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Prevalence of vitamin D deficiency rickets in adolescent school
girls in Western region, Saudi Arabia
Aisha M. Siddiqui, MRCP (London), FRCP (Edin), Hayat Z. Kamfar, MBBCH, CABP.
441
ABSTRACT
Objectives: To determine the prevalence of vitamin
D deficiency rickets among female adolescents
and assess its relation to calcium intake and sun
exposure.
Methods: Four hundred and thirty-three school
girls between 12-15 years old were selected
randomly from different schools in Jeddah,
between October 2003 - February 2004. We
identified symptoms of rickets and determined
the dietary habits and sun exposure habits, and
laboratory investigations were also carried out,
Results: It was found that, out of 433 cases, 350
(81%) had low vitamin D levels. Approximately
40% had very low levels of vitamin D and 61%
were asymptomatic. Most of the symptoms were
non specific. ere was a positive correlation
between low calcium in the diet and less sun
exposure to low levels of vitamin D. Approximately
96% had normal serum phosphate, 89% had
normal serum calcium, and 40% had normal
serum alkaline phosphatase levels.
Conclusion: Vitamin D deficiency is common
among adolescent females in Jeddah, Saudi Arabia.
Cases are missed due to lack of symptoms in most
cases and normal bone chemistry. Serum vitamin
D level should be carried out in suspected cases.
Health and nutritional education should be
encouraged in schools. Focusing on the importance
of adequate milk intake and sun exposure should
be given a priority in any health education
program.
Saudi Med J 2007; Vol. 28 (3): 441-444
From the Department of Medicine (Siddiqui) and the Department
of Pediatrics (Kamfar), King Abdulaziz University Hospital,
Jeddah, Kingdom of Saudi Arabia.
Received 21st June 2006. Accepted 4th November 2006.
Address correspondence and reprint request to: Dr. Aisha
M. Siddiqui, Associate Professor, Department of Medicine,
King Abdulaziz University Hospital, PO Box 80215, Jeddah
21589, Kingdom of Saudi Arabia. Fax. +966 (2) 6408315.
E-mail: medconf@yahoo.com
V
itamin D metabolites are important for the normal
development of bone and the metabolism of its
constituent ions. Deficiency or abnormal metabolism of
vitamin D is often responsible for rickets. ere is little
vitamin D in the ordinary diet and the major source of
vitamin D is the vitamin D
3
synthesized in the skin
when it is exposed to ultraviolet light.
1
Growing age
groups (children and adolescents) are in a critical period
for skeletal mass accretion,
2-3
where adequate sun exposure
is needed. Female adolescents may be more vulnerable
especially Asians, as it was found in many countries that
Asian females have low levels of vitamin D.
4-11
In Saudi Arabia, many studies were carried out to study
Osteomalacia and Rickets in different age groups and
both sexes, but recently, only few studies were conducted
on healthy adult females,
12-14
and few on symptomatic
adolescents with rickets.
15-18
Some data are available on
vitamin D status in adolescents carried out in 1992,
7,8
but since then, no further studies have been carried out to
assess the prevalence of vitamin D deficiency in adolescent
females, although there is an impression from clinical
practice that it is not uncommon. e aim of our study
is to screen adolescent school girls aged 12-15 years, in
which a physiological growth spurt occurs and vitamin D
deficiency can occur quickly and asymptomatically. is
study looks into the prevalence of vitamin D deficiency
rickets among this group in Jeddah City of Saudi Arabia,
studies the symptoms and blood bone chemistry, and
identifies causative factors by reviewing the dietary habits
and sun exposure.
Methods. is research was funded by King Abdulaziz
University, Jeddah. e collection of the data and blood
samples took place between October 2003 – February
2004. Six hundred female students aged 12-15 years were
randomly selected from 6 schools chosen from different
areas of Jeddah and the questionnaires were distributed to
them, which reviewed the dietary habits, dairy products
consumption, exposure to sun, and presence or absence
of any symptoms. Four hundred and thirty-three students
were included in the study, who had no history of renal,
hepatic diseases, or malabsorption, no family history of
442
Vitamin D deficiency in school ... Siddiqui & Kamfar
Saudi Med J 2007; Vol. 28 (3) www.smj.org.sa
rickets, and were not on anti-convulsant therapy or
vitamin supplementations. Laboratory investigations
included blood bone chemistry (calcium, phosphate,
and alkaline phosphatase), parathyroid hormone assay,
and serum concentration of 25-hydroxycolcalciferol
(25-OHD), which was measured using enzyme-linked
immunosorbent assay (ELISA) technique (K2110,
Immunodiagnostic [Dutch Company], Holland).
