NEW HORIZONS IN NEUROLOGY
Neurology Research: A Journal Patrick W. Jamieson, MD ~~~~
~
There have been major changes in neurology research during the past decade, but no systematic examination of the content, methods, funding, and research personnel. All scientific articles in the journals Annals of Neurology, Archives of Neurology, and Neurology were categorized by article type, number of authors, highest degree of first author, institution, disease area, reseach field, and source of support for the years 1980 and 1990. Original articles grew by 54% over the decade. The average number of authors increased by 1.3 to 5 ( p > 0.0001). Groups of MDs and PhDs wrote 39% of articles in 1990 (24% in 1980).Contributions with a diagnostic or therapeutic focus rose from 7 to 1496, whereas there was a pronounced drop in case reports from nearly 40% to just under 20%. Articles on movement disorders and neurodegenerative diseases increased more than 100% and now together comprise more than 25% of original articles. Molecular biology increased by 1,600%, and there was significant growth in epidemiology, neuroimaging, neurochemistry, and neuropsychology. The top 20 publishing institutions accounted for 40% of all original articles and 60% of US original articles. Foreign contributions doubled over the decade. The National Institutes of Health funded 46% of US articles in 1 9 0 (35.5% in 1980). More than 80% of articles in 1990 on neurodegenerative disease were supported by the National Institutes of Health. The complexity of neurological research has driven greater collaboration between basic and clinical scientists. New areas of clinical and basic knowledge are rapidly emerging in neurology. Jamieson PW. Neurology research: a journal survey, 1980-1990. Ann Neurol 1992;32:87-93
The “Decade of the Brain” resolution looks forward to great changes anticipated in neuroscience research during the 1770s and challenges the neurological community to seek new treatments for debilitating neurological disorders [I, 2). It is interesting to see, in this context, how much change has occurred over the 1980s and to project what impact these changes might have on future neurological research. Examination of these changes is important for several reasons. First, it identifies expanding neurological subdisciplines in research output that likely are fertile ground for new breakthroughs. Second, it highlights methods that have increased in importance to neurological investigation. Last, it aids in the training of future neurological clinicians and researchers by defining growing areas of knowledge that will require special emphasis. The literature provides a mechanism to examine these changes. Space is very limited in the most widely read neurology journals, and the peer-review process permits the publication only of what the neurological community perceives as the most significant investigative work. Examining this archive from a macroscopic perspective can reveal changes in the nature and direction of clinical research.
Methods Articles from the following three most widely cited journals in neurology: Annals of Neurology (Annals),Archives of Neurology (Archives), and Neurology were examined for the years 1980 and 1990. All peer-reviewed articles were included, with the exception of letters, notes, and special articles not dealing with neurological research issues. Articles were classified as original articles, brief communications,or review articles, as listed by the journal. The disease class, principal research fields, number of authors, degree of first author, and composition of research team (all MD, all PhD, or mixed) were noted. The degree of the first author was not given for some articles in the 1980s and was listed as unknown in these cases. The number of pages for each article was computed and rounded to the next whole number when there were fractions of an article’s last page. The country, institution, and sex of the lead author was recorded. I t was impossible in many cases to determine the sex of the lead author from the name alone, especially in the instance of foreign authors. If a name had ambiguous gender or could not be classified, it was listed as unknown. The principal focus of a report was classified as diagnosis, treatment, case, or other type of scientific investigation. The secondary focus was recorded as review, additional observation (confirming previously published work), or new observation. An article could have more than one principal focus, specific
From the Department of Neurology, University of Kansas Medical Center, Kansas City, KS.
Address correspondence to Dr Jamieson, Department of Neurology, University of Kansas Medical Center, 39th and Rainbow Blvd, Kansas City, KS 66103.
Received Nov 7, 1991, and in revised form Jan 8 and Jan 31, 1992. Accepted for publication Feb 1, 1992.
Copyright 0 1992 by the American Neurological Association
87
Table 1. Basic Statistical Data for the Three Leading Neurology Journals
All Articles All Journals
Number of Articles Pages Average Article Length" Average Number of Authors Average Number of Sponsors Average Number of Institutions
1990 785 4,000
5.10 4.59
0.94 1.73
Original Articles 1980
1990
1080
657 3,096 4.7 1 3.29 0.78 1.34
594 3,326 5.60 4.93 1.06
384 2,241 5.84 3.64
1.78
1.41
0.98
"Article length is measured in pages
disease class, or major research field. All articles that studied three or fewer individuals or families were classified as case reports. Investigations were classified as principally prospective, retrospective,or unknown. Prospective studies were defined as those that collected new data or performed new laboratory analysis on previously collected pathological material. Retrospective studies, such as chart reviews, analyzed or reinterpreted previously collected data. For some studies the time line could not be determined and was listed as unknown.
The number of collaborating institutions and sources of support were determined for every article. Support for the work was ascertained by reviewing the credit and acknowledgment sections. The t statistic was computed when the means of two categories were compared for 1980 and 1990. A p value was determined from the t statistic.
