Neurophobia in Brazil : Detecting and Preventing a Global

– Brazil. ABSTRACT Neurophobia is a global issue known as a fear of Neurology and Neurosciences by medical students and physicians, and it may contribute to a reduced number of trained neurologists and a global misunderstanding of neurological diseases among physicians. To date, there are no studies that address the issue of Neurophobia in Brazil. The present study aimed to evaluate the perception of Neurology and Neurosciences among Brazilian medical students. Students from four medical schools in the state of Pará, in the second (pre-clinical phase), fourth (clinical phase) and sixth (internship) years of the course, were submitted to a self-administered and written questionnaire divided into two sections: the first section included questions assessing their perceived level of interest, level of knowledge, degree of difficulty, confidence in examining patients, quality of teaching in medical school and likelihood of pursuing the career, concerning different clinical specialties (Cardiology, Endocrinology, Gastroenterology, Nephrology, Neurology, Respiratory Medicine and Rheumatology). In the second section, there were questions about possible reasons why Neurology was perceived as a difficult subject and possible ways to improve neurological education. A total of 486 questionnaires were completed. Neurology was perceived as the most difficult clinical specialty (mean score 4.00; p < 0.001), in which students feel least confident about conducting physical examinations (mean score 2.97; p < 0.001), and with the worst quality of teaching (mean score 3.12; p < 0.001). The main cause of Neurophobia was the need to know neuroanatomy and neurophysiology (very important reason for 39.4% of students), and the most frequently suggested method to improve neurological education was through more and better bedside tutorials (very important factor – 53.3%). Students developing extracurricular activities, women and older students had more unfavorable opinions about Neurology. Neurophobia is also present in Brazil, and new educational approaches must be proposed to improve the misperception of Neurology by medical students. The Medical Education Commission of the Brazilian Academy of Neurology should propose guidelines on Neurology teaching at undergraduate level.


Neurophobia is a global issue known as a fear of Neurology and Neurosciences by medical students
and physicians, and it may contribute to a reduced number of trained neurologists and a global misunderstanding of neurological diseases among physicians.To date, there are no studies that address the issue of Neurophobia in Brazil.The present study aimed to evaluate the perception of Neurology and Neurosciences among Brazilian medical students.Students from four medical schools in the state of Pará, in the second (pre-clinical phase), fourth (clinical phase) and sixth (internship) years of the course, were submitted to a self-administered and written questionnaire divided into two sections: the first section included questions assessing their perceived level of interest, level of knowledge, degree of difficulty, confidence in examining patients, quality of teaching in medical school and likelihood of pursuing the career, concerning different clinical specialties (Cardiology, Endocrinology, Gastroenterology, Nephrology, Neurology, Respiratory Medicine and Rheumatology).In the second section, there were questions about possible reasons why Neurology was perceived as a difficult subject and possible ways to improve neurological education.A total of 486 questionnaires were completed.Neurology was perceived as the most difficult clinical specialty (mean score 4.00; p < 0.001), in which students feel least confident about conducting physical examinations (mean score 2.97; p < 0.001), and with the worst quality of teaching (mean score 3.12; p < 0.001).The main cause of Neurophobia was the need to know neuroanatomy and neurophysiology (very important reason for 39.4% of students), and the most frequently suggested method to improve neurological education was through more and better bedside tutorials (very important factor -53.3%).Students developing extracurricular activities, women and older students had more unfavorable opinions about Neurology.Neurophobia   F. Josefowicz first coined the term "Neurophobia" to describe this common feeling 1 , and many authors have reported and measured its features [2][3][4][5][6][7][8][9][10] .Neurophobia has already been characterized in Asia, Europe, Africa, North America and the Caribbean.In South America, a recent study described high frequencies of inappropriate decisions in neurological diseases by students 11 , however, no analyses regarding the perception of Neurology and Neurosciences have been published to date.There is regional inequality in the distribution of neurologists in Brazil; the majority of these specialists live in the southeast region of the country and in state capitals.In 2014, regions such as the Brazilian Amazon showed an average of 0.68 neurologists per 100,000 inhabitants, the lowest ratio in the country 12 .Neurophobia may contribute to a reduced number of trained neurologists and a global misunderstanding of neurological diseases among physicians.To prevent the current shortage of neurologists in Brazil from worsening, it is essential to investigate the causes of Neurophobia and how to avoid it in medical schools.The present study is the first Brazilian survey to determine the perception of Neurology and Neurosciences among medical students in four medical schools in the state of Pará.and two years of internship rotations.The participants in the study were students from second (pre-clinical phase), fourth (clinical phase) and sixth (internship) years of medical school.

