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Abstract

Introduction

Osmophobia has been suggested as an additional symptom of migraine without aura, and a high prevalence of osmophobia of up to 50% has been reported in the literature. We conducted a nosographic study of osmophobia in all migraineurs and tension-type headache patients and a field testing of suggested diagnostic criteria of osmophobia, presented in the appendix of the second edition of The International Classification of Headache Disorders and suggested by Silva-Néto et al. and Wang et al., in migraine without aura and tension-type headache patients (n = 1934).

Materials and methods

Each patient received a validated semi-structured interview. All subjects fulfilled the diagnostic criteria of the second edition of The International Classification of Headache Disorders for migraine or tension-type headache. Statistical analyses were performed using statistical software R. The statistical R package “Caret” was used to construct a confusion matrix and retrieve sensitivity, which is defined as the suggested criteria’s ability to correctly diagnose migraine without aura patients, and specificity, defined as the suggested criteria’s ability to not wrongly diagnose tension-type headache patients.

Results

Osmophobia was present in 33.5% of patients with migraine with aura, in 36.0% of patients with migraine without aura, and in 1.2% of patients with tension-type headache. All migraineurs with osmophobia also fulfilled the current criteria for migraine by having nausea or photophobia and phonophobia. The appendix criteria had a sensitivity of 0.96 and a specificity of 0.99 for migraine without aura, and a sensitivity of 0.65 and a specificity of 0.99 for probable migraine without aura. Both the criteria by Silva-Néto et al. and Wang et al. had a sensitivity of 0.98 and a specificity of 0.99 for migraine without aura, and a sensitivity of 0.66 and a specificity of 0.99 for probable migraine without aura.

Discussion

This study demonstrates the remarkable specificity of osmophobia. The criteria by Silva-Néto et al. and Wang et al. both had a higher sensitivity than the appendix criteria for migraine without aura; all three criteria had a low sensitivity for probable migraine without aura. However, neither the appendix criteria nor the criteria by Silva-Néto et al. or Wang et al. added any extra patients that would not have been diagnosed by the current diagnostic criteria for migraine. Osmophobia is a valuable symptom that may be useful to differentiate between migraine without aura and tension-type headache in difficult clinical cases.

Conclusion

Our results do not suggest that alterations of the current diagnostic criteria for migraine without aura are needed.

Keywords

Migraine osmophobia field test nosography headache classification

Introduction

Osmophobia has been suggested as an additional associated symptom of migraine without aura (MO) in the appendix of the second edition of The International Classification of Headache Disorders (ICHD-2) (1). The Headache Classification Subcommittee encouraged researchers to test and further develop all parts of the classification, including the appendix criteria, by nosographic and epidemiologic research. Several studies have since investigated osmophobia in adult headache patients (2 –13) and in juvenile patients (14 –17) and prevalences from 20–50% in MO have been reported. A significantly higher prevalence of osmophobia among Asian patients than Western patients with migraine, and strangely enough tension-type headache (TTH), has been reported (18), which makes its usefulness in the diagnostic criteria questionable. Osmophobia seems specific (6,19 –21) in differentiating migraine from other primary headaches, but is not a very sensitive symptom (4,16). Some studies have suggested including osmophobia in the headache classification (13,18,22,23) and Silva-Néto et al. (24), Wang et al. (25), and Ghandehari et al. (26) have suggested explicit diagnostic criteria that could be tested. Osmophobia is defined as aversion to smell, and is a sensory disturbance. Other sensory disturbances associated with migraine and included in the current diagnostic criteria for MO are photophobia and phonophobia. It is important that a classification system is fairly easy to use by clinicians and it should not be more complicated than necessary. Based on these issues, we found it timely to field test the suggested criteria, which include osmophobia (1,24,25). Our study consists of two parts: A nosographic study of osmophobia in migraineurs and TTH patients, and a field testing of the diagnostic criteria previously suggested in MO and TTH patients (n = 1934).

We hypothesize that migraineurs with osmophobia are those who also fulfill current diagnostic criteria by having nausea or photophobia and phonophobia.