Results Table 1 shows the number and size of articles for each year. Overall there was an approximately 209%increase in total articles (54% for original articles) and a 29% increase in pages (48% for original articles) from 1980. There was a decrease in the total article count in Archives from 1980 to 1990 because of a reduction in brief communcations, many of which were only a single page in 1980. The greatest growth occurred in Neurology, which showed a 63% increase in total articles (126% for original articles) and a 47% increase in number of pages (81% for original articles). Although the number of articles increased substantially, the size of articles remained nearly constant with a slight drop in the size of original contributions. There was a decrease in length by more than one page in original contributions for Neurology. The average number of authors for original articles increased by 1.3 to nearly 5 during the decade. This was statistically significant ( p > 0.0001). Table 2 gives a breakdown on the distribution of authorship. There was a significant decline in single- or double-authored publications and a pronounced jump in papers with five, six, or more authors. Table 2 also shows that slightly more than 14% of contributions in 1990 had either a diagnostic or thera-
88 Annals of Neurology Vol 32
No 1 July 1992
peutic focus. This percentage nearly doubled from 1780. There was a dramatic decline in case reports from nearly 40% of journal articles in 1980 to just under 20% in 1990. Little change occurred in the percentage of articles that made new observations versus additional observations. Fully 85% of research contributions made new observations to the literature. Most published neurological research continued to be retrospective, but prospective studies increased by 7 % over the decade. Table 3 depicts the percentage of original articles devoted to different disease areas. Two areas experienced remarkable growth over the last decade, rnovement disorders and neurodegenerative diseases. Both had more than 100% growth, and these areas combined now represent approximately one-fourth of all published original articles. Most other areas experienced either modest growth or declines. Neuromuscular disease represented the largest percentage of original publications both in 1980 and 1990. Table 4 depicts the major basic science field or neurology subspecialty used in the research. Clinical skills comprised slightly less than 20% of articles in 1990, a 69% increase from 1980. Epidemiology, neuroimaging, neurochemistry, and neuropsychology showed significant growth. The most spectacular increase occurred in molecular biology, which witnessed a nearly 1,600q) climb. The institutions publishing the most in these journals are shown in Table 5. Although several of these institutions have been consistent performers over the 1980s, others have risen dramatically in rank. Figure 1 shows the importance of these top institutions in research productivity as reported in the three journals surveyed. They now comprise 40% of all original articles and 60% of original US articles. This is up from 50% of US original articles 10 years ago. Figure 2 shows the breakdown of first-author investigators by sex and degree for all article types. There was an 8.8% decline in male MD investigators and a corresponding increase in the other categories. The biggest increases were in the categories of female M D
Table 2. Compodion of Article$ by Number and Percentage for 1980 and 1990 1990
5% in 1990
1980
% in 1980
37 74 154 522 787
4.7 9.4 19.6 66.3 100.0
15 33 26 1 356 66 5
2.3 5.0 39.2 53.5 100.0
47 73 785
6.0 84.7 9.3 100.0
30 568 59 65 7
4.6 86.5 9.0 100.0
Time Line Retrospective Prospective Unknownireview Total
407 322 56 785
51.8 41.0 7.1 100.0
406 220 31 657
61.8 33.5 4.7 100.0
Number of Authors (Original Articles) One Two Three Four Five Six or more Total
16 81 86 120 101 190 594
2.7 13.6 14.5 20.2 17.0 32.0 100.0
27 83 84 56 48 384
7.0 21.6 22.4 21.9 14.6 12.5 100.0
42 114 134 152 126 2 17 785
5.4 14.5 17.1 19.4 16.1 27.6 100.0
75 161 156 124 86 55 657
11.4 24.5 23.7 18.9 13.1 8.4 100.0
Principal Focus Diagnostic Therapeutic Case
Other Total Secondary Focus Review New observation Add observation Total
Number of Authors (All Articles) One Two Three Four
Five Six or more Total
66 5
86
Several articles were classified as having multiple principal types.
investigator (9.770, increase of 2.9%) and male PhD investigator (7.9%,increase of 2.6%). Physicians with an MD/PhD contributed 6.7% of the articles in 1990, which is in close proportion (8.0%) to their percentage in full-time academic neurology for 1985 [3]. There was a 14.7% decline in articles from authors who were all MDs and a corresponding increase in research teams with MDs and PhDs. Currently, 60% of articles are written by all MDs and 38.8% by mixed teams. More research teams are including individuals from several institutions, that is, 1.73 in 1990 versus 1.34 in 1980 ( p < 0.001) (Table 1). Foreign contributions doubled over the decade to equal one-third of original contributions in 1990 (see Fig 1). Table 6 shows the output of the top 10 foreign countries and their growth since the start of the decade. Canada, Japan, England, and Germany have increased their contributions markedly. There were no German original articles in 1980, and the Germans now rank third or fourth in published articles from
foreign countries. The growth in foreign articles has come mainly at the expense of the bottom 107 neurology programs, which saw their percentage of original articles fall from 41% in 1980 to 26% in 1990. Figure 3 demonstrates the impact of the National Institutes of Health ( N I H ) in funding neuroscience investigation. The N I H was credited as a funding agency in 46% of the published US articles in 1990. This figure is up from 33.5% in 1980. If an investigation had at least one source of support, N I H support was also present 79% of the time. The NIH supported 33% of original US articles. Other sources of support either showed modest gains or losses except the “other” category, which increased from 18.7 to 23.2(7. This category includes many private foundations, small and large. Drug company support was modest; cited support was only 2.0% of US work published in 1990. There was a statistically significant increase in the number of sponsors in 1990 from 1980 ( p = 0.0062; Table I). New Horizons: Jamieson: Research-A
Journal Survey 89
Table 3. Original Articles by Major Disease Area ~~
~
g,of Change Original Articles Cerebrovascular Demyelinating Disease Developmental Epilepsy General Neurology Headache Head Trauma Infectious Disease Metabolic Movement Disorders Neurodegenerative Neuromuscular Neurooncology Sleep Disorders Spinal Cord Total
1990 76
44 8 64 63
6 1 38 11 74 84 105 20
5 13 612
% in 1990"
1980
% in 1980"
12.4 7.2 1.3 10.5 10.3 1.0 0.2 6.2 1.8 12.1 13.7 17.2 3.3 0.8 2.1 100.0
40 48 14 36 71 3 5 20 7 23 19 75 18 5 6 390
10.3 12.3 3.6 9.2 18.2 0.8 1.3 5.1 1.8 5.9 4.9 19.2 4.6 1.3 1.5 100.0 ~~
1990/ 1980 21
- 42 - 64
13 - 43
27 - 87
21 0 105 182 - 11 - 29 - 36 38 0 ~~
~
-
aNote that articles could have more than one dlsease focus Percentage is based o n the total number of diseases
Table 4. Original Articles by Basic or Clinical Science Area'
9of Change Original Articles
1990
c/c in 1990b
1980
9in 1980b
199011980
~~
Biochemistry Cell Biology Clinical Epidemiology Immunology Modeling Moiecular Biology Neurochemistry Neuroendocrinology Neuroimaging Neuropathology Neuropharmacology Neuroph ysiology Neuropsychology Neuroophthalmology Therapeutics Total
16 2 126 47 62 2 26 32 1 78 48 27 66 44 19 38 634
2.5 0.3 19.9 7.4 9.8 0.3 4.1 5.0 0.2 12.3 7.6 4.3 10.4 6.9 3.0 6.0 100.0
"Articles could have more than one science area. bPercentage is based on the total number of diseases. NA
=
not applicable.
