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Abstract

Background

Headache attributed to ingestion or inhalation of a cold stimulus (HICS), colloquially called ice-cream headache, is a common form of a primary headache in adults and children. However, previous studies on adults are limited due to the small number of patients. Furthermore, most of the subjects in previous studies had a history of other primary headaches.

Methods

Biographic data, clinical criteria of HICS and prevalence of primary headache were collected by a standardized questionnaire. A total of 1213 questionnaires were distributed; the return rate was 51.9% (n = 629); 618 questionnaires could be analyzed.

Results

In a cohort of 618 people aged between 17–63 years (females: n = 426, 68.9%), the prevalence of HICS was 51.3% (317 out of 618). There was no difference between men and women (51.3% vs. 51.6%). The duration of HICS was shorter than 30 sec in 92.7%. In the HICS group, localization of the pain was occipital in 17%. Trigemino-autonomic symptoms occurred in 22%, and visual phenomena (e.g. flickering lights, spots or lines) were reported by 18% of the HICS group. The pain intensity, but not the prevalence of HICS, was higher when tension-type headache and migraine or both were present as co-morbid primary headaches (Numeric Rating Scale (NRS) 4.58 and 6.54, p = 0.006). There was no higher risk of participants with migraine getting HICS than for those who did not have migraine (odds ratio = 1.17, 95% confidence interval (CI) 0.75–1.83; p = 0.496).

Conclusion

The results of this study modified the current criteria for HICS in the ICHD-3 regarding duration and localization. In addition, accompanying symptoms in about one fifth of the participants are not mentioned in the ICHD-3. Neither migraine nor tension-type headache seems to be a risk factor for HICS. However, accompanying symptoms in HICS are more frequent in subjects with another primary headache than in those without such a headache.

Keywords

Headache attributed to ingestion or inhalation of a cold stimulus (HICS)ice-cream headache questionnaire healthy adult subjects trigeminal stimulation

Background

Headache attributed to ingestion or inhalation of a cold stimulus (HICS) is referenced under bullet point 4.5.2 of the 3rd edition of the International Classification of Headache Disorders (ICHD-3) (1). HICS is also known as ‘ice-cream headache’ or colloquially as ‘brain-freeze’. It is most likely caused by eating ice cream, drinking slush ice drinks, or inhaling very cold gases and is characterized by a short-lasting pain sensation in the frontal or temporal region, which may be of high intensity (1). There are some studies that examine HICS in an experimental setting, in which HICS is provoked by either eating ice cream, drinking cold water or keeping an ice cube pressed to the palate (2 –10). Fewer studies explore the characteristics of HICS using questionnaires (5,11 –15). All questionnaires concerning epidemiological and clinical features of HICS were conducted in subjects of grammar school age (5,13,15). In the past, subjects for experimental studies were mainly recruited from a group of participants who suffered from another primary headache disorder (3,7). More recent experimental studies used randomly recruited volunteers (9,10).

This study examines the epidemiological and clinical features of HICS including history of other primary headache in a group of healthy adolescent and adult subjects. The data were acquired using an anonymous, standardized questionnaire.

Methods

We performed a cross-sectional study using an anonymous questionnaire with 87 items in two sections. Participants were students and staff members of the Martin-Luther-University Halle-Wittenberg. Questionnaires were distributed and collected in lectures and seminars. The period of data collection was 6 months in 2015.

All items of this questionnaire were designed to evaluate the criteria for HICS given by the IHS in 2013 (ICHD-3, beta version). However, there were no relevant changes in the diagnostic criteria of HICS from ICHD-3, beta to ICHD-3. No other questionnaire was used as a template. The questionnaires were distributed after a brief oral introduction in order to educate the participants about how to check the boxes so that the forms could be analyzed electronically. The forms were collected roughly two hours after being distributed, with the possibility of a collection after one week. This was necessary to make sure every participant had adequate time to carefully think about every item of the questionnaire.