Symptomatic vitamin D deficiency rickets was defined
by the presence of muscle, bone or back pain, muscle
spasms, or twitches in addition to serum (25-OHD)
concentrations of <25 nmol/L (n=25-125 nmol/L).
Asymptomatic vitamin D deficiency rickets was defined
by the presence of serum 25-OHD concentrations
of <25 nmol/L, with no symptoms. Severe vitamin
D deficiency was defined by the presence of serum
25-OHD concentrations of <12.5 nmol/L.
Statistical analysis was carried out using Statistical
Package for Social Sciences (SPSS) version 10. Chi
square test was used to analyze group differences for
categorical variables. For continuous variables, t-test
was used. P value of <0.05 was considered significant.
Results. Out of 433 girls, 350 (81%) had low
vitamin D levels, ranging from 2.2-24.0 nmol/L.
Approximately 194 girls were Saudi by birth (56%).
Two hundred thirteen girls were asymptomatic (61%).
Back pain was the most common complaint as
shown in Table 1. A severe vitamin D deficiency was
noticed in 173 (40%) girls of the total population
studied. e intake habits of dairy products in the
low vitamin D girls, showed that only 125 (36%) had
daily consumption versus 170 (48%) who rarely had
any, and that was statistically significant with p value of
0.013. Out of 150, only 31 (21%) took near the daily
requirement of milk such as >3 cups or equivalent of
milk products, but that was not statistically significant
with p value of 0.13 due to the girls who answered this
part of the questionnaire were few. e sun exposure
habits in the low vitamin D, girls showed that 67 (19%)
were never exposed to sun, 205 (67%) were exposed
in less than 15 minutes, and 235 (75%) had indirect
exposure. at was statistically significant with p values
of 0.013, 0.041, and 0.007.
Cases with a severe vitamin D deficiency (very
low vitamin D levels) were significantly more prevalent
with lower income and with rare sun exposure
[p=0.015 (Table 2)] and [p=0.01 (Table 3)]. Table 4
shows number of rachitic girls who had low calcium
and phosphate and high alkaline phosphatase and
parathormone levels. It was noticed that the severity
of vitamin D deficiency had no relation to the serum
levels of calcium, phosphate, and alkaline phosphatase,
but was inversely related to the parathormone levels
Table 1 - Prevalence of symptoms in 350 girls with rickets.
Symptoms n (%)
Back pain
Bone pain
Twitches
Muscle pain
Cramps
92 (26)
50 (14)
15 (4)
13 (4)
11 (3)
Table 2 - Relation of very low vitamin D level (<12.5 nmol/L) to the
family income.
Income
(Saudi Riyals)
Vitamin D level
above 12.5 nmol/L
n (%)
Vitamin D level
below 12.5 nmol/L
n (%)
Total
n (%)
3000
3000 – 8000
>8000
Total
40 (37)
42 (53)
57 (56)
139 (48)
67 (63)
38 (47)
44 (44)
149 (52)
107 (37)
80 (28)
101 (35)
288 (100)
P = 0.015
Table 3 - Relation of very low vitamin D level (<12.5 nmol/L) to sun
exposure.
Sun
exposure
Vitamin D level
above 12.5 nmol/L
n (%)
Vitamin D level
below 12.5 nmol/L
n (%)
Total
n (%)
Daily
Never
Total
129 (55)
24 (37)
153 (51)
104 (45)
43 (63)
147 (49)
233 (78)
67 (22)
300 (100)
P = 0.01
Table 4 -
Abnormal biochemical values of the 350 rachitic girls.
Normal value n (%)
High alkaline phosphatase (0 - 250 u/l)
High parathormone (1.6 – 6.5 pmol/l)
Low calcium (2.1 – 2.6 mmol/l)
Low phosphate (0.81 – 1.58 mmol/l)
211 (60)
149 (43)
39 (11)
14 (4)
Table 5 - Intake of dairy products in symptomatic and asymptomatic
girls with rickets.
