1 2 3 4 5 6 7 8 Q4 9 10 11 Q1 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 Q3 49 50 51 52 53 54 55
Surgery for Obesity and Related Diseases ] (2014) 00–00
Original article
Citation classics: Top 50 cited articles in bariatric and metabolic surgery Ali Aminian, M.D., Christopher R. Daigle, M.D., Stacy A. Brethauer, M.D., Philip R. Schauer, M.D.* Bariatric and Metabolic Institute, Cleveland Clinic, Cleveland, Ohio Received November 10, 2013; accepted December 12, 2013
Abstract
Background: The number of times an article has been cited reflects its influence in a specific field. The aim of this study was to identify and characterize the most highly cited articles published on bariatric and metabolic surgery. Methods: The 50 most frequently cited articles in bariatric and metabolic surgery were identified from the Scopus database in December 2013. Results: The median number of citations was 383.5 (range 275–2482). Most of the articles were published from 2000–2012 (n ¼ 35), followed by 1990–1999 (n ¼ 12), then before 1990 (n ¼ 3). These citation classics came from 8 countries, with the majority originating from the United States (n ¼ 34), followed by Sweden (n ¼ 4) and Australia (n ¼ 4). The 50 articles were published in 20 journals, led by New England Journal of Medicine (n ¼ 9) and Annals of Surgery (n ¼ 9). Only 10 of the articles were published in obesity-specific journals. The level of evidence of the 49 clinical publications and 1 animal study consisted of level I (n ¼ 5), II (n ¼ 11), III (n ¼ 9), IV (n ¼ 19), and V (n ¼ 6). Meta-analyses were 16% of the total citations. Metabolic (n ¼ 12) and survival (n ¼ 6) effects of surgery were among the most common fields of study. Conclusion: Extending from the early 1950s through the voluminous growth period of the early 2000s, the field of bariatric and metabolic surgery led to the emergence of many top-cited scientific articles. These articles have provided the scientific basis for the only currently effective treatment for severe obesity. Articles published in high-impact journals, innovative observational studies, metaanalyses, survival analyses, and research on postoperative metabolic changes are most likely to be cited in the field of bariatric surgery. (Surg Obes Relat Dis 2014;]:00–00.) r 2014 American Society for Metabolic and Bariatric Surgery. All rights reserved.
Keywords:
Bariatric surgery; Metabolic surgery; Morbid obesity; Weight loss; Citation; Citation classics; Reference; Gastric bypass; Sleeve; Gastric band; Gastroplasty
In scientific literature, a citation is reference to a specific book or article previously published on the subject being discussed. One barometer of the success of a manuscript is the number of citations it has garnered; the number of times an article has been cited typically reflects its influence in a This study was presented at Obesity Week 2013. * Correspondence: Philip R. Schauer, M.D., Bariatric and Metabolic Institute, Cleveland Clinic, 9500 Euclid Avenue, M61, Cleveland, OH 44195. E-mail: [email protected]
specific field. Scientific and biomedical journals are evaluated by their “ impact factor”, a numerical value that is driven by overall numbers of citations, and journals aim to attract manuscripts with high citation potential. The study of these associations aims to not only gauge the success of individuals or institutions, but also to aid in the exploration of the evolution of peer-reviewed opinion in a given field or specialty [1,2]. There have been numerous publications listing “classic” or “top” citations in various medical fields [1–7]. Many
http://dx.doi.org/10.1016/j.soard.2013.12.021 1550-7289/r 2014 American Society for Metabolic and Bariatric Surgery. All rights reserved.
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surgical specialties, including general surgery [1], now have top citation publications addressing influential works in their respective fields. To our knowledge, no such assessment exists in the field of bariatric and metabolic surgery, which has its roots in the early 1950s with the first report of a jejunoileal bypass for severe obesity [8]. Obesity surgery is currently one of the most studied fields in surgery, especially since the groundbreaking realization that bariatric surgery has the potential to cure diabetes and metabolic syndrome. Obesity surgery has gone through many changes in its turbulent history; an understanding of the evolution of current opinion has enormous value. The aim of this study was to identify and characterize the most highly cited articles published on bariatric and metabolic surgery. Methods The 50 most frequently cited articles in bariatric and metabolic surgery were identified from the Scopus database in December 2013 using the following key words, both alone and in combination: bariatric, metabolic surgery, diabetes surgery, gastric bypass, gastric banding, sleeve, obesity, morbid obesity, weight loss, intestinal bypass, jejunoileal bypass, ileal bypass, gastric stapling, and gastroplasty. Articles were ranked based on number of citations and then year of publication if 2 or more articles had the same number of citations. Articles were reviewed for several characteristics including number of citations, year of publication, authorship, country of origin, journal source, field of study, and level of evidence. The level of evidence of each article was determined based on criteria published by the Oxford Centre for Evidence–Based Medicine [9]. To account for the time bias that is inherent to bibliometric studies, we calculated average citations per year values (with reference to the year 2013) for all publications obtained from our Scopus query. Because a simple assessment of absolute citation values may favor older papers (more time to procure citations) and risks excluding more recent influential publications. Results Table 1 lists the 50 most frequently cited bariatric surgery articles. The median number of citations was 383.5 (range 275–2482). Five papers were cited 41000 times. The highest number of citations belonged to Buchwald’s landmark meta-analysis [10]. Four articles reported the results of the Swedish Obese Subject (SOS) trial [11–14]. The oldest article was published in 1967 and the most recent in 2012. Most of the articles were published from 2000–2012 (n = 35), followed by 1990–1999 (n = 12), then before 1990 (n = 3). Eighteen (36%) articles were reported in the 3-year period of 2003–2005.
These citation classics came from 8 countries, with the 126 majority originating from the United States (n = 34), 127 followed by Sweden (n = 4), Australia (n = 4), Canada 128 (n = 3), France (n = 2), Italy (n = 1), the United Kingdom 129 (n = 1), and Belgium (n = 1). A total of 182 unique authors 130 contributed to these articles. Forty-four people coauthored 2 131 or more of the top-cited articles. The top 5 first authors, who 132 all had 41000 citations, were Buchwald H (n = 4374), 133 Sjostrom L (n = 2898), Schauer PR (n = 1634), Cummings 134 DE (n = 1296), and Pories WJ (n = 1164). Institutions in 135 the United States that had a major contribution were the 136 University of Minnesota, East Carolina University, the 137 University of Washington, the University of Pittsburgh, 138 Virginia Commonwealth University, the University of Utah, 139 the University of California, and the University of Iowa 140 Hospital. Among the academic centers outside the United 141 States, studies originating from Gothenburg University in 142 Sweden, Monash University in Australia, McGill University 143 in Canada, and University of Genoa in Italy were among the 144 top-cited articles. 145 The 50 articles were published in 20 journals, led by New 146 England Journal of Medicine (n = 9) and Annals of Surgery 147 (n = 9), followed by Obesity Surgery (n = 7), and Journal 148 of the American Medical Association (n = 5). Only 10 of 149 the articles were published in obesity specific journals. 150 Among the journals that cited 1 of these 50 articles as a 151 reference, Obesity Surgery and then Surgery for Obesity 152 and Related Diseases were at the top. 153 Of the 50 articles, 39 were clinical experience, 10 were 154 clinical review articles, and one was an experimental animal 155 study. Meta-analyses were 16% of the total citations. First 156 reports of gastric bypass (ranked #42) [15], vertical banded 157 gastroplasty (ranked #27) [16], duodenal switch (ranked 158 #30, 33) [17,18], and laparoscopic gastric bypass (ranked 159 #21) [19] were among the top-cited papers. The studies on 160 this list consisted of level I (n ¼ 5), II (n ¼ 11), III (n ¼ 9), 161 IV (n ¼ 19), and V (n ¼ 6) evidence. 162 Effect of surgery on co-morbidities (n ¼ 12, including 163 diabetes [n ¼ 10] and fatty liver [n ¼ 2]), survival benefit 164 of bariatric surgery (n ¼ 6), and perioperative complica- 165 tions (n ¼ 5) were among the most common fields of 166 study. “Metabolic surgery” was the main focus in only 167 14% of studies published before 2003. However, the rate 168 increased to 32% of studies published after that time. All 169 of the 6 mechanistic studies on the list that tried to 170 examine how bariatric surgery leads to weight loss and 171 improvement of co-morbidities were published between 172 2002 and 2009. 173 Table 2 ranks the top 10 articles based on the highest T2 174 average citations per year. Of note, this list includes 2 175 recent randomized clinical trials pertaining to “metabolic 176 surgery” and its effect on diabetes (ranked #1, 4) [20,21]. 177 Seven of the studies were published between 2007 and 178 2012. New England Journal of Medicine led the list with 7 179 articles. 180
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181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235
3
Table 1 Top 50 cited articles in bariatric and metabolic surgery Rank
First author
Title
Journal
Year
No. of citations
1 2 3
Buchwald, H. [10] Sjöström, L. [11] Sjöström, L. [12]
