Narrative review article on epidemiology, diagnosis, treatment: a bibliometric analysis of the global scientific research progress on esophageal cancer

Introduction

Esophageal cancer (EC) rank 6^th among the main causes of death (1), and 8^th among types of cancer with a poor survival rate for 5 years (<20%) in the world (2,3). Evidence shows that EC is not common in the United States and Western societies, whereas in China represented 17,650 (1%) of tumors, 16,080 (2.6%) of cancer deaths and 50% of all new cases (1).

Squamous cell carcinoma (SCC), was spread in the developing countries, while adenocarcinoma (AC) was spread in the developed countries (4,5). AC was associated with gastric reflux and Barrett’s esophagus (4,6). Whereas, SCC was associated with alcohol consumption, hot tea drinking, red meat consumption, poor oral health, low intake of fresh fruits and vegetables, smoking and low socioeconomic status (7-10). Clinical symptoms includes enlargement in lymph glands around the collarbone, dry cough, weight loss, and hematemesis and difficult in swallowing (11).

Poor nutrition, poor oral hygiene, and social deprivation were reported risk factors associated with EC in many countries. In addition the others risk actors were includes age, male gender, habits (tobacco use, alcohol, hot drinks, carbonated soft drinks consumption) (12,13), nutritional deficiencies (vitamin and mineral deficiencies), gastro-esophageal reflux disease (GERD), obesity, exposures to silica and asbestos, and low socioeconomic status (14,15). Esophageal squamous cell carcinoma (ESCC) geographic distribution varies significantly more than 10-fold between countries (16). The geographical variation reflect the genetic and environmental factors (17). We present the following article in accordance with the Narrative Review reporting checklist (available at http://dx.doi.org/10.21037/dmr-20-121).

Epidemiology of EC

SCC is a common histological subtype of EC in the world. The burden of EC occur within two geographic belts, one from North Central China through the Central Asian countries to Northern Iran, and the second from Eastern to Southern Africa (18). The incidence of AC was dramatically increased over the past 40 years in Western countries (18). Recently, AC was common in the United States, United Kingdom, and Australia (18). The highest incidences rate was reported in Eastern and Southeastern Asia, sub-Saharan Africa, and Central Asia (7,19,20). SCC incidence has escalated in few developing countries exceeding 100 per 100,000 per year, particularly in China and South Africa (21). In 2008, 482,000 people were diagnosed with EC, and 407,000 were died (22). EC was the 4^th leading cause of death in African Americans. White have 2-fold risk of developing AC compared with Hispanics, and 3- to 4-fold increased risk compared with Blacks (23). In recent study, the incidence is high in black people and white women (24). The incidence of EC increased with a predictive model to 808,508 by 2035, causing 728,920 deaths (19,20).

In sub-Saharan Africa, the incidence of SCC has a regional variation, with the highest incidence rates in Southern and Eastern regions (17). The prevalence of SCC is higher than AC in Africa (25). Therefore, differences in risk factors were associated with regional variations (26,27). Previous studies showed that esophagus cancer was common in Eastern Africa (28) and rare in Western Africa (17,29). Minimizing smoking and alcohol consumption reduced SCC cases by 13% in Uganda (30).

Risk factors of EC

Esophagus cancer is the less studied cancer, and has aggressive nature and poor survival rate (19). Many risk factors has been reported such as age, sex, alcohol consumption (31,32) smoking, tobacco use (33-35), hot tea drink, consumption of red meat, poor oral health, low intake of vegetables and fruits, reducing nutritional supplements intake such as selenium and zinc (31). A higher risk of SCC was associated with low socioeconomic status (19), medical history, obesity (34), exposure to environmental factor (31), diet and physical activity for both sexes (36) and other lifestyle, and medical factors (37). Sex, duration of smoking and BMI are associated with EC mortality (38).

Age and sex

Worldwide, the risk of AC was increased in individual older than 50 years (3). The majorities of new cases were diagnosed in people aged from 65 to 74 years (39). The male preponderance was (7:1) with 11:1 in those aged 50 to 54 and 4:1 in those aged 75 to 79. The prediction for males was irrespective of race (40).

Nutrition

Diet represents 30–35% of EC risk factors (41,42). High intakes of fruits and vegetables has a protective benefit against EC (43,44). In high-risk areas, poor nutritional is responsible for EC (45,46). Vitamin A, vitamin E, selenium, and zinc deficiencies were associated with SCC (47). The Seattle Barrett Esophagus Research Program demonstrated an association between the daily use of multivitamins, vitamin C, and vitamin E, and the reduction in the risk of AC (48). In contrast, carbohydrate intake was link with EC, in the United States carbohydrate intake increased EAC and decreased SCC (49).

