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Trofimova et al.
Imaging of Nontraumatic Pediatric Headaches
FOCUS ON:
activities, and academic performance [8]. The were identified through PubMed searches of available (ICHD-3 beta) [31]. This version
effect of headaches on quality of life in chil- English-language articles published between is more evidence based than the previous
dren and adolescents has been likened to that January 1995 and December 2017. The fol- two versions, and clinicians are encouraged
of rheumatoid arthritis or cancer [12]. There lowing three search strategies were used: to use the most updated edition in their ev-
are multiple risk factors for headaches in chil- first, (Headache/classification OR Headache/ eryday practice [13]. The ICHD-3 beta clas-
diagnosis OR Headache/diagnostic imag- sifies headaches into three main groups:
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Red Flags in Childhood Headache In 1997, a retrospective study of 315 chil- of less than 6 months’ duration; age younger
The cornerstone of parental anxiety and dren with headaches identified a set of clini- than 6 years; no family history of migraine
clinicians’ uncertainty about pediatric head- cal criteria that were each highly predictive or primary headaches; occipital headache;
aches is the possibility of an underlying brain of space-occupying lesions: persistent head- change in type of headache; subacute onset
tumor. Associations between headaches and aches of less than 6 months’ duration, head- and progressive headache severity; a new-on-
set headache in a child with immunosuppres-
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brain tumors have been studied extensively. aches with abnormal neurologic examina-
In a cohort of 72 children with brain tumors, tion, persistence of headaches with absence sion; first or worst headache; systemic symp-
88% had headaches for 2 weeks to 2 months of a family history of migraine or primary toms and signs; and a headache associated
before the physical examination revealed any headache, persistent headaches associated with confusion, mental status changes, or
other abnormalities [36]. At the same time, with substantial confusion, headaches awak- focal neurologic complaints [41]. These red
the general frequency of brain disease in ening the child from sleep or immediately af- flags were eventually adapted to become the
children with headache as the only symptom ter waking up, and family history or medical SNOOOPPPPY mnemonic for use in pediat-
is quoted as less than 1% [37]. In 1991, the history predisposing to CNS lesions [2]. ric populations [13, 42] (Table 1). The pedi-
Childhood Brain Tumor Consortium Study The mnemonic SNOOP (systemic disease, atric red flags include systemic symptoms or
analyzed 3276 children with brain tumors neurologic symptoms, onset, occipital, and illness (e.g., fever, altered level of conscious-
and found that, overall, 62% of children with pattern) for clinical criteria that can serve ness, anticoagulation therapy, pregnancy,
brain tumors had headaches [38]. Most com- as a red flag for underlying significant le- cancer, or HIV infection), neurologic signs
monly, headaches were seen with infratento- sions was first introduced by Dodick in 2003 or symptoms (e.g., papilledema, asymmet-
rial tumors (70%); supratentorial tumors were [40] (Table 1). This rule initially was devel- ric cranial nerve function, asymmetric mo-
associated with headache in 58% of patients, oped for adults. In 2010, Kabbouche and tor function, abnormal cerebellar function,
and spinal canal tumors were associated with Cleves [41] summarized the existing litera- new seizure, or focal findings at examina-
headache in 34% of patients. In this cohort, ture and concluded that children with head- tion), onset recently or suddenly (thunderclap
fewer than 1% of those who presented with aches should undergo neuroimaging if they headache), occipital localization of pain, pre-
headaches had no other recorded symptoms met one or more of the following criteria: cipitated by Valsalva maneuver, positional,
on clinical examination at the time of diag- abnormal findings at neurologic examina- progressive, parent (i.e., lack of family histo-
nosis [38]. Another study reported that three tion; atypical presentation, including verti- ry), and years (i.e., age < 6 years) [13, 40, 42].