J. Am. Med. Assoc. New Engl. J. Med. New Engl. J. Med.
2004 2007 2004
2482 1464 1434
4 5
Cummings, D.E. [34] Pories, W.J. [30]
New Engl. J. Med. Ann. Surg.
2002 1995
1296 1164
6 7 8 9
Adams, T.D. [43] Schauer, P.R. [26] Maggard, M.A. [44] Christou, N.V. [45]
New Engl. J. Med. Ann. Surg. Ann. Intern. Med. Ann. Surg.
2007 2000 2005 2004
916 813 701 656
10
Buchwald, H. [37]
Am. J. Med.
2009
639
11
Nguyen, N.T. [28]
Ann. Surg.
2001
602
12
Dixon, J.B. [32]
J. Am. Med. Assoc.
2008
584
13 14
Schauer, P.R. [31] Wittgrove, A.C. [25]
Ann. Surg. Obes. Surg.
2003 2000
544 531
15 16 17
Grundy, S.M. [46] Santry, H.P. [47] Buchwald, H. [38]
Ann. Intern. Med. J. Am. Med. Assoc. New Engl. J. Med.
1991 2005 1990
509 500 494
18 19
Buchwald, H. [39] Cancello, R. [48]
Obes. Surg. Diabetes
2004 2005
436 427
20
DeMaria, E.J. [49]
Ann. Surg.
2002
391
21 22 23 24
Wittgrove, A.C. [19] Podnos, Y.D. [50] Steinbrook, R. [51] Sjöström, C.D. [13]
Obes. Surg. Arch. Surg. New Engl. J. Med. Obes. Res.
1994 2003 2004 1999
390 389 386 385
25 26
Scopinaro, N. [24] Dixon, J.B. [52]
World J. Surg. Hepatology
1998 2004
384 383
27 28
Mason, E.E. [16] Le Roux, C.W. [53]
Arch. Surg. Ann. Surg.
1982 2006
381 379
29
Higa, K.D. [27]
Obes. Surg.
2000
379
30 31
Hess, D.S. [17] Sugerman, H.J. [23]
Obes. Surg. Ann. Surg.
1998 1987
366 366
32
New Engl. J. Med.
2009
360
33 34
Flum, D.R. (LABS Consortium) [54] Marceau, P. [18] Chapman, A.E. [55]
Bariatric surgery: a systematic review and meta-analysis Effects of bariatric surgery on mortality in Swedish obese subjects Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus Long-term mortality after gastric bypass surgery Outcomes after laparoscopic Roux-en-Y gastric bypass for morbid obesity Meta-analysis: surgical treatment of obesity Surgery decreases long-term mortality, morbidity, and health care use in morbidly obese patients Weight and Type 2 diabetes after bariatric surgery: systematic review and meta-analysis Laparoscopic versus open gastric bypass: a randomized study of outcomes, quality of life, and costs Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial Effect of laparoscopic Roux-en-Y gastric bypass on Type 2 diabetes mellitus Laparoscopic gastric bypass, roux en-Y-500 patients: technique and results, with 3–60 month follow-up Gastrointestinal surgery for severe obesity Trends in bariatric surgical procedures Effect of partial ileal bypass surgery on mortality and morbidity from coronary heart disease in patients with hypercholesterolemia: report of the program on the surgical control of the hyperlipidemias (POSCH) Bariatric surgery worldwide 2003 Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgeryinduced weight loss Results of 281 consecutive total laparoscopic Roux-en-Y gastric bypasses to treat morbid obesity Laparoscopic gastric bypass, Roux-en-Y: Preliminary report of five cases Complications after laparoscopic gastric bypass: A review of 3464 cases Surgery for Severe Obesity Reduction in incidence of diabetes, hypertension and lipid disturbances after intentional weight loss induced by bariatric surgery: The SOS intervention study Biliopancreatic diversion Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss Vertical banded gastroplasty for obesity Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters Complications of the laparoscopic Roux-en-Y gastric bypass: 1,040 patients What have we learned? Biliopancreatic diversion with a duodenal switch A randomized prospective trial of gastric bypass versus vertical banded gastroplasty for morbid obesity and their effects on sweets versus nonsweets eaters Perioperative safety in the longitudinal assessment of bariatric surgery
World J. Surg. Surgery
1998 2004
356 339
35
Rubino, F. [33]
Ann. Surg.
2006
325
36
Buchwald, H. [40]
Obes. Surg.
2009
323
Biliopancreatic diversion with duodenal switch Laparoscopic adjustable gastric banding in the treatment of obesity: a systematic literature review The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes Metabolic/bariatric surgery worldwide 2008
236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290
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4
291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345
Table 1 Continued. Rank
First author
Title
Journal
Year
No. of citations
37
Faraj, M. [56]
J. Clin. Endocrinol. Metab.
2003
322
38
Flum, D.R. [57]
J. Am. Med. Assoc.
2005
320
39
318
2009
316
41
Regan, J.P. [29]
J. Gastrointest. Surg. Proc. Natl. Acad. Sci. U. S. A. Obes. Surg.
1997
40
MacDonald Jr. K.G. [36] Zhang, H. [35]
Plasma acylation-stimulating protein, adiponectin, leptin, and ghrelin before and after weight loss induced by gastric bypass surgery in morbidly obese subjects Early mortality among Medicare beneficiaries undergoing bariatric surgical procedures The gastric bypass operation reduces the progression and mortality of noninsulin-dependent diabetes mellitus Human gut microbiota in obesity and after gastric bypass
2003
315
42
Mason, E.E. [15]
1967
311
43 44
Flum, D.R. [58] Inge, T.H. [59]
Surg. Clin. North Am. J. Am. Coll. Surg. Pediatrics
2004 2004
308 294
45
Luyckx, F.H. [60]
Int. J. Obes.
1998
290
46
Karlsson, J. [14]
Int. J. Obes.
1998
290
47
Service, G.J. [61]
New Engl. J. Med.
2005
284
48 49
Brolin, R.E. [62] Schauer, P.R. [20]
J. Am. Med. Assoc. New Engl. J. Med.
2002 2012
278 277
50
O'Brien, P.E. [63]
Br. J. Surg.
1999
275
Early experience with two-stage laparoscopic Roux-en-Y Gastric bypass as an alternative in the super-super obese patient Gastric bypass in obesity Impact of gastric bypass operation on survival: a population-based analysis Bariatric surgery for severely overweight adolescents: concerns and recommendations Liver abnormalities in severely obese subjects: Effect of drastic weight loss after gastroplasty Swedish obese subjects (SOS) - An intervention study of obesity. Two-year follow-up of health-related quality of life (HRQL) and eating behavior after gastric surgery for severe obesity Hyperinsulinemic hypoglycemia with nesidioblastosis after gastric-bypass surgery Bariatric surgery and long-term control of morbid obesity Bariatric surgery versus intensive medical therapy in obese patients with diabetes Prospective study of a laparoscopically placed, adjustable gastric band in the treatment of morbid obesity
Discussion In our study, we identified, ranked and characterized the 50 top-cited publications in the field of bariatric and
metabolic surgery. This assessment offers, for the first time, invaluable insight into the evolution of popular opinion in a field, which has undergone considerable change over the years. It also serves to identify key authors, institutions, and
Table 2 Top 10 articles in bariatric and metabolic surgery based on average citations per year Rank
First author
Title
Journal
Year
1
Schauer, P.R. [20]
New Engl. J. Med.