Materials and methods

Nosographic analysis of osmophobia

The nosographic analysis is a systematic description of osmophobia within patients with migraine and TTH. The analysis is based on semi-structured interviews of patients with migraine with aura (MA), MO, and TTH. In order to perform a proper description of osmophobia, data were divided in three headache groups: MA, MO, and TTH. The relationship between the different headaches (MA, MO, and TTH) and osmophobia was analysed. Furthermore, the relationship between nausea, photo- and phonophobia, and osmophobia was analysed.

The study population

The study population consisted of adult men and women (≥18 years of age) from the Danish Headache Center and their adult family members suffering from the full range of the International Headache Society (IHS) defined migraine with and without aura (1). Family members without migraine but with TTH were also included in the cohort. Subjects were excluded if they had headaches thought to be related to trauma or injuries; complicated neurological problems, that is, underlying brain or systemic illness related to their headaches; suffered from other concomitant headaches than TTH; declined to, or were cognitively not able to, participate in the semi-structured interview; if they had other than Danish ethnicity; and if they were ≤18 years of age. Data were collected in three phases as previously described (27 –29). We used data from our patients with MA (n = 274) and probable MA (n = 72), MO (n = 439) and probable MO (n = 61), infrequent episodic TTH (n = 136) and frequent episodic TTH (n = 36) for the nosographic study, and patients with probable MO and MO and TTH for the field testing. Each patient had received a validated semi-structured interview (30,31) performed by a trained physician or a senior medical student specifically trained in headache diagnostics. All subjects fulfilled the ICHD-2 diagnostic criteria for MO or TTH.

Semi-structured interview

The interview included information about aura, headache characteristics, accompanying symptoms, frequency, duration, precipitating and provoking factors, treatment response, comorbidities and familial occurrence, and it enabled equal assessment of probands with migraine and relatives. The diagnosis relied on a detailed recording of the above-mentioned symptoms and explicit diagnostic criteria of the ICHD-2 (1). All interviews performed in the study were validated by a trained physician, enabling high quality data material.

We tested the diagnostic criteria for MO suggested in the appendix of ICHD-2 (1) and by Silva-Néto et al. (24) and Wang et al. (25). The suggested revision of the ICHD-2 criterion D for MO in the appendix of ICHD-2 by the Headache Committee was as follows: “During headache at least two of the following: (1) nausea; (2) vomiting; (3) photophobia; (4) phonophobia; (5) osmophobia” (1). The suggested revision of the ICHD-2 criterion D by Silva-Néto et al. was as follows: “During headache at least one of the following: (a) nausea and/or vomiting; (b) photophobia and phonophobia; and (c) osmophobia” (24). The suggested revision of the ICHD-2 criterion D by Wang et al. was as follows: “Nausea and/or vomiting or two among osmophobia, photophobia, or phonophobia” (25). Ghandehari et al. suggested a new set of criteria for the diagnosis of migraine: “Seven items: (i) unilateral location; (ii) throbbing quality; (iii) nausea and/or vomiting; (iv) photophobia and/or sonophobia; (v) osmophobia; (vi) family history of migraine; and (vii) aura. At least three items in adults and at least two items in children are necessary [for migraine diagnosis]” (26). This is a suggestion for totally new criteria for migraine and not just strictly relating to osmophobia, therefore, we did not test the suggested criteria by Ghandehari et al. in this paper.

Statistical analysis

Statistical analyses were performed using statistical software R version 3 and R Studio version 1. Standard deviations and t-tests were used to compare the means after checking that data were normally distributed. Most data are descriptive information, absolute numbers, and percentages. Categorical variables such as osmophobia, nausea, and photo/phonophobia were expressed in percentages and their frequencies compared using Fisher’s exact test. A two tailed p-value was used, and the cutoff statistical significance was p < 0.05. We report the resulting p-value, odds ratio (OR), and 95% confidence interval for the OR for having osmophobia in migraineurs versus patients with TTH. We constructed a confusion matrix to calculate sensitivity and specificity using the statistical R package “Caret”. Sensitivity is the suggested criteria’s ability to correctly detect patients who have MO and is defined by $\frac{number of true positives}{number of true positives + number of false negatives}$ , and specificity is the suggested criterion’s ability to correctly not diagnose ICHD-2 classified TTH patients with MO, and is defined by $\frac{number of true negatives}{number of true negatives + number of false positives}$ .