of 709 (0.4%) neurologically normal children go, intractable vomiting, or headache wak- These criteria have not been validated in
had significant brain abnormalities [39]. ing the child from sleep; a recent headache pediatric populations, and although authors
TABLE 1: Evolution of Adult Clinical Headache Evaluation Criteria Over Time and Adaptation to the Pediatric Setting
Acronym, Study
Letter SNOOP, Dodick 2003 [40] SNOOP, Nye and Ward 2015 [42] SNOOPPPPY, Gofshteyn and Stephenson 2016 [13]
a Consultation for “a” particular headache
S Systemic symptoms and signs (fever, myalgias, Systemic symptoms: fever, chills, weight Systemic symptoms or illness: fever, altered level of
weight loss) loss, HIV infection, history of cancer consciousness, anticoagulation therapy,
pregnancy, cancer, HIV infection (especially
concerning in new HIV diagnosis, poor control or
compliance, or associated fever)
S Systemic disease (malignancy, AIDS)
N Neurologic symptoms or signs Neurologic signs or symptoms: confusion, Neurologic symptoms or signs: papilledema,
change in mental status, asymmetric asymmetric cranial nerve function, asymmetric
reflexes, or other abnormalities at motor function, abnormal cerebellar function, new
examination seizure, focal findings at examination
O Onset: sudden (thunderclap headache) Onset: acute, sudden, or split-second Onset recently or suddenly (thunderclap headache)
thunderclap headache
O Onset after age 40 years Older patient: 50 years old with new onset Occipital localization of pain
or progressive headache
P Pattern change: progressive headache with Previous headache history: first headache Pattern: precipitated by Valsalva maneuver
loss of headache-free periods or different (change in attack frequency,
severity, or clinical features)
P Pattern change: change in type of headache Pattern: positional
P Pattern: progressive
P Parents: lack of family history
Y Headache in children < 5 years Years < 6
None Headache worsening under observation
Note—Changes from one version to another are highlighted in bold.
generally agree on many of the included clin- tients with occipital headaches were more The following symptoms were listed as
ical features, there is no consensus on some likely to undergo neuroimaging [49]. Occipi- significantly increasing the odds of finding
of the other features, such as the age below tal location of headache was associated with a significant abnormality at neuroimaging:
which children require neuroimaging or par- Chiari I malformation, but no significant as- rapidly increasing headache frequency, his-
ticular headache characteristics (Table 1 and sociations were found with elevated intracra- tory of dizziness or lack of coordination, sub-
nial pressure, tumor, benign cyst, or sinusitis
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Fig. 2). A retrospective study of 1562 pa- jective numbness or tingling, headache caus-
tients with recurrent headaches, which in it- [49]. The authors concluded that neuroimag- ing awakening from sleep, and history of
self is not considered an imaging indication, ing in patients with occipital pain without an headache worsening with Valsalva maneu-
found neuroimaging abnormalities in 9.3% otherwise concerning history or abnormal ver [4, 15]. In 2002, the AAN and the Child
of patients; of these, only 0.71% of findings findings at neurologic examination can be Neurology Society released clinical guide-
(11/1562) represented lesions requiring surgi- foregone [49]. lines that adapted the U.S. Headache Con-
cal excision [43]. The strongest predictor for One factor that is not currently consid- sortium recommendations to the pediatric
a serious intracranial lesion in that study was ered as a red flag is parental concern. A re- population (ages 3–18 years) with recurrent
an abnormal neurologic examination, and the cent study investigated 449 patients with headaches not associated with trauma, fever,
authors requested stricter guidelines for use headaches who were referred to a neurology or other secondary causes [15]. These 2002
of neuroimaging in children with headaches clinic and of whom 72.2% underwent brain recommendations were based on six studies
[43]. There were no lesions requiring surgical MRI. Of the patients who underwent imag- conducted between 1980 and 2000 (one class
excision in patients who underwent neuroim- ing, 18.2% of the MRI examinations were II and five class III studies) and included a
aging for a change in their type of headache, performed because of an atypical headache total of 1275 children with recurrent head-
and the authors even suggested removing pattern or presence of neurologic abnormali- aches [15]. Almost half (605) of these chil-