Study design and sample
All four institutions approved the study.

Instrument
To evaluate the perception of Neurology and Neurosciences, causes of misperception and suggestions for how to improve the teaching of these disciplines, we used a self-administered and written questionnaire based on previous studies 2,8,9 divided into two sections.The first section assessed the perceived level of interest, level of knowledge, degree of difficulty, confidence in examining patients, quality of teaching at medical school and likelihood of pursuing a career in the specialty.For example: "What is your current level of interest in…", or "Do you think the discipline is easy or difficult?"The responses were ranked on a maximum Likert scale of 5 ('1' -lowest possible score and '5' -highest possible score; the scale was inverted for the "degree of difficulty" question).The following seven specialties were considered: Cardiology, Endocrinology, Gastroenterology, Nephrology, Neurology, Respiratory Medicine and Rheumatology.
In the second section, participants were asked to rate selected reasons why Neurology was perceived as a difficult subject and possible ways to improve neurological education.For example: "Neurology may be difficult for a number of reasons.Please rate the importance of the possible reasons," or "Please rate the utility of the following methods as possible alternatives to improve neurological education".These selected options had been previously used 9 .Responses were ranked on a maximum Likert scale of 4 ('1' -lowest possible score and '4' -highest possible score).Finally, we asked participants to answer one open-ended question about how teaching in Neurology and Neurosciences could be improved.Age, gender, medical school year and extracurricular activities were also registered.
Following regular lectures, questionnaires were distributed to the students who accepted participating in the survey and were asked not to indicate their names.Questionnaires with less than 50% of the questions answered were excluded.

Statistical analysis
Analyses were performed using SPSS version 16.0.0and Prism version 5.0 (both for Windows).Normal data were described as mean ± SEM.Differences between three or more independent samples were calculated using Kruskal-Wallis test and Dunn procedures for multiple comparisons (continuous variables) or X 2 test (categorical variables).Multivariate logistic re-gressions were performed, with the dependent variable being the presence of Neurophobia in the questions of the first section of the questionnaire, and the independent variables being age, sex and extracurricular activities.For the dependent variable, values < 2 were regarded as presence of Neurophobia and > 3 as absence of Neurophobia (for "degree of difficulty", values < 2 corresponded to absence of Neurophobia and > 2 to presence of Neurophobia).Differences were considered significant when p < 0.05.

