International Journal of Neuroscience, 2014; Early Online: 1–4 copyright © 2014 Informa Healthcare USA, Inc. ISSN: 0020-7454 print / 1543-5245 online DOI: 10.3109/00207454.2014.951041
ORIGINAL ARTICLE
Different types of headache in patients with systemic lupus erythematosus Reda Badry1 and Rania M. Gamal2 Department of Neurology and Psychiatry, Assiut University Hospital, Egypt; 2 Department of Rheumatology and physiotherapy, Assiut University Hospital, Egypt, Nobles Hospital, Staff Grade Rheumatology and General Medicine Department, UK
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1
Background: Headache in patients with systemic lupus erythematosus (SLE) is considered a common neurological finding, although the relationship is unclear. Aim: In this study, we aimed to evaluate frequency and characteristics of different types of headache in patients with SLE. Methods: 40 SLE patients were chosen from those referred to the out patient clinic using the American College of Rheumatology (ACR) criteria for the diagnosis of SLE. Headache classification was done regarding the ICD-II criteria in the patients. Headache severity was assessed by visual analog scale (VAS), and subjects with VAS ≥4 were included in the study. Results: 30 patients out of 40 SLE patients (75%) have different headache types: tension type in 37.5% (n = 15) and migraine in 30% (n = 12), cluster 2.5% (n = 1), and intracranial hypertension 5% (n = 2) of all patients. Conclusion: Headache is frequent in SLE especially tension and migraine types, but overall, it is not associated with disease activity. KEYWORDS: Headache, systemic lupus erythematosus, autoimmune
Introduction Systemic lupus erythematosus (SLE) is a systemic autoimmune disease where the immune system is overactive, attacking healthy joints and organs of the body including the nervous system [1]. Studies suggest that up to 38% of neurological and psychiatric events in lupus patients are a result of the disease itself [2]. BatuecasCaletr´ıo A and his colleagues stated that recurrent headache was found in 50/89 patients, and 26 of them had diagnostic criteria for migraine [3]. Nearly similar data was given by Espinosa-Sanchez JM [4]. However, the association between headache disorders and lupus is debatable, with prior research reporting prevalence rates that range from 24% to 72% [5]. The exact prevalence of headache in SLE is unknown [6]. Much of the discrepancies in previous studies may be due to difference in methodology and the lack of uniform definition of headache, which is a common occurrence in the general population, especially among women. Received 13 April 2014; revised 25 July 2014; accepted 30 July 2014. Correspondence: Reda Badry, M.D., Lecturer of Neurology, Assiut University Hospital, Egypt. Tel: 002-088-236-9541. E-mail: [email protected]
It was found that 18% of lupus patients experienced headache at the onset of their disease with that number increasing to 58% after 10 years [5]. Only 2% of subjects reporting a “lupus headache” that is described by the Systemic Lupus Erythematosus Disease Activity Index 2000 [7] as a “severe, persistent headache: which may be migrainous, but unresponsive to narcotic analgesia.” Although headaches were linked to a lower healthrelated quality of life, these episodes resolved over time independent of specific treatment to lupus and were not associated with disease activity [1]. Researchers found that there is no association between headache and specific lupus autoantibodies or lupus medications, such as steroids, antimalarials, and immunosuppressives [8]. No pathogenic mechanism has so far been described to fully explain headache in patients with SLE. The role of circulating cytokines, vascular injury, neuronal damage or antiphospholipid antibodies (aPL) in the development of headache in SLE patients is also a matter of debate [9]. Other concomitant causes such as infection or hypertension should be excluded before assuming that headache is a feature of SLE activity. Therapeutic approach of SLE-related headache remains empirical and based on clinical experience [6]. 1
2
R. Badry and R. M. Gamal
Table 1.
Some clinical data of involved patients.