this indication for imaging from the pediat- ties, and 81.8% of MRI examinations were dren underwent neuroimaging and neurolog-
ric guidelines [43]. Another study found that ordered because of parental concerns [50]. ic examination [15]. The analysis found that
three abnormal findings at neurologic ex- Interestingly, the rate of abnormal MRI find- lesions requiring surgical treatment were
amination—papilledema, reduced conscious ings in this study was similar between pa- found in 14 children (2.3%) and all of them
level, and paralysis—had a strong positive tients for whom neuroimaging was indicat- were accompanied by abnormal findings at
predictive value for underlying significant ed per clinical indications (16.9%) and those neurologic examination [15]. No lesions re-
pathologic findings and therefore justified for whom parental concern was the driver for quiring surgical intervention were found in
neuroimaging [44]. A retrospective chart neuroimaging (21.9%) [50]. Significant brain patients with normal neurologic examination
analysis of 409 children found that blurry vi- abnormalities relevant to headaches were findings [15]. Thus, similar to the recommen-
sion and ataxia were the only clinical features found in 0.6% of patients who underwent im- dations in adults, it was suggested that neu-
that could predict an underlying intracranial aging because of clinical indications. For pa- roimaging is not indicated in children with
lesion [45]. Another study found that a bilat- tients who underwent imaging because of pa- recurrent headaches and a normal neurolog-
eral headache in children with focal neuro- rental concerns, imaging findings were made ic examination [15]. Neuroimaging should be
logic deficits had the highest odds of having a as well, but these were not necessarily caus- considered for children with recurrent head-
secondary headache cause [46]. ative of headaches (e.g., Chiari I malforma- aches and abnormal neurologic examination
There is continued debate about whether tion, arachnoid cysts, demyelinating lesions, (e.g., focal findings, signs of increased intra-
occipital location of headache should be con- subdural hygroma, fibrous dysplasia, and pi- cranial pressure, or significant alteration of
sidered as a red flag. In a study of 283 chil- neal gland cyst) [50]. The magnitude of im- consciousness), the coexistence of seizures,
dren, an occipital location was the third most aging studies performed because of paren- or both; recent onset of severe headache;
common finding after right and left unilat- tal concern (81.8%) indicates how difficult it change in the type of headache; or headaches
eral locations. In 271 of these patients (96%) can be for physicians to argue against neuro- with associated neurologic dysfunction [15].
with occipital headache, neuroimaging find- imaging. The fact that findings were made, Since 2002, several European countries
ings were normal; only incidental abnormali- regardless of their relevance to the initial have developed clinical guidelines on head-
ties were found in the remaining 12 patients, symptoms, may reinforce parental attitudes ache management for adults and children,
and none of these patients required surgical in favor of obtaining more tests. most of which have been translated to Eng-
intervention [47]. Another study prospective- lish [52–54]. Both U.S. guidelines (AAN
ly evaluated 1029 patients with headaches, Clinical and Imaging Guidelines 2002) and European guidelines [15] have
and 48 of them (4.7%) experienced recurrent To make an informed decision about the been rated as having low-to-moderate qual-
occipital headaches for a mean course of 2.3 workup of headaches, clinicians can use di- ity [55]. It was found that the lack of homo-
years [48]. In this group, brain imaging find- agnostic criteria for each type of headache, geneity among these various guidelines may
ings were normal in 46 patients (95.8%), and as well as evidence-based tools to assess the affect their applicability in everyday practice
incidental nonsignificant findings were found risk for an underlying significant lesion and [55]. Another study confirmed that practice
in two patients. The frequency of occipital appropriateness criteria to guide the selec- patterns had not changed significantly after
headache was 5% in patients with migraine tion of imaging modalities [51]. implementation of clinical practice param-
and 4.4% in those with nonmigraine head- American Academy of Neurology—In eters [56]. The study reviewed 725 children