Smoking and alcohol consumption

Tobacco use and alcohol consumption were major risk factors for EC (18,50), associated with the development of SCC (51). Smokers had 5 folds risk of developing EC compared to non smokers (19). In Taiwan, or was 4.2 and 3.4, for smokers and non smokers, respectively (52). The risk of alcohol increases with the amount of alcohol ingested ranged between 1.8 and 7.4 depend on the weekly volume consumption (52). The intake of specific types of drink creates “hot spots” in SCC (24). Whereas, in Northern China, the risk was not associated with alcohol consumption (52).

Obesity

Obesity is a risk factor for AC, and is a serious public health disease in the developed countries. In 2015, 75% of American population were overweight and 41% were obese (53). High level BMI was associated with increased risk for AC (54). The development of AC in obese patient was associated with increased incidence of GERD and hormonal dependent mechanism that mediated by inflammatory markers secreted by adipocytes (52).

Gastro-esophageal reflux disease (GERD)

GERD was risk factor for Barrett’s esophagus and esophageal AC (55,56). Patients having recurrent heartburn or regurgitation was increased the risk to AC 5-fold compared to those without GERD symptoms (57).

Pathogens infection

Several studies have found that Ethnicity is more likely associated with the development of EAC (58). People have decreased esophageal microbial richness and diversity in saliva microbial are prone to develop esophageal squamous dysplasia (59) the precursor of SCC in China (60). Clostridiales and Erysipelotrichales in the gastric corpus increase esophageal squamous dysplasia and SCC in Iran (61). Porphyromonas gingivalis was detected in 61% of SCC tissues compared with tissues from healthy people (62). The prevalence of HPV DNA in SCC tumor tissue was ranged from 0 to 70% (63). Serologic test for L1 and E6/E7 to determine the role of HPV in SCC etiology, identified only four positive SCC samples (64). In addition, lack of association between SCC and HPV DNA, HPV mRNA, or p16 (INK4a) up regulation was documented (65). Genome sequence studies did not find evidence for integration of HPV DNA in SCC (66). Kaposi sarcoma and SCC incidence rates was increased in Malawi (67). Association of HIV with SCC was reported in Zambia (68). Similarly, Schistosoma mansoni was associated SCC (69).

Diagnosis of EC

The clinical symptoms of EC include difficulty or pain on swallowing, progressive weight loss and cough. Patient may vomit blood or pass Malena, fatigue may occur due to anemia in the presence of chronic occult bleeding (70). Clinical investigation depend on evaluation of clinically apparent metastatic disease e.g., supraclavicular lymph nodes and hepatomegaly. Endoscopy, which may be enhanced using narrow-band imaging or Lugol’s solution for squamous dysplasia is the mainstay of evaluation (71).

Previous studies indicated that patient with EC was presented with dysphagia, prompting endoscopy and biopsy. The most useful imaging tools for diagnosis of clinical staging were computed tomography (CT) and positron-emission tomography (PET) (72). Patient presented with dysphagia have T2 or T3 disease (73).

A barium swallow coat the lining of esophagus and shown on the X-ray. The test is not using nowadays, tissue samples taken during an endoscopy is the best way to confirm a diagnosis (74).

The middle and upper third esophageal carcinomas were increased at the time of diagnosis. Bronchoscopy reveal either impingement or invasion of the main airways over 30% of new patients with cancer in the upper third of the esophagus. In some cases, bronchoscopy alone, can confirm that the tumor is locally unrespectable (75).

Treatment of EC

The management is generally similar for ESCC and AC, the difference is in choice of chemotherapy or surgery (76). The treatment was clearly presented in the guidelines for diagnosis and treatment of carcinoma of the esophagus (77). Generally EC management protocol includes endoscopic and surgical treatment, chemo-radiotherapy, molecular target therapy and palliative treatment. Mucosal cancers are cured used endoscopic mucosal resection (EMR) and endoscopic sub mucosal dissection (ESD). Lesion not exceed the mucosal layer (T1a), remaining within the mucosal epithelium (EP) or lamina propria mucosa (LPM) are extremely associated with LN metastasis (78). Surgery is a treatment for Tis, T1 and T2 carcinoma (79). Despite advances in surgery, long term survival after surgery only for advanced EC was remained poor, perioperative chemotherapy was improved survival rates. The advantage of adding chemotherapy to EC treatment decreased the risk of distant metastasis (80). Radiotherapy plus cetuximab significantly improves overall survival for 5 years compared with radiotherapy alone for patients with locoregionally advanced head and neck cancers (81). A majority of EC patients required palliative therapy, because more than half of patients who are treated with curative intent developed tumor recurrence. Palliative chemotherapy is predominantly platinum and fluoropyrimidine based, while irinotecan may be an alternative in patients unsuitable for platinum (78).

Host genetics

Genetics analysis using high throughput sequencing technology was detected genomic alterations in SCC (74). The whole-genome sequencing, whole-exome sequencing, and array comparative genomic hybridization, identified more than 83% somatic mutation in SCCs (82). Detection of reliable markers to predict treatment outcome is still limited in the available medical research literature (74). Genetic polymorphisms may play important role in the carcinogenesis of EC (3).