Age (in yrs: mean ± SD) Duration of SLE (in yrs: mean ± SD) SLE severity index (mean ± SD) SLE involvement of the CNS Family history of headache a
With headache (n = 30)
Without headache (n = 10)
p valuea
41 ± 5.1 7.3 ± 1.5 3.9 ± 1.7 9 12
37 ± 4.9 5.9 ± 2.1 3.2 ± 1.09 1∗ 2∗
NS NS NS 0.001 0.004
There is significant difference between both groups if p value ≤ 0.05. NS: Non-significant.
Int J Neurosci Downloaded from informahealthcare.com by Universitat de Girona on 11/26/14 For personal use only.
In this study, we aimed to determine the frequency and characteristics of different types of headache in patients with SLE as well as the significance of lupus headache and its relationship to the disease expression.
Subjects and Methods Subjects 40 patients (35 females and 5 males) with mean age of (39 yrs ± 4.7) with SLE of >2 year duration, fulfilling at least four of the 11 classification criteria of the American College of Rheumatology [10], were interviewed. Patients with end-stage renal failure undergoing dialysis were excluded.
Methods The research was conducted over 4 stages: 1st stage: screening for the presence of headache among patients by asking every one whether he or she has at least an attack of headache every 2 weeks over the last year. If his answer is (yes), he/she is considered as headache sufferer. 2nd stage: Basic demographic data was collected, e.g. age, sex, level of education, marital state, and residence. 3rd stage: Some detailed data about headache was collected, e.g. visual symptoms before, during or after headache, triggers of headache, pain character, site of headache, associated symptoms with headache (e.g., vomiting, photophobia, phonophobia), the frequency of headache, what makes headache worse, past history of headache, the use and response of analgesic medication, life impact of headache, and the family history of headache were evaluated in all patients. 4th stage: Clinical features, treatment, disease severity of SLE and its relation to headache. According to the International Headache Society criteria [11], we classified the clinical types of headache. Statistical analysis was done using SPSS package 13. Independent sample t-test and Chi-square were used in comparison between groups for quantitative and nominal data, respectively.
Results As shown in Table 1, there is no significant difference between both groups of SLE patients (with and without headache) regarding age, duration of SLE or disease severity index of SLE. Regarding the presence of CNS involvement by SLE (seizure: 4, psychosis: 3, hemiparesis: 2) and positive family history of headache, both are significantly higher in headache group in comparison to the other group. Table 2 shows that about 2/3 of patients suffering from headache have daily or at least twice weekly attacks of headache and additionally 2/3 of patients have moderate to severe headache attacks which indicate the burden of headache in their lives. Table 3 shows types of headache and triggering factors. Tension type of headache is significantly more common than the other types of headache among SLE patients and also it is more common than in normal population, additionally, stress is the most significant trigger of headache among those patients as shown in Table 3. According to the questionnaire we used in this study, the occurrence of headache was not related neither to SLE activity nor specific treatment for SLE (non-steroidal anti-inflammatory drugs, antimalarials, corticosteroids, azathioprine, or cyclophosphamide) and the response to non steroidal anti-inflammatory drugs and narcotic analgesics was adequate in all patients except 2 patients whose illness necessitate increasing the dose of steroids.
Table 2.
Some criteria of headache. SLE patients
Frequency of headache: Daily 2 ∼ 3/week Once/week Once/2 weeks Severity of headache: Mild Moderate Severe Life impact of headache: Yes No
11 9 8 2 11 15 4 14 16
International Journal of Neuroscience
Headache in SLE Table 3.
Shows types of headache and triggering factors.
Types of headache: Tension type: Migraine with aura: Migraine without aura: Intracranial hypertension: Cluster type: Triggering factors Stress: Menses: Sun exposure: Lack of sleep:
SLE patients
p. value
15∗ 4 2 8 1
0.02 NS NS NS NS
17∗ 7 3 3
0.03 NS NS NS
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∗ Tension type headache and stress are the most common type of headache and trigger, respectively, among patients: p value ≤ 0.05.
