ORIGINALS / Rev Osteoporos Metab Miner.

2018;10(1):30-36
30

Mir-Perelló C1, Galindo Zavala R2, González Fernández MI3, Graña Gil J4, Sevilla Pérez B5, Magallares López B6, Bou Torrent R7
(En representación del Grupo de Trabajo en Osteoporosis Infantil y Osteogénesis Imperfecta de la Sociedad Española de
Reumatología Pediátrica)
1 Unidad de Reumatología Pediátrica - Servicio de Pediatría - Hospital Universitario Son Espases - Palma de Mallorca (España).
Grupo de Investigación en Litiasis Renal y Biomineralización - Instituto de Investigación Sanitaria de la Universidad de las Islas Baleares (IUNICS) -
Palma de Mallorca (España)
2 Sección de Reumatología Pediátrica - Unidad de Gestión Clínica de Pediatría - Hospital Regional Universitario de Málaga - Málaga (España).
Departamento de Pediatría y Farmacología - Facultad de Medicina - Universidad de Málaga - Málaga (España)
3 Unidad de Reumatología Pediátrica - Hospital Universitario y Politécnico La Fe - Valencia (España)
4 Servicio de Reumatología - Estructura Organizativa de Gestión Integrada (EOXI) - Complejo Hospitalario Universitario de A Coruña - A Coruña (España)
5 Unidad de Gestión Clínica de Pediatría - Hospital Universitario San Cecilio - Granada (España)
6 Servicio de Reumatología - Hospital Santa Creu i Sant Pau - Barcelona (España)
7 Unidad de Reumatología Pediátrica - Hospital Sant Joan de Déu - Esplugues de Llobregat - Barcelona (España)

Prevention and early diagnosis of

childhood osteoporosis: are we
doing the right thing?
DOI: http://dx.doi.org/10.4321/S1889-836X2018000100005

Correspondence: Concepción Mir-Perelló - Servicio de Pediatría - Hospital Universitari Son Espases - Ctra. de
Valldemossa 79 - 07010 Palma de Mallorca (Spain)
e-mail: [email protected]

Date of receipt: 17/10/2017

Date of acceptance: 08/01/2018

Summary
Objectives: To assess prevention, early diagnosis and training received regarding osteoporosis among the
pediatrics professionals in our area.
Material and methods: Survey directed to physicians of pediatricians of Primary Care (PC) and Specialized
Care (SC) in order to evaluate their activity in prevention, detection and training received in osteoporo-
sis. The survey was disseminated through the relevant scientific societies.
Results: 420 pediatricians participated (324 from PC and 96 from SC). 93.5% of PC pediatricians and 89.6%
of SC pediatricians valued the physical activity of the patients; 85.19% and 35.4% of them, respectively, the
intake of dairy products. 45.68% of PC and 70.2% of SC recommended calcium and vitamin D supplements
in the case of low nutritional intake, whereas 39.2% of PC and 47.2% of SC favored follow-up. 39.6% of SC
pediatricians requested bone densitometry for this disease or risk treatment, and 47.9% measured the levels
of 25-OH-vitamin D. 25.93% of PC and 45.3% of SC asked about the existence of fractures, 90.4% and 96.8%
requested etiopathogenic mechanism. 40% of PC and 86.2% of SC requested a bone densitometry or refe-
rred to the specialist for fractures due to low trauma energy, with specific criteria in 13.7% and 5.86%, res-
pectively. 92% of PC and 82.3% of SC had not received recent training in childhood osteoporosis.
Conclusion: Detection, derivation circuits and the training of pediatricians regarding bone health in our
country can be improved. Optimizing these aspects is essential to favor the peak of bone mass in our
population.

Key words: bone health, osteoporosis prevention, early diagnosis of osteoporosis.