Trend of EC in the world

Objective

The aim of the study is to review the epidemiology, diagnosis and treatment of EC, and provide an overview of the global scientific research in overall survival. The result will assists the decision makers at the national and international level, research organization, funding agenesis for better understanding the growth and development of the research output on EC.

Methods

A comprehensive literature search of EC was conducted in July 15, 2020, the citation search was performed using Science Citation Index Expanded (SCI-E) and Social Science Citation Index (SSCI) of ISI Web of Science (WoS). Articles published in WoS were reviewed by two reviewers, THM and IHM, with respect to their year of publication, reported authors, country of origin, journals and the affiliated institutions of the authors. We performed the search on WoS using entry terms of the medical subject headings (MesH) database of the US National Library of Medicine [National Institutes of Health (NIH)]. The used search term includes (esophagus*AND osophagus* carcinoma* OR cancer esophagus* OR cancer of the esophagus*OR esophageal cancer* OR esophagus cancer* OR esophagus neoplasm* OR neoplasms, esophageal*). The filtered result contained 9,021 original articles and review paper. The bibliometric indicators included productive annual trends of publications, citation report, author names, affiliations, WoS subject categories, h-index (83), language, and journal names. The recent impact factor (IF) for each journal was obtained from 2020 journal citation reports (JCR) (84). There was no institutional review board approval required for this study, because WoS is a public database, and our research does not involve any human subjects.

Data analysis

Bibliometric analysis was performed using a quantitative analysis approach and knowledge mapping technique. Quantitative analysis was performed based on the WoS information. Knowledge mapping (i.e., network analysis) was performed using VOSViewer 1.6.10. (www.vosviewer.com) (85), to visualize the author keywords, countries, institutions and authors. HistCite software an open-source tool was used for analyzing the research productivity (86), in addition to a bibliometrix: a R-tool for comprehensive science mapping analysis (using R-studio cloud) was used (87,88).

Results

Characteristic of the retrieved documents

Bibliometric analysis was conducted for the published data of EC between 1961 and 2019. Total number of 9,021 documents, 222,721 citations and 160 h-indexes were reported. Average years from publication was 13.2, and the average citations per documents was 25.73. The documents were distributed research article 7,871 (87.25%), book chapter 4 (0.04%), early access 8 (0.09%), proceeding paper 479 (5.31%), retracted publication 4 (0.04%), and review paper 655 (7.26%) (Table 1). Bibliometric analysis was performed for article published in English 8,453 (94%), French 233 (3%), German 137 (2%), among others languages (Figure 1). The trend shows an increasing research production and total citation score start in 1980 (Figure 2).

Figure 1 Language of publication on EC retrieved documents. EC, esophageal cancer.

Figure 2 Annual trend of publications and TGCS in the field of EC research. TGCS, Total Global Citations Score; EC, esophageal cancer.

Top journal cited EC articles

Among the top 16 journals each was contributed more than 100 published manuscripts. Journal of Diseases of the Esophagus with (IF =2.388) was published the highest number of articles (n=401), followed by Annals of Surgical Oncology (IF =4.061) with published (n=194) articles, Annals of Thoracic Surgery (IF =3.639) and published (n=167) articles and International Journal of Cancer (IF =5.145) and published (n=166) articles in EC with high citation score [Total Global Citations Score (TGCS) =10,104] times (Table 2).

Top 10 highly cited authors

The study notice that the first top author based on TGCS is Doki Y published 93 articles with (TGCS =2,827) times. The second author is Wang Y published 83 articles with (TGCS =1,368) times, and the third author is Kuwano H published 82 articles with (TGCS =1,577). The top authors whom published more than 50 research article in EC are presented in Table 3.

Top 10 highly cited articles

Table 4 displays the top-cited articles on EC literature (1961–2019), where the first top article is entitled “Preoperative chemo-radiotherapy for esophageal or junctional cancer” with account of (TGCS =2,276) for article published by van Hagen et al. (2012), followed by “Medical progress esophageal cancer” published in 2008, and article entitled “Combined chemotherapy and radiotherapy compared with radiotherapy alone in patients with cancer of the esophagus” obtained (TGCS =1,493). The top 10 articles received citation range from 676 to 2,276. Collaboration in research provide opportunity to increase the impact and scope of research in EC. Collaboration of countries/regions involved in EC research is shown in Figure 3.

Figure 3 The collaboration of countries/regions involved in EC research. EC, esophageal cancer.

Co-citation analysis between authors and organization

Of 162 authors were distributed into six clusters with total length strength [total link strength (TLS) =3,514]. Doki Yuichiro reported high TLS (TLS =395), followed by Yamasaki Makoto (TLS =311), and Mori Masaki (TLS =288) (Figure 4). The total of 231 organizations were distributed into the eight clusters with TLS 5,361. Furthermore, the visualization results show that the Chinese Academy of Science was high rank (TLS =351), followed by the National Cancer Center (TLS =301), and the University of Texas (TLS =235) (Figure 5).