Discussion This study showed that previous year prevalence of headache in patients with SLE is common (75%: tension type: 37.5, migraine: 30, intracranial hypertension: 5, cluster type: 2.5); additionally exposure to stress is the most common headache trigger among those patients. This study revealed that tension type of headache is significantly more common than the other types of headache among SLE patients which is in accordance with [8] and [5] who stated that tension headache occurs in 38.6% of SLE patients. Moreover, the prevalence of tension headache among patients with SLE is more common than in general population in Egypt as stated by Tallawy et al. [12] who assumed the prevalence of headache to be around 3%. Migraine is the second most common type of headache in this study (30%) which is in accordance with [1] who reported that tension type headache represents 39% of patients with SLE, and [13] who stated that the life-time prevalence of headache among SLE patients was around 34% and 27% of migrainous and non migrainous headaches respectively. The variation may be due to the differences in the approach, i.e., 1 year versus life time prevalence. On the other hand, besides the age and sex, income, place of living and climate factors may all influence the prevalence of headache [14]. The percent of migraine headache among SLE in our study is more than that reported by [15] who stated that migraine represents only 19% of patients with SLE. This difference is attributed to the different sample size. Results of this study indicate that headache in patients with SLE is not significantly related to the disease expression or severity which is not in consistent with the idea that intractable headaches are particularly common in patients with active SLE [16,17]. This difference may be attributed to the increasing understanding of headache as a symptom with major morbidity, as well C
2014 Informa Healthcare USA, Inc.
3
as the management of patients with SLE becoming more effective. Another explanation of our finding is that there is no pathogenic mechanism has so far been described that can fully explain headache induced by SLE. Additionally it was reported that the roles of circulating cytokines, vascular injury, neuronal damage or aPL in the development of headache in SLE patients are also a matter of debate [6]. Other concomitant causes such as infection or hypertension should be excluded before assuming that headache is a feature of SLE activity. Therapeutic approach of headache SLE-related remains empirical and based on clinical experience. In conclusion, we can assume that headaches, essentially tension and migraine types are common among SLE patients; especially those with CNS lupus involvement and those with positive family history of headache, yet, the presence and severity of headache are not suggestive of SLE activity or the use of specific anti-lupus drugs. A detailed neurological evaluation and radiological investigation, if necessary, should be performed in SLE patients with prolonged disease and advanced age, regardless of headache characteristics.
Declaration of Interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Grant information: No special fund was given.
References 1. Bicakci S, Ozbek S, Bicakci K, et al. Recurrent headache and MRI findings in systemic lupus erythematosus. J Natl Med Assoc 2008 Mar;100(3):323–6. 2. Fragoso-Loyo H, Atisha-Fregoso Y, Llorente L, S´anchezGuerrero J. Inflammatory profile in cerebrospinal fluid of patients with headache as a manifestation of neuropsychiatric systemic lupus erythematosus. Rheumatology (Oxford) 2013 Dec;52(12):2218–22. 3. Batuecas-Caletr´ıo A, Pino-Montes JD, Cordero-Civantos C, et al. Hearing and vestibular disorders in patients with systemic lupus erythematosus. Lupus 2013;22(5):437–42. 4. Espinosa-Sanchez J, Lopez-Escamez J. Migraine, sudden sensorineural hearing loss and autoimmune ear disease. Cephalalgia 2013 Oct;33(14):1206–7. 5. Hanly J, Urowitz M, O’Keeffe A, et al. Headache in systemic lupus erythematosus: Results from a prospective, international, inception cohort study. Arthritis Rheum 2013;65(11):2887–97. 6. Cuadrado M, Sanna G. Headache and systemic lupus erythematosus. Lupus 2003;12(12):943–6. 7. (SLEDAI) SLEDAI. American College of Rheumatology. 2000. 8. Sfikakis P, Mitsikostas D, Manoussakis M, et al. Headache in systemic lupus erythematosus: a controlled study. Br J Rheumatol 1998 Mar;37(3):300–3.