2012
277
277
2
Buchwald, H. [10]
Bariatric surgery versus intensive medical therapy in obese patients with diabetes Bariatric surgery: a systematic review and meta-analysis
2004
2482
276
3 4
Sjöström, L. [11] Mingrone, G. [21]
J. Am. Med. Assoc. New Engl. J. Med. New Engl. J. Med.
2007 2012
1464 220
244 220
5
Buchwald, H. [37]
Am. J. Med.
2009
639
160
6
Sjöström, L. [12]
New Engl. J. Med.
2004
1434
159
7 8
Adams, T.D. [43] Cummings, D.E. [34]
New Engl. J. Med. New Engl. J. Med.
2007 2002
916 1296
153 118
9
Dixon, J.B. [32]
2008
584
117
10
Flum, D.R. (LABS Consortium) [54]
J. Am. Med. Assoc. New Engl. J. Med.
2009
360
90
Effects of bariatric surgery on mortality in Swedish obese subjects Bariatric surgery versus conventional medical therapy for type 2 diabetes Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery Long-term mortality after gastric bypass surgery Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial Perioperative safety in the longitudinal assessment of bariatric surgery
No. of citations
Average citations/yr
346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400
Citation Classics / Surgery for Obesity and Related Diseases ] (2014) 00–00
401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455
journals that have played an integral role in shaping bariatric surgery into the modern specialty it has become. Furthermore, it reveals the characteristics of articles that garner the most attention and summarizes current trends in a rapidly evolving field. The 50 top-cited articles in bariatric and metabolic surgery were cited between 275 and 2482 times. Generally, with increasing age, each paper has more time to be cited, but in this analysis, 2 thirds of the top-cited papers were reported after 2000. The period from 1998–2003 has been coined as the “Bariatric Revolution”, a period where bariatric case numbers (mainly gastric bypass) and public awareness increased dramatically [22]. This formative period led to a flurry of academic publications that have been instrumental in molding modern concepts in bariatric surgery, a phenomenon that is mirrored in this report. Many medical and surgical specialties have published top-citation articles in the past. The number of citations and times dominating reference tells us a lot about the academic timeline of that field. Brandt et al. [3] offered the top 100 cited obstetrics and gynecology papers, reporting a citation range of 312–1090 and 1980–1989 as the dominant period. In a recent report, the most cited urology paper had 2088 citations [4]. Tao et al. [5] published the top 50 cited articles on sepsis, a hot topic that affects all corners of medicine. The number of citations ranged from 372–2932, with a mean of 678 citations, and over 50% of the articles occurred after 1995 [5]. The most cited studies in the plastic surgery and burn literature had 1007 and 711 citations, respectively [6,7]. Recently, Yoon et al. [2] found a citation mean of 664.3 (range: 371–6931) in their assessment of the top 100 cited radiology publications; the most dominant decade was the 1990s [2]. The status of top-cited articles in bariatric surgery is rather impressive when you consider we are comparing a focused subspecialty to more general fields. Furthermore, the bariatric surgery publications listed tend to be more current than other top-citation studies. The presented list of citation classics also reflects major advances in the history of bariatric and metabolic surgery. Mason and Ito [15] (ranked #42) initially described gastric bypass in the 1960s. In 1982, Mason [16] (ranked #27) explained the technique of vertical banded gastroplasty. In the first randomized clinical trial (RCT) on the list, Sugerman et al. [23] (ranked #31) compared gastric bypass and vertical banded gastroplasty. Scopinaro et al. [24] (ranked #25) reported long-term data on biliopancreatic diversion in 1998. In the same year, Hess and Hess [17] (ranked #30) and Marceau et al. [18] (ranked #33) reported the results of the duodenal switch variant. Wittgrove et al. [19] described the technique of laparoscopic gastric bypass in 5 cases in 1994 (ranked #21) and then Wittgrove and Clark [25] presented the data of 500 patients in 2000 (ranked #14). In the same year, Schauer et al. [26] (ranked #7) and Higa et al. [27] (ranked #29) published modified techniques of laparoscopic gastric bypass. A year later, an RCT by
5
Nguyen et al. [28] (ranked #11) compared open and laparoscopic gastric bypass. In 2003, Regan et al. [29] (ranked #41) reported a 2-stage laparoscopic approach in high-risk patients. In terms of metabolic effects of surgery, Pories et al. [30] (ranked #5) reported in their landmark 1995 paper entitled, “Who would have thought it? An operation proves to be the most effective therapy for adultonset diabetes mellitus” the remarkable effect of open gastric bypass on diabetes. Schauer et al. [31] (ranked #13) published similar antidiabetic results using a laparoscopic approach. In 2008, Dixon et al. [32] (ranked #12) reported the first RCT that clearly showed the superiority of surgical treatment of diabetes in morbidly obese patients over medical management. A recent RCT (ranked #49) confirmed the later findings [20]. In the only experimental study listed in the top 50 most cited articles, Rubino et al. [33] (ranked #35) described the weight-independent mechanism of diabetes improvement after bypassing a short segment of proximal intestine. Cummings et al. [34] (ranked #4) showed that gastric bypass is associated with suppressed appetite hormone (i.e., ghrelin). Zhang et al. [35] (ranked #40) studied human gut microbiota in obesity and after gastric bypass. Back in 1997, MacDonald et al. [36] (ranked #39) reported on the survival benefit of gastric bypass. Without a doubt, Buchwald H had a fundamental influence in bariatric surgical literature with 4374 citations and first-authorship in 5 of the top papers (ranked #1, 10, 17, 18, 36; 4 of them were review papers) [10,37–40]. His landmark meta-analysis (ranked #1), which is among the most highly cited articles in general surgery with 2482 citations, comprehensively analyzed the effect of bariatric surgery on weight and co-morbidities for the first time [10]. The major limitation of this review, however, was the absence of high quality studies at that time (only 5 of 134 studies in the systematic review were RCTs). The SOS data, which is level II evidence by definition, was the source of almost 100 high quality studies, and 4 of them (ranked #2, 3, 24, 46) are among the top-cited papers on our list [11–14]. The SOS is an ongoing prospective intervention trial designed to investigate the effects of bariatric surgery on mortality (ranked #2) and multiple other objective endpoints (ranked #3, 24, 46). The surgically treated arm of SOS underwent gastric banding (n = 376), vertical banded gastroplasty (n = 1369), or gastric bypass (n = 265) operations [41]. Because 68% of the patients had an outdated procedure, 89% of all operations were done open, and several baseline risk factors were less favorable in the surgery group, the results of SOS may underestimate the true benefits of bariatric surgery. A relative paucity of studies with high-level evidence is seen on this list; only 30% of the studies provided level I or II evidence. This is inherent to research in the field of surgery. Conducting RCTs for comparison of surgical procedures head-to-head or for comparison of surgery with
456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510
6
511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565
