 or less than pH 7.20 in the optimal conventional treatment to a center with ECMO to significantly improve survival without serious problems. Interestingly, in their study, they found a life quality increase of 0.03 in 6 months follow-up in patients with ECMO.14

The ECMO team and E-CPR should be continuously trained. Sepsis and renal failure still negatively affect outcomes. Adjusting the fluid volume balance with high flow; cytokine levels and reducing inflammation response can help weaning. The current issues relating to ECMO should be continuously monitored and interpreted. Questions to be taken into consideration in the decision of ECMO application indication include these; “Is the problem life-threatening?” and “Can the disease be reversed?” The most important parameters for improving ECMO results are timing, management of the system, experience and experience of the team. ECMO support can be life-saving in the treatment of temporary cardiopulmonary insufficiency. In the minds of clinicians dealing with critically ill patients, an alternative to ECMO should be included.

Study Limitations

Similar to all bibliometric studies, this study has many limitations. First, ISI and PubMed, WOS were used to search for the most cited articles. It is known that the number of citations varies between databases. The studies were evaluated on the basis of the number of citations and the mean number of annual citations, but were not ranked accordingly. Additionally, although the number of citations and the mean annual citation rate are traditional parameters in the scientific evaluation of an article, its contribution to science cannot be assessed only by these measures.


CONCLUSION

Bibliographic studies are important as they allow for the following of the citation variances of elite publications according to years, study types, study areas and journals in determining the topics of most interest and citation. In the analysis of the elite articles related to ECMO, it was determined that those studies published after 2005, those studies relating to prospective studies, those studies relating to adult ECMO applications, and the references of those studies related to ARDS and Yd PPHT were at a higher rate.

MAIN POINTS

• Our study is the first study to evaluate and analyze the first 100 studies related to ECMO in the literature.

• In the literature analysis from September 1975 to 2018, among the top 100 most cited studies, the highest number of citations was 1,212, and the lowest was 105.

• When the 100 most cited studies were evaluated, it was found that the mean number of annual citations of the studies published between 2005-2009 and after 2010 was significantly higher than other periods (p<0.001).

• The first three topics of the 100 most referenced studies in the area of ECMO were ARDS (25%), CPR (17%) and neonatal respiratory distress syndrome with peritoneopericardial diaphragmatic hernia (13%).

• All of the 100 most cited articles in the field of ECMO were in the SCI index. When the distribution of the studies by country was examined, the first three countries were determined to be the United States (57%), Germany (7%) and France (7%).

ETHICS

Ethics Committee Approval: This study was conducted following Dokuz Eylül University Faculty of Medicine Non-Interventional Research Ethics Committee approval with the number 6264-GOA 2018/25-24 and then performed using the advanced mode of the WOS search engines.

Informed Consent: There was no need for patient consent for the study information.

Peer-review: Externally peer-reviewed.

Authorship Contributions

Concept: S.B., T.G., S.B., Ç.B., G.A., V.H., Design: S.B., T.G., S.B., Ç.B., G.A., V.H., Supervision: S.B., T.G., S.B., Ç.B., G.A., V.H., Data Collection and/or Processing: S.B., T.G., S.B., Ç.B., G.A., V.H., Analysis and/or Interpretation: S.B., T.G., S.B., Ç.B., G.A., V.H., Literature Search: S.B., T.G., S.B., Ç.B., G.A., V.H., Writing: S.B., T.G., S.B., Ç.B., G.A., V.H., Critical Review: S.B., T.G., S.B., Ç.B., G.A., V.H.

DISCLOSURES

Conflict of Interest: No conflict of interest was declared by the authors.

Financial Disclosure: The author declared that this study had received no financial support.