All items were designed in a multiple-choice manner to simplify an electronic evaluation. In most cases the items were designed in a dichotomous way (“yes” or “no”) to avoid possible confusion.

The first section of the questionnaire contained items concerning the participant’s age, sex, preexisting headache disorders and medication habits. The second section contained items relating to the characteristics of HICS (duration, intensity, quality, localization), circumstances of occurrence of HICS and habits of consuming chilled beverages and food as well as behavior regarding the management of preventing a probable HICS attack. A full version of the questionnaire is attached in the supplemental material.

Exclusion criteria were a failure to state sex, age and an age <17 years. No limitations regarding other primary headache disorders and regular intake of analgesics were made.

The ethics committee of the Martin-Luther-University approved the conducting of this study. Even though the data collection was anonymous, participants were able to contact the Department of Neurology via an email address provided in case of further questions or problems.

Statistical analysis

The obtained data were analyzed using IBS SPPS 23. A p-value of < 0.05 had to be attained in the statistical tests used to be considered statistically significant. To produce a p-value, Student’s t-test, χ² test, Fisher’s exact test, Kruskal-Wallis H test and one-way ANOVA were used appropriately on differing constellations of variables. Not every individual included in this study filled out every item of the questionnaire.

Results

In total, 1213 questionnaires were distributed. There were 629 collected questionnaires (response rate 51.9%). Eleven questionnaires were invalid because of missing key details (sex, age). Thus, the final sample size was 618, with 68.9% (n = 426) females. The age range was 17–63 years (see flowchart, Figure 1).

Figure 1.

Flowchart of study population.

Prevalence of HICS and other additional headache disorders

In total, 317 (51.3%) participants experienced HICS at least once (67.8% females). The number of participants who did not have HICS (the non-HICS group) was 301, including 211 (70.1%) females. The mean age in the HICS group was 23.3 ± 6.5 years (SD) and 24.5 ± 7.9 years (SD) in the group without HICS (p = 0.046). The flowchart in Figure 1 gives an overview of the sample population. The analysis of four age-related groups (n = 311) showed a non-significant decrease of HICS frequency with age (Figure 2).

Figure 2.

Age-related distribution of participants with and without HICS. The percentage of HICS was not significantly different between the four groups.

The prevalence of HICS in females was 50.5%, in males 53.0% (p = 0.541). The prevalence of migraine in all participants was 16% (99/618), that of tension-type headache (TTH) was 24% (150/618). The frequency of migraine in the HICS group was 15.5% (49/317) and in the non-HICS group 17.7% (50/301). This difference was not significant. The prevalence of HICS in the migraine group was 49.5% (49/99) and in the non-migraine group 51.6% (268/519). This was not significantly different (p = 0.55). The frequency of TTH in the HICS group was 24% (76/317); and in the non-HICS group 25% (74/301). The prevalence of HICS in the TTH group was 50.6% (76/150) and in the non-TTH group 49.4% (241/468). This was not significantly different (p = 0.553). The analysis of the odds ratio (OR) in patients with migraine and HICS and TTH and HICS was 1.17 (95% CI 0.75–1.83; p = 0.496) and 1.16 (95% CI 0.80–1.70; p = 0.438) respectively.

Clinical characteristics of HICS (summarized in Table 1 and Table 2)

Intensity: The mean headache intensity in the HICS group without any other coincidental primary headache disorder (n = 186/235) was 4.58 ± 2.2 (SD) (NRS 0–10). Participants with migraine (10/235) or TTH (26/235) stated a higher intensity (mean: 5.7 ± 2.058 (SD) and 5.27 ± 2.07 (SD)) than those without any other primary headache disorder. This difference, however, was not significant.

