REVIEW

Trends in Anorexia Nervosa Research: An Analysis of the Top 100 Most Cited Works Nir Lipsman1*, D. Blake Woodside2 & Andres M. Lozano1 1 2

Division of Neurosurgery, Department of Surgery, University Health Network, University of Toronto, Toronto, Canada Department of Psychiatry, University Health Network, University of Toronto, Toronto, Canada

Abstract Analysis of highly cited papers provides unique insights into the status of research in a given field. We sought to identify the top 100 most highly cited papers in the field of anorexia nervosa (AN). A free, publically accessible software was used to conduct an online search of publications with accompanying citation data. Search terms were selected to focus on papers dealing predominantly with AN, and the results manually screened to exclude out-of-scope publications. Papers in bulimia nervosa, eating disorder not otherwise specified and binge-eating disorder, were not included. The top 100 most highly cited papers in the AN field were identified. Of these, 34 garnered greater than 400 citations, classifying them as ‘citation classics’. These works were divided into five categories, those dealing with epidemiological trends, medical/psychiatric comorbidities, treatment, mechanisms of disease and measurement/classification. Publications examining the epidemiology and underlying mechanisms of AN account for the majority of the top 100 papers. Scales and measurement tools have had the greatest impact, garnering the greatest number of average citations per paper. Although reasonably diverse, the top 100 papers highlight areas still lagging behind, including the neuroscience of AN as well as research into novel treatment strategies. Copyright © 2013 John Wiley & Sons, Ltd and Eating Disorders Association. Keywords citations; anorexia nervosa; epidemiology *Correspondence Nir Lipsman, Toronto Western Hospital, 399 Bathurst St. 4W-431, M5T 2S8. Email: [email protected] Published online 14 November 2013 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/erv.2270

Introduction The number of times a publication is cited can be an indication of its relative impact in a given field. A large number of citations implies that a publication is widely read and that others in the field view it as worthy of continued discussion. The fields of bibliometrics and citation analysis have been developed to understand and analyze trends in citations over time in specific fields. The term ‘Citation Classic’ refers to a publication that has been cited over 400 times (Garfield, 1987). An examination of the citation classics in a given medical field can provide both novice and experienced clinicians with a snapshot of works that are objectively viewed as particularly important (Ibrahim, Snead, Rutka, & Lozano, 2012; Lipsman & Lozano, 2012; Yang & Pan, 2006). It can also provide a sense of the relative size and breadth of a given domain. For example, we have previously shown that the field of major depression contains more than double the citation classics (243) than the entire field of neurosurgery (106) (Lipsman & Lozano, 2011; Ponce & Lozano, 2010). An analysis of highly cited works in anorexia nervosa (AN) has not yet been carried out and can be important for several reasons. Identifying such works helps shed light on where the field has been and more importantly, the direction it is headed. Such questions may be important when determining, for example, areas of unmet needs and allocating research funds. A list of highly cited papers is also of significant educational value for both new and experienced

researchers and clinicians who want to learn about the current state of AN literature. Here too, one can identify at a glance, relative areas of strength and weakness and where additional work needs to be carried out. Also, as in other compilations of citation classics, such lists convey a sense of the ‘types’ of papers that can have impact in one’s field. Our objective was to compile a list of those papers in the AN field deemed important by virtue of their number of citations. We expanded our list beyond the citation classics to include the top 100 given the relatively small size of the field. As genetic, neuroimaging, pre-clinical and clinical studies grow at an exponential rate, this list will certainly change, but in its current form will serve as a ‘snapshot’ of the present status of the field.

Methods To identify the top 100 most highly cited papers in AN, we used a publically accessible software that is available free for download online (Harzing’s Publish or Perish) (Harzing, 2007). We searched for all papers with the words ‘anorexia nervosa’, ‘anorexia’ and/or ‘eating disorders’ in the title, without date or other restrictions, and then sorted the results from largest number of citations to lowest. In order to identify the top 100, we manually examined each of the 150 top results and excluded those that were not relevant to our search. We excluded: (i) papers dealing solely with a condition

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that wasn’t AN, such as bulimia nervosa or eating disorder not otherwise specified. In papers where several eating disorders were discussed, we included publications where anorexia as a unique diagnosis was a major theme; (ii) papers that utilized the term anorexia in an unrelated context (e.g. anorexia as a symptom secondary to a medical condition) and (iii) books, manuals, non-peer reviewed published guidelines, patents or other non-biomedical publications. Our focus was exclusively on publications that dealt with AN as a distinct clinical entity. We included major reviews in our results, as these were viewed as potentially important means of synthesizing large amounts of information.