RESULTS
A total of 486 questionnaires were completed, and the participation per medical course year was as follows: second year -224 (46%; female 55.3%); fourth year -167 (34.3%; female 53.2%); sixth year -95 (19.5%; female 55.7%).The mean age of the participants was 22.7±0.15(second year -21.3±0.21;fourth year -23.1±0.24;sixth year -25.1±0.3)(Table 1).The response rate was 55.1% (second year -67%; fourth year -55%; sixth year -37%), representing approximately 18% of all medical students in the state of Pará.Neurology was perceived as the most difficult discipline (4.00; p < 0.001, Figure 1A), in which they had the least confidence when examining patients (2.97; p < 0.001, Figure 1B) and the worst quality of teaching (3.12; p < 0.001, Figure 1C) among seven clinical specialties.Interest in Neurology was considerable (2.78, third place; p < 0.001, Figure 1D) and the level of knowledge was limited (2.49, fourth place; p < 0.001, Figure 1E).Neurology was the first career choice for 19.4% of the students (decreasing frequency -second year -22%; fourth year -18.2%; sixth year -15.3%) and the last choice for 27.2% (increasing frequency -second year -23.9%; fourth year -28.7%; sixth year -34.6%), but differences were not significant (X 2 = 2.67, p = 0.26).Comparing the three different moments of medical school (Figure 2), over 70% of the students in the second, fourth and sixth medical school year graded Neurology as "difficult" and "very difficult" (Figure 2A), with no differences between the groups.There were differences between 122 the second, fourth and sixth year in terms of confidence in examining patients (X 2 = 7.89, p = 0.01; Figure 2B), quality of teaching (X 2 = 29.23,p < 0.001; Figure 2C), level of knowledge (X 2 = 6.35, p = 0.04; Figure 2E) and likelihood of specializing in Neurology (X 2 = 6.44, p = 0.04; Figure 2F) -unfavorable opinions about Neurology were more common in the final years of the medical course.Concerning the causes of Neurophobia, the most important contributor to the perception of Neurology as difficult was the need to understand neuroanatomy and neurophysiology (very important reason to 39.4% of students), which was more frequently reported in the clinical and internship periods (second year -37.9%; fourth year -74.4%; sixth year -71.2%) (Table 2).Limited exposure to neurological patients and a large number of rare and difficult diagnoses were considered as the second and third most important contributors, respectively.The most important contributor for second year students was the large number of rare and difficult diagnoses (60.9%), whereas for fourth year students it was the need to understand neuroanatomy and neurophysiology (74.4%) and for sixth year students it was not enough teaching (74.4%).

* p value for difference of opinions among medical students from three year groups (X 2 test). NS, non-significant
According to the students, when answering both the Likert-style question and open-ended question, the most important methods to improve Neurology and Neurosciences teaching and learning were more/better bedside tutorials (very important factor -53.3%) and more/better traditional lectures (very important factor -46.9%) (Table 3).Pre-clinical students believed more in online resources (X 2 = 6.57, p = 0.03) and textbooks (X 2 = 20.34,p < 0.001) as learning tools.About 30% of students did not answer the open-text suggestions.To assess the influence of some variables on the unfavorable opinion about Neurology in the six questions of the first section of the questionnaire, we performed multivariate lo-gistic regression analyses adjusted for age, gender and extracurricular activities for each question (Table 4).Women held more unfavorable opinions about Neurology than men in the questions "level of interest" (OR 1.96, 95% CI 1.2-2.9),"confidence in examining patients" (OR 1.89, 95% CI 1.2-2.9)and "likelihood of pursuing career" (OR 2.11, 95% CI 1.32-3.37).Older students had more unfavorable opinions than younger students in the questions regarding "quality of teaching" (OR 1.08, 95% CI 1.0-1.17)and "likelihood of pursuing career" (OR 1.09, 95% CI 1.01-1.17).Students with extracurricular activities had more unfavorable opinions in the questions regarding "level of knowledge" (OR 1.98, 95% CI 1.1-3.57)and "quality of teaching" (OR 2.7, 95% CI 1.43-5.0).No multicollinearity was found between independent variables.