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R. Badry and R. M. Gamal
14.
15.
16.
17.
antibodies against phospholipids. J Neurol 1992;239:39– 42. Mitsikostas D, Tsaklakidou D, Athanasiadis N, Thomas A. The prevalence of headache in Greece:Correlations to latitude and climatological factors. Headache 1996;36:168–73. Tjensvoll A, Harboe E, Gøransson L, et al. Migraine is frequent in patients with systemic lupus erythematosus: a case-control study. Cephalalgia 2011 Mar;31(4):401–8. Wallace D, Metzger A. Systemic lupus erythematosus and the nervous system. In: Wallace DJ, Hahn BH, eds. Dubois’ lupus erythematosus. 5th ed. Philadelphia: Lea & Febiger. 1997:723–54. Gladman D, Urowitz M. Sytemic lupus erythematosus. Clinical features. In: Schumacher HR, ed. Primer of the rheumatic diseases. 10th ed. Atlanta: Arthritis Foundation. 1993:106–12.
Int J Neurosci Downloaded from informahealthcare.com by Universitat de Girona on 11/26/14 For personal use only.
9. Fragoso-Loyo H, Richaud-Patin Y, Orozco-Narv´aez A, et al. Interleukin-6 and chemokines in the neuropsychiatric manifestations of systemic lupus erythematosus. Arthritis Rheum. 2007;56:1242–50. 10. Tan E, Cohen A, Fries J. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271–7. 11. Society HCSotIH. The international classification of headache disorders, 2nd edition. Cephalalgia 2004;13(1):S5–S12. 12. Tallawy H, Farghaly W, Rageh T, et al. Door-to-door survey of major neurological disorders (project) in Al Quseir City, Red Sea Governorate, Egypt. Neuropsychiatr Dis Treat 2013;9:767–71. 13. Markus H, Hopkinson N. Migraine and headache in systemic lupus erythematosus and their relationship with
International Journal of Neuroscience
ORIGINAL ARTICLE
Different types of headache in patients with systemic lupus erythematosus Reda Badry1 and Rania M. Gamal2 Department of Neurology and Psychiatry, Assiut University Hospital, Egypt; 2 Department of Rheumatology and physiotherapy, Assiut University Hospital, Egypt, Nobles Hospital, Staff Grade Rheumatology and General Medicine Department, UK
Int J Neurosci Downloaded from informahealthcare.com by Universitat de Girona on 11/26/14 For personal use only.
1
Background: Headache in patients with systemic lupus erythematosus (SLE) is considered a common neurological finding, although the relationship is unclear. Aim: In this study, we aimed to evaluate frequency and characteristics of different types of headache in patients with SLE. Methods: 40 SLE patients were chosen from those referred to the out patient clinic using the American College of Rheumatology (ACR) criteria for the diagnosis of SLE. Headache classification was done regarding the ICD-II criteria in the patients. Headache severity was assessed by visual analog scale (VAS), and subjects with VAS ≥4 were included in the study. Results: 30 patients out of 40 SLE patients (75%) have different headache types: tension type in 37.5% (n = 15) and migraine in 30% (n = 12), cluster 2.5% (n = 1), and intracranial hypertension 5% (n = 2) of all patients. Conclusion: Headache is frequent in SLE especially tension and migraine types, but overall, it is not associated with disease activity. KEYWORDS: Headache, systemic lupus erythematosus, autoimmune
Introduction Systemic lupus erythematosus (SLE) is a systemic autoimmune disease where the immune system is overactive, attacking healthy joints and organs of the body including the nervous system [1]. Studies suggest that up to 38% of neurological and psychiatric events in lupus patients are a result of the disease itself [2]. BatuecasCaletr´ıo A and his colleagues stated that recurrent headache was found in 50/89 patients, and 26 of them had diagnostic criteria for migraine [3]. Nearly similar data was given by Espinosa-Sanchez JM [4]. However, the association between headache disorders and lupus is debatable, with prior research reporting prevalence rates that range from 24% to 72% [5]. The exact prevalence of headache in SLE is unknown [6]. Much of the discrepancies in previous studies may be due to difference in methodology and the lack of uniform definition of headache, which is a common occurrence in the general population, especially among women. Received 13 April 2014; revised 25 July 2014; accepted 30 July 2014. Correspondence: Reda Badry, M.D., Lecturer of Neurology, Assiut University Hospital, Egypt. Tel: 002-088-236-9541. E-mail: [email protected]