Results By using the previous strategy, we identified the top 100 most highly cited works in the field of AN. The number of citations ranged from 3046 for the top cited paper to 252 for the 100th (see Supplementary Table 1 for a complete list of the top 100). There were 34 ‘citation classics’, with over 400 citations, and these are listed in order in Table 1. A PubMed search using the term ‘Anorexia Nervosa’ yielded 12 004 results, suggesting that 0.3% of all papers in the AN field ultimately become ‘citation classics’. By comparison, 0.1% of papers in the major depression field are citation classics (Lipsman & Lozano, 2011). The journals that have published at least two top 100 papers are listed in Table 2. This list confirms the finding in our previous publication examining citation classics in major depression (Lipsman & Lozano, 2011), which most highly cited papers are published in specialty specific journals, rather than broad medical journals. In order to facilitate further analysis, we classified each paper as belonging to one of five broad categories: measurement/classification, epidemiology, mechanisms of disease, treatment and medical/ psychiatric. These categories allowed us to examine the relative trends of publication over time, as well which areas have previously been, and are currently, of particular interest. The number of papers in each category is shown in Figure 1a. Measurement/Classification This category included publications dealing with any aspect of AN assessment, including descriptions and classification of the illness or its subtypes, as well as measures of severity. Scales and interviews published in peer-reviewed journals were included, and indeed, accounted for a substantial proportion of ‘citation classics’ (25%). There were 14 papers in the top 100 in this category, including the top 4 most highly cited papers in the field, combining for almost 8000 citations. Epidemiology In this category, we included papers dealing predominantly with epidemiologic descriptions of AN, including measurements of prevalence, incidence and other population trends over time. There were 24 papers in this category including nine citation classics. Eight out of 24 papers dealt specifically with outcomes in AN, with three additional papers focusing on mortality trends. Four of the top 10 most highly cited papers in AN were in this category. 10

Mechanisms of disease Elucidating the mechanisms underlying AN symptoms is an area of significant research interest. Here, we included papers that examined or discussed theories of AN aetiology and/or maintenance, including family linkage analyses, genetic and heritability studies, biological theories, personality, as well as psychosocial and cultural factors. There were 35 papers in this category, the most of any, including eight citation classics. Fourteen out of 35 papers dealt explicitly with personality and/or cognitive-perceptual disturbances as potential contributing factors to AN pathophysiology. Two papers examined brain-based mechanisms, one reviewing hypothalamic-pituitary-adrenal disturbance and the other investigating serotonin metabolite levels in the cerebrospinal fluid of AN patients. Treatment This category included any paper that dealt exclusively with the management of AN, including the theoretical basis of therapeutic approaches, medication trials and long-term management outcomes. We also included papers dealing with the mitigation of risk factors as ways to treat AN. There were 12 papers in this category, the fewest of any category, although four papers were citation classics (4/12; 33%). Eight papers examined psychotherapeutic approaches, including three papers on family therapy and two papers examined the use of medications, including one, and the only, double-blind, placebo controlled medication trial. Medical/Psychiatric Anorexia nervosa is a complex illness that often sees patients straddle the border between psychiatric and medical complications. As a result, we included a category to address the medical and psychiatric corollaries of AN, including comorbidities and complications. There were 15 papers in this category, including four citation classics. Seven papers dealt with psychiatric comorbidities with an additional five dealing specifically with osteoporosis in AN. Figure 2 displays the number of top 100 papers published per year, beginning in 1874 with the oldest paper and ending in 2007 with the most recent. As shown also in Table 3, which displays the number of top 100 papers published per decade by category, there was a peak of productivity in the 1990s, with 41 papers published in that decade.