Results

Nosographic analysis

Data were divided in three headache groups: MA, MO, and TTH. Patients diagnosed with either 1.1, migraine without aura or 1.6.1, probable migraine without aura, were included in the group “migraine without aura”; patients diagnosed with 1.2, migraine with aura, 1.6.2 probable migraine with aura and a combination of 1.2 and 1.1, MAMO, were included in the group “migraine with aura”. Eighty percent of the patients with MA also suffered from TTH, and 75.4% of the patients with MO also suffered from TTH. Chronic migraine patients were not included. Patients who did not suffer from migraine but only suffered from TTH were included in the third group “tension-type headache”. The TTH group consisted of patients with 2.1, infrequent episodic TTH and 2.2, frequent episodic TTH. Chronic TTH and probable TTH patients were not included, see Table 1.

Table 1.

Prevalence of osmophobia in this study.

Headache type	ICHD-II code	Diagnosis	Osmophobia	No osmophobia	Osmophobia %
MA	1.2, 1.6.2	MA, pMA	116	230	33.5
MO	1.1, 1.6.1	MO, pMO	180	320	36.0
TTH	2.1, 2.2, 2.3	iTTH, fTTH	2	170	1.2
Total			298	720

MA: migraine with aura; pMA: probable migraine with aura; MO: migraine without aura; pMO: probable migraine without aura; iTTH: infrequent episodic tension-type headache; fTTH: frequent episodic tension-type headache.

Relationship between different headaches and osmophobia

No statistically significant difference in the frequency of osmophobia was found between patients with MA and MO. There was a statistically significant difference between patients with TTH with osmophobia and MA with osmophobia and between patients with TTH with osmophobia and MO with osmophobia (Table 2).

Table 2.

Relationship between headaches with osmophobia in this study.

Headache type	p-value (CI)	OR
MA with osmophobia vs. MO with osmophobia	0.4645 (0.664–1.208)	0.897
TTH with osmophobia vs. MA with osmophobia	<0.0001 (0.003–0.086)	0.023
TTH with osmophobia vs. MO with osmophobia	<0.0001 (0.002–0.076)	0.020

Relationship between nausea, photo- and phonophobia, and osmophobia

The demographics and phobias of patients with MA, MO, and TTH are presented in Tables 3 and 4. Table 3 shows the relationship between nausea and osmophobia; 109 of 116 patients with MA who experienced osmophobia also experienced nausea, only seven patients did not report nausea. One hundred and seventy of 180 patients with MO who experienced osmophobia also experienced nausea; only 10 patients did not report nausea. Two of two patients with TTH who reported osmophobia did not report nausea. Table 4 shows the relationship between photo-, phono- and osmophobia in patients who reported no nausea; all seven patients with osmophobia and no nausea also experienced photophobia and phonophobia, leaving no undiagnosed MA patients with osmophobia by the current classification. All 10 MO patients with osmophobia and no nausea also experienced photophobia and phonophobia, leaving no undiagnosed MO patients with osmophobia by the current classification. The two TTH patients with osmophobia and no nausea from Table 3 also reported photophobia and phonophobia.

Table 3.

Relationship between nausea and osmophobia for MA, MO and TTH.

Nausea	Osmophobia	No osmophobia	NA	Total
MA
Yes	109	146	1035	1290
No	7	84	293	384
NA	0	0	77	77
Total	116	230	1405	1751
MO
Yes	170	238	991	1399
No	10	81	159	250
NA	0	1	27	28
Total	180	320	1177	1677
TTH
Yes	0	3	1	4
No	2	167	77	246
NA	0	0	1	1
Total	2	170	79	251

Table 4.

Relationship between photo- and phonophobia and osmophobia for subjects with MA, MO and TTH with no nausea.