Localization: According to the methods, the participants could select multiple locations for HICS. The most commonly affected area was the forehead with 73.6% (n = 220) followed by the temporal region with 72.5% (n = 219). Some participants stated a localization of HICS near the upper nose (26.2%; n = 76), the vertex region (20.3%; n = 58), the occiput (16.9%; n = 49) and in the region of the eyes (12.8%; n = 37). An overview is given in Figure 2. HICS was reported as unilateral in 20.1% (n = 61) and as bilateral in 36.5% (n = 111).

Duration: All participants had to decide between the four specifications in the questionnaire regarding the duration of the HICS (shorter than 10 seconds, about 15–30 seconds, longer than 1 minute, longer than 10 minutes). In 46.8% (n = 108), HICS lasted less than 10 sec. A further 45.9% (n = 106) stated that their headache completely resolved after 15–30 sec, 4.3% (n = 10) described a duration of >1 minute and only 1.3% (n = 3) reported a duration of >10 minutes. In all, 1.7% (n = 4) were not able to specify the duration of their headache with the provided items. Participants with a preexisting other primary headache disorder did not suffer from a longer duration of HICS than those without (p = 0.575; Kruskal-Wallis H test).

Quality: The most common pain quality of HICS was stabbing (51.8%; n = 162), pulling (28.1%; n = 88), dull/pressing (9.6%; n = 30) and pulsatile (3.8%; n = 12). None of these pain qualities were significantly associated with either TTH or migraine (p = 0.278; Fisher’s exact test) as co-morbid primary headaches.

Accompanying symptoms: 53% (n = 166) reported additional symptoms during HICS. Some participants reported lacrimation (n = 34, 11%), rhinorrhea (n = 19, 6%) and conjunctival injection (n = 15, 5%). A further 18.5% (n = 57) related visual phenomena, which included flashing light (n = 30, 9.7%) and shimmering spots (n = 27, 8.8%). In all, 1.3% (n = 4) of the participants with HICS experienced a transient loss of sensitivity in sections of the face. Conjunctival injection, flashing light and shimmering spots were significantly more frequent in participants with preexisting primary headache disorders than in those without (p = 0.002, p = 0.008, p < 0.001, Fisher’s exact test) (Table 1).

Table 1.

Characteristics of HICS.

	n	(% of the participants)
Localization
Solely single sided	61	(20.1)
Solely on both sides	111	(36.5)
No side association	132	(36.5)
Forehead	220	(73.6)
Temple region	219	(72.9)
Upper nose	76	(26.2)
Vertex region	58	(20.3)
Occiput	49	(20.1)
Region of the eyes	37	(12.8)
Duration
<10 sec	108	(46.8)
15–30 sec	106	(45.6)
>1 min	10	(4.3)
>10 min	3	(1.3)
Pain quality
Stabbing	162	(51.8%)
Pulling	88	(28.1%)
Dull/pressing	30	(9,6%)
Pulsatile	12	(3.8%)
Attendant symptoms
No attendant symptoms	108	(46.8%)
Probable trigeminal autonomic symptoms	66	(22%)
Lacrimation	34	(11%)
Rhinorrhea	17	(6%)
Conjunctival injection	15	(5%)
Flashing light dots	30	(9.7%)
Loss of sensitivity in the face	4	(1.3%)

Discussion

Frequency

In this study, the lifetime prevalence of HICS (51.3%) is higher than in the group examined by Fuh et al. (40.6%) (13), but lower than in the recent publication by Zierz et al. (62%) (15). In both previous studies, children of school age were examined, whereas in our study adolescents and adults have been enrolled. In this study, 73.2% of the participants reported that the occurrence or the intensity of HICS was reduced by slower velocity of ingestion of cold food or beverages. It may be assumed that adults have learned to prevent HICS by consuming cold food with more caution. Therefore, the higher prevalence of HICS in the study of Zierz et al. may be attributed to the younger age of the participants. Fuh et al. conducted their study in Asia (Taiwan); the study of Zierz et al. and this study were conducted in Europe (Germany). It is known that headache disorders show a variant prevalence between different countries and regions; for example, migraine (with a prevalence of 9% in Asia compared to 15% in Europe (23)). It remains open whether those geographical differences might also be relevant for HICS. Fuh et al. reported a higher prevalence of HICS in boys (13). In the study of Zierz et al. (15) and in the present study, there was no influence of sex on the prevalence of HICS. Analyzing four age-related groups, there were no significant differences between the age groups (Figure 3). However, participants from 30–63 tended to have a slightly, but not significantly, lower prevalence than in the other groups. It remains open whether this corresponds to our previous findings showing that parents and teachers have stated a lower prevalence of HICS than young students (15).