Discussion We have identified the top 100 cited works including 34 ‘citation classics’ in the AN field. Classifying these papers into categories allows us to highlight current and emerging trends and to answer the following questions. What types of papers are in the top 100? Publications examining the mechanisms of AN account for both the largest number of top 100 papers (35) and the highest number of total cumulative citations (12 939). A large minority of mechanism papers (14/35) dealt with personality factors contributing to and maintaining AN symptoms. Very few papers dealt with neurobiological factors, and only one examined the role of putative neurotransmitter dysfunction in AN. The relative paucity of papers addressing neuroanatomic-based and neurophysiological-based explanations for AN

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Table 1 Citation classics (>400 citations) in the field of anorexia nervosa Rank

Citations

Paper

Category

1

3046

Meas/Class

2

2295

3

1401

4

1099

5

1040

6

918

7

907

8

781

9 10

703 674

11

651

12

645

13

644

14

616

15 16

597 592

17 18

587 584

19

570

20

559

21

545

22

524

23

494

24

483

25

450

26

448

Garner DM, Olmsted MP, Polivy J. Development and validation of a multidimensional eating disorder inventory for anorexia nervosa and bulimia. Int J Eat Disord 1983; 2; 2: 15–34 Garner DM, Garfinkel PE. The Eating Attitudes Test: an index of the symptoms of anorexia nervosa. Psychol Med. 1979 May;9(2):273–279. Fairburn CG, Beglin SJ. Assessment of eating disorders: interview or self-report questionnaire? Int J Eat Disord. 1994 Dec;16(4):363–370. Cooper PJ, Taylor MJ, Cooper Z, Fairburn CG. The development and validation of the Body Shape Questionnaire. Int J Eat Disord. 1987 Jul; 6(4):484–494. Hudson JI, Hiripi E, Pope HG Jr, Kessler RC. The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biol Psychiatry. 2007 Feb 1;61(3):348–358. Fairburn CG, Cooper Z, Shafran R. Cognitive behaviour therapy for eating disorders: a “transdiagnostic” theory and treatment. Behav Res Ther. 2003 May;41(5):509–528. Hoek HW, van Hoeken D. Review of the prevalence and incidence of eating disorders. Int J Eat Disord. 2003 Dec;34(4):383–396. Steinhausen HC. The outcome of anorexia nervosa in the 20th century. Am J Psychiatry. 2002 Aug;159(8):1284–1293. Sullivan PF. Mortality in anorexia nervosa. Am J Psychiatry. 1995 Jul;152(7):1073–1074. Garner DM, Garfinkel PE. Socio-cultural factors in the development of anorexia nervosa. Psychol Med. 1980 Nov;10(4):647–656. Cooper Z, Fairburn C. The eating disorder examination: A semi-structured interview for the assessment of the specific psychopathology of eating disorders. Int J Eat Disord. 1987 Jan;6(1):1–8 Russell GF, Szmukler GI, Dare C, Eisler I. An evaluation of family therapy in anorexia nervosa and bulimia nervosa. Arch Gen Psychiatry. 1987 Dec;44(12):1047–1056. Bruch H. Perceptual and conceptual disturbances in anorexia nervosa. Psychosom Med. 1962 Mar-Apr;24:187–194. Strober M, Freeman R, Morrell W. The long-term course of severe anorexia nervosa in adolescents: survival analysis of recovery, relapse, and outcome predictors over 10–15 years in a prospective study. Int J Eat Disord. 1997 Dec;22(4):339–360. Gull WW. Anorexia Nervosa. Transactions of the clinical society of London. 1874 Morgan HG, Russell GF. Value of family background and clinical features as predictors of long-term outcome in anorexia nervosa: four-year follow-up study of 41 patients. Psychol Med. 1975 Nov;5(4):355–371. Polivy J, Herman CP. Causes of eating disorders. Annu Rev Psychol. 2002;53:187–213 Jacobi C, Hayward C, de Zwaan M, Kraemer HC, Agras WS. Coming to terms with risk factors for eating disorders: application of risk terminology and suggestions for a general taxonomy. Psychol Bull. 2004 Jan;130(1):19–65. Garfinkel PE, Moldofsky H, Garner DM. The heterogeneity of anorexia nervosa. Bulimia as a distinct subgroup. Arch Gen Psychiatry. 1980 Sep;37(9):1036–1040. Lucas AR, Beard CM, O’Fallon WM, Kurland LT. 50-year trends in the incidence of anorexia nervosa in Rochester, Minn.: a population-based study. Am J Psychiatry. 1991 Jul;148(7):917–922. Otto B, Cuntz U, Fruehauf E, Wawarta R, Folwaczny C, Riepl RL, Heiman ML, Lehnert P, Fichter M, Tschöp M. Weight gain decreases elevated plasma ghrelin concentrations of patients with anorexia nervosa. Eur J Endocrinol. 2001 Nov;145(5):669–673. Theander S. Anorexia nervosa. A psychiatric investigation of 94 female patients. Acta Psychiatr Scand Suppl. 1970;214:1–194. Crisp AH, Palmer RL, Kalucy RS. How common is anorexia nervosa? A prevalence study. Br J Psychiatry. 1976 Jun;128:549–554. Casper RC, Eckert ED, Halmi KA, Goldberg SC, Davis JM. Bulimia. Its incidence and clinical importance in patients with anorexia nervosa. Arch Gen Psychiatry. 1980 Sep;37(9):1030–1035. Fairburn CG, Cooper Z, Doll HA, Welch SL. Risk factors for anorexia nervosa: three integrated case–control comparisons. Arch Gen Psychiatry. 1999 May;56(5):468–476. Patton GC, Selzer R, Coffey C, Carlin JB, Wolfe R. Onset of adolescent eating disorders: population based cohort study over 3 years. BMJ. 1999 Mar 20;318(7186):765–768.

