J Pediatr Endocrinol Metab 2017; aop
Mini Review
Artemis E. Doulgeraki*, Emmanouel M. Manousakis and Nikolaos G. Papadopoulos
Bone health assessment of food allergic children
on restrictive diets: a practical guide
DOI 10.1515/jpem-2016-0162
Received April 26, 2016; accepted November 28, 2016
Abstract
Background: Food allergy in childhood is on the rise glob-
ally and is managed with avoidance diets; recent case
reports of food allergic children with nutritional rickets in
the literature highlight the importance of close monitor-
ing of bone health in this population.
Methods: There is no consensus as yet with regard to
bone health evaluation in food allergic children; there-
fore, extensive literature search was performed and the
existing evidence is presented, along with a relevant
algorithm.
Results: Children allergic to cow’s milk protein or present-
ing with allergy in more than three food items, as well as
patients with severe allergic phenotypes or comorbidities
known to affect the skeleton, seem to be at risk of meta-
bolic bone disorders. As a practical guide, suspicious
cases can be investigated with basic bone profile, whereas
more severe cases (persistent bone pain and fractures)
may undergo advanced bone health assessment, with
bone mineral density (BMD) and metabolic bone markers’
evaluation. Of note, these diagnostic steps call for further
studies in the field of food allergy, as they are not per-
formed as a routine. Evidence is accumulating with regard
to vitamin D deficiency, osteopenia and imbalanced bone
metabolism in those food allergic children who show
poor dietary compliance or have inadequate medical
supervision.
*Corresponding author: Dr. Artemis E. Doulgeraki, PhD, MRCPCH,
Consultant Pediatrician, Head of the Department of Bone and
Mineral Metabolism, Institute of Child Health, “Agia Sophia”
Children’s Hospital, 115 27, Goudi, Athens, Greece,
Phone: +30 213 2037 360, Fax: +30 210 77 00 111,
E-mail: doulgeraki@yahoo.com
Emmanouel M. Manousakis: Allergy Unit, 2nd Pediatric Clinic,
University of Athens, Greece
Nikolaos G. Papadopoulos: Allergy Unit, 2nd Pediatric Clinic,
University of Athens, Greece; and Centre for Pediatrics and
Child Health, Institute of Human Development, The University of
Manchester, UK
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Conclusions: Ensuring optimal bone accrual in a food
allergic child is an important task for the clinician and
requires close monitoring of the restrictive diet and
prompt therapeutic intervention, in an effort to avoid
­rickets or osteopenia.
Keywords: bone; children; dual-energy X-ray absorptiom-
etry (DXA); food allergy; vitamin D.
Introduction
Food allergy is on the increase globally [1]; it affects
approximately 5% of the pediatric population [2–4]. It is
either IgE- or non-IgE mediated and can involve a single
food item (usually cow’s milk allergy [CMA], which is the
commonest amongst infants, with a prevalence of 2%–3%
[5]) or multiple food items (e.g. fish, egg and nuts). In
general, the most common food allergens are milk, egg,
soy and wheat. Milk and wheat, in particular, are major
constituents of a child’s diet; so, in allergic children, alter-
native sources with comparable nutritional value should
be sought [6].
It is important that a correct diagnosis of food
allergy is reached, as lack or removal of a responsible
food allergen may lead to the exacerbation or presen-
tation of other allergic disorders, e.g. asthma, atopic
dermatitis, etc. [7]. A child is diagnosed with single or
multiple food allergies on the basis of clinical presen-
tation, detailed dietary history and special diagnostic
allergy tests, such as skin prick tests or serum-specific
IgE determination. Then, he/she is put on a restrictive
diet, avoiding the particular food allergen that triggers
symptoms. For several foods, such as milk and egg, this
is not a life-long strategy; regular review of the response
to the special diet is mandatory to avoid unnecessary
limitations [8].