DISCUSSION
This is the first investigation into perceptions of Neurology among medical students in Brazil.Our results showed students from the four medical schools of Pará perceive Neurology as the most difficult clinical specialty, with the worst quality of teaching and which they feel the least confidence in examining patients.These indicators suggest the presence of Neurophobia in Brazil, as already reported in other countries.This is also the first study to analyze the differences of Neurophobia among students from pre-clinical, clinical and internship stages of study, and to seek predictors of Neurophobia by means of logistic regression.Six previous studies already identified that Neurology is seen as the most difficult clinical specialty 2,3,4,6,8,10 (Table 5).Compared to the other questions, the one regarding the student's perception of the degree of difficulty seems to be the best question to recognize Neurophobia in a student sample.Furthermore, confidence in examining neurological patients was the worst in the four studies, as compared to other clinical specialties 2,3,6,10 .A moderate perception of interest and knowledge was also previously described 2,3,4,8 and, even so, Neurology was the first choice clinical specialty for one fifth of the students, similar to the findings of an Indian study 7 .Flanagan et al. 3 explained the disparity between difficulty and knowledge/interest by the fact that students perceive that they have to struggle more at Neurology to gain knowledge.Gupta et al. 7 showed two factors influenced medical students' choice of Neurology as a career: intellectual challenge (73%) and inspiration by Neurology teachers (63%).Neurophobia has also been described in general practitioners (GP) 2,3,8 and it can worsen the quality of global neurological care.GPs affected by Neurophobia may be less confident about diagnosing and treating patients with neurological disorders commonly encountered in primary care, such as headache, epilepsy and stroke 13 .A low degree of effective GP management of neurological diseases generates an excess of referrals to neurologists, thus overloading health systems.
In Brazil, the number of neurologists in underdeveloped regions, such as the Brazilian Amazon, is critically low 14 .Ac-cording to a recent survey, the state of Pará had 0.53 neurologists per 100,000 inhabitants in 2014, half of the minimum rate of 1 neurologist per 100,000 inhabitants recommended by the World Health Organization 12 .In the Brazilian Amazon, referral mechanisms from primary to tertiary care are slow and obsolete, and transport of patients from the hinterland to larger cities, where the majority of the neurologists live, is impaired by infrastructural limitations 14 .Besides the possible low degree of effective GP management of neurological disorders, Neurophobia can also be detrimental for the training of new neurologists.
A need to understand neuroanatomy and neurophysiology was seen as the most important reason for Neurophobia.The same top reason was described in previous studies 2,4,5,6,8 .But is detailed knowledge of neurosciences really necessary to practice Neurology?Zinchuk et al. 6 reported that residents perceived neuroanatomy as a minor contributor to the difficulty of Neurology compared to students 6 , however our results and data from Matthias et al. 8 showed students in clinical and internship stages described knowledge of neurosciences as essential to Neurophobia.Some authors argue a thorough knowledge of neuroanatomy may not be essential for the management of common neurological disorders, such as headaches and epilepsy -Schon et al. used the metaphor "most people learn to drive safely with limited knowledge of how the engine works" 2 .
Other important reasons to Neurophobia were limited exposure to neurological patients and large number of complex and rare diagnoses, already described by other authors 3,8 .Limited exposure to patients is a direct consequence of the most suggested strategy to improve Neurology teaching: more bedside lectures.The association of complex and rare diagnoses with 125 Neurophobia shows students have a misunderstanding of the most common neurological disorders, such as headaches, epilepsy and stroke, which frequently do not require several complementary exams and rarely involve differential diagnoses.
The main suggested methods to improve Neurology teaching, i.e. more and better bedside tutorials and traditional lectures, have also been reported in all other studies as the most important strategies to reduce Neurophobia.Online resources were seen as the least important method by students, an unexpected result for millennials, known as great users of the Internet.This finding corroborates a previous study 3 .
In his original article, Josefowicz attributed Neurophobia to the lack of integration between basic Neurosciences and clinical Neurology 1 .Our students also identified this issue as the main reason for Neurophobia and asked for more and better practical and expositive lectures.One third of all students specifically suggested a better integration between basic and clinical sciences.One author used a case-based teaching for undergraduate students and described an improvement in their perception of Neurology 15 , and a systematic review designed to evaluate the impact of new methodologies to prevent Neurophobia showed several different strategies and evidence of low quality in effective neurological education 16 .
However, Ridsdale et al. 17 reported few changes as regards Neurophobia after a substantial curricular modification, which consisted in increased time and focus on Neurology.A recent article suggested that medical schools with 4-week Neurology internships and/or Neurology residencies had more graduates assuming Neurology residencies positions 18 .Therefore, increased practical contact with neurological patients and practical training of neurological skills also can improve the perception of Neurology among students.We believe both better integration of Neuroscience and Neurology and more practical neurological training can be key to preventing Neurophobia.
We expected the medical school to be capable of modifying previous misconceptions, acquired in family and society, about Neurology.Unfortunately, our data suggest Neurophobia is actually developed and caused by medical schools 17 .
This was the first study to analyze demographic predictors of Neurophobia.Our results suggest older female students involved in extracurricular activities were more likely to develop Neurophobia.Previous studies have not addressed these issues, but other authors have reported that male students are more confident in approaching patients with complex complaints, whatever the specialty; male students preferred Cardiology and female students showed a preference for Psychiatry 17 .
Our study had some limitations.The sample included students from only one state (Pará), and future Brazilian studies must include medical schools from other states, different regions and settings, for a national analysis of this problem.A low sample (18%) of all Pará medical students can limit the generalization of these results, but an average response rate of 55% is similar to other studies 4,6,9 .We could not evaluate whether the overall quality of the medical school is correlated to the perceived difficulty of Neurology.Furthermore, no correlation was found between Neurophobia and the poor performance of students (written tests and patients care assessments).Possible institutional bias (differences across medical schools) and responder bias could not be totally excluded.The unbalanced high number of students from the pre-clinical stage (n = 224) and the low number of internship students (n = 95), who have different practical experiences, may increase the bias in the overall data.To reduce this possible bias, we performed isolated analyses between medical school year groups.