 ORIGINALS / Rev Osteoporos Metab Miner. 2018;10(1):30-36 31

Introduction center, which accepted the approach. The resear-

Bone mass increases during childhood and ado- chers were the only ones who had access to the
lescence until it reaches its maximum value shortly survey data, which were collected exclusively for
after puberty1,2. Several factors are involved in this statistical purposes.
process among which the genetic load determines
up to 80% while the remaining 20% depends on Results
modifiable external factors, such as nutrition, exer- In all, 420 professionals participated in the survey,
cise and exposure to sunlight and osteotoxic subs- 324 PC pediatricians and 96 from different pedia-
tances, among others3-5. The optimization of all of tric specialties. The pediatric specialty of those sur-
them is essential to achieve the maximum bone veyed in the hospital setting is shown in Table 1.
mass at the end of development6. Regarding preventive habits assessment, 93.5%
Children suffering from chronic conditions of PC pediatricians and 89.6% of SC reported
usually have difficulties reaching an optimal peak assessing the patients’ amount and type of physi-
of bone mass. In general, they present a higher cal exercise and concerning daily intake of dairy
incidence of malnutrition, practice less physical products, 85.2% and 35.4%, respectively. The
exercise and are less exposed to solar radiation detailed results are shown in Table 2. Regarding
because of their disease7. In addition, the inflam- preventive treatment, 45.68% of primary and
matory activity present in some diseases inhibits 70.2% of specialized pediatricians referred to cal-
bone formation and stimulates its reabsorption, as cium and vitamin D supplements to patients with
in the case of some medication treatments (espe- low nutritional intake of these elements.
cially glucocorticoids)8. Complementary test follow-up in the patients who
Several studies indicate that the best way to received a supplement was carried out by 39.2%
prevent adult osteoporosis is to favor optimal of the PC and 47.2% of the SC.
bone mass peak acquisition at the end of the Regarding the detection of patients with risk of
growth stage9-11. Thus, controlling bone mineraliza- osteoporosis in PC, only 25.93% of professionals
tion during childhood is an unavoidable obliga- asked specifically about fractures within the child
tion for pediatricians, who must promote healthy health program. 90.43% reported assessing the
living habits in their patients, minimize osteotoxic etiopathogenic mechanism and 40% recognized
medication use and recognize warning signs to that SC should be referred to patients with fractu-
make an early diagnosis if there is bone metabo- res due to low-energy trauma. 94.2% admitted not
lism disorder. having specific referral criteria in the presence of
Our study aimed to evaluate preventive activity osteoporosis (Table 3).
and early diagnosis of osteoporosis that is As for managing chronic SC patients, 39.6%
currently carried out, as well as the training recei- reported requesting a dual-energy densitometry
ved in this field, by primary care (PC) pediatricians (DXA) in case of prolonged corticotherapy or
and hospital pediatricians who care for children chronic disease that affected the bone although
with chronic diseases in our country. there were no fractures, and 49.7% did not moni-
tor 25-OH-vitamin D levels in patients with risk
Material and methods factors. 86.2% requested DXA or referred to rheu-
Two online surveys were prepared, one for PC matology or endocrinology for fractures due to
sector pediatricians and the other for pediatricians commonplace injuries. 13.7% admitted having
in specialized care (SC). These surveys collected specific referral criteria in the presence of osteo-
data on prevention, detection and treatment of porosis (Table 4).
children at risk of osteoporosis in routine clinical In reference to the training received, 92% of PC
practice. It also queried them about the training pediatricians and 82.3% of those of SC had not
received about this condition. received training in childhood osteoporosis in the
The surveys were designed using Google Docs last 5 years, and 88.27% and 79.8%, respectively,
technology and disseminated through different considered it insufficient.
scientific societies between November 2014 and
October 2015. In addition, in order for the survey Discussion
to reach the maximum number of physicians, reci- This is the first reported study of similar characte-
pients were urged to forward the questionnaire to ristics both nationally and throughout European.
their pediatric colleagues working in this area. Our important finding is the great variability of pre-
Each participant was sent both surveys indicating vention regarding childhood osteoporosis in our
that they had to answer one or the other whether environment and the limited training in pediatrics.
they were working in PC or SC activity. A descrip- The promotion of bone health in the pediatric
tive study of our obtained data was carried out. age is the best strategy for reducing fracture risk
The results were expressed as percentages. and physical disability in old age12. The need for
Statistical analysis was carried out using the SPSS osteoporosis prevention programs has been analy-
v21 package. zed in different publications on behavior and kno-
Since the surveys did not include patient data wledge in the adult population, although few have
and were anonymous and voluntary, ethics com- been effective13. At the school level, programs
mittee approval was not required. However, the aimed at improving children’s health are carried
study was reported to the committee coordinating out, but these interventions are more effective
 ORIGINALS / Rev Osteoporos Metab Miner. 2018;10(1):30-36
32