Figure 4 Co-citation analysis of the authorship analysis. Authors with 20 documents were selected which resulted to a threshold of 102. Weigh based on total link strength (TLS).

Figure 5 Co-citation of authors and organization enhanced research, with 15 documents were selected which resulted to a threshold of 231 organizations. Weigh by total link strength (TLS).

WoS categories

Oncology research covered 3,735 (41.403%) of scientific categories during the study period, followed by Surgery 2,177 (24.133%), gastroenterology hematology 1,663 (18.435%), radiology nuclear medicine medical image 582 (6.452%), respiratory system 492 (5.454%), general internal medicine 456 (5.055%), experimental medicine 363 (4.024%), cardiovascular system cardiology 344 (3.813%), and cell biology 283 (3.137%) (Figure 6).

Figure 6 Top 20 WoS categories of EC research. WoS, Web of Science; EC, esophageal cancer.

Funding agencies

National Natural Science Foundation of China rank first 637 (7.061%) on supporting EC research, followed by United States Department of Health Human Services 544 (6.030%), NIH USA 541 (5.997%), NIH National Cancer Institute NCI 354 (3.924%), Ministry of Education, Culture, Sports, Science and Technology Japan MEXT 151 (1.674%), Japan Society for The Promotion of Science 65 (0.721%), NIH National Institute of Diabetes Digestive Kidney Diseases NIDDK 54 (0.599%), Natural Science Foundation of Jiangsu Province 53 (0.588%), National Basic Research Program of China 52 (0.576%), and Swedish Cancer Society 48 (0.532) (Figure 7).

Figure 7 Top 20 funding agencies on supporting research on EC. EC, esophageal cancer.

Organizations-enhanced

The top most organization enhanced indexed in WoS databases on EC are University of Texas system 287 (3.181%), followed by Zhengzhou University 261 (2.839%), UTMD Anderson Cancer Center 251 (2.782%), Chinese Academy of Medical Sciences, Peking Union Medical College 248 (2.749%), NIH USA 168 (1.862%), and NIH National Cancer Institute NCI 163 (1.807%) (Figure 8).

Figure 8 Top 20 organizations-enhanced research on EC. EC, esophageal cancer.

Keywords analysis

EC, esophagectomy, prognosis and cancer were the most frequency used keywords Plus. SCC and AC were the most frequency authors keywords used on EC published documents. Whereas, cancer, esophageal and patients were the most frequency keywords used in research title (Table 5).

Discussion

The EC was the main cause of cancer death in the world, with poor survival rate. A wealth of articles were published on esophagus cancer indexed in many database in the world. But there is no comprehensive bibliometric analysis to summarized EC research. In the present study we summarize the quantitative analysis of EC and research trends. The frequency analysis of the growth and citation scores indicated a noticeable increase in the EC publications in the past years, and this may be due to implementation of surgery EC treatment. Since EC was ranked 6^th causing cancer death worldwide (89), the incidence of new cancer cases was 455,800 and the death was occurred in 400,200 cases (83). The rapid increase in the EC and noticeable contribution in publication growth during the period of 1985 to 2019 might be due to increased number of the scientific journal that indexed in WoS databases. Currently, the evidence highlighted that WoS platform includes over 21,000 of the highest impact journals worldwide.

As shown in the bibliometric mapping the most cited articles were “Preoperative chemo-radiotherapy for esophageal or Junctional cancer”, followed by “Medical progress esophageal cancer” and “Combined chemotherapy and radiotherapy compared with radiotherapy alone in patients with cancer of the esophagus”. Whereas, most occurrence authors keywords retrieved were SCC and AC. The National Natural Science foundation, China is top funding agency for EC research. The underlying reasons might be due to their higher Gross Domestic Product (GDP) and fund used for research in well-developed countries compared with under developing countries.

Using of a bibliometric analysis is a straightforward for tracking research, standardized method of detecting the author keywords in the articles and assessing trends frequency of reported keywords, link strengths, and gaps in any published literature. keywords analysis showed a 6-fold increased in the number of publications from 1961 to 2019. Our current bibliometric study was given a snapshot of the current situation based on certain keywords used by the authors.

Limitations

A bibliometric study was 100% accurate and perfect, was a snapshot of the current situation based on certain keywords used in EC data collection. However, the electronic database was not accurate for data collection. System updates, affiliation of the authors, different name spelling, and sometimes missing funding agency or electronic databases which commonly effected bibliometric studies.