Intake
Symptomatic
n (%)
Asymptomatic
n (%)
Total
n (%)
Daily
Twice/week
Rarely
Total
45 (36)
14 (26)
78 (45)
137 (39)
80 (64)
41 (74)
92 (55)
213 (61)
125 (36)
55 (16)
170 (48)
350 (100)
P = 0.024
443
www. smj.org.sa Saudi Med J 2007; Vol. 28 (3)
Vitamin D deficiency in school ... Siddiqui & Kamfar
time, it is alarming as many cases of rickets could be
missed if 25-OHD was not measured, especially that
alkaline phosphatase levels were also normal in many
cases. e presence of normal calcium levels in vitamin
D deficient patients were also observed by Sedrani
32
in Saudi Arabia. e presence of compensatory high
parathormone levels could contribute to normal serum
calcium levels, which were observed in our study. An
adolescent period is important in female life. Good
nutrition to maintain calcium and vitamin D stores, and
enough sun exposure is important for bone formation
and prevention of osteomalacia/rickets. Adolescent
rickets if not diagnosed, can progress to osteomalacia in
adulthood and during pregnancy with probably serious
consequences to both mother and the baby. ere is
also high risk of postmenopausal osteoporosis in these
girls.
35
In conclusion, vitamin D deficiency has a high
prevalence in adolescent females in Jeddah area and
probably in Saudi Arabia in general. Most of the cases
are asymptomatic and if present, symptoms are non
specific. is high prevalence of vitamin D deficiency
is attributed to both lack of dietary dairy intake and to
lack of sun exposure. Many cases of adolescent rickets
are undiagnosed and we urge physicians to have a
higher degree of clinical suspicion for hypovitaminosis
D and to screen all the patients with non specific
musculoskeletal pain by measuring 25-OHD. We
also recommend improved dietary supplies of highly
bioavailable calcium (such as milk) and vitamin
D from food fortification, the improvement of sun
exposure facilities in schools and the integration of the
topic of vitamin D deficiency, and osteomalacia/rickets
into the school syllabus in order to improve the
health education of the students and the population
as a whole. Furthermore, screening studies are needed
in different regions of Saudi Arabia to assess the
magnitude of this preventable problem.
References
1. Inzucchi SE. Diseases of calcium metabolism and metabolic
bone disease. In: Federman DD, Dale DC, editors. Scientific
American Medicine. New York (NY): Web Inc; 2003.
2. Glastre C, Braillon P, David L, Cochat P, Meunier PJ, Delmas
PD. Measurement of bone mineral content of the lumbar
spine by dual energy x-ray in normal children: Correlation
with growth parameters. J Clin Endocrinol Metab 1990; 70:
1330-1333.
3. Sabatier JP, Guaydier-Souquieres G, Laroche D, Benmalek A,
Fournier L, Guillon-Metz F, et al. Bone mineral acquisition
during adolescence and early adulthood: a study in 574
healthy females 10-24 years of age. Osteoporos Int 1996; 6:
141-148.
4. O’ Hare AE, Uttley WS, Belton NR, Westwood A, Levin SD,
Anderson F. Persistence of Vitamin D deficiency in the Asian
adolescents. Arch Dis Child 1984; 59: 766-770.
with a significant p value of 0.002. Symptoms of rickets
had no relation to the severity of vitamin D deficiency,
to serum calcium levels nor to the sun exposure habits
(p=0.3, 0.25, 0.3), however, they were related to daily
intake of dairy products with p=0.024, that were
statistically significant. Table 5 shows intake habits of
dairy products in the symptomatic and asymptomatic
girls with rickets.
Discussion. In the past, vitamin D deficiency
rickets was seen in the poor areas of Europe and North
America, before it was eradicated by fortification of
milk and infant foods with vitamin D.
19
In Europe,
it is mainly seen in the Asian community,
4,6,9,20
but
recently, few studies show its presence in Europe and
North America in the winter, specially in adolescents and
young adults.
21-25
In Saudi Arabia, inadequate vitamin
D levels were detected in a population based study and is
shown that vitamin D deficient osteomalacia/rickets is
not uncommon and it is higher in female adolescents
and adults.