when they come from the health personnel of their greater risk of developing osteoporosis in
reference13. Therefore, it is the pediatrician who adulthood13. So pediatricians should explore
must identify children and adolescents at risk of patients’ living habits and correct those aspects
presenting or developing low bone mass in order that are harmful to the proper skeletal develop-
to apply appropriate preventive and therapeutic ment in children and adolescents. In our study,
measures to prevent their progression and the most primary care pediatricians reported being
appearance of fragility fractures13. interested in their patients’ physical activity and
The main measures for osteoporosis preven- dairy intake and reported making specific recom-
tion in childhood are adequate daily intake of cal- mendations to optimize these aspects.
cium and promotion of physical exercise, espe- In the case of children with chronic conditions,
cially those forms that involve weight bearing14. it is even more important to favor bone mass
Other beneficial measures include the control of acquisition by promoting healthy lifestyles. These
body weight, regular sun exposure and avoiding patients have a special risk of developing osteopo-
tobacco and alcohol14. Adolescence is the time of rosis in adulthood, since any chronic systemic
greatest bone mass acquisition, so the presence of disorder can influence bone mineral density:
unhealthy lifestyle habits (low physical activity, nephropathies, metabolic, hematological, endocri-
decreased intake of dairy products, tobacco, alco- nological, gastrointestinal and rheumatological
hol, etc., relatively frequent at this stage of life) diseases16-18. However, in our study, although more
has a very negative impact on its final peak15. than 80% of pediatric hospital specialists were
Therefore, adolescents are the main risk group interested in their patients’ physical activity, only
and the population on which prevention measures 34.5% asked about the intake of dairy products as
should focus, especially on women because of a matter of course.

Table 1. Profile of Specialized Care respondents

Pediatric specialty (n=96) Percentage of the total (%)

Hemato-oncology 27.1
Traumatology 11.5
Infectology 10.4
Pneumo-allergology 10.4
Neuropediatry 9.4
General Pediatrics 9.4
Digestive and Nutrition 5.2
Nephrology 5.2
Rheumatology 4.2
Cardiology 3.1
Endocrinology 3.1

Table 2. Evaluation of the preventive habits of childhood osteoporosis in the Child Health Program (PC) and
in the chronic patient consultation (SC). (n=420 completed surveys)

Question Percentage (%)

PC (n=324) SC (n=96)
Yes No YEs No
Are you interested in the amount and type of exercise
93.5% 6.5% 89.6% 10.4%
that your patients perform?
Do you systematically ask how many dairy products your
85.2% 14.8% 35.4% 64.6%
patients consume on a daily basis?
Do you recommend the intake of at least 2 glasses of
94.4% 5.6% 72.9% 27.1%
milk per day or equivalent?
Do you consider that soy milk, almond, etc., are
equivalent to cow's milk as sources of calcium and 9.9% 90.1% 10.5% 89.5%
vitamin D?
 ORIGINALS / Rev Osteoporos Metab Miner. 2018;10(1):30-36 33

Table 3. Early detection and referral of PC patients. (n=324 completed surveys)

Question Percentage (%)

Yes No

Within the Child Health Program, do you specifically ask if

25.9% 74.1%
your patients have had a fracture?

If a patient reports having had a fracture, do you inquire 90.43% 9.57%

into the mechanism involved?

Faced with fractures due to low-energy trauma, does it lead

40% 60%
to SC for screening for osteoporosis?

- 2 fractures: 29.10%
From what number of fractures does your patient refer to - 3 fractures: 51.40%
Specialized Care for osteoporosis screening? - 4 fractures: 4.19%
- 5 or more fractures: 9.26%

Do you have specific referral criteria for suspected

5.86% 94.14%
osteoporosis to Specialized Care?

CHP: Children's Health Program.