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medical management is a challenging issue [42]. For example, the SOS study of the late 1980s was originally intended as an RCT but was rejected by the local ethics board because of concern of randomizing patients to surgical treatment, which at that time carried an estimated mortality risk of 1–2%. It proceeded as a nonrandomized matched controlled study that resulted in a much lower than expected perioperative mortality rate (0.25%) and ultimately a mortality risk reduction of 30% [41]. Notably, most classic studies that were published many years ago introduced a novel technique, presented the result of a new surgical intervention in a small case series, or performed a comprehensive review for the first time. Although they are not categorized as high-level evidence studies, one cannot ignore the enormous effect they had in the advancement of bariatric surgery. It is no surprise that meta-analysis and review articles accounted for a high proportion (20%) of the list, which is a common finding in top citation assessments for any medical specialty. Authors frequently cite such publications as they convey outcome generalities of many different single site studies. It should be noted that citation credit for these publications should also go to the many “anonymous” investigators who conducted the studies and contributed the data, in addition to the authors who organized and wrote the meta-analysis and review papers. In terms of study topics, reports on perioperative safety of surgery, effects of surgery on obesity-related co-morbidities (including diabetes and fatty liver), and long-term survival benefit of surgical weight loss were among the hot topics in this history of bariatric surgery. While the major theme of early publications was surgical treatment of “obesity”, a trend toward “metabolic surgery” was prominent in studies published after 2003. Concurrently, The American Society for Bariatric Surgery changed its name to the American Society for Metabolic and Bariatric Surgery in 2007 to reflect mounting evidence that showed bariatric surgery can treat metabolic disease including diabetes, hypertension, dyslipidemia, and fatty liver disease. The present methodology does have limitations. Remarkably, many influential surgeons and scientists have not been mentioned here. Unfortunately, this short list fails to reveal their contributions to the development of bariatric and metabolic surgery in the past 60 years. Despite a meticulous search in the Scopus database, there is a chance that some studies have been missed. In addition, analysis in other database platforms such as Thomson Reuters (ISI) Web of Knowledge may lead to a different list. The first known article by Kremen et al. [8] on surgery to elicit weight loss is an obvious omission from the list. Furthermore, articles describing results of extinct procedures like jejunoileal bypass and horizontal gastroplasty were insufficiently cited to make this list, but were nonetheless important in the development of bariatric surgery. Similarly, the current list does not include recently published high quality studies, a
limitation which is related to the effect of time on citations. For example, while the Mingrone et al. [21] trial had 220 citations in 1 year after publication in 2012, it is not on the top 50 list. However, we could minimize the effect of time with the assessment of average citations per year. Obviously, this is a dynamic list that will change over time and eventually include more high-level evidence studies. Conclusion These landmark articles, according to citation rank, catalogue a pivotal portion of the storied and fascinating history of bariatric/metabolic surgery, a relatively new field of the late 20th and early 21st century. The authors and investigators have directly and positively affected the lives of millions of people worldwide suffering from severe obesity, a dreadful disease of modern times for which there currently is no medical treatment of sufficient efficacy. Furthermore, through these articles and studies, the authors have contributed to much of our understanding of the pathophysiology of the disease of obesity and its co-morbidities, especially type 2 diabetes. Contrary to prior beliefs, these articles and others have shown us that the gut plays a much more important role in obesity, weight regulation, and metabolic disease. Better medical and surgical treatments are likely to result from this body of knowledge. The bariatric surgery revolution of the early 2000s led to the emergence of many (if not most) of the top-cited articles. In a relatively brief period, the interest in bariatric surgery has spread much beyond its specialty boundary as evidenced by publications and citations in high impact, general medical journals. Articles published in high-impact journals, innovative observational studies, meta-analyses, survival analyses, and research on postoperative metabolic changes are most likely to be cited in the field of bariatric surgery. The presented list provides surgical educators, surgical residency program directors, and bariatric fellowship directors with a group of classic articles that can be included in didactic sessions for trainees. Furthermore, all surgeons who claim expertise in bariatric surgery should have a working knowledge of these important contributions to the relatively nascent field of bariatric and metabolic surgery. Disclosures ■■■ References [1] Paladugu R, Schein M, Gardezi S, Wise L. One hundred citation classics in general surgical journals. World J Surg 2002;26:1099–105. [2] Yoon DY, Yun EJ, Ku YJ, et al. Citation classics in radiology journals: the 100 top-cited articles, 1945–2012. AJR Am J Roentgenol 2013;201:471–81. [3] Brandt JS, Downing AC, Howard DL, Kofinas JD, Chasen ST. Citation classics in obstetrics and gynecology: the 100 most
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7
[27] Higa KD, Boone KB, Ho T. Complications of the laparoscopic Rouxen-Y gastric bypass: 1,040 patients—what have we learned? Obes Surg 2000;10:509–13 [28] Nguyen NT, Goldman C, Rosenquist CJ, et al. Laparoscopic versus open gastric bypass: a randomized study of outcomes, quality of life, and costs. Ann Surg 2001;234:279–91. [29] Regan JP, Inabnet WB, Gagner M, Pomp A. Early experience with two-stage laparoscopic Roux-en-Y gastric bypass as an alternative in the super-super obese patient. Obes Surg 2003;13:861–4. [30] Pories WJ, Swanson MS, MacDonald KG, et al. Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg 1995;222:339–52. [31] Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en-Y gastric bypass on type 2 diabetes mellitus. Ann Surg 2003;238:467–85. [32] Dixon JB, O'Brien PE, Playfair J, et al. Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA 2008;299:316–23. [33] Rubino F, Forgione A, Cummings DE, et al. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg 2006;244:741–9. [34] Cummings DE, Weigle DS, Scott Frayo R, et al. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 2002;346:1623–30. [35] Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 2009;106: 2365–70. [36] MacDonald KG Jr, Long SD, Swanson MS, et al. The gastric bypass operation reduces the progression and mortality of non-insulindependent diabetes mellitus. J Gastrointest Surg 1997;1:213–20. [37] Buchwald H, Estok R, Fahrbach K, et al. Weight and Type 2 Diabetes after Bariatric Surgery: Systematic Review and Meta-analysis. Am J Med 2009;122:248–56. [38] Buchwald H, Varco RL, Matts JP, et al. Effect of partial ileal bypass surgery on mortality and morbidity from coronary heart disease in patients with Hypercholesterolemia: Report of the program on the surgical control of the Hyperlipidemias (POSCH). N Engl J Med 1990;323:946–55. [39] Buchwald H, Williams SE. Bariatric surgery worldwide 2003. Obes Surg 2004;14:1157–64. [40] Buchwald H, Oien DM. Metabolic/bariatric surgery worldwide 2008. Obes Surg 2009;19:1605–11. [41] Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med 2013;273:219–34. [42] Shukla AP, Moreira M, Dakin G, et al. Medical versus surgical treatment of type 2 diabetes: the search for level 1 evidence. Surg Obes Relat Dis 2012;8:476–82. [43] Adams TD, Gress RE, Smith SC, et al. Long-term mortality after gastric bypass surgery. N Engl J Med 2007;357:753–61. [44] Maggard MA, Shugarman LR, Suttorp M, et al. Meta-analysis: Surgical treatment of obesity. Ann Intern Med 2005;142:547–59. [45] Christou NV, Sampalis JS, Liberman M, et al. Surgery decreases long-term mortality, morbidity, and health care use in morbidly obese patients. Ann Surg 2004;240:416–24. [46] Grundy SM, Barondess JA, Bellegie NJ, et al. Gastrointestinal surgery for severe obesity. Ann Intern Med 1991;115:956–61. [47] Santry HP, Gillen DL, Lauderdale DS. Trends in bariatric surgical procedures. JAMA 2005;294:1909–17. [48] Cancello R, Henegar C, Viguerie N, et al. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 2005;54:2277–86.