  1. Ahmad SS, Ahmad SS, Kohl S, Ahmad S, Ahmed AR. The hundred most cited articles in bariatric surgery. Obes Surg. 2015; 25(5): 900-9.
  2. Paladugu R, Schein M, Gardezi S, Wise L. One hundred citation classics in general surgical journals. World J Surg. 2002; 26(9): 1099-105.
  3. Terajima K, Aneman A. Citation classics in anaesthesia and pain journals: a literature review in the era of the internet. Acta Anaesthesiol Scand. 2003; 47(6): 655-63.
  4. Ohba N, Nakao K. The 101 most frequently cited articles in ophthalmology journals from 1850 to 1950. Arch Ophthalmol. 2010; 128(12): 1610-7.
  5. Garfield E. 100 citation classics from the journal of the American Medical Association. JAMA. 1987; 257(1): 52-9.
  6. Ohba N, Nakao K, Isashiki Y, Ohba A. The 100 most cited articles in ophthalmology journals. Arch Ophthalmol. 2007; 125(7): 952-60.
  7. Garfield E. 100 citation classics from the Journal of the American Medical Association. JAMA. 1987; 257(1): 52-9.
  8. Paladugu R, Schein M, Gardezi S, Wise L. One hundred citation classics in general surgical journals. World J Surg. 2002; 26(9): 1099-105.
  9. Lefaivre KA, Shadgan B, O’Brien PJ. 100 most cited articles in orthopaedic surgery. Clin Orthop Relat Res. 2011; 469(5): 1487-97.
  10. Thomson Scientific ISI Web of Knowledge: http://scientific.thomson.com/webofknowledge
  11. Aminian A, Daigle CR, Brethauer SA, Schauer PR. Citation classics: top 50 cited articles in bariatric and metabolic surgery. Surg Obes Relat Dis. 2014; 10(5): 898-905.
  12. Bayramlar H, Çakıcı Ö, Karadağ R, Yıldırım A, Sarı Ü. The most frequently cited 100 Turkish articles in Ophthalmic literature. Medeniyet Medical Journal. 2015; 30(1): 13-21.
  13. Yoon DY, Yun EJ, Ku YJ, Baek S, Lim KJ, Seo YL, et al. Citation classics in radiology journals: the 100 top-cited articles, 1945-2012. AJR Am J Roentgenol. 2013; 201(3): 471-81.
  14. Peek GJ, Mugford M, Tiruvoipati R, Wilson A, Allen E, Thalanany MM, et al. Efficacy and economic assessment of conventional ventilatory support versus extracorporeal membrane oxygenation for severe adult respiratory failure (CESAR): a multicentre randomised controlled trial. Lancet. 2009; 374(9698): 1351-63. Erratum in: Lancet. 2009; 374(9698): 1330.
  15. Koster A, Huebler M, Boettcher W, Redlin M, Berger F, Hetzer R. A new miniaturarised cardiopulmonary bypass circuit reduces transfusion requirements during neonatal surgery: initial experiences in 13 consecutive patients. J Thorac Cardiovasc Surg. 2009; 137(6): 1565-8.
  16. Redlin M, Huebler M, Boettcher W, Kukucka M, Schoenfeld H, Hetzer R, et al. Minimizing intraoperative hemodilution by use of a very low priming volume cardiopulmonary bypass in neonates with transposition of the great arteries. J Thorac Cardiovasc Surg. 2011; 142(4): 875-81.
  17. Jackson HT, Oyetunji TA, Thomas A, Oyetunji AO, Hamrick M, Nadler Ep, et al. The impact of leukoreduced red blood cell transfusion on mortality of neonates undergoing extracorporeal membrane oxygenation. J Surg Res. 2014; 192(1): 6-11.
  18. Bjerke HS, Kelly RE Jr, Foglia RP, Barcliff L, Petz L. Decreasing transfusion exposure risk during extracorporeal membrane oxygenation (ECMO). Transfus Med. 1992; 2(1): 43-9.
  19. Kim SY, Cho S, Choi E, Kim WH. Effects of Mini-Volume Priming During Cardiopulmonary Bypass on Clinical Outcomes in Low-Bodyweight Neonates: Less Transfusion and Postoperative Extracorporeal Membrane Oxygenation Support. Artif Organs. 2016; 40(1): 73-9.