90 Annals of Neurology Vol 32 No 1 July 1992
29
6 48 15 37 0 1 15 1 34 57 31 66 21 17 28 406
7.1 1.5 11.8 3.7 9. I 0.0 0.2 3.7 0.2 8.4 14.0 7.6 16.3 5.2 4.2 6.9 100.0
65 -79 68 101
-
7
NA 1,565 37 - 36 47 - 46 - 44 - 36 34 - 28 - 13 0
Table 5. Rank of Domestic Institutions by Number of Original Publications
Top Twenty American Institutions in 1770 National Institutes of Health Harvard Columbia Johns Hopkins University Mayo Clinic Foundation UCLA UCSF University of Pennsylvania Baylor University of Michigan University of Texas Health University of Iowa New England Medical Center University of Washington University of Minnesota Yale UCSD University of Colorado University of Pittsburgh Duke Total
Number of Original Articles in 1770
Rank in 1780
32 30 20 18
1 2 23 12
16 16
3 3 6
14
7 7 7 8 8 8 7 7
7 6 6 6 6 242
7 7
1990
Foreign
1980
0Top Twenty US Insltlutions
Other US
Fig I . Number of original articles written by investigators at foreign institutions, top 20 US institutions, and other US institutions.
57 40 12
57 12 23
57 40 12 12 40
...
Institutions with the same number of original publications in 1980 are listed by the hghest rank for that number. UCLA = University of California, Los Angeles, CA; UCSF = University of California, San Francisco, CA; University of Texas Health = University of Texas Health Science Center at Houston, TX; UCSD = University of California, San Diego, La Jolla, CA. MBIeMD
FMlalsMD
MalsPhD
FmalePhD
Male MDPhD
US articles reporting no funding decreased from 52% in 1980 to 42% in 1990. US articles that reported one or two sources of funding increased from 39.7 to 46.2%. Thirteen percent of US articles in 1990 had three or more sources of support. Funding was quantified by field (not shown). There have been major increases in the percentage of publications supported by the N I H in cerebrovascular disease, infectious disease, neurodegenerative disease, and neurooncology. Elghty-one percent of articles dealing with neurodegenerative disease were supported by the NIH, and 92.5% of articles in this field received support from some source in 1990. This was much higher than that of the second highest supported field, demyelinating disease (71.4% of articles were supported). Discussion Although only a small percentage of the total output of clinical neurological research is published in the three leading neurology journals, it is likely this sample reflects underlying research trends. They reach the wid-
Female MDPhD
Fig 2. Percentage of articles written by dzperent author groups.
est audience of neurological clinicians. The average paid circulation of these journals is more than 13,000 copies, which is more than the entire membership of the American Academy of Neurology (AAN) (11,300) and nearly equal to the number of US physicians who identify neurology as their primary specialty (Ubel C , personal communication, 1991). High quality research is represented because the three leading clinical neuroscience journals publish fewer than one-third of submitted manuscripts [4, 51. However, it is possible they are not representative because there are many other neurology journals and forums for dissemination of research results. The current composition of articles may have been influenced by the growth of subspecialty and basic neuroscience journals. Additionally, articles of general neurological interest and significant clinical import are often published in general medical journals New Horizons: Jamieson: Research-A
Journal Survey 91
Table 6. Rank of Foreign Institutions lu, Number of Original Publications
Top Ten Foreign Countries
Number of Original Articles in 1990
Number of Original Articles in 1980
Canada Japan England Germany France Italy The Netherlands Australia Spain Belgium
33 21 23 23 21
11 7
16 13 7 6 4
6 2 2
~~~
5 0
4
0
5
% of Increase” 200 200 360 NA 425 167 550 250 NA - 20
~
aPercentage of increase is computed from base year of 1980.
NA = not applicable.