Table 4. Management of the chronic risk patient in Specialized Care. (n=96 completed surveys)

Question Percentage (%)

- yes: 1.1%
In the absence of fractures, do you periodically - if prolonged corticosteroid therapy: 16.7%
request dual energy densitometry (DXA) or some - if chronic pathology that affects BMD: 7.3%
other imaging test to assess bone mineral density - if prolonged corticotherapy and/or chronic
(BMD)? condition affecting BMD: 39.6%
- no: 35.4%

In the absence of fractures, do you periodically - yes: 7.3 %

request levels of plasma 25-hydroxyvitamin D3 - yes, if factors of hypovitaminosis D: 51.1%
in your patients with risk factors? - no: 41.7%

Do you specifically ask your patients if they have

- yes: 45.3% - no: 54.7%
had a fracture since the last visit?

If they have suffered one, are you interested in the

- yes: 96.8% - no: 3.2%
mechanism involved?

If it seems a low-energy trauma to cause a fracture,

do you request DXA or refer the patient to
- yes: 86.2% - no: 13.8%
specialized care for osteoporosis screening?

- 2 fractures: 72.4%
From what number of fractures does DXA request
- 3 fractures: 23%
or refer its patients to specialized care for
- 4 fractures: 2.3%
osteoporosis screening?
- 5 or more fractures: 2.3%

Do you have specific referral criteria for suspected

- yes: 13.7% - no: 86.3%
osteoporosis to specialized consultation?
 ORIGINALS / Rev Osteoporos Metab Miner. 2018;10(1):30-36
34