  20. Kolkailah AA, Fugar S, Vondee N, Hirji SA, Okoh AK, Ayoub A, et al. Bibliometric Analysis of the Top 100 Most Cited Articles in the First 50 Years of Heart Transplantation. Am J Cardiol. 2019; 123(1): 175-86.
  21. Usman MS, Siddiqi TJ, Khan MS, Fatima K, Butler J, Manning WJ, et al. A Scientific Analysis of the 100 Citation Classics of Valvular Heart Disease. Am J Cardiol. 2017; 120(8): 1440-9.
  22. Lai P, Liu YH, Xue JH, He PC, Qiu YQ. The 100 most-cited articles on aortic dissection. BMC Cardiovasc Disord. 2017; 17(1): 30.
  23. Liao J, Wang J, Liu Y, Li J, He Q, Jiang W, et al. The most cited articles in coronary heart disease: A bibliometric analysis between 1970 and 2015. Int J Cardiol. 2016; 222: 1049-52.
  24. Shuaib W, Khan MS, Shahid H, Valdes EA, Alweis R. Bibliometric analysis of the top 100 cited cardiovascular articles. Am J Cardiol. 2015; 115(7): 972-81.
  25. Pennell DJ, Baksi AJ, Kilner PJ, Mohiaddin RH, Prasad SK, Alpendurada F, et al. Review of Journal of Cardiovascular Magnetic Resonance 2013. J Cardiovasc Magn Reson. 2014; 16: 100.
  26. Oh YS, Galis ZS. Anatomy of success: the top 100 cited scientific reports focused on hypertension research. Hypertension. 2014; 63(4): 641-7.
  27. Friedmacher F, Pakarinen MP, Rintala RJ. Congenital diaphragmatic hernia: a scientometric analysis of the global research activity and collaborative networks. Pediatr Surg Int. 2018; 34(9): 907-17.
  28. Kilchemmann C, Vallejos C, Román A. Cost effectiveness and budget impact analysis of inhaled nitric oxide in a neonatal unit from the perspective of the public health system. Rev Chil Pediatr. 2016; 87(6): 463-7.
  29. Eldredge RS, Zhai Y, Cochran A. Effectiveness of ECMO for burn-related acute respiratory distress syndrome. Burns. 2019; 45(2): 317-21.
  30. Bautista-Rodriguez C, Sanchez-de-Toledo J, Da Cruz EM. The Role of Echocardiography in Neonates and Pediatric Patients on Extracorporeal Membrane Oxygenation. Front Pediatr. 2018; 6: 297.
  31. Senst B, Diaz RR. Cardiac Surgery. StatPearls. Treasure Island (FL): StatPearls Publishing; 2018.
  32. Bacon MK, Gray SB, Schwartz SM, Cooper DS. Extracorporeal Membrane Oxygenation (ECMO) Support in Special Patient Populations-The Bidirectional Glenn and Fontan Circulations. Front Pediatr. 2018; 6: 299.
  33. Iantorno M, Ben-Dor I, Rogers T, Gajanana D, Attaran S, Buchanan KD, et al. Emergent valve-in-valve transcatheter aortic valve replacement in patient with acute aortic regurgitation and cardiogenic shock with preoperative extracorporeal membrane oxygenator: A case report and review of the literature. Cardiovasc Revasc Med. 2018; 19(8S): 68-70.
  34. Patroniti N, Bonatti G, Senussi T, Robba C. Mechanical ventilation and respiratory monitoring during extracorporeal membrane oxygenation for respiratory support. Ann Transl Med. 2018; 6(19): 386.
  35. Cohen S, Gilutz H, Marelli AJ, Iserin L, Benis A, Bonnet D, et al. Administrative health databases for addressing emerging issues in adults with CHD: a systematic review. Cardiol Young. 2018; 28(6): 844-53.
  36. Loomba RS, Anderson RH. Are we allowing impact factor to have too much impact: The need to reassess the process of academic advancement in pediatric cardiology? Congenit Heart Dis. 2018; 13(2): 163-6.