7,8
Our study shows a higher prevalence of vitamin D
deficiency than in other studies. e United Kingdom
reported 6% and 44%,
4,26
Lebanon 53.5% and 74%;
5
Saudi Arabia 38.6%;
8
China 54.6%;
10
Spain 31%,
21
Finland 67.7%,
23
and France 34%.
27
e mean level of
vitamin D was also lower than in other studies.
5,7,21,23
Our
study also shows that the daily intake of dairy products was
less in the girls with low vitamin D levels, and that 80%
were taking below the daily allowance recommended
by National Institute of Health.
28,29
It was also noted
that girls who had symptoms did not consume dairy
products daily, it means that the symptoms are directly
and significantly related to the daily calcium intake. e
reasons probably for less intake were ignorance or lack
of education, the increased consumption of soft drinks
instead of milk, and the fear from gaining weight. ere
was a direct relation between less sun exposure and low
serum levels of vitamin D in our study. e issue of
the duration of the sunlight exposure needed to maintain
adequate stores of vitamin D has been controversial,
30
but
recently, it was recommended to be 15 minutes of sunlight
daily.
31
In Saudi Arabia, the exposure of people generally
to the sun is limited, despite of abundant sunlight due
to high daytime temperature.
8,32-34
Females tend to have
less sun exposure due to sociocultural reasons, lack of
awareness of the importance of sun exposure for bone
health, and for cosmetic reasons thinking that it is
harmful. It was noted that girls who had a severe vitamin
D deficiency were rarely exposed to the sun and came
from lower income families and that may be related to
smaller crowded houses where sunlight does not reach.
e presence of normal calcium and normal phosphate
levels in most of the cases is interesting, and at the same
444
Vitamin D deficiency in school ... Siddiqui & Kamfar
Saudi Med J 2007; Vol. 28 (3) www.smj.org.sa
5. El-Hajj Fuleihan G, Nabulsi M, Choucair M, Salamoun M,
Hajj Shahine C, Kizirian A, et al. Hypovitaminosis D in Healthy
School Children. Pediatrics 2001; 107: e53.
6. Nisbet JA, Eastwood JB, Colston KW, Ang L, Flanagan AM,
Chambers TJ, et al. Detection of osteomalacia in British Asians:
A comparison of clinical score with biochemical measures. Clin
Sci (Lond) 1990; 78: 383-389.
7. Sedrani SH, Al-Arabi K, Abanmy A, Elidrissy A. Vitamin D
status of Saudis: I. Effect of age, sex and living accommodation.
Saudi Med J 1992; 13: 151-158.
8. Sedrani SH, Al-Arabi K, Abanmy A, Elidrissy A. Vitamin
D status of Saudis: III. Prevalence of inadequate plasma 25
hydroxyvitamin D concentrations. Saudi Med J 1992; 13:
214-219.
9. Koch HC, Burmeister W. Vitamin D status of children and
adolescents of African and Asian diplomats in Germany. Klin
Padiatr 1993; 205: 416-420.
10. Du X, Greenfield H, Fraser DR, Ge K, Trube A, Wang Y.
Vitamin D deficiency and associated factors in adolescents girls
in Beijing. Am J Clin Nutr 2001; 74: 494-500.
11. Mishal AA. Effects of different dress styles on vitamin D levels
in healthy young Jordanian Women. Osteoporos Int 2001; 12:
931-935.
12. Abanmy A, Salman H, Cheriyan M, Shuja M, Sedrani S.
Vitamin D deficiency rickets in Riyadh. Ann Saudi Med 1991;
11: 35-39.
13. Ardawi MS, Nasrat HAN, Ba’Aqueel HSM, Ghafoury HM,
Bahnassy AA. Vitamin D status and calcium regulating
hormones in Saudi pregnant females and their babies: a cross
sectional study. Saudi Med J 1997; 18: 15-25.
14. Ghannam NN, Hammami MM, Bakheet SM, Khan BA. Bone
mineral density of the spine and femur in healthy Saudi females:
relation to vitamin D status, pregnancy and lactation. Calcif
Tissue Int. 1999; 65: 23-28.