Figure 3.

Localization of HICS (localizations with a percentage less than 10% are not shown in the graphic); (a) face frontal, (b) face lateral.

Pain intensity

The ICHD-3 classification does not state a characteristic intensity of HICS (1). A score of ≤5 on the NRS is regarded as a mild intensity, whereas 6–7 correspond to moderate intensity. Intensities ≥8 are considered as severe (19). In our study, HICS has a mean intensity of 4.6 (SD ± 2.2; NRS 0–10) which corresponds to a mild intensity consistent to the results of Fuh et al., who reported a mild intensity of HICS in 65.5% of the cases. The mean pain intensity reported by Olivera and Valença was slightly higher (5.5 ± 2.2; NRS 0–10) (9). Mean pain intensities in participants with coexisting primary headache disorders (migraine and TTH) was slightly higher than those without a coexistent primary headache disorder (migraine: 5.7 ± 2.058, TTH: 5.27 ± 2.07). The higher HICS pain intensity in patients with additional migraine has also been described by Raskin and Knittle (21), Fuh et al. (13) and Olivera and Valença (9). Participants with a preexisting primary headache may experience a higher level of pain due to central sensitization (20).

Localization

The most frequent sites of HICS found by this study were to those previously described (3,4,7,9,10,13,21,22). Thus, temporal and frontal localizations can be regarded as typical sites for the occurrence of HICS. Occipital localization is not mentioned in the ICHD-3 classification for HICS (1). However, this localization of HICS was reported in 17.5% (13), 16.9% (present study) and was also mentioned by De Olivera and Valença (9). Thus, the occipital localization should be included in the comments of the classification criteria of HICS.

Duration

According to the current classification (ICHD-3), HICS should resolves within 10 minutes. However, the median duration of HICS in an experimental setting using ice water was 10 sec (range: 2–36 sec) and 42 sec (range: 8–125 sec) in an ice cube protocol (10). Fuh et al. reported a duration <30 sec in 72.3% of cases (13). In our study, the duration of HICS was <30 sec in 94.3% of cases. This shorter time limit should be included in the comment section of the classification criteria. However, in 1.3% (n = 3) the duration was even longer than 10 minutes.

Pain quality

In this study, most participants (51.8%; n = 162) stated a stabbing pain quality during HICS. This is in line with the results of Mages et al. (64%) (10). In all, 3.8% of the participants reported a pulsatile pain quality in this study. As a result, at least the stabbing pain quality should be part of the classification criteria of HICS.

Accompanying symptoms

In this study, 22% of the participants reported trigemino-autonomic symptoms (lacrimation, rhinorrhea and conjunctival injection) and 18.5% visual phenomena during HICS. Mages et al. also described lacrimation during HICS (10). The susceptibility for accompanying symptoms during HICS was higher when the patient suffered from another primary headache. In the present study, visual phenomena were significantly more frequent in subjects with another primary headache disorder. The described visual symptoms also typically occur during visual migraine aura. However, it remains open whether these visual symptoms in HICS and in migraine aura are due to similar mechanisms. These accompanying symptoms during HICS are not mentioned by the ICHD-3 classification (1).