1
40
30
20
10
0 NIH
~~
VA
~
MDA
EDlleDSy
MS
PDF
ALS
ALL
MG
DrugCo
Ofher
~
Fig 3. Percentage of domestic articles w i t h support from various sponsors. Some articles bad multiple sources of support.
such as the New EngkzndJournal of Medicine. Nevertheless, the ability to reach the widest audience of neurological clinicians, the prestige of publishing in the most frequently cited journals, and the decline in general neurology articles make it likely that research trends derived from these journals are not artifacts. The nature of neurological research changed both qualitatively and quantitatively in the 1980-1990 decade. There is significantly more research being published by groups of five or more individuals and by groups that contain a mix of MDs and PhDs. There also is greater interaction among medical centers. This shift reflects the complexity of neuroscience investigation. Healy 161 wrote, “with more emphasis on career differentiation, the burden will shift to the academic 92 Annals of Neurology Vol 32 No I July 1992
institution to ensure interaction among basic research, clinical investigation, and practice . . . .” The changes in neurological research over the last 10 years support this view. The contribution of women is roughly parallel to their numbers in the specialty. Although females represented 14.6% of neurologists in 1986, unlike males they are disproportionately distributed with 80% being younger than 44 years of age. Many of these women are currently in training 181 and thus their total future academic contribution may be higher. The low percentage of publications dealing with diagnosis or therapy may seem unusual for clinical journals, but it confirms the “Inverse Practice Law” of Menken 191 which states there is an inverse likelihood of a publication being accepted based on its percentage of clinical content. Nevertheless, there was an increase over the decade in articles that used predominantly clinical skills (19.9% in 1990 vs. 11.8% in 1980), although there was a pronounced reduction, by 2076, in case reports. Petersdorf [lo] commented that “the research agenda of our medical centers surely requires modification to include health services research, outcome measures, clinical trials, and health care economics.” The AAN is committed to this type of research 1111. Possibly, research dealing with neurological care should receive greater priority. The striking increase in the published literature in molecular biology, epidemiology, neuroimaging, neuropsychology, and neurochemistry suggests if future clinicians are to make sense of the literature that neurology programs must change their emphasis. The clinician remains a key individual in neurogenetic research and patient counseling 1121. An understanding of neuroepidemiology is crucial to well-performed clinical trials [13]. The challenge will be to master these
newer areas while maintaining a strong emphasis on bedside observation and clinical care [14]. The three major US neurology journals have truly become international in the last decade. The increase in percentage of literature by foreign research organizations reflects both the prestige of these top neurology journals and the growing quality of foreign research programs. Active programs were instituted by the journals to solicit work from overseas and changes were made in the editorial boards to reflect more accurately the international character of neurological research (Asbury AK, personal communication, 1991). Growth of N I H sponsorship may reflect the doubling of the NIH budget in current dollars from 1982 to 1990 and a 40% increase in purchasing power 1151. Although there is a current feeling of a funding crisis in the biomedical community, similar discussions took place in 1980 [lb}.The N I H commands a record 8.8 billion dollar budget, which represents 40% of federal nondefense research and development funding [ 17, 18J Sharp increases in future federal support are unrealistic given the budgetary constraints imposed by other federal programs. It is unlikely that funding will be increasingly linked to perceptions of the public health value of new knowledge [19]. There are some interesting disparities between the frequency of neurological disease and neurological research publications. Patients with headache comprise 13% of new patients seen by UK neurologists 120) and 21% of US neurologists [21), but comprise only 1% of original article subjects. Patients with pain and Parkinson’s disease comprise approximately the same number of patients seen by neurologists (5%). The literature on Parkinson’s disease is voluminous. Articles about pain comprise less than 1% of published articles in the three neurology journals surveyed. Problems of conflict of interest and medical ethics have surfaced because of the growing importance of drug company sponsorship in research and clinical trials {22, 231. The relatively few studies that acknowledge drug company support suggest that this is currently a small problem in neurological research. The trends in neuroscience research strongly argue for increased training of new clinician investigators. Trainees will need greater exposure to basic science and rigorous formal coursework 1241. MD/PhD programs are successful at training and retaining clinicians for faculty roles [25}. It will be increasingly important for neurologists doing clinical research to work closely with their basic science counterparts. New types of programs that emphasize training in basic research will also be necessary to make the Decade of the Brain a reality.
This work was supported in part by a grant from the National Library of Medicine (Grant No. LM05074).
I thank Drs Dewey Ziegler, Stan Spurlin, Chi-Wan Lai, and Michael Giuliani for their helpful advice and criticism.