It was found that 18% of lupus patients experienced headache at the onset of their disease with that number increasing to 58% after 10 years [5]. Only 2% of subjects reporting a “lupus headache” that is described by the Systemic Lupus Erythematosus Disease Activity Index 2000 [7] as a “severe, persistent headache: which may be migrainous, but unresponsive to narcotic analgesia.” Although headaches were linked to a lower healthrelated quality of life, these episodes resolved over time independent of specific treatment to lupus and were not associated with disease activity [1]. Researchers found that there is no association between headache and specific lupus autoantibodies or lupus medications, such as steroids, antimalarials, and immunosuppressives [8]. No pathogenic mechanism has so far been described to fully explain headache in patients with SLE. The role of circulating cytokines, vascular injury, neuronal damage or antiphospholipid antibodies (aPL) in the development of headache in SLE patients is also a matter of debate [9]. Other concomitant causes such as infection or hypertension should be excluded before assuming that headache is a feature of SLE activity. Therapeutic approach of SLE-related headache remains empirical and based on clinical experience [6]. 1
2
R. Badry and R. M. Gamal
Table 1.
Some clinical data of involved patients.
Age (in yrs: mean ± SD) Duration of SLE (in yrs: mean ± SD) SLE severity index (mean ± SD) SLE involvement of the CNS Family history of headache a
With headache (n = 30)
Without headache (n = 10)
p valuea
41 ± 5.1 7.3 ± 1.5 3.9 ± 1.7 9 12
37 ± 4.9 5.9 ± 2.1 3.2 ± 1.09 1∗ 2∗
NS NS NS 0.001 0.004
There is significant difference between both groups if p value ≤ 0.05. NS: Non-significant.
Int J Neurosci Downloaded from informahealthcare.com by Universitat de Girona on 11/26/14 For personal use only.
In this study, we aimed to determine the frequency and characteristics of different types of headache in patients with SLE as well as the significance of lupus headache and its relationship to the disease expression.
Subjects and Methods Subjects 40 patients (35 females and 5 males) with mean age of (39 yrs ± 4.7) with SLE of >2 year duration, fulfilling at least four of the 11 classification criteria of the American College of Rheumatology [10], were interviewed. Patients with end-stage renal failure undergoing dialysis were excluded.
Methods The research was conducted over 4 stages: 1st stage: screening for the presence of headache among patients by asking every one whether he or she has at least an attack of headache every 2 weeks over the last year. If his answer is (yes), he/she is considered as headache sufferer. 2nd stage: Basic demographic data was collected, e.g. age, sex, level of education, marital state, and residence. 3rd stage: Some detailed data about headache was collected, e.g. visual symptoms before, during or after headache, triggers of headache, pain character, site of headache, associated symptoms with headache (e.g., vomiting, photophobia, phonophobia), the frequency of headache, what makes headache worse, past history of headache, the use and response of analgesic medication, life impact of headache, and the family history of headache were evaluated in all patients. 4th stage: Clinical features, treatment, disease severity of SLE and its relation to headache. According to the International Headache Society criteria [11], we classified the clinical types of headache. Statistical analysis was done using SPSS package 13. Independent sample t-test and Chi-square were used in comparison between groups for quantitative and nominal data, respectively.