Additional headache disorder

In the present study, the frequency of HICS in migraineurs was 49.5%; this is consistent with the number of 55% by Fuh et al. (11). However, both frequencies are considerably lower than those found by Raskin and Knittle (93%) (21). However, the frequency of HICS in non-migraineurs in the present study (55%) was higher than that found by Raskin and Knittel (31%) and Fuh et al. (29%). In our study, TTH was more frequent than migraine (24% vs. 15%). The frequency of HICS was similar in the migraine group, the TTH group, and in the group without additional headache. Thus, in contrast to previous studies, migraine seems not to be a risk factor for HICS. For comparison, the data of the present study and of relevant previous studies are summarized in Table 2. The comparison between the established ICHD-3 criteria of HICS (1) and key findings of our study are presented in Table 3.

Table 2.

Frequency and intensity of HICS in additional headache disorders. Pain intensity was determined using the NRS ranging from 0–10 (most severe). For comparison, relevant previous studies are also shown in this table. CI: confidence interval, TTH: tension type headache.

Additional headache	HICS	Pain intensity of HICS
Present study
No additional headache	51.3% (182/356)	4.6 ± 2.2
(58%; 356/618)
95% CI	46.1–53.5
Migraine (16%; 99/618)	49.5% (49/99)	5.7 ± 2.1
95% CI	39.5–59.5
No migraine	51.6% (268/519)
95% CI	46.8–56.3
TTH (24%; 150/618)	50.6% (76/150)	5.3 ± 2.1
95% CI	45.8–58.8
No TTH	51.5 % (241/468)
95% CI	47.0–56.0
Raskin & Knittle (1976)
Migraine	93% (55/59)	Intense pain
95% CI	86.4–99.6
No other headache	31% (15/49)	Mild pain
95% CI	17.6–44.4
Fuh et al. (2003)
Migraine	55.2%	More severe than in non-migraine (p = 0.003)
Non-migraine headache	45.5%
No other	29.1%
headache
Zierz et al. (2016)
Any other headache	75.5% (71/94)	n.a.
95% CI	66.6–84.4
No other headache	55.4% (102/184)
95% CI	48.1–62.7

Table 3.

Comparison between the established ICHD-3 criteria of HICS and key findings in our study. TAS: trigemino-autonomic symptoms; TTH: tension-type headache; n.m.: not mentioned.

	Criteria of ICHD-3	Results of this study
Intensity (NRS 0–10)	n.m.	Mean intensity: 4–6/10
Duration	Resolving within 10 minutes	Resolving within 30 sec in >90% of the experimenters
Localization	Frontal or temporal	Frontal (73.6%) Temporal (72.5%) Occipital (16.9%)
Quality of pain	n.m.	Stabbing (51.8%) Pulling (28.1%)
Accompanying symptoms	n.m.	Visual phenomena (18.5%); TAS (22.4%)
Connection to other primary headaches	May be lateralized to the side of usual migraine headache	Higher intensity with comorbid TTH and migraine

Limiting factors: The evaluation of primary co-morbid headache disorders was only based on a standardized questionnaire. This was not confirmed by a personal interview. The use of headache-specific medication, especially prophylactic treatment of migraine, was not asked about in the questionnaire. This may influence both prevalence and intensity of HICS and the appearance of accompanying symptoms.

Article highlights

In adults, HICS has a prevalence of 51.3%.

Accompanying symptoms during HICS occurred in 53% of the participants (22% trigeminal-autonomic symptoms and 18.5% visual phenomena).

Our data expand the ICHD-3 criteria for HICS.

Neither migraine nor TTH are risk factors for HICS.

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 received no financial support for the research, authorship, and/or publication of this article.

References

Headache Classification Committee of the International Headache Society (IHS). The International Classification of Headache Disorders, 3rd edition. Cephalalgia 2018; 38: 1–211.

Smith

. Ice cream headache. Va Med Mon (1918) 1963; 90: 562–564.

Bird

MacGregor

Wilkinson

. Ice cream headache – site, duration, and relationship to migraine. Headache 1992; 32: 35–38.