The existing guidelines for children with food allergy
highlight the importance of close growth monitoring and
regular assessment of the diet regime quality [8–13]. Mul-
tiple nutritional deficiencies, referring both to macro-
nutrients (protein [14], carbohydrates and fat) and to
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134 Doulgeraki et al.: Bone health assessment of food allergic children
micronutrients (vitamins, minerals and trace elements),
can occur as a result of prolonged, unsupervised restric-
tive diets [6]. In addition to specific food avoidance, this
is also because there is evidence that an allergic reaction
may lead to chronic gut inflammation, which adversely
affects mucosal permeability and absorbance of nutri-
ents. This, in turn, increases the demands for calories and
other elements of the diet, as it was found in a study of
children with food allergy and severe atopic dermatitis
[2]. Also, research on infants with CMA revealed that they
were receiving less calories, fat, protein and calcium com-
pared to healthy controls [15–17], and there is evidence
that many nutrients interact with each other, as is the case
between iron deficiency anemia and vitamin D deficiency
[18, 19].
Another reason why regular growth monitoring is
justified in allergic children is the fact that food allergy
is usually found at a very young age (e.g. infants and tod-
dlers). It is established that this period is crucial for linear
growth; this also applies to adolescence, where a second
growth spurt occurs, which is critical to peak bone mass
accrual [20].
This article aims at addressing issues of everyday
practice, not only for pediatric allergists, but also for
general pediatricians who are involved in allergic chil-
dren’s care. It includes an algorithm that could be a
diagnostic tool for prompt detection and management
of calcium and vitamin D disorders in children with food
allergy on special avoidance diets. Of note, to our knowl-
edge, no such algorithm exists on the subject, although
there are numerous case reports of allergic children on
restrictive diets who went on to develop rickets and/or
spontaneous (osteoporotic) fractures [3, 4, 7, 21–23]. It
is hoped that this review will raise awareness among
health professionals and will contribute to the improve-
ment of growth potential of these particular patients,
protecting them also from osteopenia or osteoporosis in
adulthood.
Indications for assessing bone
health in a child with food allergy
on special diet
The approach to the aforementioned issue is structured
and includes the combination of history, physical exami-
nation and application of available evidence from the
literature.
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History taking
During consultation, one should inquire about the
following:
A) Is there a single or multiple food allergies? What food
is the child allergic to?
When there is a single food allergy, the most important
for skeletal status is CMA. According to the study of
Flammarion et al. [2], infants and toddlers with CMA
were receiving less calcium from other dietary sources
and their height and weight were less compared to
their healthy counterparts. The same researchers
found that those subjects with multiple food allergies
( ≥ 3 food items) had more compromised growth com-
pared to the children with allergy to one or two foods
and this has been confirmed in other studies [24].
Additionally, an Australian study on infants showed
that history of allergy to two foods increased the risk
of vitamin D deficiency (25[OH]D < 50 nmol/L or < 20
ng/mL) 10-fold, whereas when the infant was allergic
to only one food, the same risk increased 2-fold com-
pared to the general population [25].
Synopsis: Children with CMA or multiple food allergies
( ≥ 3 foods) are at greater risk of calcium and/or vitamin
D deficiency.
B) What is the age of the patient?
Infants, toddlers and teenagers with food allergy are
more prone to bone disorders, as during these periods
of growth, very rapid skeletal maturation occurs [20].
Eighty percent of peak bone mass is achieved from
birth through adolescence and 60% of calcium intake
ideally should be received through dairy products
[24–26]. A Greek study of healthy adolescents [27]
revealed high prevalence of severe vitamin D defi-
ciency (25[OH]D < 25 nmol/L or < 10 ng/mL), espe-
cially during winter (30% of the study population).
Ensuring adequate calcium intake (dietary and/or
with supplements) for every child on restrictive diet is
of paramount importance.
Synopsis: Crucial ages to focus on with regard to bone
health surveillance: 0–3 years and 13–18 years.