aches without any significant cause [48]. A 2000, the U.S. Headache Consortium re- with nonacute headache and normal neuro-
retrospective study of 356 children referred leased clinical guidelines on diagnosis and logic examination findings who presented to
to a pediatric neurologic clinic found that pa- management of migraine in adults [15]. a clinic during the years 1992, 1996, 2000,
and 2004 [56]. The study found increased used for pediatric patients. In a 2008 com- Secondary benign headaches are, by far,
neuroimaging use ratios, from 2:1 in 1992 to mentary, Lewis [61] summarized the results the most common presentation in children
7:1 in 2004 [56]. of five studies, and the following features (35–63%), followed by primary headaches
Choosing Wisely Campaign—In Novem- were found to be more often associated with (10–25%); secondary life-threatening head-
ber 2013, the American Board of Internal life-threatening causes of headache in chil- aches are the least common (4–15%) [9]. The
dren presenting to the ED: younger age (2–5 frequency of all pediatric patients present-
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being nonessential on the basis of the final tice, are excluded from consideration for the for children undergoing helical CT, report-
ED diagnosis [65]. Improving primary care appropriateness ratings. edly needed in only 8.6% of cases, because
services for patients with headaches could Exposure to ionizing radiation is an im- of the high speed of the examination acquisi-
also contribute to lower rates of patients pre- portant consideration because of increased tion [75]. The need for anesthesia sedation in
senting to the ED with first-time headache radiosensitivity of certain tissues in children children was reported to be as high as 28%
in an accountable care organization in 2014,
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symptoms [68]. For example, a study showed and the long lifetime after exposure [69]. The
that 22% of adult patients with headaches re- average effective dose for a head CT is list- with 72% of all sedations performed for head
ported first to an ED before seeking care in a ed as 2 mSv for adults [70]. A dose simula- imaging [76].
general neurology outpatient clinic; 9% had tion study in children found that the effective A cost-effectiveness analysis from the so-
been admitted to the hospital for headaches. dose for a head CT can be up to four times cietal perspective compared three groups
All of these patients received a diagnosis of higher in neonates than it is in adults [71]. of children by risk for underlying brain tu-
primary headache [68]. Assuming, on the basis of these data points, mor and cost of cross-sectional imaging [1].
that the effective dose of a pediatric head CT The first group were children with low risk
CT Versus MRI scan can be 2–8 mSv, this would still be be- (0.01%) for brain tumor who had chronic non-
Once a determination is made that imag- low the level of concern for a significant risk migraine headaches for longer than 6 months’
ing should be performed, providers need to of fatal cancer, which is reported to be 10– duration; the second group were children
decide which imaging modality is most ap- 100 mSv [69]. An effective dose of 10 mSv with intermediate risk (0.4%) for brain tumor
propriate. The ACR Appropriateness Crite- may be associated with a fatal cancer risk of who had migraine headaches and a normal
ria [6] provide evidence-based guidance for 1 in 2000 cases; by comparison, the natural neurologic examination; the third group were
this decision. Although the ACR Appropri- risk for fatal cancer in the United States is children with high risk (4%) for brain tumor
ateness Criteria currently include informa- 400 in 2000 cases [72]. who had migraine headaches for less than 6
tion on levels of ionizing radiation exposure Access to CT versus MRI can vary widely months’ duration and an abnormal neurologic
for each listed imaging procedure, this fac- across the United States. A study of availabil- examination (Fig. 4). The study found that the
tor is not considered for the appropriateness ity of CT versus MRI in U.S. EDs reported effective strategy was the use of MRI in the
ratings. Similarly, factors such as access to that 94% had around-the-clock access to CT high-risk group, which yielded a cost-effec-
imaging modalities, need for sedation, and but only 39% had such access to MRI [73]. tiveness ratio of $113,800 per quality-of-life
cost, which may play a role in clinical prac- The level of urgency may influence whether years gained, as compared with more than
an imaging workup will be performed with $1 million in the intermediate-risk group [1].