Photo- and phonophobia	Osmophobia and no nausea	No osmophobia and no nausea	NA	Total
MA
Yes	7	84	293	384
No	0	0	0	0
NA	0	0	0	0
Total	7	84	293	384
MO
Yes	10	81	159	250
No	0	0	0	0
NA	0	0	0	0
Total	10	81	159	250
TTH
Yes	2	167	77	246
No	0	0	0	0
NA	0	0	0	0
Total	2	167	77	246

Field test of osmophobia

We field tested the ICHD-2 appendix criteria (1), the proposed criteria for MO that include osmophobia by Silva-Néto et al. (24) and by Wang et al. (32). The suggested diagnostic criteria were applied to all patients with MO, probable migraine without aura (pMO) and TTH. If patients with MA reported osmophobia, they would already be diagnosed with MA according to the ICHD-2 criteria because of the aura symptoms; these patients were therefore not included in the field testing. One thousand, nine hundred and twenty eight patients were included in our field test; they were all diagnosed according to the ICHD-2 criteria: 1567 patients had MO, 110 patients had pMO, and 251 patients had TTH. The ICHD-2 appendix criteria for MO were fulfilled by 1506 out of 1567 patients who were diagnosed with MO by the ICHD-2 criteria. Thus, 61 patients with MO were not diagnosed with MO by the appendix criteria. The ICHD-2 appendix criteria for MO were fulfilled by 52 out of 110 patients who were diagnosed with pMO by the ICHD-2 criteria. Thus, 58 patients with pMO were not diagnosed with MO by the appendix criteria. Two patients who fulfilled the ICHD-2 diagnostic criteria for TTH fulfilled the appendix criteria for MO. The criteria by Silva-Néto et al. for MO were fulfilled by 1542 out of 1567 patients who were diagnosed with MO by the ICHD-2 criteria. Thus, 25 patients with MO were not diagnosed with MO by the Silva-Néto et al. criteria. The criteria by Silva-Néto et al. for MO were fulfilled by 53 out of 110 patients who were diagnosed with pMO by the ICHD-2 criteria. Thus, 57 patients with pMO were not diagnosed with MO by the Silva-Néto et al. criteria. Three patients who fulfilled the ICHD-2 diagnostic criteria for TTH fulfilled the criteria by Silva-Néto et al. for MO. The criteria by Wang et al. for MO were fulfilled by 1542 out of 1567 patients who were diagnosed with MO by the ICHD-2 criteria. Thus, 25 patients with MO were not diagnosed with MO by the Wang et al. criteria. The criteria by Wang et al. for MO were fulfilled by 53 out of 110 patients who were diagnosed with pMO by the ICHD-2 criteria. Thus, 57 patients with pMO were not diagnosed with MO by Wang et al. criteria. Three patients who fulfilled the ICHD-2 diagnostic criteria for TTH fulfilled the criteria by Wang et al. for MO. The appendix criteria had a sensitivity of 0.96 $(\frac{1567}{1567 + 61})$ and a specificity of 0.99 $(\frac{251}{251 + 2})$ for MO and a sensitivity of 0.65 $(\frac{110}{110 + 58})$ and a specificity of 0.99 for pMO $(\frac{251}{251 + 2})$ . The criteria by Silva-Néto et al. had a sensitivity of 0.98 $(\frac{1567}{1567 + 25})$ and a specificity of 0.99 $(\frac{251}{251 + 3})$ for MO and a sensitivity of 0.66 $(\frac{110}{110 + 57})$ and a specificity of 0.99 $(\frac{251}{251 + 3})$ for pMO. The criteria by Wang et al. had a sensitivity of 0.98 $(\frac{1567}{1567 + 25})$ and a specificity of 0.99 $(\frac{251}{251 + 3})$ for MO and a sensitivity of 0.66 $(\frac{110}{110 + 57})$ and a specificity of 0.99 $(\frac{251}{251 + 3})$ for pMO.