The appearance of low impact fractures (resul- The main limitation of our work is that we
ting from bone fragility) means a significant could not ascertain the percentage of participa-
decrease in bone mineral density, and appears in tion, since the surveys were not only disseminated
established phases of the disease1-3. Therefore, the by different scientific societies, but the participants
active search for children at risk is important, were encouraged to forward the survey to their
including in the medical history of child health pediatric contacts who might be interested in
programs, the assessment of the fractures they taking part. Even so, taking into account the total
present and the monitoring of calcium and vita- pediatricians with healthcare activity in our
min D levels. In our study, the low percentage country, we consider that the number of surveys
stands out of pediatricians of PC that include in implemented could be improved.
the case history the number and characteristics of In addition, participation was voluntary, so it is
the fractures of the child referred to SC for low likely that there is a certain participation bias. The
impact fractures. On the other hand, more than physicians were more aware of the issue in question
half of SC pediatricians do not monitor vitamin D and responded to the survey. In any case, this does
levels or bone mineral density in the chronic risk not invalidate the main conclusion of the study: the
patient, although most assess the etiopathogenic great variability in the approach of this entity.
mechanism and report the reference units of their In conclusion, the preventive activity in rela-
center. tion to childhood osteoporosis that is carried out
As for calcium supplements, multiple studies in our environment varies greatly, and the training
restrict their use to individuals with insufficient that pediatricians receive concerning osteoporosis
contributions through diet, not supporting syste- is very scarce. In addition, there are no specific
matic supplementation neither in healthy children protocols in our environment to address children
nor with osteoporosis if they have an adequate at risk. Consequently, adequate prevention and
contribution19-22. Similarly, there are no data that treatment measures are not being carried out in
allow us to systematically recommend supplemen- our child population, especially in patients with
tation with vitamin D23,24. However, calcium and/or chronic disorders.
vitamin D supplements are recommended when It is essential to optimize these aspects and
the contribution of these elements is low at base- involve pediatricians in detecting and preventing
line. Adequate levels of vitamin D3 (25-OH children at risk, to promote the maximum peak of
Vitamin D) in childhood are between 20 and 30 bone mass in children, and thus reduce the inci-
ng/ml (75-50 nmol/l), although recent studies dence of osteoporosis in the future.
place optimal levels above 30 ng/ml. ml (75
nmol/l)27,28. The recommended daily amount of Conflict of interests: The authors declare no
vitamin D3 and calcium is shown in table 5. In the conflict of interest.
case of vitamin D, we can measure its plasma
levels (25-OH vitamin D), while the calcium inta- Bibliography
ke should be estimated by means of a dietary sur-
vey. In our study, only half of the PC pediatricians 1. Rauch F, Plotkin H, DiMeglio L, Engelbert RH,
and 86% of SC referred to calcium and vitamin D Henderson RC, Munns C. Fracture prediction and the
supplements in these situations. Such supplemen- definition of osteoporosis in children and adolescents:
the ISCD 2007 Pediatric Official Positions. J Clin
tation implies the need to control plasma levels Densitom. 2008;11:22-8.
and to detect possible complications, such as 2. Nevitt MC. Epidemiology of osteoporosis. Rheum Dis
hypercalciuria, renal lithiasis or cardiovascular Clin North Am. 1994;20:535-9.
complications29,30. In our study, it is noteworthy 3. Diez Pérez A, Puig Manresa J, Martínez Izquierdo MT,
Guelar Grimberg AM, Cucurull Canosa J, Mellibovsky
that most pediatricians of both groups did not Saidler L, et al. Aproximación a los costes de fractura
carry out analytical monitoring or follow-up with osteoporótica de fémur en España. Med Clin.
complementary examinations during treatment. 1989;92:721-3.
In terms of managing childhood osteoporosis 4. Von Scheven E, Corbin KJ, Stagi S, Cimaz R.
guidelines, the European Society of Children's Glucocorticoid-associated osteoporosis in chronic
inflammatory diseases: epidemiology, mechanisms,
Endocrinology28 and International Society of diagnosis, and treatment. Curr Osteoporos Rep.
Clinical Densitometry (ISCD)29 have published 2014;12:289-99.
recommendations as has the nutrition committee 5. Bryant RJ, Wastney ME, Martin BR, Wood O, McCabe
of Spain’s Pediatric Society on infant nutrition and GP, Morshidi M. Racial differences in bone turnover
and calcium metabolism in adolescent females. J Clin
bone health30. Despite this, most of the respon- Endocrinol Metab. 2003;88:1043-7.
dents from both the PC and SC groups reported 6. Carrascosa A, Del Río L, Gussinyé M, Yeste D, Audí L.
that they lacked specific protocols to address this Mineralización del esqueleto óseo durante la infancia
condition and referral networks for these patients, y adolescencia. Factores reguladores y patrones de
both at outpatient and hospital levels. normalidad. An Esp Pediatr. 1994:40:246-52.
7. Loud KJ, Gordon CM. Adolescence: bone disease. En:
Furthermore, the training of our physicians Walker, Watkins, Duggan, editores. Nutrition in
regarding bone health is limited, the percentage Pediatrics. Basic Science and Clinical Applications. 3ª
being lower in PC pediatricians, a fundamental ed. Ontario. 2003.
pillar in child care. In addition, most pediatricians 8. Van der Sluis IM, de Muinck Keizer-Scharama SM.
Osteoporosis in childhood: bone density of children in
in both areas consider their training on these health and disease. J Pediatr Endocrinol Metab.
aspects to be inadequate. 2001;14:817-32.
 ORIGINALS / Rev Osteoporos Metab Miner. 2018;10(1):30-36 35

Table 5. Recommended daily amount of calcium and vitamin D3 in the child population

Group Daily amount

400 IU vitamin D3
Calcium:
Healthy children 700 mg from 1 to 3 years
1,000 mg from 4 to 8 years
1,300 mg from 9 to 18 yearss

400 to 1,000 IU of vitamin D3

Children at risk
Higher doses of calcium

2,000 IU of vitamin D3 per day for 6 weeks, increasing from 4,000

to 6,000 IU per day for 6 weeks if they associate malabsorption,
Children with hypovitaminosis D
obesity or treatment with drugs that accelerate the catabolism of
vitamin D