Mattsson

. Headache caused by drinking cold water is common and related to active migraine. Cephalalgia 2001; 21: 230–235.

Kaczorowski

. Ice cream evoked headaches. Ice cream evoked headaches (ICE-H) study: Randomised trial of accelerated versus cautious ice cream eating regimen. BMJ 2002; 325: 1445–1446.

Selekler

Erdogan

Budak

. Prevalence and clinical characteristics of an experimental model of “ice-cream headache” in migraine and episodic tension-type headache patients. Cephalalgia 2004; 24: 293–297.

Selekler

Budak

. Idiopathic stabbing headache and experimental ice cream headache (short-lived headaches). Eur Neurol 2004; 51: 6–9.

Blatt

Falvo

Jasien

, et al. Cerebral vascular blood flow changes during “brain freeze”. FASEB J 2012; 26(S1): 685.4–685.4–685.4–685.4.

de Oliveira

Valença

. The characteristics of head pain in response to an experimental cold stimulus to the palate: An observational study of 414 volunteers. Cephalalgia 2012; 32: 1123–1130.

10.

Mages

Hensel

Zierz

, et al. Experimental provocation of “ice-cream headache” by ice cubes and ice water. Cephalalgia 2016; 37: 464–469.

11.

Drummond

Lance

. Neurovascular disturbances in headache patients. Clin Exp Neurol 1983; 20: 93–99.

12.

Rasmussen

Jensen

Olesen

. Impact of headache on sickness absence and utilization of medical services: A Danish population study. J Epidemiol Community Health 1992; 46: 443–446.

13.

Fuh

J-L

Wang

S-J

S-R

, et al. Ice-cream headache – a large survey of 8359 adolescents. Cephalalgia 2003; 23: 977–981.

14.

Sjaastad

Bakketeig

. Hydrogen sulphide headache and other rare, global headaches: Vågå study. Cephalalgia 2006; 26: 466–476.

15.

Zierz

Mehl

Kraya

, et al. Ice cream headache in students and family history of headache: A cross-sectional epidemiological study. J Neurol 2016; 263: 1106–1110.

16.

Peng

Wang

S-J

. Epidemiology of headache disorders in the Asia-Pacific region. Headache 2014; 54: 610–618.

17.

Burstein

Noseda

Borsook

. Migraine: Multiple processes, complex pathophysiology. J Neurosci 2015; 35: 6619–6629.

18.

Steiner

Stovner

Katsarava

, et al. The impact of headache in Europe: Principal results of the Eurolight project. J Headache Pain 2014; 15: 31–31.

19.

Boonstra

Stewart

Köke

AJA

, et al. Cut-off points for mild, moderate, and severe pain on the numeric rating scale for pain in participants with chronic musculoskeletal pain: Variability and influence of sex and catastrophizing. Front Psychol 2016; 7: 1466–1466.

20.

Woolf

. Central sensitization: Implications for the diagnosis and treatment of pain. Pain 2011; 152: 2–15.

21.

Raskin

Knittle

. Ice cream headache and orthostatic symptoms in participants with migraine. Headache 1976; 16: 222–225.

22.

Hulihan

. Ice cream headache. BMJ 1997; 314: 1364–1364.

23.

Stovner

Hagen

Jensen

, et al. The global burden of headache: A documentation of headache prevalence and disability worldwide. Cephalalgia 2007; 27: 193–210.

Prevalence and characteristics of headache attributed to ingestion or inhalation of a cold stimulus (HICS): A cross-sectional study

Abstract

Background

Methods

Results

Conclusion

Keywords

Background

Methods

Statistical analysis

Results

Prevalence of HICS and other additional headache disorders

Clinical characteristics of HICS (summarized in Table 1 and Table 2)

Discussion

Frequency

Pain intensity

Localization

Duration

Pain quality

Accompanying symptoms

Additional headache disorder

Article highlights

Footnotes

Declaration of conflicting interests

Funding

References