References 1. Goldstein M. The Decade of the Brain. Neurology 1990;40:321 2. Rosenberg RN,Rowland LP.The 1990s-Decade of the Brain: the need for a national priority. Neurology 1990;40:322 3. Griggs RC, Martin JB, Penn AS, et al. Training clinical neuroscientists. Ann Neurol 1987;21:197-201 4. Asbury AK. Message from the editor. Ann Neurol 1991;29:1 5. Daroff RB, Harik SI. Message from the editor’s office. Neurology 1990;40:1811 6. Healy B. Innovators for the 21st century: will we face a crisis in biomedical research brainpower? N Engl J Med 1988;319: 1058- 1064 7. Eiler MA, Pasko TJ. Specialty profiles. 1988 ed. Chicago: American Medical Association, 1988:562 8. Ringel SP. Neurologists-1990. Neurology 1991;41:18631866 9. Menken M. The practice of neurology. Arch Neurol 1990;47: 1173 10. Petersdorf RG. Remodeling the house of academe. JAMA 1989;262:826 11. Ringel SP. The transformation of neurologic practice. Neurology 1990;401487-1488 12. Payne CS, Roses AD. The molecular genetic revolution: its impact on clinical neurology. Arch Neurol 1988;45:1366-1376 13. Kurttke JF. Neuroepidemiology. Part 11: Assessment of therapeutic trials. Ann Neurol 1986;19:311-319 14. Landau WM. Training of the neurologist for the 21st century. Arch Neurol 1989;4621-22 15. Bromely DA. Support for biomedical research: the administration’s perspective. Acad Med 1991;66:336-337 16. Stetten DW. Research in a no-growth economy-can excellence be preserved? Perspect Biol Med 1980;23:357-369 17. Fredrickson DS. Biomedical research in the 1980s. N Engl J Med 1981;304:509-517 18. Culliton BJ. Shaping science policy: what’s happening to biomedical research in America. Acad Med 1991;66:188-191 19. Brown GW. Science policy, science funding, and the science community. Acad Med 1991;66:375-379 20. Hopkins A, Menken M, Defriese G. A record of patient encounters in neurologic practice in the United Kingdom. J Neurol Neurosurg Psychiatry 1989;52:436-438 21. Franklin GM, Ringel SP, Jones M, Baron A. A prospective study of principal care among Colorado neurologists. Neurology 1990;40:701-704 22. Hillman AL, Eisenberg JM, Pauly MV, et al. Avoiding bias in the conduct and reporting of cost-effectiveness research sponsored by pharmaceutical companies. N Engl J Med 1991;324: 1362- 1365 23. Inglehart JK. The Food and Drug Administration and its problems. N Engl J Med 1991;325:217-220 24. Martin JB. Training physician-scientists for the 1990s. Acad Med 1991;66:123-129 25. Freiden C , Fox B. Career choices of graduates from Washington University’s Medical Scientist Training Program. Acad Med 1991;66:162-164
New Horizons: Jamieson: Research-A
Journal Survey 93
Neurology Research: A Journal Patrick W. Jamieson, MD ~~~~
~
There have been major changes in neurology research during the past decade, but no systematic examination of the content, methods, funding, and research personnel. All scientific articles in the journals Annals of Neurology, Archives of Neurology, and Neurology were categorized by article type, number of authors, highest degree of first author, institution, disease area, reseach field, and source of support for the years 1980 and 1990. Original articles grew by 54% over the decade. The average number of authors increased by 1.3 to 5 ( p > 0.0001). Groups of MDs and PhDs wrote 39% of articles in 1990 (24% in 1980).Contributions with a diagnostic or therapeutic focus rose from 7 to 1496, whereas there was a pronounced drop in case reports from nearly 40% to just under 20%. Articles on movement disorders and neurodegenerative diseases increased more than 100% and now together comprise more than 25% of original articles. Molecular biology increased by 1,600%, and there was significant growth in epidemiology, neuroimaging, neurochemistry, and neuropsychology. The top 20 publishing institutions accounted for 40% of all original articles and 60% of US original articles. Foreign contributions doubled over the decade. The National Institutes of Health funded 46% of US articles in 1 9 0 (35.5% in 1980). More than 80% of articles in 1990 on neurodegenerative disease were supported by the National Institutes of Health. The complexity of neurological research has driven greater collaboration between basic and clinical scientists. New areas of clinical and basic knowledge are rapidly emerging in neurology. Jamieson PW. Neurology research: a journal survey, 1980-1990. Ann Neurol 1992;32:87-93
The “Decade of the Brain” resolution looks forward to great changes anticipated in neuroscience research during the 1770s and challenges the neurological community to seek new treatments for debilitating neurological disorders [I, 2). It is interesting to see, in this context, how much change has occurred over the 1980s and to project what impact these changes might have on future neurological research. Examination of these changes is important for several reasons. First, it identifies expanding neurological subdisciplines in research output that likely are fertile ground for new breakthroughs. Second, it highlights methods that have increased in importance to neurological investigation. Last, it aids in the training of future neurological clinicians and researchers by defining growing areas of knowledge that will require special emphasis. The literature provides a mechanism to examine these changes. Space is very limited in the most widely read neurology journals, and the peer-review process permits the publication only of what the neurological community perceives as the most significant investigative work. Examining this archive from a macroscopic perspective can reveal changes in the nature and direction of clinical research.
Methods Articles from the following three most widely cited journals in neurology: Annals of Neurology (Annals),Archives of Neurology (Archives), and Neurology were examined for the years 1980 and 1990. All peer-reviewed articles were included, with the exception of letters, notes, and special articles not dealing with neurological research issues. Articles were classified as original articles, brief communications,or review articles, as listed by the journal. The disease class, principal research fields, number of authors, degree of first author, and composition of research team (all MD, all PhD, or mixed) were noted. The degree of the first author was not given for some articles in the 1980s and was listed as unknown in these cases. The number of pages for each article was computed and rounded to the next whole number when there were fractions of an article’s last page. The country, institution, and sex of the lead author was recorded. I t was impossible in many cases to determine the sex of the lead author from the name alone, especially in the instance of foreign authors. If a name had ambiguous gender or could not be classified, it was listed as unknown. The principal focus of a report was classified as diagnosis, treatment, case, or other type of scientific investigation. The secondary focus was recorded as review, additional observation (confirming previously published work), or new observation. An article could have more than one principal focus, specific
From the Department of Neurology, University of Kansas Medical Center, Kansas City, KS.
Address correspondence to Dr Jamieson, Department of Neurology, University of Kansas Medical Center, 39th and Rainbow Blvd, Kansas City, KS 66103.
Received Nov 7, 1991, and in revised form Jan 8 and Jan 31, 1992. Accepted for publication Feb 1, 1992.