676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730
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Original article
Citation classics: Top 50 cited articles in bariatric and metabolic surgery Ali Aminian, M.D., Christopher R. Daigle, M.D., Stacy A. Brethauer, M.D., Philip R. Schauer, M.D.* Bariatric and Metabolic Institute, Cleveland Clinic, Cleveland, Ohio Received November 10, 2013; accepted December 12, 2013
Abstract
Background: The number of times an article has been cited reflects its influence in a specific field. The aim of this study was to identify and characterize the most highly cited articles published on bariatric and metabolic surgery. Methods: The 50 most frequently cited articles in bariatric and metabolic surgery were identified from the Scopus database in December 2013. Results: The median number of citations was 383.5 (range 275–2482). Most of the articles were published from 2000–2012 (n ¼ 35), followed by 1990–1999 (n ¼ 12), then before 1990 (n ¼ 3). These citation classics came from 8 countries, with the majority originating from the United States (n ¼ 34), followed by Sweden (n ¼ 4) and Australia (n ¼ 4). The 50 articles were published in 20 journals, led by New England Journal of Medicine (n ¼ 9) and Annals of Surgery (n ¼ 9). Only 10 of the articles were published in obesity-specific journals. The level of evidence of the 49 clinical publications and 1 animal study consisted of level I (n ¼ 5), II (n ¼ 11), III (n ¼ 9), IV (n ¼ 19), and V (n ¼ 6). Meta-analyses were 16% of the total citations. Metabolic (n ¼ 12) and survival (n ¼ 6) effects of surgery were among the most common fields of study. Conclusion: Extending from the early 1950s through the voluminous growth period of the early 2000s, the field of bariatric and metabolic surgery led to the emergence of many top-cited scientific articles. These articles have provided the scientific basis for the only currently effective treatment for severe obesity. Articles published in high-impact journals, innovative observational studies, metaanalyses, survival analyses, and research on postoperative metabolic changes are most likely to be cited in the field of bariatric surgery. (Surg Obes Relat Dis 2014;]:00–00.) r 2014 American Society for Metabolic and Bariatric Surgery. All rights reserved.
Keywords:
Bariatric surgery; Metabolic surgery; Morbid obesity; Weight loss; Citation; Citation classics; Reference; Gastric bypass; Sleeve; Gastric band; Gastroplasty
In scientific literature, a citation is reference to a specific book or article previously published on the subject being discussed. One barometer of the success of a manuscript is the number of citations it has garnered; the number of times an article has been cited typically reflects its influence in a This study was presented at Obesity Week 2013. * Correspondence: Philip R. Schauer, M.D., Bariatric and Metabolic Institute, Cleveland Clinic, 9500 Euclid Avenue, M61, Cleveland, OH 44195. E-mail: [email protected]
specific field. Scientific and biomedical journals are evaluated by their “ impact factor”, a numerical value that is driven by overall numbers of citations, and journals aim to attract manuscripts with high citation potential. The study of these associations aims to not only gauge the success of individuals or institutions, but also to aid in the exploration of the evolution of peer-reviewed opinion in a given field or specialty [1,2]. There have been numerous publications listing “classic” or “top” citations in various medical fields [1–7]. Many
http://dx.doi.org/10.1016/j.soard.2013.12.021 1550-7289/r 2014 American Society for Metabolic and Bariatric Surgery. All rights reserved.
56 57 58 59 60 61 62 63 64 65 66 67 68 69 70
2
71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 T1 116 117 118 119 120 121 122 123 124 125
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surgical specialties, including general surgery [1], now have top citation publications addressing influential works in their respective fields. To our knowledge, no such assessment exists in the field of bariatric and metabolic surgery, which has its roots in the early 1950s with the first report of a jejunoileal bypass for severe obesity [8]. Obesity surgery is currently one of the most studied fields in surgery, especially since the groundbreaking realization that bariatric surgery has the potential to cure diabetes and metabolic syndrome. Obesity surgery has gone through many changes in its turbulent history; an understanding of the evolution of current opinion has enormous value. The aim of this study was to identify and characterize the most highly cited articles published on bariatric and metabolic surgery. Methods The 50 most frequently cited articles in bariatric and metabolic surgery were identified from the Scopus database in December 2013 using the following key words, both alone and in combination: bariatric, metabolic surgery, diabetes surgery, gastric bypass, gastric banding, sleeve, obesity, morbid obesity, weight loss, intestinal bypass, jejunoileal bypass, ileal bypass, gastric stapling, and gastroplasty. Articles were ranked based on number of citations and then year of publication if 2 or more articles had the same number of citations. Articles were reviewed for several characteristics including number of citations, year of publication, authorship, country of origin, journal source, field of study, and level of evidence. The level of evidence of each article was determined based on criteria published by the Oxford Centre for Evidence–Based Medicine [9]. To account for the time bias that is inherent to bibliometric studies, we calculated average citations per year values (with reference to the year 2013) for all publications obtained from our Scopus query. Because a simple assessment of absolute citation values may favor older papers (more time to procure citations) and risks excluding more recent influential publications. Results Table 1 lists the 50 most frequently cited bariatric surgery articles. The median number of citations was 383.5 (range 275–2482). Five papers were cited 41000 times. The highest number of citations belonged to Buchwald’s landmark meta-analysis [10]. Four articles reported the results of the Swedish Obese Subject (SOS) trial [11–14]. The oldest article was published in 1967 and the most recent in 2012. Most of the articles were published from 2000–2012 (n = 35), followed by 1990–1999 (n = 12), then before 1990 (n = 3). Eighteen (36%) articles were reported in the 3-year period of 2003–2005.
These citation classics came from 8 countries, with the 126 majority originating from the United States (n = 34), 127 followed by Sweden (n = 4), Australia (n = 4), Canada 128 (n = 3), France (n = 2), Italy (n = 1), the United Kingdom 129 (n = 1), and Belgium (n = 1). A total of 182 unique authors 130 contributed to these articles. Forty-four people coauthored 2 131 or more of the top-cited articles. The top 5 first authors, who 132 all had 41000 citations, were Buchwald H (n = 4374), 133 Sjostrom L (n = 2898), Schauer PR (n = 1634), Cummings 134 DE (n = 1296), and Pories WJ (n = 1164). Institutions in 135 the United States that had a major contribution were the 136 University of Minnesota, East Carolina University, the 137 University of Washington, the University of Pittsburgh, 138 Virginia Commonwealth University, the University of Utah, 139 the University of California, and the University of Iowa 140 Hospital. Among the academic centers outside the United 141 States, studies originating from Gothenburg University in 142 Sweden, Monash University in Australia, McGill University 143 in Canada, and University of Genoa in Italy were among the 144 top-cited articles. 145 The 50 articles were published in 20 journals, led by New 146 England Journal of Medicine (n = 9) and Annals of Surgery 147 (n = 9), followed by Obesity Surgery (n = 7), and Journal 148 of the American Medical Association (n = 5). Only 10 of 149 the articles were published in obesity specific journals. 150 Among the journals that cited 1 of these 50 articles as a 151 reference, Obesity Surgery and then Surgery for Obesity 152 and Related Diseases were at the top. 153 Of the 50 articles, 39 were clinical experience, 10 were 154 clinical review articles, and one was an experimental animal 155 study. Meta-analyses were 16% of the total citations. First 156 reports of gastric bypass (ranked #42) [15], vertical banded 157 gastroplasty (ranked #27) [16], duodenal switch (ranked 158 #30, 33) [17,18], and laparoscopic gastric bypass (ranked 159 #21) [19] were among the top-cited papers. The studies on 160 this list consisted of level I (n ¼ 5), II (n ¼ 11), III (n ¼ 9), 161 IV (n ¼ 19), and V (n ¼ 6) evidence. 162 Effect of surgery on co-morbidities (n ¼ 12, including 163 diabetes [n ¼ 10] and fatty liver [n ¼ 2]), survival benefit 164 of bariatric surgery (n ¼ 6), and perioperative complica- 165 tions (n ¼ 5) were among the most common fields of 166 study. “Metabolic surgery” was the main focus in only 167 14% of studies published before 2003. However, the rate 168 increased to 32% of studies published after that time. All 169 of the 6 mechanistic studies on the list that tried to 170 examine how bariatric surgery leads to weight loss and 171 improvement of co-morbidities were published between 172 2002 and 2009. 173 Table 2 ranks the top 10 articles based on the highest T2 174 average citations per year. Of note, this list includes 2 175 recent randomized clinical trials pertaining to “metabolic 176 surgery” and its effect on diabetes (ranked #1, 4) [20,21]. 177 Seven of the studies were published between 2007 and 178 2012. New England Journal of Medicine led the list with 7 179 articles. 180
Citation Classics / Surgery for Obesity and Related Diseases ] (2014) 00–00
181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235
3
Table 1 Top 50 cited articles in bariatric and metabolic surgery Rank
First author
Title
Journal
Year
No. of citations
1 2 3
Buchwald, H. [10] Sjöström, L. [11] Sjöström, L. [12]
J. Am. Med. Assoc. New Engl. J. Med. New Engl. J. Med.
2004 2007 2004
2482 1464 1434
4 5
Cummings, D.E. [34] Pories, W.J. [30]
New Engl. J. Med. Ann. Surg.