Discussion

In the present study, osmophobia was present in 33.5% of patients with MA, in 36.0% of patients with MO, and in 1.2% of patients with TTH in accordance with previous literature (2 –12,18). All migraineurs with osmophobia in this study also fulfilled the ICHD-2 criteria for migraine by having nausea or photophobia and phonophobia. The present study is the first field testing of the ICHD-2 appendix criteria, the criteria by Silva-Néto et al., and the criteria by Wang et al. for MO including osmophobia. The appendix criteria had a sensitivity of 0.96 and specificity of 0.99 for MO, and a sensitivity of 0.65 and specificity of 0.99 for pMO. Both the criteria by Silva-Néto et al. and Wang et al. had a sensitivity of 0.98 and specificity of 0.99 for MO, and a sensitivity of 0.66 and specificity of 0.99 for pMO.

A previous, very thorough, review (18) has highlighted that there has been an increased interest in osmophobia in relation to migraine within the last 12 years and that the prevalences reported are varying, due to: Anamnestic difficulties in investigating osmophobia; differences among selected patients with regards to sex, age distribution, type of migraine, and comorbidities; and ethnic differences. This study demonstrates the remarkable specificity of osmophobia, as previous studies also have reported (6,19). Since osmophobia almost always occurs with photophobia and phonophobia, it seems as if osmophobia is part of a generalized hypersensitivity to environmental stimuli. Osmophobia may be a valuable symptom in daily clinical routine and a good clinical parameter for migraine (18), because it is highly specific for migraine, and the high prevalence, up to 50%, makes it a very relevant symptom. In those patients that are borderline between MO and TTH, osmophobia makes MO the certain diagnosis (7,18,25,33,34). However, the nosographic analysis showed that osmophobia always occurred in patients who also had nausea or photo- and phonophobia. The appendix criteria missed 61 of the patients with ICHD-2 MO and 58 of the patients with ICHD-2 pMO and added two patients diagnosed with ICHD-2 TTH, and the criteria by Silva-Néto et al. and Wang et al. missed 25 of the patients with ICHD-2 MO and 57 of the patients with ICHD-2 pMO and added three patients diagnosed with ICHD-2 TTH. The criteria by Silva-Néto et al. and Wang et al. had a slightly higher sensitivity than the appendix criteria for MO; on the other hand, all three criteria had a low sensitivity for pMO. A classification system should be easy to understand and be as simple as possible. Thus, in order to revise criteria, the new criteria need to add sensitivity or specificity. This was not the case with any of the suggested criteria that included osmophobia. Osmophobia added only three out of 251 patients previously diagnosed with TTH. This is just 1% added, and it missed 5% of MO and pMO patients. Therefore, we feel confident that osmophobia should not be included in the diagnostic criteria.

Conclusion

Osmophobia occurs in one third of migraine patients with or without aura, and not in TTH. Its inclusion in the diagnostic criteria for MO is, however, not warranted.

Clinical implications

Osmophobia does not add more migraine without aura patients than the current ICHD-2 criteria. The inclusion of osmophobia in the diagnostic criteria for migraine without aura is not warranted.

Osmophobia may be a valuable symptom in clinical practice, because it is highly specific for migraine without aura.

In patients that are borderline between migraine without aura and tension-type headache, osmophobia makes migraine without aura the certain diagnosis.

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Our research group has received grants from Candys Foundation (CEHEAD). The funding body had no role in the study.

Ethics board approval

Our research group has permissions and approval from the Data Protection Agency (GLO-2010-10) and the Ethical Committee (H-2-2010-122).

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Nosographic analysis of osmophobia and field testing of diagnostic criteria including osmophobia

Abstract

Introduction

Materials and methods

Results

Discussion

Conclusion

Keywords

Introduction

Materials and methods

Nosographic analysis of osmophobia

The study population

Semi-structured interview

Statistical analysis

Results

Nosographic analysis

Relationship between different headaches and osmophobia

Relationship between nausea, photo- and phonophobia, and osmophobia

Field test of osmophobia

Discussion

Conclusion

Clinical implications

Footnotes

Declaration of conflicting interests

Funding

Ethics board approval

References