CONCLUSIONS
This cross sectional study was conducted from May to December 2015 at four medical schools in the state of Pará: the Federal University of Pará, the State University of Pará at Belém, the State University of Pará at Santarém and the University Center of Pará.Brazilian medical schools have a six-year curriculum: two years of biomedical sciences, two years of clinical training 121 Bruno Lopes Santos-Lobato et al.DOI: http://dx.doi.org/10.1590/1981-52712015v41n3RB20160105

Figure 1 Figure 2
Figure 1 Mean survey score results of seven clinical specialties (red bar represents Neurology).(A) Level of difficulty.(B) Confidence in examining patients.(C) Quality of teaching.(D) Level of interest.(E) Level of knowledge.* p value for comparison to Neurology < 0.05.Car, Cardiology; End; Endocrinology; Gas, Gastroenterology; Nep, Nephrology; Neu, Neurology; Res, Respiratory Medicine; Rhe, Rheumatology In this study, we report the presence of Neurophobia in Brazil.Better integration between Neurosciences and Clinical Neurology and increased neurological practical activities are earmarked by the students as the actions required to improve their perception of Neurology.Further nationwide studies are needed.The Medical Education Commission of the Brazilian Academy of Neurology must be aware of this problem and propose guidelines on Neurology teaching at undergraduate level.ETHICS APPROVAL AND CONSENT TO PARTICIPATEPermission for the study was obtained from the Deans' Offices of the Medical Schools (Federal University of Pará, State University of Pará at Belém, State University of Pará at Santarém and University Center of Pará).
is also present in Brazil, and new educational approaches must be proposed to improve the misperception of Neurology by medical students.The Medical Education Commission of the Brazilian Academy ofNeurology should propose guidelines on Neurology teaching at undergraduate level.

Table 1 Breakdown of medical school students in each year by sex
* p value for difference regarding gender among medical students from three year groups (X 2 test).NS, non-significant Bruno Lopes Santos-Lobato et al.DOI: http://dx.doi.org/10.1590/1981-52712015v41n3RB20160105

Table 3 Methods to improve Neurology and Neurosciences teaching and learning. Frequencies show proportion of answers rating these options as important and very important factors to Neurophobia
* p value for difference of opinions among medical students from three year groups (X 2 test).NS, non-significant