2002 1995
1296 1164
6 7 8 9
Adams, T.D. [43] Schauer, P.R. [26] Maggard, M.A. [44] Christou, N.V. [45]
New Engl. J. Med. Ann. Surg. Ann. Intern. Med. Ann. Surg.
2007 2000 2005 2004
916 813 701 656
10
Buchwald, H. [37]
Am. J. Med.
2009
639
11
Nguyen, N.T. [28]
Ann. Surg.
2001
602
12
Dixon, J.B. [32]
J. Am. Med. Assoc.
2008
584
13 14
Schauer, P.R. [31] Wittgrove, A.C. [25]
Ann. Surg. Obes. Surg.
2003 2000
544 531
15 16 17
Grundy, S.M. [46] Santry, H.P. [47] Buchwald, H. [38]
Ann. Intern. Med. J. Am. Med. Assoc. New Engl. J. Med.
1991 2005 1990
509 500 494
18 19
Buchwald, H. [39] Cancello, R. [48]
Obes. Surg. Diabetes
2004 2005
436 427
20
DeMaria, E.J. [49]
Ann. Surg.
2002
391
21 22 23 24
Wittgrove, A.C. [19] Podnos, Y.D. [50] Steinbrook, R. [51] Sjöström, C.D. [13]
Obes. Surg. Arch. Surg. New Engl. J. Med. Obes. Res.
1994 2003 2004 1999
390 389 386 385
25 26
Scopinaro, N. [24] Dixon, J.B. [52]
World J. Surg. Hepatology
1998 2004
384 383
27 28
Mason, E.E. [16] Le Roux, C.W. [53]
Arch. Surg. Ann. Surg.
1982 2006
381 379
29
Higa, K.D. [27]
Obes. Surg.
2000
379
30 31
Hess, D.S. [17] Sugerman, H.J. [23]
Obes. Surg. Ann. Surg.
1998 1987
366 366
32
New Engl. J. Med.
2009
360
33 34
Flum, D.R. (LABS Consortium) [54] Marceau, P. [18] Chapman, A.E. [55]
Bariatric surgery: a systematic review and meta-analysis Effects of bariatric surgery on mortality in Swedish obese subjects Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus Long-term mortality after gastric bypass surgery Outcomes after laparoscopic Roux-en-Y gastric bypass for morbid obesity Meta-analysis: surgical treatment of obesity Surgery decreases long-term mortality, morbidity, and health care use in morbidly obese patients Weight and Type 2 diabetes after bariatric surgery: systematic review and meta-analysis Laparoscopic versus open gastric bypass: a randomized study of outcomes, quality of life, and costs Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial Effect of laparoscopic Roux-en-Y gastric bypass on Type 2 diabetes mellitus Laparoscopic gastric bypass, roux en-Y-500 patients: technique and results, with 3–60 month follow-up Gastrointestinal surgery for severe obesity Trends in bariatric surgical procedures Effect of partial ileal bypass surgery on mortality and morbidity from coronary heart disease in patients with hypercholesterolemia: report of the program on the surgical control of the hyperlipidemias (POSCH) Bariatric surgery worldwide 2003 Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgeryinduced weight loss Results of 281 consecutive total laparoscopic Roux-en-Y gastric bypasses to treat morbid obesity Laparoscopic gastric bypass, Roux-en-Y: Preliminary report of five cases Complications after laparoscopic gastric bypass: A review of 3464 cases Surgery for Severe Obesity Reduction in incidence of diabetes, hypertension and lipid disturbances after intentional weight loss induced by bariatric surgery: The SOS intervention study Biliopancreatic diversion Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss Vertical banded gastroplasty for obesity Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters Complications of the laparoscopic Roux-en-Y gastric bypass: 1,040 patients What have we learned? Biliopancreatic diversion with a duodenal switch A randomized prospective trial of gastric bypass versus vertical banded gastroplasty for morbid obesity and their effects on sweets versus nonsweets eaters Perioperative safety in the longitudinal assessment of bariatric surgery
World J. Surg. Surgery
1998 2004
356 339
35
Rubino, F. [33]
Ann. Surg.
2006
325
36
Buchwald, H. [40]
Obes. Surg.
2009
323
Biliopancreatic diversion with duodenal switch Laparoscopic adjustable gastric banding in the treatment of obesity: a systematic literature review The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes Metabolic/bariatric surgery worldwide 2008
236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290
A. Aminian et al. / Surgery for Obesity and Related Diseases ] (2014) 00–00
4
291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345
Table 1 Continued. Rank
First author
Title
Journal
Year
No. of citations
37
Faraj, M. [56]
J. Clin. Endocrinol. Metab.
2003
322
38
Flum, D.R. [57]
J. Am. Med. Assoc.
2005
320
39
318
2009
316
41
Regan, J.P. [29]
J. Gastrointest. Surg. Proc. Natl. Acad. Sci. U. S. A. Obes. Surg.
1997
40
MacDonald Jr. K.G. [36] Zhang, H. [35]
Plasma acylation-stimulating protein, adiponectin, leptin, and ghrelin before and after weight loss induced by gastric bypass surgery in morbidly obese subjects Early mortality among Medicare beneficiaries undergoing bariatric surgical procedures The gastric bypass operation reduces the progression and mortality of noninsulin-dependent diabetes mellitus Human gut microbiota in obesity and after gastric bypass
2003
315
42
Mason, E.E. [15]
1967
311
43 44
Flum, D.R. [58] Inge, T.H. [59]
Surg. Clin. North Am. J. Am. Coll. Surg. Pediatrics
2004 2004
308 294
45
Luyckx, F.H. [60]
Int. J. Obes.
1998
290
46
Karlsson, J. [14]
Int. J. Obes.
1998
290
47
Service, G.J. [61]
New Engl. J. Med.
2005
284
48 49
Brolin, R.E. [62] Schauer, P.R. [20]
J. Am. Med. Assoc. New Engl. J. Med.
2002 2012
278 277
50
O'Brien, P.E. [63]
Br. J. Surg.
1999
275
Early experience with two-stage laparoscopic Roux-en-Y Gastric bypass as an alternative in the super-super obese patient Gastric bypass in obesity Impact of gastric bypass operation on survival: a population-based analysis Bariatric surgery for severely overweight adolescents: concerns and recommendations Liver abnormalities in severely obese subjects: Effect of drastic weight loss after gastroplasty Swedish obese subjects (SOS) - An intervention study of obesity. Two-year follow-up of health-related quality of life (HRQL) and eating behavior after gastric surgery for severe obesity Hyperinsulinemic hypoglycemia with nesidioblastosis after gastric-bypass surgery Bariatric surgery and long-term control of morbid obesity Bariatric surgery versus intensive medical therapy in obese patients with diabetes Prospective study of a laparoscopically placed, adjustable gastric band in the treatment of morbid obesity
Discussion In our study, we identified, ranked and characterized the 50 top-cited publications in the field of bariatric and
metabolic surgery. This assessment offers, for the first time, invaluable insight into the evolution of popular opinion in a field, which has undergone considerable change over the years. It also serves to identify key authors, institutions, and
Table 2 Top 10 articles in bariatric and metabolic surgery based on average citations per year Rank
First author
Title
Journal
Year
1
Schauer, P.R. [20]
New Engl. J. Med.