CT or could be accomplished with MRI [74]. The authors found that no imaging modali-
Another factor influencing the access to CT ty was more cost effective than either CT or
versus MRI is that sedation is rarely needed MRI in the low-risk group [1]. A study from
Spain estimated that the economic burden of
migraine was €1076 million [77]. The use of
clinical decision support (CDS) systems has
been shown to yield substantial decreases in
MRI utilization for headache and other com-
mon indications for advanced imaging, and,
in 2017, CMS was already accepting applica-
tions for preliminary qualification for CDS
mechanisms [78, 79].
There are only a few cost-effectiveness
studies from the patient’s perspective. One
study from the United Kingdom tracked 103
patients with primary headaches who were
randomized to be offered imaging versus no
imaging, and of these patients, 44% scored as
being anxious on the Hospital Anxiety and
Depression Scale at baseline [80]. Patients
A B
who underwent imaging evaluation were less
Fig. 4—14-year-old boy with intracranial neoplasm. Patient was referred to neurology department by his
pediatrician for persistent headaches. Patient had started to experience headaches approximately 3 months anxious at the 3-month follow-up, but were
ago, and initially headaches were attributed to migraine. However, recently his headaches had worsened and similarly anxious as they were at baseline
were accompanied by one episode of emesis. Patient did not have history of seizures. He denied any visual by 1 year. Interestingly, the health care cost
symptoms, subjective numbness, or weakness. Mass was seen at MRI. Patient underwent neurosurgical
resection of mass, which was identified as pilocytic astrocytoma at pathologic examination. Case illustrates
for anxious patients who underwent imaging
that brain tumors can present initially with isolated headache with benign characteristics, but may eventually was significantly lower compared with anx-
develop additional symptoms. ious patients who had not undergone a scan.
A, Axial T2-weighted MR image of brain shows large T2-hyperintense pineal region mass (arrow) with dilation This is likely explained by higher utilization
of atrium of right lateral ventricle.
B, Sagittal contrast-enhanced T1-weighted MR image of brain shows vividly enhancing heterogeneous solid of other medical resources in anxious pa-
mass (arrow) centered in pineal region with mass effect on tectum of midbrain. tients who did not undergo imaging [80].
Outstanding Issues That sure. There are downsides and societal cost 2. Medina LS, Pinter JD, Zurakowski D, Davis RG,
Warrant Research associated with MRI, such as longer exami- Kuban K, Barnes PD. Children with headache:
There is a wealth of material that can be nation times and a possible need for sedation, clinical predictors of surgical space-occupying le-
used to develop interventions for improving which can result in cost in the form of longer sions and the role of neuroimaging. Radiology
the appropriateness of imaging utilization in leave from school and longer parental leave 1997; 202:819–824
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pediatric headache. One major issue that re- from work. In the past, cost-benefit analyses 3. Olesen J, Steiner T, Bousser MG, et al. Proposals
mains is that none of the proposed criteria of pediatric headaches focused on compar- for new standardized general diagnostic criteria
sets have been validated in larger pediatric ing CT and MRI [1]; future analyses should for the secondary headaches. Cephalalgia 2009;
cohorts. Unless the safety as well as the spec- consider the cost of missing a significant 29:1331–1336
ificity and sensitivity of workup algorithms finding or delaying treatment, including 4. Frishberg BM, Rosenberg JH, Matchar DB, et al.
or sets of red flag criteria are known, it may medicolegal cost, cost of parental anxiety, Evidence-based guidelines in the primary care set-
be difficult to get buy-in from stakeholders cost of radiation exposure cancer risk rela- ting: neuroimaging in patients with nonacute head-
into projects aimed at decreasing imaging tive to background radiation cancer risk, and ache. American Academy of Neurology website.
utilization for pediatric headache. the possibility of offering a shorter MRI pro- tools.aan.com/professionals/practice/pdfs/gl0088.