Results As shown in Table 1, there is no significant difference between both groups of SLE patients (with and without headache) regarding age, duration of SLE or disease severity index of SLE. Regarding the presence of CNS involvement by SLE (seizure: 4, psychosis: 3, hemiparesis: 2) and positive family history of headache, both are significantly higher in headache group in comparison to the other group. Table 2 shows that about 2/3 of patients suffering from headache have daily or at least twice weekly attacks of headache and additionally 2/3 of patients have moderate to severe headache attacks which indicate the burden of headache in their lives. Table 3 shows types of headache and triggering factors. Tension type of headache is significantly more common than the other types of headache among SLE patients and also it is more common than in normal population, additionally, stress is the most significant trigger of headache among those patients as shown in Table 3. According to the questionnaire we used in this study, the occurrence of headache was not related neither to SLE activity nor specific treatment for SLE (non-steroidal anti-inflammatory drugs, antimalarials, corticosteroids, azathioprine, or cyclophosphamide) and the response to non steroidal anti-inflammatory drugs and narcotic analgesics was adequate in all patients except 2 patients whose illness necessitate increasing the dose of steroids.
Table 2.
Some criteria of headache. SLE patients
Frequency of headache: Daily 2 ∼ 3/week Once/week Once/2 weeks Severity of headache: Mild Moderate Severe Life impact of headache: Yes No
11 9 8 2 11 15 4 14 16
International Journal of Neuroscience
Headache in SLE Table 3.
Shows types of headache and triggering factors.
Types of headache: Tension type: Migraine with aura: Migraine without aura: Intracranial hypertension: Cluster type: Triggering factors Stress: Menses: Sun exposure: Lack of sleep:
SLE patients
p. value
15∗ 4 2 8 1
0.02 NS NS NS NS
17∗ 7 3 3
0.03 NS NS NS
Int J Neurosci Downloaded from informahealthcare.com by Universitat de Girona on 11/26/14 For personal use only.
∗ Tension type headache and stress are the most common type of headache and trigger, respectively, among patients: p value ≤ 0.05.
Discussion This study showed that previous year prevalence of headache in patients with SLE is common (75%: tension type: 37.5, migraine: 30, intracranial hypertension: 5, cluster type: 2.5); additionally exposure to stress is the most common headache trigger among those patients. This study revealed that tension type of headache is significantly more common than the other types of headache among SLE patients which is in accordance with [8] and [5] who stated that tension headache occurs in 38.6% of SLE patients. Moreover, the prevalence of tension headache among patients with SLE is more common than in general population in Egypt as stated by Tallawy et al. [12] who assumed the prevalence of headache to be around 3%. Migraine is the second most common type of headache in this study (30%) which is in accordance with [1] who reported that tension type headache represents 39% of patients with SLE, and [13] who stated that the life-time prevalence of headache among SLE patients was around 34% and 27% of migrainous and non migrainous headaches respectively. The variation may be due to the differences in the approach, i.e., 1 year versus life time prevalence. On the other hand, besides the age and sex, income, place of living and climate factors may all influence the prevalence of headache [14]. The percent of migraine headache among SLE in our study is more than that reported by [15] who stated that migraine represents only 19% of patients with SLE. This difference is attributed to the different sample size. Results of this study indicate that headache in patients with SLE is not significantly related to the disease expression or severity which is not in consistent with the idea that intractable headaches are particularly common in patients with active SLE [16,17]. This difference may be attributed to the increasing understanding of headache as a symptom with major morbidity, as well C
2014 Informa Healthcare USA, Inc.
3
as the management of patients with SLE becoming more effective. Another explanation of our finding is that there is no pathogenic mechanism has so far been described that can fully explain headache induced by SLE. Additionally it was reported that the roles of circulating cytokines, vascular injury, neuronal damage or aPL in the development of headache in SLE patients are also a matter of debate [6]. Other concomitant causes such as infection or hypertension should be excluded before assuming that headache is a feature of SLE activity. Therapeutic approach of headache SLE-related remains empirical and based on clinical experience. In conclusion, we can assume that headaches, essentially tension and migraine types are common among SLE patients; especially those with CNS lupus involvement and those with positive family history of headache, yet, the presence and severity of headache are not suggestive of SLE activity or the use of specific anti-lupus drugs. A detailed neurological evaluation and radiological investigation, if necessary, should be performed in SLE patients with prolonged disease and advanced age, regardless of headache characteristics.