C) Is the child compliant with the dietary regime?
A balanced diet is essential for children with food
allergy who follow a restrictive diet. During follow-
up, the adequacy of the dietary program should be
reviewed, along with the need for supplementation.
Children who are supervised by a trained pediat-
ric dietician, with regular monitoring of the dietary
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 Doulgeraki et al.: Bone health assessment of food allergic children
plan, do better in terms of growth and sufficiency of
calcium and vitamin D [15].
Synopsis: Poor dietary compliance puts the allergic chil-
dren at risk of bone disorders. Compliance should be mon-
itored regularly.
D) Review of the patient’s past medical history.
There is always the possibility that the allergic child
suffers from comorbidities that affect skeletal health,
either directly or because of medications used for the
chronic condition, such as corticosteroids. If this is the
case, the risk of calcium or vitamin D disorder is con-
siderably higher. One should be familiar with exist-
ing guidelines on pediatric bone health for patients
with celiac disease, diabetes mellitus, cystic fibrosis,
idiopathic juvenile arthritis, etc. [12]. Corticosteroid
intake should be taken into account.
Synopsis: The presence of chronic diseases and/or
chronic medication use may increase the risk of calcium
and vitamin D disorders in the child with food allergy.
E) What are the patient’s symptoms?
A history of seizures, hypotonia or frequent respira-
tory infections during infancy should raise suspi-
cion of possible hypocalcemia or very low vitamin D
levels. During adolescence, these disorders are more
insidious, manifesting as chronic fatigue or vague,
poorly localized skeletal pain. Moreover, enquiry
for fractures should not be omitted; if spontaneous,
low-energy fractures are reported, they could be
attributed to a metabolic bone disorder. For example,
there is a case report in the literature describing a
child with CMA who sustained four long bone frac-
tures with no history of serious injury. His diagnos-
tic workup revealed severe osteopenia as a result of
nutritional rickets, which occurred because he did
not follow his dietary plan [28]. Also, a strong posi-
tive association (r = 0.89, p < 0.01) has been found
between bone mineral density (BMD) and calcium
intake [26].
Synopsis: An allergic patient on a restrictive diet should
have a full diagnostic workup to exclude rickets, if he
reports low-energy fractures or his clinical presenta-
tion is compatible with severe calcium or/and vitamin D
deficiency.
Clinical examination
A) What is the clinical presentation of the child’s food
allergy?
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135
Most of the available evidence focuses on IgE-medi-
ated food allergy. According to research data, patients
with moderate to severe atopic dermatitis are more
prone to vitamin D deficiency, both because of sun
exposure avoidance and because of the presence of
chronic inflammation [29]. Conversely, correcting
vitamin D deficiency may result in dramatic improve-
ment of eczema [30]. Furthermore, epidemiological
studies have shown that food allergies are more prev-
alent in latitudes where ultraviolet B (UVB) radiation
is suboptimal [31, 32] (hence the observed low vitamin
D status) and also in infants who were born during
autumn and winter [17, 33].
Regarding coexistence of asthma, the chances of
detecting low calcium or vitamin D are even higher,
with a 5-fold increase in detecting low vitamin D levels
in asthmatic children compared to healthy controls, as
suggested by two studies in the USA and Qatar [34, 35].
Synopsis: Children with food allergy and severe clinical
phenotype are more prone to calcium and/or vitamin D
disorders.
B) Are there clinical signs of rickets?
The treating physician should look for bone defor-
mations such as marked genu varum (“bow legs”)
or genu valgum (“knock knees”), wrist enlargement,
Harrison’s sulcus or “rachitic rosary”. Although not
common, there are several case reports of children
with food allergy and the above findings [4, 7, 22].
Their common feature is history of CMA and pro-
longed, exclusive breastfeeding with no supplemen-
tation of calcium or vitamin D.