9. Daci E, van Cromphaut S, Bouillon R. Mechanisms 21. Dibba B, Prentice A, Ceesay M, Stirling DM, Cole TJ,
influencing bone metabolism in chronic illness. Horm Poskitt EM. Effect of calcium supplementation on bone
Res. 2002;58(Suppl 1):44-51. mineral accretion in Gambian children accostumed to
10. Klibanski A, Adams CL. NIH Consensus Development a low-calcium diet. Am J Clin Nutr. 2000;71:544-9.
Panel: Osteoporosis prevention, diagnosis and the- 22. Greene DA, Naughton GA. Calcium and vitamin-D
rapy. JAMA. 2001;285:785-95. supplementation on bone structural properties in peri-
11. National Osteoporosis Foundation. Osteoporosis: pubertal female identical twins: A randomized contro-
Review of the evidence for prevention, diagnosis and lled trial. Osteoporos Int. 2011;22:489-98.
treatment, and cost-effectiveness analysis. Executive 23. Nieves JW, Melsop K, Curtis M, Kelsey JL, Bachrach
summary. Osteoporos Int. 1998;8(Suppl 4):S3-6. LK, Greendale G, et al. Nutritional factors that influen-
12. DeBar LL, Ritenbaugh C, Vuckovic N, Stevens VJ, ce change in bone density and stress fracture risk
Aickin M, Elliot D, et al. Youth: decisions and challen- among young female cross-country runners. PM R.
ges in designing an osteoporosis prevention interven- 2010;2:740-50.
tion for teen girls. Prev Med. 2004;39(5):1047-55. 24. Winzenberg TM, Shaw KA, Fryer J, Jones G. Calcium
13. Tussing L, Chapman-Novakofski K. Osteoporosis pre- supplementation for improving bone mineral density
vention education: behavior theories and calcium inta- in children. Cochrane Database Syst Rev.
ke. J Am Diet Assoc. 2005;105:92-7. 2006;(2):CD005119.
14. Behringer M, Gruetzner S, McCourt M, Mester J. Effects 25. Winzenberg T, Powell S, Shaw KA, Jones G. Effects of
of weight-bearing activities on bone mineral content vitamin D supplementation on bone density in healthy
and density in children and adolescents: A meta-analy- children: Systematic review and meta-analysis. BMJ.
sis. J Bone Mineral Res. 2014;29:467-78. 2011;342:c7254.
15. Institute of Medicine (IOM). Dietary reference intakes 26. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon
for calcium and vitamin D. Washington, DC: The CM, Hanley DA, Heaney RP, et al. Evaluation, treat-
National Academies Press; 2011. ment and prevention of vitamin D deficiency: an
16. Högler W, Ward L. Osteoporosis in Children with Endocrine Society Clinical Practice Guideline. J Clinic
Chronic Disease. Endocr Dev. 2015;28:176-95. Endocrinol Metab. 2011;96:1911-30.
17. Cassidy JT, Hillman LS. Abnormalities in skeletal 27. Bolland MJ, Avenell A, Baron JA, Grey A, Maclennan
growth in children with Juvenile Rheumatoid Arthritis. GS, Gamble GD, et al. Effect of calcium supplements
Rheum Dis Clin North Am. 1997;23:499-522. on risk of myocardial infarction and cardiovascular
18. García Nieto V, Ferrández C, Monge M, de Sequera M, events: Meta-analysis. BMJ. 2010;341:c3691.
Rodrigo MD. Bone mineral density in pediatric patients 28. Shaw NJ. Management of osteoporosis in children. Eur
with idiopathic hypercalciuria. Pediatr Neprhol. J Endocrinol. 2008;159:S33-9.
1997;11:578-83. 29. Baim S, Leonard MB, Bianchi ML, Hands DB, Kalkwarf
19. Galindo Zavala R, Núñez Cuadros E, Díaz Cordovés- HJ, Langman CB, et al. Official Positions of the
Rego G, Urda Cardona AL. Avances en el tratamiento International Society for Clinical Densitometry and
de la osteoporosis secundaria. An Pediatr (Barc). Executive Summary of the 2007 ISCD Pediatric
2014;81:399.e1-7. Position Development Conference. J Clin Densitom.
20. Recker RR, Cannata Andía JB, del Pino Montes J, Díaz 2008;11:6-21.
Curiel M, Nogués i Solán X, Valdés Llorca C. Papel del 30. Alonso Franch M, Redondo del Río MP, Suárez Cortina
calico y la vitamin D en el tratamiento de la osteopo- L. Nutrición infantil y salud ósea. An Pediatr (Barc).
rosis. Rev Osteoporos Metab Miner. 2010;2(1):61-72. 2010;72:80.e1-11.