Conclusions

This study provides an overview on the epidemiology, diagnosis, treatment and bibliometric analysis of the global scientific research progress in EC related field. EC ranks 6^th in the world due to the mortality rate connected with malignant tumors, and it is eighth the most common cancer in the world. EC was associated with many risk factors such as age, sex, alcohol smoking, tobacco use, red meat, poor oral health, low intake of fresh food, and socioeconomic status. The study demonstrates that the literature on EC was continuously growing, in the field of SCC and AC. The efforts should be made by the developed countries to help developing countries with high prevalence of EC. National Natural Science Foundation of China and the United States Department of Health Human Services were the top funding agency on EC research. University of Texas and Chinese academy of medical sciences are the top organization enhance research on EC. Disease of the Esophagus was the top leading journal publishing articles on EC. China, USA and Japan are more productive countries on EC. There is need for collaboration towards diagnostic and treatment of EC in the world and control the risk associated with EC.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at http://dx.doi.org/10.21037/dmr-20-121

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at http://dx.doi.org/10.21037/dmr-20-121). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Boyko V, Dubrovina N, Zamyatin P, et al. Epidemiology and forecast of the prevalence of esophageal cancer in the Countries of Central and Eastern Europe. Procedia Econ Financ 2015;24:93-100. [Crossref]
2. Hynes TJ, Thomas CS, Zumbusch AS, et al. Early life adversity potentiates expression of addiction-related traits. Prog Neuropsychopharmacol Biol Psychiatry 2018;87:56-67. [Crossref] [PubMed]
3. Huang FL, Yu SJ. Esophageal cancer: risk factors, genetic association, and treatment. Asian J Surg 2018;41:210-5. [Crossref] [PubMed]
4. Schweigert M, Dubecz A, Stein HJ. Oesophageal cancer--an overview. Nat Rev Gastroenterol Hepatol 2013;10:230-44. [Crossref] [PubMed]
5. Napier KJ, Scheerer M, Misra S. Esophageal cancer: a review of epidemiology, pathogenesis, staging workup and treatment modalities. World J Gastrointest Oncol 2014;6:112-20. [Crossref] [PubMed]
6. Griffin SM, Wahed S. Oesophageal cancer. Surgery (Oxford) 2011;29:557-62. [Crossref]
7. Umar SB, Fleischer DE. Esophageal cancer: epidemiology, pathogenesis and prevention. Nat Clin Pract Gastroenterol Hepatol 2008;5:517-26. [Crossref] [PubMed]
8. Zhang HZ, Jin GF, Shen HB. Epidemiologic differences in esophageal cancer between Asian and Western populations. Chin J Cancer 2012;31:281-6. [Crossref] [PubMed]
9. Pennathur A, Gibson MK, Jobe BA, et al. Oesophageal carcinoma. Lancet 2013;381:400-12. [Crossref] [PubMed]
10. Mao WM, Zheng WH, Ling ZQ. Epidemiologic risk factors for esophageal cancer development. Asian Pac J Cancer Prev 2011;12:2461-6. [PubMed]
11. Crucitti A. editor. Surgical management of elderly patients. Cham: Springer, 2018.
12. Hemmatzadeh M, Mohammadi H, Karimi M, et al. Differential role of microRNAs in the pathogenesis and treatment of esophageal cancer. Biomed Pharmacother 2016;82:509-19. [Crossref] [PubMed]
13. Dine J, Gordon R, Shames Y, et al. Immune checkpoint inhibitors: an innovation in immunotherapy for the treatment and management of patients with cancer. Asia Pac J Oncol Nurs 2017;4:127-35. [Crossref] [PubMed]
14. Wang X, Niu H, Fan Q, et al. Predictive value of EGFR overexpression and gene amplification on icotinib efficacy in patients with advanced esophageal squamous cell carcinoma. Oncotarget 2016;7:24744-51. [Crossref] [PubMed]
15. Lin J, Kligerman S, Goel R, et al. State-of-the-art molecular imaging in esophageal cancer management: Implications for diagnosis, prognosis, and treatment. J Gastrointest Oncol 2015;6:3-19. [PubMed]
16. Kitagawa H, Namikawa T, Iwabu J, et al. Outcomes of abdominal esophageal cancer patients who were treated with esophagectomy. Mol Clin Oncol 2018;8:286-91. [PubMed]
17. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin 2011;61:69-90. [Crossref] [PubMed]
18. Dong J, Thrift AP. Alcohol, smoking and risk of oesophago-gastric cancer. Best Pract Res Clin Gastroenterol 2017;31:509-17. [Crossref] [PubMed]