2012
277
277
2
Buchwald, H. [10]
Bariatric surgery versus intensive medical therapy in obese patients with diabetes Bariatric surgery: a systematic review and meta-analysis
2004
2482
276
3 4
Sjöström, L. [11] Mingrone, G. [21]
J. Am. Med. Assoc. New Engl. J. Med. New Engl. J. Med.
2007 2012
1464 220
244 220
5
Buchwald, H. [37]
Am. J. Med.
2009
639
160
6
Sjöström, L. [12]
New Engl. J. Med.
2004
1434
159
7 8
Adams, T.D. [43] Cummings, D.E. [34]
New Engl. J. Med. New Engl. J. Med.
2007 2002
916 1296
153 118
9
Dixon, J.B. [32]
2008
584
117
10
Flum, D.R. (LABS Consortium) [54]
J. Am. Med. Assoc. New Engl. J. Med.
2009
360
90
Effects of bariatric surgery on mortality in Swedish obese subjects Bariatric surgery versus conventional medical therapy for type 2 diabetes Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery Long-term mortality after gastric bypass surgery Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial Perioperative safety in the longitudinal assessment of bariatric surgery
No. of citations
Average citations/yr
346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400
Citation Classics / Surgery for Obesity and Related Diseases ] (2014) 00–00
401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455
journals that have played an integral role in shaping bariatric surgery into the modern specialty it has become. Furthermore, it reveals the characteristics of articles that garner the most attention and summarizes current trends in a rapidly evolving field. The 50 top-cited articles in bariatric and metabolic surgery were cited between 275 and 2482 times. Generally, with increasing age, each paper has more time to be cited, but in this analysis, 2 thirds of the top-cited papers were reported after 2000. The period from 1998–2003 has been coined as the “Bariatric Revolution”, a period where bariatric case numbers (mainly gastric bypass) and public awareness increased dramatically [22]. This formative period led to a flurry of academic publications that have been instrumental in molding modern concepts in bariatric surgery, a phenomenon that is mirrored in this report. Many medical and surgical specialties have published top-citation articles in the past. The number of citations and times dominating reference tells us a lot about the academic timeline of that field. Brandt et al. [3] offered the top 100 cited obstetrics and gynecology papers, reporting a citation range of 312–1090 and 1980–1989 as the dominant period. In a recent report, the most cited urology paper had 2088 citations [4]. Tao et al. [5] published the top 50 cited articles on sepsis, a hot topic that affects all corners of medicine. The number of citations ranged from 372–2932, with a mean of 678 citations, and over 50% of the articles occurred after 1995 [5]. The most cited studies in the plastic surgery and burn literature had 1007 and 711 citations, respectively [6,7]. Recently, Yoon et al. [2] found a citation mean of 664.3 (range: 371–6931) in their assessment of the top 100 cited radiology publications; the most dominant decade was the 1990s [2]. The status of top-cited articles in bariatric surgery is rather impressive when you consider we are comparing a focused subspecialty to more general fields. Furthermore, the bariatric surgery publications listed tend to be more current than other top-citation studies. The presented list of citation classics also reflects major advances in the history of bariatric and metabolic surgery. Mason and Ito [15] (ranked #42) initially described gastric bypass in the 1960s. In 1982, Mason [16] (ranked #27) explained the technique of vertical banded gastroplasty. In the first randomized clinical trial (RCT) on the list, Sugerman et al. [23] (ranked #31) compared gastric bypass and vertical banded gastroplasty. Scopinaro et al. [24] (ranked #25) reported long-term data on biliopancreatic diversion in 1998. In the same year, Hess and Hess [17] (ranked #30) and Marceau et al. [18] (ranked #33) reported the results of the duodenal switch variant. Wittgrove et al. [19] described the technique of laparoscopic gastric bypass in 5 cases in 1994 (ranked #21) and then Wittgrove and Clark [25] presented the data of 500 patients in 2000 (ranked #14). In the same year, Schauer et al. [26] (ranked #7) and Higa et al. [27] (ranked #29) published modified techniques of laparoscopic gastric bypass. A year later, an RCT by
5
Nguyen et al. [28] (ranked #11) compared open and laparoscopic gastric bypass. In 2003, Regan et al. [29] (ranked #41) reported a 2-stage laparoscopic approach in high-risk patients. In terms of metabolic effects of surgery, Pories et al. [30] (ranked #5) reported in their landmark 1995 paper entitled, “Who would have thought it? An operation proves to be the most effective therapy for adultonset diabetes mellitus” the remarkable effect of open gastric bypass on diabetes. Schauer et al. [31] (ranked #13) published similar antidiabetic results using a laparoscopic approach. In 2008, Dixon et al. [32] (ranked #12) reported the first RCT that clearly showed the superiority of surgical treatment of diabetes in morbidly obese patients over medical management. A recent RCT (ranked #49) confirmed the later findings [20]. In the only experimental study listed in the top 50 most cited articles, Rubino et al. [33] (ranked #35) described the weight-independent mechanism of diabetes improvement after bypassing a short segment of proximal intestine. Cummings et al. [34] (ranked #4) showed that gastric bypass is associated with suppressed appetite hormone (i.e., ghrelin). Zhang et al. [35] (ranked #40) studied human gut microbiota in obesity and after gastric bypass. Back in 1997, MacDonald et al. [36] (ranked #39) reported on the survival benefit of gastric bypass. Without a doubt, Buchwald H had a fundamental influence in bariatric surgical literature with 4374 citations and first-authorship in 5 of the top papers (ranked #1, 10, 17, 18, 36; 4 of them were review papers) [10,37–40]. His landmark meta-analysis (ranked #1), which is among the most highly cited articles in general surgery with 2482 citations, comprehensively analyzed the effect of bariatric surgery on weight and co-morbidities for the first time [10]. The major limitation of this review, however, was the absence of high quality studies at that time (only 5 of 134 studies in the systematic review were RCTs). The SOS data, which is level II evidence by definition, was the source of almost 100 high quality studies, and 4 of them (ranked #2, 3, 24, 46) are among the top-cited papers on our list [11–14]. The SOS is an ongoing prospective intervention trial designed to investigate the effects of bariatric surgery on mortality (ranked #2) and multiple other objective endpoints (ranked #3, 24, 46). The surgically treated arm of SOS underwent gastric banding (n = 376), vertical banded gastroplasty (n = 1369), or gastric bypass (n = 265) operations [41]. Because 68% of the patients had an outdated procedure, 89% of all operations were done open, and several baseline risk factors were less favorable in the surgery group, the results of SOS may underestimate the true benefits of bariatric surgery. A relative paucity of studies with high-level evidence is seen on this list; only 30% of the studies provided level I or II evidence. This is inherent to research in the field of surgery. Conducting RCTs for comparison of surgical procedures head-to-head or for comparison of surgery with
456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510
6
511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565
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medical management is a challenging issue [42]. For example, the SOS study of the late 1980s was originally intended as an RCT but was rejected by the local ethics board because of concern of randomizing patients to surgical treatment, which at that time carried an estimated mortality risk of 1–2%. It proceeded as a nonrandomized matched controlled study that resulted in a much lower than expected perioperative mortality rate (0.25%) and ultimately a mortality risk reduction of 30% [41]. Notably, most classic studies that were published many years ago introduced a novel technique, presented the result of a new surgical intervention in a small case series, or performed a comprehensive review for the first time. Although they are not categorized as high-level evidence studies, one cannot ignore the enormous effect they had in the advancement of bariatric surgery. It is no surprise that meta-analysis and review articles accounted for a high proportion (20%) of the list, which is a common finding in top citation assessments for any medical specialty. Authors frequently cite such publications as they convey outcome generalities of many different single site studies. It should be noted that citation credit for these publications should also go to the many “anonymous” investigators who conducted the studies and contributed the data, in addition to the authors who organized and wrote the meta-analysis and review papers. In terms