Meas/Class Meas/Class Meas/Class Epidem Treatment Epidem Epidem Epidem Mechanism Meas/Class

Treatment Mechanism Epidem

Meas/Class Epidem

Mechanism Mechanism

Meas/Class

Epidem Mechanism

Meas/Class Epidem Meas/Class Mechanism

Epidem

(Continues)

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Table 1 (Continued) Rank

Citations

27

447

28

447

29

444

30

443

31

439

32 33

433 422

34

404

Paper Rigotti NA, Nussbaum SR, Herzog DB, Neer RM. Osteoporosis in women with anorexia nervosa. N Engl J Med. 1984 Dec 20;311(25):1601–1606. Lilenfeld LR, Kaye WH, Greeno CG, Merikangas KR, Plotnicov K, Pollice C, Rao R, Strober M, Bulik CM, Nagy L. A controlled family study of anorexia nervosa and bulimia nervosa: psychiatric disorders in first-degree relatives and effects of proband comorbidity. Arch Gen Psychiatry. 1998 Jul;55(7):603–610. Halmi KA, Eckert E, Marchi P, Sampugnaro V, Apple R, Cohen J. Comorbidity of psychiatric diagnoses in anorexia nervosa. Arch Gen Psychiatry. 1991 Aug;48(8):712–718. Garner DM, Bemis J. A cognitive-behavioural approach to anorexia nervosa. Cognitive Therapy and Research 1982;6(2):123–150 Braun DL, Sunday SR, Halmi KA. Psychiatric comorbidity in patients with eating disorders. Psychol Med. 1994 Nov;24(4):859–867. Pike KM, Rodin J. Mothers, daughters, and disordered eating. J Abnorm Psychol. 1991 May;100(2):198–204. Kaye WH, Bulik CM, Thornton L, Barbarich N, Masters K. Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am J Psychiatry. 2004 Dec;161(12):2215–2221. Vitousek K, Watson S, Wilson GT. Enhancing motivation for change in treatment-resistant eating disorders. Clin Psychol Rev. 1998 Jun;18(4):391–420