Copyright 0 1992 by the American Neurological Association
87
Table 1. Basic Statistical Data for the Three Leading Neurology Journals
All Articles All Journals
Number of Articles Pages Average Article Length" Average Number of Authors Average Number of Sponsors Average Number of Institutions
1990 785 4,000
5.10 4.59
0.94 1.73
Original Articles 1980
1990
1080
657 3,096 4.7 1 3.29 0.78 1.34
594 3,326 5.60 4.93 1.06
384 2,241 5.84 3.64
1.78
1.41
0.98
"Article length is measured in pages
disease class, or major research field. All articles that studied three or fewer individuals or families were classified as case reports. Investigations were classified as principally prospective, retrospective,or unknown. Prospective studies were defined as those that collected new data or performed new laboratory analysis on previously collected pathological material. Retrospective studies, such as chart reviews, analyzed or reinterpreted previously collected data. For some studies the time line could not be determined and was listed as unknown.
The number of collaborating institutions and sources of support were determined for every article. Support for the work was ascertained by reviewing the credit and acknowledgment sections. The t statistic was computed when the means of two categories were compared for 1980 and 1990. A p value was determined from the t statistic.
Results Table 1 shows the number and size of articles for each year. Overall there was an approximately 209%increase in total articles (54% for original articles) and a 29% increase in pages (48% for original articles) from 1980. There was a decrease in the total article count in Archives from 1980 to 1990 because of a reduction in brief communcations, many of which were only a single page in 1980. The greatest growth occurred in Neurology, which showed a 63% increase in total articles (126% for original articles) and a 47% increase in number of pages (81% for original articles). Although the number of articles increased substantially, the size of articles remained nearly constant with a slight drop in the size of original contributions. There was a decrease in length by more than one page in original contributions for Neurology. The average number of authors for original articles increased by 1.3 to nearly 5 during the decade. This was statistically significant ( p > 0.0001). Table 2 gives a breakdown on the distribution of authorship. There was a significant decline in single- or double-authored publications and a pronounced jump in papers with five, six, or more authors. Table 2 also shows that slightly more than 14% of contributions in 1990 had either a diagnostic or thera-
88 Annals of Neurology Vol 32
No 1 July 1992
peutic focus. This percentage nearly doubled from 1780. There was a dramatic decline in case reports from nearly 40% of journal articles in 1980 to just under 20% in 1990. Little change occurred in the percentage of articles that made new observations versus additional observations. Fully 85% of research contributions made new observations to the literature. Most published neurological research continued to be retrospective, but prospective studies increased by 7 % over the decade. Table 3 depicts the percentage of original articles devoted to different disease areas. Two areas experienced remarkable growth over the last decade, rnovement disorders and neurodegenerative diseases. Both had more than 100% growth, and these areas combined now represent approximately one-fourth of all published original articles. Most other areas experienced either modest growth or declines. Neuromuscular disease represented the largest percentage of original publications both in 1980 and 1990. Table 4 depicts the major basic science field or neurology subspecialty used in the research. Clinical skills comprised slightly less than 20% of articles in 1990, a 69% increase from 1980. Epidemiology, neuroimaging, neurochemistry, and neuropsychology showed significant growth. The most spectacular increase occurred in molecular biology, which witnessed a nearly 1,600q) climb. The institutions publishing the most in these journals are shown in Table 5. Although several of these institutions have been consistent performers over the 1980s, others have risen dramatically in rank. Figure 1 shows the importance of these top institutions in research productivity as reported in the three journals surveyed. They now comprise 40% of all original articles and 60% of original US articles. This is up from 50% of US original articles 10 years ago. Figure 2 shows the breakdown of first-author investigators by sex and degree for all article types. There was an 8.8% decline in male MD investigators and a corresponding increase in the other categories. The biggest increases were in the categories of female M D
Table 2. Compodion of Article$ by Number and Percentage for 1980 and 1990 1990
5% in 1990
1980
% in 1980
37 74 154 522 787
4.7 9.4 19.6 66.3 100.0
15 33 26 1 356 66 5
2.3 5.0 39.2 53.5 100.0
47 73 785
6.0 84.7 9.3 100.0
30 568 59 65 7
4.6 86.5 9.0 100.0
Time Line Retrospective Prospective Unknownireview Total
407 322 56 785
51.8 41.0 7.1 100.0
406 220 31 657
61.8 33.5 4.7 100.0
Number of Authors (Original Articles) One Two Three Four Five Six or more Total
16 81 86 120 101 190 594
2.7 13.6 14.5 20.2 17.0 32.0 100.0
27 83 84 56 48 384
7.0 21.6 22.4 21.9 14.6 12.5 100.0
42 114 134 152 126 2 17 785
5.4 14.5 17.1 19.4 16.1 27.6 100.0
75 161 156 124 86 55 657
11.4 24.5 23.7 18.9 13.1 8.4 100.0
Principal Focus Diagnostic Therapeutic Case
Other Total Secondary Focus Review New observation Add observation Total
Number of Authors (All Articles) One Two Three Four
Five Six or more Total
66 5
86
Several articles were classified as having multiple principal types.