Other suspicious findings on examination include
very wide anterior and posterior fontanelle, delayed
tooth eruption (> 14 months) and delay in achieving
gross motor milestones, e.g. walking > 18 months.
Synopsis: Clinical indications of possible rickets in a
child with food allergy should be promptly investigated.
Taken together, the list of absolute indications for
diagnostic workup of a possible metabolic bone disorder
in a child with food allergy on a restrictive diet can be pro-
posed as illustrated in Table 1.
Bone health surveillance of children
with food allergy on a special diet:
suggestions for everyday practice
After suspecting a possible bone disorder in the child with
food allergy, the next step is to investigate the underlying
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136 Doulgeraki et al.: Bone health assessment of food allergic children

Table 1: Indications for full diagnostic workup of food allergic hormone (PTH). To avoid high costs, one could monitor
­children for bone disorders. ALP and proceed to further tests only when elevated ALP
levels are detected.
Children with CMA or with multiple food allergies ( ≥ 3 food items)
Additionally, if the patient is scheduled for prolonged
Infants, toddlers and adolescents
Poor adherence to the existing dietary plan supplementation with calcium and/or vitamin D or if he/
Comorbidities and/or medications known to adversely affect the she is on chronic corticosteroid treatment (> 3 months) for
skeleton other chronic conditions, then measuring calcium/creati-
Symptoms of nutritional rickets and/or history of low-energy nine ratio (2nd morning void) is reasonable for prompt
fractures
detection of hypercalciuria, which has been reported in
Severe allergic phenotype
Clinical signs indicative of rickets
adult patients [12].
If 25(OH)D < 50 nmol/L (< 20 ng/mL), then admin-
CMA, cow’s milk allergy. istration of chole- or ergo-calciferol is advised (D3, D2,
respectively). If vitamin D levels are very low (< 25 nmol/L
cause. No established algorithm exists, to our knowledge, or < 10 ng/mL), then an X-ray of wrist or knee should be
with regard to the diagnostic steps to be taken in this par- ordered and be repeated after 3 months of treatment to
ticular group of patients. The following suggestions are ensure proper response [38, 39].
not a substitute for clinical judgement; however, they are
in agreement with existing guidelines for evaluation of
bone health in children with chronic diseases [12, 36, 37] Advanced bone profile
and they are illustrated in Figures 1 and 2.
A very small portion of children with food allergy might have
to be investigated further, with more sophisticated methods,
Basic bone profile to assess skeletal status (Figures 2). More specifically, the
proposed tests are intended only for those with signifi-
In high-risk groups, as they were defined previously, it
cant fracture history, early osteoporosis in the family (age
is considered good practice to obtain baseline labora-
< 50 years), comorbidities with detrimental effect on the
tory tests for bone health and then annually, along with
skeleton, persistent bone pain (e.g. back ache) and severe
monitoring of growth, adequacy of dietary intake, dental
growth compromise (body mass index [BMI] < 3rd centile for
review and counseling on healthy lifestyle (safe sun expo-
age and sex).
sure, exercise and weight control) (Figures 1). Fasting
The above patients could benefit from measurement of
serum samples are collected for calcium, phosphate,
their BMD with dual-energy X-ray absorptiometry (DXA),
magnesium, alkaline phosphatase level (ALP) (age-
which is considered the “gold standard” for this purpose.
dependent cut-offs), creatinine, 25(OH)D and parathyroid
According to the recently revised pediatric guidelines for
clinical densitometry (International Society of Clinical
Children with Densitometry, 2013) [36], a pediatric DXA software should
food allergy be used and two measurements should be performed of
Baseline and
annual workup the lumbar spine and total body, excluding head. DXA
scan provides the clinician with valuable information on
bone dimensions and geometry, bone-muscle interaction
Ca, P, ALP, Creatinine
25(OH) D, PTH
and body composition (absolute values of bone, muscle
Dietary history and fat mass).