19. Zhang Y. Epidemiology of esophageal cancer. World J Gastroenterol 2013;19:5598-606. [Crossref] [PubMed]
20. Wheeler JB, Reed CE. Epidemiology of esophageal cancer. Surg Clin North Am 2012;92:1077-87. [Crossref] [PubMed]
21. Le Bras GF, Farooq MH, Falk GW, et al. Esophageal cancer: The latest on chemoprevention and state of the art therapies. Pharmacol Res 2016;113:236-44. [Crossref] [PubMed]
22. Ferlay J, Shin HR, Bray F, et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127:2893-917. [Crossref] [PubMed]
23. El-Serag HB, Mason AC, Petersen N, et al. Epidemiological differences between adenocarcinoma of the oesophagus and adenocarcinoma of the gastric cardia in the USA. Gut 2002;50:368-72. [Crossref] [PubMed]
24. Domper Arnal MJ, Ferrández Arenas Á, Lanas Arbeloa Á. Esophageal cancer: risk factors, screening and endoscopic treatment in Western and Eastern countries. World J Gastroenterol 2015;21:7933-43. [Crossref] [PubMed]
25. Kgomo M, Elnagar AA, Nagel J, et al. Prevalence of squamous cell carcinoma of the esophagus in a single tertiary center of south africa: a cross sectional analytic study. J Public Health Afr 2017;8:563. [Crossref] [PubMed]
26. Engel LS, Chow WH, Vaughan TL, et al. Population attributable risks of esophageal and gastric cancers. J Natl Cancer Inst 2003;95:1404-13. [Crossref] [PubMed]
27. Machoki SM, Saidi H, Raja A, et al. Risk factors for esophageal squamous cell carcinoma in a Kenyan population. Ann African Surg 2015;12:38-43.
28. Bray F, Ren JS, Masuyer E, et al. Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer 2013;132:1133-45. [Crossref] [PubMed]
29. Jemal A, Center MM, DeSantis C, et al. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev 2010;19:1893-907. [Crossref] [PubMed]
30. Elamin A, Ibrahim ME, Abuidris D, et al. Part I: cancer in Sudan—burden, distribution, and trends breast, gynecological, and prostate cancers. Cancer Med 2015;4:447-56. [Crossref] [PubMed]
31. Yousefi MS, Sharifi-Esfahani M, Pourgholam-Amiji N, et al. Esophageal cancer in the world: incidence, mortality and risk factors. Biomed Res Ther 2018;5:2504-17. [Crossref]
32. Sewram V, Sitas F, O'Connell D, et al. Tobacco and alcohol as risk factors for oesophageal cancer in a high incidence area in South Africa. Cancer Epidemiol 2016;41:113-21. [Crossref] [PubMed]
33. González CA, Pera G, Agudo A, et al. Smoking and the risk of gastric cancer in the European Prospective Investigation Into Cancer and Nutrition (EPIC). Int J Cancer 2003;107:629-34. [Crossref] [PubMed]
34. Lindblad M, Rodríguez LA, Lagergren J. Body mass, tobacco and alcohol and risk of esophageal, gastric cardia, and gastric non-cardia adenocarcinoma among men and women in a nested case-control study. Cancer Causes Control 2005;16:285-94. [Crossref] [PubMed]
35. Zambon P, Talamini R, La Vecchia C, et al. Smoking, type of alcoholic beverage and squamous-cell oesophageal cancer in northern Italy. Int J Cancer 2000;86:144-9. [Crossref] [PubMed]
36. Bosetti C, Levi F, Ferlay J, et al. Trends in oesophageal cancer incidence and mortality in Europe. Int J Cancer 2008;122:1118-29. [Crossref] [PubMed]
37. Navarro Silvera SA, Mayne ST, Gammon MD, et al. Diet and lifestyle factors and risk of subtypes of esophageal and gastric cancers: classification tree analysis. Ann Epidemiol 2014;24:50-7. [Crossref] [PubMed]
38. Wu M, Zhao JK, Hu XS, et al. Association of smoking, alcohol drinking and dietary factors with esophageal cancer in high- and low-risk areas of Jiangsu Province, China. World J Gastroenterol 2006;12:1686-93. [Crossref] [PubMed]
39. Horner MJ, Ries LAG, Krapcho M, et al. SEER Cancer Statistics Review, 1975-2006. Bethesda: National Cancer Institute, 2009. Available online: https://seer.cancer.gov/csr/1975_2006/
40. Mathieu LN, Kanarek NF, Tsai HL, et al. Age and sex differences in the incidence of esophageal adenocarcinoma: results from the Surveillance, Epidemiology, and End Results (SEER) Registry (1973-2008). Dis Esophagus 2014;27:757-63. [Crossref] [PubMed]
41. Shridhar R, Almhanna K, Meredith KL, et al. Radiation therapy and esophageal cancer. Cancer Control 2013;20:97-110. [Crossref] [PubMed]
42. National Cancer Institute. Radiation therapy for cancer. 2010.
43. Bradbury KE, Appleby PN, Key TJ. Fruit, vegetable, and fiber intake in relation to cancer risk: findings from the European Prospective Investigation into Cancer and Nutrition (EPIC). Am J Clin Nutr 2014;100:394S-8S. [Crossref] [PubMed]