investigator (9.770, increase of 2.9%) and male PhD investigator (7.9%,increase of 2.6%). Physicians with an MD/PhD contributed 6.7% of the articles in 1990, which is in close proportion (8.0%) to their percentage in full-time academic neurology for 1985 [3]. There was a 14.7% decline in articles from authors who were all MDs and a corresponding increase in research teams with MDs and PhDs. Currently, 60% of articles are written by all MDs and 38.8% by mixed teams. More research teams are including individuals from several institutions, that is, 1.73 in 1990 versus 1.34 in 1980 ( p < 0.001) (Table 1). Foreign contributions doubled over the decade to equal one-third of original contributions in 1990 (see Fig 1). Table 6 shows the output of the top 10 foreign countries and their growth since the start of the decade. Canada, Japan, England, and Germany have increased their contributions markedly. There were no German original articles in 1980, and the Germans now rank third or fourth in published articles from
foreign countries. The growth in foreign articles has come mainly at the expense of the bottom 107 neurology programs, which saw their percentage of original articles fall from 41% in 1980 to 26% in 1990. Figure 3 demonstrates the impact of the National Institutes of Health ( N I H ) in funding neuroscience investigation. The N I H was credited as a funding agency in 46% of the published US articles in 1990. This figure is up from 33.5% in 1980. If an investigation had at least one source of support, N I H support was also present 79% of the time. The NIH supported 33% of original US articles. Other sources of support either showed modest gains or losses except the “other” category, which increased from 18.7 to 23.2(7. This category includes many private foundations, small and large. Drug company support was modest; cited support was only 2.0% of US work published in 1990. There was a statistically significant increase in the number of sponsors in 1990 from 1980 ( p = 0.0062; Table I). New Horizons: Jamieson: Research-A
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Table 3. Original Articles by Major Disease Area ~~
~
g,of Change Original Articles Cerebrovascular Demyelinating Disease Developmental Epilepsy General Neurology Headache Head Trauma Infectious Disease Metabolic Movement Disorders Neurodegenerative Neuromuscular Neurooncology Sleep Disorders Spinal Cord Total
1990 76
44 8 64 63
6 1 38 11 74 84 105 20
5 13 612
% in 1990"
1980
% in 1980"
12.4 7.2 1.3 10.5 10.3 1.0 0.2 6.2 1.8 12.1 13.7 17.2 3.3 0.8 2.1 100.0
40 48 14 36 71 3 5 20 7 23 19 75 18 5 6 390
10.3 12.3 3.6 9.2 18.2 0.8 1.3 5.1 1.8 5.9 4.9 19.2 4.6 1.3 1.5 100.0 ~~
1990/ 1980 21
- 42 - 64
13 - 43
27 - 87
21 0 105 182 - 11 - 29 - 36 38 0 ~~
~
-
aNote that articles could have more than one dlsease focus Percentage is based o n the total number of diseases
Table 4. Original Articles by Basic or Clinical Science Area'
9of Change Original Articles
1990
c/c in 1990b
1980
9in 1980b
199011980
~~
Biochemistry Cell Biology Clinical Epidemiology Immunology Modeling Moiecular Biology Neurochemistry Neuroendocrinology Neuroimaging Neuropathology Neuropharmacology Neuroph ysiology Neuropsychology Neuroophthalmology Therapeutics Total
16 2 126 47 62 2 26 32 1 78 48 27 66 44 19 38 634
2.5 0.3 19.9 7.4 9.8 0.3 4.1 5.0 0.2 12.3 7.6 4.3 10.4 6.9 3.0 6.0 100.0
"Articles could have more than one science area. bPercentage is based on the total number of diseases. NA
=
not applicable.
90 Annals of Neurology Vol 32 No 1 July 1992
29
6 48 15 37 0 1 15 1 34 57 31 66 21 17 28 406
7.1 1.5 11.8 3.7 9. I 0.0 0.2 3.7 0.2 8.4 14.0 7.6 16.3 5.2 4.2 6.9 100.0
65 -79 68 101
-
7
NA 1,565 37 - 36 47 - 46 - 44 - 36 34 - 28 - 13 0
Table 5. Rank of Domestic Institutions by Number of Original Publications
Top Twenty American Institutions in 1770 National Institutes of Health Harvard Columbia Johns Hopkins University Mayo Clinic Foundation UCLA UCSF University of Pennsylvania Baylor University of Michigan University of Texas Health University of Iowa New England Medical Center University of Washington University of Minnesota Yale UCSD University of Colorado University of Pittsburgh Duke Total
Number of Original Articles in 1770
Rank in 1780
32 30 20 18
1 2 23 12
16 16
3 3 6
14
7 7 7 8 8 8 7 7
7 6 6 6 6 242
7 7
1990
Foreign
1980
0Top Twenty US Insltlutions
Other US
Fig I . Number of original articles written by investigators at foreign institutions, top 20 US institutions, and other US institutions.
57 40 12
57 12 23
57 40 12 12 40
...
Institutions with the same number of original publications in 1980 are listed by the hghest rank for that number. UCLA = University of California, Los Angeles, CA; UCSF = University of California, San Francisco, CA; University of Texas Health = University of Texas Health Science Center at Houston, TX; UCSD = University of California, San Diego, La Jolla, CA. MBIeMD
FMlalsMD
MalsPhD
FmalePhD
Male MDPhD
US articles reporting no funding decreased from 52% in 1980 to 42% in 1990. US articles that reported one or two sources of funding increased from 39.7 to 46.2%. Thirteen percent of US articles in 1990 had three or more sources of support. Funding was quantified by field (not shown). There have been major increases in the percentage of publications supported by the N I H in cerebrovascular disease, infectious disease, neurodegenerative disease, and neurooncology. Elghty-one percent of articles dealing with neurodegenerative disease were supported by the NIH, and 92.5% of articles in this field received support from some source in 1990. This was much higher than that of the second highest supported field, demyelinating disease (71.4% of articles were supported). Discussion Although only a small percentage of the total output of clinical neurological research is published in the three leading neurology journals, it is likely this sample reflects underlying research trends. They reach the wid-
Female MDPhD
Fig 2. Percentage of articles written by dzperent author groups.