Declaration of Interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Grant information: No special fund was given.
References 1. Bicakci S, Ozbek S, Bicakci K, et al. Recurrent headache and MRI findings in systemic lupus erythematosus. J Natl Med Assoc 2008 Mar;100(3):323–6. 2. Fragoso-Loyo H, Atisha-Fregoso Y, Llorente L, S´anchezGuerrero J. Inflammatory profile in cerebrospinal fluid of patients with headache as a manifestation of neuropsychiatric systemic lupus erythematosus. Rheumatology (Oxford) 2013 Dec;52(12):2218–22. 3. Batuecas-Caletr´ıo A, Pino-Montes JD, Cordero-Civantos C, et al. Hearing and vestibular disorders in patients with systemic lupus erythematosus. Lupus 2013;22(5):437–42. 4. Espinosa-Sanchez J, Lopez-Escamez J. Migraine, sudden sensorineural hearing loss and autoimmune ear disease. Cephalalgia 2013 Oct;33(14):1206–7. 5. Hanly J, Urowitz M, O’Keeffe A, et al. Headache in systemic lupus erythematosus: Results from a prospective, international, inception cohort study. Arthritis Rheum 2013;65(11):2887–97. 6. Cuadrado M, Sanna G. Headache and systemic lupus erythematosus. Lupus 2003;12(12):943–6. 7. (SLEDAI) SLEDAI. American College of Rheumatology. 2000. 8. Sfikakis P, Mitsikostas D, Manoussakis M, et al. Headache in systemic lupus erythematosus: a controlled study. Br J Rheumatol 1998 Mar;37(3):300–3.
4
R. Badry and R. M. Gamal
14.
15.
16.
17.
antibodies against phospholipids. J Neurol 1992;239:39– 42. Mitsikostas D, Tsaklakidou D, Athanasiadis N, Thomas A. The prevalence of headache in Greece:Correlations to latitude and climatological factors. Headache 1996;36:168–73. Tjensvoll A, Harboe E, Gøransson L, et al. Migraine is frequent in patients with systemic lupus erythematosus: a case-control study. Cephalalgia 2011 Mar;31(4):401–8. Wallace D, Metzger A. Systemic lupus erythematosus and the nervous system. In: Wallace DJ, Hahn BH, eds. Dubois’ lupus erythematosus. 5th ed. Philadelphia: Lea & Febiger. 1997:723–54. Gladman D, Urowitz M. Sytemic lupus erythematosus. Clinical features. In: Schumacher HR, ed. Primer of the rheumatic diseases. 10th ed. Atlanta: Arthritis Foundation. 1993:106–12.
Int J Neurosci Downloaded from informahealthcare.com by Universitat de Girona on 11/26/14 For personal use only.
9. Fragoso-Loyo H, Richaud-Patin Y, Orozco-Narv´aez A, et al. Interleukin-6 and chemokines in the neuropsychiatric manifestations of systemic lupus erythematosus. Arthritis Rheum. 2007;56:1242–50. 10. Tan E, Cohen A, Fries J. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271–7. 11. Society HCSotIH. The international classification of headache disorders, 2nd edition. Cephalalgia 2004;13(1):S5–S12. 12. Tallawy H, Farghaly W, Rageh T, et al. Door-to-door survey of major neurological disorders (project) in Al Quseir City, Red Sea Governorate, Egypt. Neuropsychiatr Dis Treat 2013;9:767–71. 13. Markus H, Hopkinson N. Migraine and headache in systemic lupus erythematosus and their relationship with
International Journal of Neuroscience