44. Yamaji T, Inoue M, Sasazuki S, et al. Fruit and vegetable consumption and squamous cell carcinoma of the esophagus in Japan: the JPHC study. Int J Cancer 2008;123:1935-40. [Crossref] [PubMed]
45. Islami F, Kamangar F, Nasrollahzadeh D, et al. Oesophageal cancer in Golestan Province, a high-incidence area in northern Iran - a review. Eur J Cancer. 2009;45:3156-65. [Crossref] [PubMed]
46. Islami F, Pourshams A, Nasrollahzadeh D, et al. Tea drinking habits and oesophageal cancer in a high risk area in northern Iran: population based case-control study. BMJ 2009;338:b929. [Crossref] [PubMed]
47. Holmes RS, Vaughan TL. Epidemiology and pathogenesis of esophageal cancer. Semin Radiat Oncol 2007;17:2-9. [Crossref] [PubMed]
48. Dong LM, Kristal AR, Peters U, et al. Dietary supplement use and risk of neoplastic progression in esophageal adenocarcinoma: a prospective study. Nutr Cancer 2008;60:39-48. [Crossref] [PubMed]
49. Thompson CL, Khiani V, Chak A, et al. Carbohydrate consumption and esophageal cancer: an ecological assessment. Am J Gastroenterol 2008;103:555-61. [Crossref] [PubMed]
50. Mao N, Nie S, Hong B, et al. Association between alcohol dehydrogenase-2 gene polymorphism and esophageal cancer risk: a meta-analysis. World J Surg Oncol 2016;14:191. [Crossref] [PubMed]
51. Vaughan TL, Davis S, Kristal A, et al. Obesity, alcohol, and tobacco as risk factors for cancers of the esophagus and gastric cardia: adenocarcinoma versus squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 1995;4:85-92. [PubMed]
52. Oze I, Matsuo K, Ito H, et al. Cigarette smoking and esophageal cancer risk: an evaluation based on a systematic review of epidemiologic evidence among the Japanese population. Jpn J Clin Oncol 2012;42:63-73. [Crossref] [PubMed]
53. Renehan AG, Tyson M, Egger M, et al. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 2008;371:569-78. [Crossref] [PubMed]
54. Chow WH, Blot WJ, Vaughan TL, et al. Body mass index and risk of adenocarcinomas of the esophagus and gastric cardia. J Natl Cancer Inst 1998;90:150-5. [Crossref] [PubMed]
55. Tsuda H, Sakamaki C, Tsugane S, et al. A prospective study of the significance of gene and chromosome alterations as prognostic indicators of breast cancer patients with lymph node metastases. Breast Cancer Res Treat 1998;48:21-32. [Crossref] [PubMed]
56. Green JA, Amaro R, Barkin JS. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. Dig Dis Sci 2000;45:2367-8. [Crossref] [PubMed]
57. Cook MB, Corley DA, Murray LJ, et al. Gastroesophageal reflux in relation to adenocarcinomas of the esophagus: a pooled analysis from the Barrett's and Esophageal Adenocarcinoma Consortium (BEACON). PLoS One 2014;9:e103508. [Crossref] [PubMed]
58. Chen Z, Ren Y, Du XL, et al. Incidence and survival differences in esophageal cancer among ethnic groups in the United States. Oncotarget 2017;8:47037-51. [Crossref] [PubMed]
59. Yu G, Dye BA, Gail MH, et al. The association between the upper digestive tract microbiota by HOMIM and oral health in a population-based study in Linxian, China. BMC Public Health 2014;14:1110. [Crossref] [PubMed]
60. Chen X, Winckler B, Lu M, et al. Oral microbiota and risk for esophageal squamous cell carcinoma in a high-risk area of China. PLoS One 2015;10:e0143603. [Crossref] [PubMed]
61. Nasrollahzadeh D, Malekzadeh R, Ploner A, et al. Variations of gastric corpus microbiota are associated with early esophageal squamous cell carcinoma and squamous dysplasia. Sci Rep 2015;5:8820. [Crossref] [PubMed]
62. Gao S, Li S, Ma Z, et al. Presence of Porphyromonas gingivalis in esophagus and its association with the clinicopathological characteristics and survival in patients with esophageal cancer. Infect Agent Cancer 2016;11:3. [Crossref] [PubMed]
63. Zhang SK, Guo LW, Chen Q, et al. Prevalence of human papillomavirus 16 in esophageal cancer among the Chinese population: a systematic review and meta-analysis. Asian Pac J Cancer Prev 2014;15:10143-9. [Crossref] [PubMed]
64. Sitas F, Egger S, Urban MI, et al. InterSCOPE study: Associations between esophageal squamous cell carcinoma and human papillomavirus serological markers. J Natl Cancer Inst 2012;104:147-58. [Crossref] [PubMed]