Although it seems intuitive that obtaining tocol at a cheaper rate. pdf. Published 2000. Accessed August 21, 2017
imaging tests could at least have a reassur- 5. Loder E, Weizenbaum E, Frishberg B,
ing effect on families and patients when the Summary Silberstein S; American Headache Society Choosing
findings are negative, research indicates that Considerable challenges remain in the im- Wisely Task Force. Choosing wisely in headache
obtaining diagnostic tests makes hardly any aging of pediatric headache. The high cost of medicine: the American Headache Society’s list of
contribution to the level of patient and family imaging and large number of normal exami- five things physicians and patients should question.
reassurance [81]. Because the implementation nations in patients without red flags are mo- Headache 2013; 53:1651–1659
of CDS systems for use in headache will like- tivations to implement programs that can in- 6. Strain JD. ACR Appropriateness Criteria on
ly become mandatory in the near future and crease the rate of positive findings at imaging. headache: child. J Am Coll Radiol 2007; 4:18–23
because new strategies for including patients On the other hand, data regarding the safe- 7. Scheller JM. The history, epidemiology, and
in the decision-making process are being de- ty and validity of workup algorithms and red classification of headaches in childhood. Semin
veloped, providers need to build communica- flag criteria remain to be shown scientifically Pediatr Neurol 1995; 2:102–108
tion skills to help them balance patient expec- to increase practitioners’ and families’ confi- 8. Alfonzo MJ, Bechtel K, Babineau S. Management
tations with medical evidence [82, 83]. dence in applying them in daily practice. of headache in the pediatric emergency depart-
Besides lack of awareness of evidence and We have identified several areas for im- ment. Pediatr Emerg Med Pract 2013; 10:1–25
guidelines and responding to patient anxiety, proving the care of children with headaches 9. Conicella E, Raucci U, Vanacore N, et al. The
providers may also order diagnostic tests in- at our institution. We promote the use of the child with headache in a pediatric emergency de-
appropriately because of medicolegal worries SNOOPPPPY criteria [13] (Table 1) to iden- partment. Headache 2008; 48:1005–1011
[70, 84]. For example, Randolph W. Evans, tify children with a high likelihood of an un- 10. Kabbouche M, Khoury CK. Management of pri-
a coauthor of the American Headache Soci- derlying pathologic process as the cause of mary headache in the emergency department and
ety’s Choosing Wisely list, describes in a let- their headaches. For emergent presentations, inpatient headache unit. Semin Pediatr Neurol
ter to the editor of JAMA Internal Medicine we recommend an initial CT scan, followed 2016; 23:40–43
a medicolegal reality in which physicians are by MRI if there are abnormal findings. For 11. Burton LJ, Quinn B, Pratt-Cheney JL, Pourani M.
protected when they order unnecessary ex- nonemergent imaging evaluations in likely Headache etiology in a pediatric emergency de-
aminations but are possibly liable when they secondary headaches, we perform routine partment. Pediatr Emerg Care 1997; 13:1–4
miss a significant finding while following a unenhanced MRI; for nonemergent imag- 12. Powers SW, Patton SR, Hommel KA, Hershey
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tioner concerns, but it may not be enough to on our MRI vendor’s platform [87]. We an- 13. Gofshteyn JS, Stephenson DJ. Diagnosis and man-
achieve a meaningful change in practice. ticipate that, by 2018, our pediatric hospital agement of childhood headache. Curr Probl
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cost-to-benefit ratio in pediatric headache ing a commercial product. In preparation for 14. Ramsawh HJ, Chavira DA, Kanegaye JT, Ancoli-
imaging may be to consider either an im- the CDS system, we are planning to develop Israel S, Madati PJ, Stein MB. Screening for adoles-
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