Category Med/Psych Mechanism

Med/Psych

Treatment Med/Psych Mechanism Med/Psych Treatment

Epidem: epidemiology; Meas/Class: measurement and classification and Med/Psych: medical and psychiatric corollaries

may be explained by the traditional emphasis in the literature on psychological root-causes. In addition, advances in neuroscience, such as those in imaging, have occurred relatively recently, and so insufficient time may have passed for these publications to accumulate citations. Notably, however, 26% of publications in the top 100 were published between 2000 and 2007. As in other psychiatric disciplines, such as major depression (Lipsman & Lozano, 2011), methods of measurements, including scales and inventories, aggregate near the top of the list. Not only are these instruments widely read and used, but also their relative position indicates that the highest impact papers are those that seek to clarify the illness experience, classify its severity and understand its symptoms in a way that facilitates communication between researchers and clinicians. The value of these papers can be expressed in another way, if one divides the number of papers in each category by the total number of citations in that category, yielding an average ‘citations per paper’ score per category (Figure 1b). Doing so illustrates that although there are more than twice as many mechanisms than measurement papers in the top 100, the average citations per paper in the latter are more than double the former. Excluding the measurement category, the other categories are equally represented among the citation classics. Notably, however, there are as many papers dealing with outcomes and mortality in AN as there are in the entire ‘Treatment’ category. Therapeutic strategies, and particularly clinical trials, have yet to make an impact on the AN field, indicating this is an area ripe for further development. The relative paucity of papers in the ‘Treatment’ category suggests that further attention is warranted to the barriers preventing research in to treatment for AN. This might be seen as especially important given the relatively poor results from the treatment in terms of relapse and the development of chronicity. What are the publishing trends over time? Anorexia nervosa has been recognized for many years, with the first published reports emerging in the second half of the 19th 12

century (Vandereycken & van Deth, 1989). Analysis of the top 100 works indicates that the 1990s was the most productive time for AN research in the last century. Although it typically takes time for publications to accumulate citations, and certainly to become a citation classic, it is remarkable that 26 papers in the top 100 have been published since 2000, including four papers in the top 10, with one as recent as 2007. In keeping with the overall trend, most of the Top 100 papers published in the 2000s deal with epidemiological trends (seven papers) and mechanisms of disease (nine papers). These points underscore that the rate of citation accumulation over time may be as, if not more important, than the absolute number. For example, two papers with 300 citations may differ in relative impact if one was published 30 years ago (10 citations/year) and one was published 5 years ago (60 citations/yet). The rate at which a paper is cited hints at its relative impact and how valuable it is for others in the field. Among the top 100 there are four publications that exceed 90 citations/year, all citation classics, including one paper with greater than 170 citations per year. How do citation trends in anorexia nervosa compare with those in other fields? Although AN has among the highest mortality rate of any psychiatric illness, it remains a relatively small field (Hoek, 2006). In general, the number of citation classics is an indirect measure of a field’s size and breadth, as well as how active researchers are in that area. For example, 243 citation classics in the field of major depression can be contrasted with the 107 in the field of Parkinson’s Disease (Lipsman & Lozano, 2011; Ponce & Lozano, 2011). Such figures may reflect disease prevalence as well as research fund allocation. Among the top 100 papers in AN, we identified 34 citation classics, about a third of the total field of Parkinson’s Disease, and 14% of those in field of major depression. These differences are reflected also in the citation data of the most highly cited paper within each field. For example, the

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Table 2 Journals containing at least two top 100 papers

Journal International Journal of Eating Disorders Archives of General Psychiatry Psychological medicine American Journal of Psychiatry Journal of Clinical Endocrinology and Metabolism Journal of consulting and clinical psychology The New England journal of medicine Journal of the American Academy of Child and Adolescent Psychiatry British Medical Journal Behaviour research and therapy British Journal of Psychiatry Journal of abnormal psychology Cognitive Therapy and Research Clinical psychology review Biological psychiatry American Psychologist American journal of obstetrics and gynaecology Psychological Bulletin

Number of papers in top 100 13 12 8 8 4 4 3 3 3 3 3 2 2 2 2 2 2 2

Figure 2. Number of Top 100 papers published per year

Table 3 Top 100 papers by decade and by category Years Categories Epidem Meas/Class Mech Med/Psych Treatment Total

Trends in anorexia nervosa research: an analysis of the top 100 most cited works.

Analysis of highly cited papers provides unique insights into the status of research in a given field. We sought to identify the top 100 most highly c...
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