est audience of neurological clinicians. The average paid circulation of these journals is more than 13,000 copies, which is more than the entire membership of the American Academy of Neurology (AAN) (11,300) and nearly equal to the number of US physicians who identify neurology as their primary specialty (Ubel C , personal communication, 1991). High quality research is represented because the three leading clinical neuroscience journals publish fewer than one-third of submitted manuscripts [4, 51. However, it is possible they are not representative because there are many other neurology journals and forums for dissemination of research results. The current composition of articles may have been influenced by the growth of subspecialty and basic neuroscience journals. Additionally, articles of general neurological interest and significant clinical import are often published in general medical journals New Horizons: Jamieson: Research-A
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Table 6. Rank of Foreign Institutions lu, Number of Original Publications
Top Ten Foreign Countries
Number of Original Articles in 1990
Number of Original Articles in 1980
Canada Japan England Germany France Italy The Netherlands Australia Spain Belgium
33 21 23 23 21
11 7
16 13 7 6 4
6 2 2
~~~
5 0
4
0
5
% of Increase” 200 200 360 NA 425 167 550 250 NA - 20
~
aPercentage of increase is computed from base year of 1980.
NA = not applicable.
1
40
30
20
10
0 NIH
~~
VA
~
MDA
EDlleDSy
MS
ALS
ALL
MG
DrugCo
Ofher
~
Fig 3. Percentage of domestic articles w i t h support from various sponsors. Some articles bad multiple sources of support.
such as the New EngkzndJournal of Medicine. Nevertheless, the ability to reach the widest audience of neurological clinicians, the prestige of publishing in the most frequently cited journals, and the decline in general neurology articles make it likely that research trends derived from these journals are not artifacts. The nature of neurological research changed both qualitatively and quantitatively in the 1980-1990 decade. There is significantly more research being published by groups of five or more individuals and by groups that contain a mix of MDs and PhDs. There also is greater interaction among medical centers. This shift reflects the complexity of neuroscience investigation. Healy 161 wrote, “with more emphasis on career differentiation, the burden will shift to the academic 92 Annals of Neurology Vol 32 No I July 1992
institution to ensure interaction among basic research, clinical investigation, and practice . . . .” The changes in neurological research over the last 10 years support this view. The contribution of women is roughly parallel to their numbers in the specialty. Although females represented 14.6% of neurologists in 1986, unlike males they are disproportionately distributed with 80% being younger than 44 years of age. Many of these women are currently in training 181 and thus their total future academic contribution may be higher. The low percentage of publications dealing with diagnosis or therapy may seem unusual for clinical journals, but it confirms the “Inverse Practice Law” of Menken 191 which states there is an inverse likelihood of a publication being accepted based on its percentage of clinical content. Nevertheless, there was an increase over the decade in articles that used predominantly clinical skills (19.9% in 1990 vs. 11.8% in 1980), although there was a pronounced reduction, by 2076, in case reports. Petersdorf [lo] commented that “the research agenda of our medical centers surely requires modification to include health services research, outcome measures, clinical trials, and health care economics.” The AAN is committed to this type of research 1111. Possibly, research dealing with neurological care should receive greater priority. The striking increase in the published literature in molecular biology, epidemiology, neuroimaging, neuropsychology, and neurochemistry suggests if future clinicians are to make sense of the literature that neurology programs must change their emphasis. The clinician remains a key individual in neurogenetic research and patient counseling 1121. An understanding of neuroepidemiology is crucial to well-performed clinical trials [13]. The challenge will be to master these
newer areas while maintaining a strong emphasis on bedside observation and clinical care [14]. The three major US neurology journals have truly become international in the last decade. The increase in percentage of literature by foreign research organizations reflects both the prestige of these top neurology journals and the growing quality of foreign research programs. Active programs were instituted by the journals to solicit work from overseas and changes were made in the editorial boards to reflect more accurately the international character of neurological research (Asbury AK, personal communication, 1991). Growth of N I H sponsorship may reflect the doubling of the NIH budget in current dollars from 1982 to 1990 and a 40% increase in purchasing power 1151. Although there is a current feeling of a funding crisis in the biomedical community, similar discussions took place in 1980 [lb}.The N I H commands a record 8.8 billion dollar budget, which represents 40% of federal nondefense research and development funding [ 17, 18J Sharp increases in future federal support are unrealistic given the budgetary constraints imposed by other federal programs. It is unlikely that funding will be increasingly linked to perceptions of the public health value of new knowledge [19]. There are some interesting disparities between the frequency of neurological disease and neurological research publications. Patients with headache comprise 13% of new patients seen by UK neurologists 120) and 21% of US neurologists [21), but comprise only 1% of original article subjects. Patients with pain and Parkinson’s disease comprise approximately the same number of patients seen by neurologists (5%). The literature on Parkinson’s disease is voluminous. Articles about pain comprise less than 1% of published articles in the three neurology journals surveyed. Problems of conflict of interest and medical ethics have surfaced because of the growing importance of drug company sponsorship in research and clinical trials {22, 231. The relatively few studies that acknowledge drug company support suggest that this is currently a small problem in neurological research. The trends in neuroscience research strongly argue for increased training of new clinician investigators. Trainees will need greater exposure to basic science and rigorous formal coursework 1241. MD/PhD programs are successful at training and retaining clinicians for faculty roles [25}. It will be increasingly important for neurologists doing clinical research to work closely with their basic science counterparts. New types of programs that emphasize training in basic research will also be necessary to make the Decade of the Brain a reality.
This work was supported in part by a grant from the National Library of Medicine (Grant No. LM05074).
I thank Drs Dewey Ziegler, Stan Spurlin, Chi-Wan Lai, and Michael Giuliani for their helpful advice and criticism.
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