65. Halec G, Schmitt M, Egger S, et al. Mucosal alpha-papillomaviruses are not associated with esophageal squamous cell carcinomas: Lack of mechanistic evidence from South Africa, China and Iran and from a world-wide meta-analysis. Int J Cancer 2016;139:85-98. [Crossref] [PubMed]
66. Liu W, Snell JM, Jeck WR, et al. Subtyping sub-Saharan esophageal squamous cell carcinoma by comprehensive molecular analysis. JCI Insight 2016;1:e88755. [Crossref] [PubMed]
67. Mlombe Y, Dzamalala C, Chisi J, et al. Oesophageal cancer and Kaposi's sarcoma in Malawi: a comparative analysis. Malawi Med J 2009;21:66-8. [Crossref] [PubMed]
68. Kayamba V, Bateman AC, Asombang AW, et al. HIV infection and domestic smoke exposure, but not human papillomavirus, are risk factors for esophageal squamous cell carcinoma in Zambia: a case-control study. Cancer Med 2015;4:588-95. [Crossref] [PubMed]
69. McCormack VA, Menya D, Munishi MO, et al. Informing etiologic research priorities for squamous cell esophageal cancer in Africa: A review of setting-specific exposures to known and putative risk factors. Int J Cancer 2017;140:259-71. [Crossref] [PubMed]
70. Stein J, Connor S, Virgin G, et al. Anemia and iron deficiency in gastrointestinal and liver conditions. World J Gastroenterol 2016;22:7908-25. [Crossref] [PubMed]
71. Morita FH, Bernardo WM, Ide E, et al. Narrow band imaging versus lugol chromoendoscopy to diagnose squamous cell carcinoma of the esophagus: a systematic review and meta-analysis. BMC Cancer 2017;17:54. [Crossref] [PubMed]
72. Rankin SC, Taylor H, Cook GJ, et al. Computed tomography and positron emission tomography in the pre-operative staging of oesophageal carcinoma. Clin Radiol 1998;53:659-65. [Crossref] [PubMed]
73. Mansfield SA, El-Dika S, Krishna SG, et al. Routine staging with endoscopic ultrasound in patients with obstructing esophageal cancer and dysphagia rarely impacts treatment decisions. Surg Endosc 2017;31:3227-33. [Crossref] [PubMed]
74. Zhang L, Zhou Y, Cheng C, et al. Genomic analyses reveal mutational signatures and frequently altered genes in esophageal squamous cell carcinoma. Am J Hum Genet 2015;96:597-611. [Crossref] [PubMed]
75. Scarlata S, Fuso L, Lucantoni G, et al. The technique of endoscopic airway tumor treatment. J Thorac Dis 2017;9:2619-39. [Crossref] [PubMed]
76. Rustgi AK, El-Serag HB. Esophageal carcinoma. N Engl J Med 2014;371:2499-509. [Crossref] [PubMed]
77. Kuwano H, Nishimura Y, Oyama T, et al. Guidelines for diagnosis and treatment of carcinoma of the esophagus April 2012 edited by the Japan Esophageal Society. Esophagus 2015;12:1-30.
78. Sohda M, Kuwano H. Current status and future prospects for esophageal cancer treatment. Ann Thorac Cardiovasc Surg 2017;23:1-11. [Crossref] [PubMed]
79. Sancheti M, Fernandez F. Management of T2 esophageal cancer. Surg Clin North Am 2012;92:1169-78. [Crossref] [PubMed]
80. Kato H, Nakajima M. Treatments for esophageal cancer: a review. Gen Thorac Cardiovasc Surg 2013;61:330-5. [Crossref] [PubMed]
81. Gillison ML, Trotti AM, Harris J, et al. Radiotherapy plus cetuximab or cisplatin in human papillomavirus-positive oropharyngeal cancer (NRG Oncology RTOG 1016): a randomised, multicentre, non-inferiority trial. Lancet 2019;393:40-50. [Crossref] [PubMed]
82. Song Y, Li L, Ou Y, et al. Identification of genomic alterations in oesophageal squamous cell cancer. Nature 2014;509:91-5. [Crossref] [PubMed]
83. Hirsch JE. An index to quantify an individual’s scientific research output that takes into account the effect of multiple coauthorship. Scientometrics 2010;85:741-54. [Crossref]
84. Shanbhag VKL. Journal impact factor. Biomed J 2016;39:225. [Crossref] [PubMed]
85. van Eck NJ, Waltman L. Citation-based clustering of publications using CitNetExplorer and VOSviewer. Scientometrics 2017;111:1053-70. [Crossref] [PubMed]
86. Garfield E, Paris S, Stock WG. HistCiteTM: A software tool for informetric analysis of citation linkage. Information Wissenschaft und Praxis 2006;57:391-400.
87. Ishimaru S, Weppner J, Poxrucker A, et al. Shiny-an activity logging platform for Google Glass. In: 2014 ACM International Joint Conference on Pervasive and Ubiquitous Computing, UbiComp 2014. Association for Computing Machinery, Inc., 2014.
88. Aria M, Cuccurullo C. bibliometrix: An R-tool for comprehensive science mapping analysis. J Informetr 2017;11:959-75. [Crossref]
89. Wilkinson J. Bibliometrics and Research Evaluation: Uses and Abuses. Journal of Web Librarianship 2016;136:80. [Crossref]