Growth (Wt, Ht, HC, BMI) There is evidence that correction of suboptimal
Counseling calcium and vitamin D levels can improve BMD, espe-
Dental review
cially of the total body, which mostly represents cortical
bone status [12, 24, 40, 41]. Also, in a case series of chil-
Low Ca and/or VIT D dren with CMA on a restrictive diet for at least 4 years, it
Lab workup:
normal Supplementation was reported that their calcium intake was only 25% of
and repeat workup
counseling
in 3 months
the recommended daily allowance and, when they had
DXA scan, their bones were found to be of low weight and
Figure 1: Suggested pathway for assessment of bone health in chil- length (possible mineralization defect) and they also had
dren with food allergy on a restrictive diet (basic bone profile). low bone mineral density [42].

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 Doulgeraki et al.: Bone health assessment of food allergic children
History of Family Comorbidities
low-energy history of affecting the
fractures early skeleton
osteoporosis
Bone mineral
density (BMD)
DXA scan
BMD Z-score > – 1 BMD Z-score < – 2
Monitor every Monitor
2–3 years annually plus
metabolic bone
markers
Figure 2: Advanced bone profile of children with food allergy on a special diet and predisposing factors for low-energy fracture.
The experience of our institution is comparable to
the existing evidence [38, 43]. In the last 2 years, 20 chil-
dren with multiple food allergies have been examined at
the Department of Bone and Mineral Metabolism. One
in four patients (25%) had low-normal BMD for age and
sex, with a BMD Z-score between –1 and –2 (paper under
preparation). This BMD profile is comparable to the work
of Nachshon et al., who reported low BMD in 27% of their
study population, which comprised young adults with
CMA [38]. Our local policy is to advise monitoring of BMD
every 2–3 years, when baseline BMD is normal and annu-
ally when BMD Z-score is low-normal (between – 1 and
– 2) or low (BMD Z-score < – 2).
An even smaller number of allergic patients undergo
measurement of metabolic bone markers. This only
applies to those subjects with low BMD Z-score (< – 2 for
age and sex, after appropriate adjustment for height).
Fasting serum and urine samples (2nd morning void) are
collected for evaluation of bone formation markers (e.g.
osteocalcin) and bone resorption markers (e.g. urine
deoxypyridinoline). Despite their low diagnostic value,
these markers provide insight into the pathophysiology of
bone fragility of children with fractures.
Regarding children with food allergy, very few studies
have focused on the metabolic bone cycle. It seems that
there is possibly an imbalance between bone forma-
tion (which is reduced) and bone resorption (which is
increased) and this is an early finding, preceding DXA
BMD measurement [44–47]. The fact that bone formation
is compromised and bone resorption is favored could, at
least in part, explain the low growth velocity encountered
in allergic children with no monitoring of their diet.
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137
Persistent Compromised
bone pain growth
(BMI < 3rd
centile)
BMD Z-score – 1 to – 2
Monitor annually
Conclusions
In summary, bone health surveillance of children with
food allergy on a restrictive diet should be thorough and
reviewed at regular intervals. The treating physician
should have a low threshold of investigating suspicious
cases, in an effort to ensure attainment of peak bone mass
and a better quality of life, with no fractures or skeletal
pain in adulthood and beyond.
Author contributions: All the authors have accepted
responsibility for the entire content of this submitted arti-
cle and approved submission.
Research funding: AED and EMM declare no conflict of
interest. NGP has received payments for consultancy
(Abbvie, Novartis, Menarini, Meda, Alk-Abello, GSK,
Chiesi), lectures including service on speakers bureaus
(Novartis, Uriach, GSK, Allergopharma, Stallergens,
MSD), educational presentations (Abbrie, Sanofi, Menar-
ini, MEDA) and grants from Nestle, MSD.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played
no role in the study design; in the collection, analysis, and
interpretation of data; in the writing of the report; or in the
decision to submit the report for publication.
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