of study topics, reports on perioperative safety of surgery, effects of surgery on obesity-related co-morbidities (including diabetes and fatty liver), and long-term survival benefit of surgical weight loss were among the hot topics in this history of bariatric surgery. While the major theme of early publications was surgical treatment of “obesity”, a trend toward “metabolic surgery” was prominent in studies published after 2003. Concurrently, The American Society for Bariatric Surgery changed its name to the American Society for Metabolic and Bariatric Surgery in 2007 to reflect mounting evidence that showed bariatric surgery can treat metabolic disease including diabetes, hypertension, dyslipidemia, and fatty liver disease. The present methodology does have limitations. Remarkably, many influential surgeons and scientists have not been mentioned here. Unfortunately, this short list fails to reveal their contributions to the development of bariatric and metabolic surgery in the past 60 years. Despite a meticulous search in the Scopus database, there is a chance that some studies have been missed. In addition, analysis in other database platforms such as Thomson Reuters (ISI) Web of Knowledge may lead to a different list. The first known article by Kremen et al. [8] on surgery to elicit weight loss is an obvious omission from the list. Furthermore, articles describing results of extinct procedures like jejunoileal bypass and horizontal gastroplasty were insufficiently cited to make this list, but were nonetheless important in the development of bariatric surgery. Similarly, the current list does not include recently published high quality studies, a
limitation which is related to the effect of time on citations. For example, while the Mingrone et al. [21] trial had 220 citations in 1 year after publication in 2012, it is not on the top 50 list. However, we could minimize the effect of time with the assessment of average citations per year. Obviously, this is a dynamic list that will change over time and eventually include more high-level evidence studies. Conclusion These landmark articles, according to citation rank, catalogue a pivotal portion of the storied and fascinating history of bariatric/metabolic surgery, a relatively new field of the late 20th and early 21st century. The authors and investigators have directly and positively affected the lives of millions of people worldwide suffering from severe obesity, a dreadful disease of modern times for which there currently is no medical treatment of sufficient efficacy. Furthermore, through these articles and studies, the authors have contributed to much of our understanding of the pathophysiology of the disease of obesity and its co-morbidities, especially type 2 diabetes. Contrary to prior beliefs, these articles and others have shown us that the gut plays a much more important role in obesity, weight regulation, and metabolic disease. Better medical and surgical treatments are likely to result from this body of knowledge. The bariatric surgery revolution of the early 2000s led to the emergence of many (if not most) of the top-cited articles. In a relatively brief period, the interest in bariatric surgery has spread much beyond its specialty boundary as evidenced by publications and citations in high impact, general medical journals. Articles published in high-impact journals, innovative observational studies, meta-analyses, survival analyses, and research on postoperative metabolic changes are most likely to be cited in the field of bariatric surgery. The presented list provides surgical educators, surgical residency program directors, and bariatric fellowship directors with a group of classic articles that can be included in didactic sessions for trainees. Furthermore, all surgeons who claim expertise in bariatric surgery should have a working knowledge of these important contributions to the relatively nascent field of bariatric and metabolic surgery. Disclosures ■■■ References [1] Paladugu R, Schein M, Gardezi S, Wise L. One hundred citation classics in general surgical journals. World J Surg 2002;26:1099–105. [2] Yoon DY, Yun EJ, Ku YJ, et al. Citation classics in radiology journals: the 100 top-cited articles, 1945–2012. AJR Am J Roentgenol 2013;201:471–81. [3] Brandt JS, Downing AC, Howard DL, Kofinas JD, Chasen ST. Citation classics in obstetrics and gynecology: the 100 most
566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 Q5 610 611 612 613 614 615 616 617 618 619 620
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621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675
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[27] Higa KD, Boone KB, Ho T. Complications of the laparoscopic Rouxen-Y gastric bypass: 1,040 patients—what have we learned? Obes Surg 2000;10:509–13 [28] Nguyen NT, Goldman C, Rosenquist CJ, et al. Laparoscopic versus open gastric bypass: a randomized study of outcomes, quality of life, and costs. Ann Surg 2001;234:279–91. [29] Regan JP, Inabnet WB, Gagner M, Pomp A. Early experience with two-stage laparoscopic Roux-en-Y gastric bypass as an alternative in the super-super obese patient. Obes Surg 2003;13:861–4. [30] Pories WJ, Swanson MS, MacDonald KG, et al. Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg 1995;222:339–52. [31] Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en-Y gastric bypass on type 2 diabetes mellitus. Ann Surg 2003;238:467–85. [32] Dixon JB, O'Brien PE, Playfair J, et al. Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA 2008;299:316–23. [33] Rubino F, Forgione A, Cummings DE, et al. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg 2006;244:741–9. [34] Cummings DE, Weigle DS, Scott Frayo R, et al. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 2002;346:1623–30. [35] Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 2009;106: 2365–70. [36] MacDonald KG Jr, Long SD, Swanson MS, et al. The gastric bypass operation reduces the progression and mortality of non-insulindependent diabetes mellitus. J Gastrointest Surg 1997;1:213–20. [37] Buchwald H, Estok R, Fahrbach K, et al. Weight and Type 2 Diabetes after Bariatric Surgery: Systematic Review and Meta-analysis. Am J Med 2009;122:248–56. [38] Buchwald H, Varco RL, Matts JP, et al. Effect of partial ileal bypass surgery on mortality and morbidity from coronary heart disease in patients with Hypercholesterolemia: Report of the program on the surgical control of the Hyperlipidemias (POSCH). N Engl J Med 1990;323:946–55. [39] Buchwald H, Williams SE. Bariatric surgery worldwide 2003. Obes Surg 2004;14:1157–64. [40] Buchwald H, Oien DM. Metabolic/bariatric surgery worldwide 2008. Obes Surg 2009;19:1605–11. [41] Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med 2013;273:219–34. [42] Shukla AP, Moreira M, Dakin G, et al. Medical versus surgical treatment of type 2 diabetes: the search for level 1 evidence. Surg Obes Relat Dis 2012;8:476–82. [43] Adams TD, Gress RE, Smith SC, et al. Long-term mortality after gastric bypass surgery. N Engl J Med 2007;357:753–61. [44] Maggard MA, Shugarman LR, Suttorp M, et al. Meta-analysis: Surgical treatment of obesity. Ann Intern Med 2005;142:547–59. [45] Christou NV, Sampalis JS, Liberman M, et al. Surgery decreases long-term mortality, morbidity, and health care use in morbidly obese patients. Ann Surg 2004;240:416–24. [46] Grundy SM, Barondess JA, Bellegie NJ, et al. Gastrointestinal surgery for severe obesity. Ann Intern Med 1991;115:956–61. [47] Santry HP, Gillen DL, Lauderdale DS. Trends in bariatric surgical procedures. JAMA 2005;294:1909–17. [48] Cancello R, Henegar C, Viguerie N, et al. Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 2005;54:2277–86.
676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730
8
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[49] DeMaria EJ, Sugerman HJ, Kellum JM, Meador JG, Wolfe LG. Results of 281 consecutive total laparoscopic Roux-en-Y gastric bypasses to treat morbid obesity. Ann Surg 2002;235:640–7. [50] Podnos YD, Jimenez JC, Wilson SE, Stevens CM, Nguyen NT. Complications after laparoscopic gastric bypass: a review of 3464 cases. Arch Surg 2003;138:957–61. [51] Steinbrook R. Surgery for severe obesity. N Engl J Med 2004;350:1075–9. [52] Dixon JB, Bhathal PS, Hughes NR, O'Brien PE. Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss. Hepatology 2004;39:1647–54. [53] Le Roux CW, Aylwin SJB, Batterham RL, et al. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg 2006;243:108–14. [54] Flum DR, Belle SH, King WC, et al. Perioperative safety in the longitudinal assessment of bariatric surgery. N Engl J Med 2009;361:445–54. [55] Chapman AE, Kiroff G, Game P, et al. Laparoscopic adjustable gastric banding in the treatment of obesity: A systematic literature review. Surgery 2004;135:326–51. [56] Faraj M, Havel PJ, Phélis S, Blank D, Sniderman AD, Cianflone K. Plasma acylation-stimulating protein, adiponectin, leptin, and ghrelin before and after weight loss induced by gastric bypass surgery in
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