15. Narchi H. Case control study of diet and sun exposure in
adolescents with symptomatic rickets. Ann Trop Paediatr 2000;
20: 217-221.
16. Narchi H, El Jamil M, Kulaylat N. Symptomatic rickets in
adolescence. Arch Dis child 2001; 84: 501-503.
17. Al-Jurayyan NA, El-Desouki ME, Al-Herbish AS, Al-Mazyad
AS, Al-Qhtani MM. Nutritional rickets and osteomalacia in
school children and adolescents. Saudi Med J 2002; 23: 182-
185.
18. Abdullah MA, Salhi HS, Bakry LA, Okamoto E, Abomelha Am,
Stevens B, et al. Adolescent rickets in Saudi Arabia: a rich and
sunny country. J Pediatr Endocrinol Metab 2002; 15: 1017-
1025.
19. Arniel GC, Crosbie JC. Infantile rickets returns to Glosgow.
Lancet 1963; 185: 423-425.
20. Nellen JF, Smulder YM, Jos Frissen PH, Slaat ED, Silberbusch J.
Hypovitaminosis D in immigrant women: slow to be diagnosed.
Br Med J 1996; 3: 47-48.
21. Docio S, Riancho JA, Perez A, Olmos JM, Amado JA, Gonzalez-
Macias J. Seasonal deficiency of vitamin D in children: a
potential target for osteoporosis preventing strategies. J Bone
Miner Res 1998; 13: 544-548.
22. Guillemant J, Taupin P, Le HT, Taright N, Alemandou A, Peres
G, et al. Vitamin D status during puberty in French healthy
male adolescents. Osteoporos Int 1999; 10: 222-225.
23. Lehtonen-Veromaa M, Mottonen T, Irjala K, Karkkainen M,
Lamberg-Allardt C, Hakola P, et al. Vitamin D intake is low
and hypovitaminosis D common in healthy 9 to 15 years-old
Finnish girls. Eur J Clin Nutr 1999; 53: 746-751.
24. Vieth R, Cole DE, Hawker GA, Trang HM, Rubin LA.
Wintertime vitamin D insufficiency is common in young
Canadian women, and their vitamin D intake does not prevent
it. Eur J Clin Nutr 2001; 55: 1091-1097.
25. Tangpricha V, Pearce EN, Chen TC, Holick MF. Vitamin D
insufficiency among free-living healthy young adults. Am J Med
2002; 112: 659-662.
26. Stephens WP, Klimiuk PS, Warrington S, Taylor JL, Berry JL,
Mawer EB. Observations on the natural history of vitamin D
deficiency among Asian immigrants. Q J Med 1982; 51: 171-
188.
27. Guillemant J, Allemandou A, Cabrol S, Peres G, Guillemant
S. Vitamin D status in the adolescent: seasonal variations
and effects of winter supplementation with vitamin D3. Arch
Pediatr 1998; 5: 1211-1215.
28. NIH Consensus conference. Optimal calcium intake. NIH
Consensus Development Panel on Optimal Calcium Intake.
JAMA 1994; 272: 1942-1948.
29. Fraser DR. Physiology of vitamin D and calcium homeostasis
In: Glorieux FH editor. Rickets of Nestle Nutrition Workshop
Series. New York (USA): Raven Press; 1991. p. 23-31.
30. Gesensway D. Vitamin D.
Ann Intern Med 2000; 133: 318.
31. Lambing CL. Osteoporosis 2003. Proceeding of the American
Academy of Family Physicians. Annual Scientific Assembly;
2003 Oct 1-5; New Orleans, Louisiana.
32. Sedrani SH. Are Saudis at risk of developing Vitamin D
deficiency? Saudi Med J 1986; 7: 427-433.
33. El Idrissy ATH. Vitamin D Deficiency rickets in a sunny
country: pathogenesis, clinical picture and management. Ann
Saudi Med 1987; 7: 119-125.
34. Sedrani SH, Al-Arabi, Abanmy A, Elidrissy A. Vitamin D status
of Saudis: IV. Seasonal variations. Saudi Med J 1992; 13: 423-
429.
35. Weaver CM, Peacock M, Johnston CC Jr. Adolescents Nutrition
in the Prevention of Postmenopausal Osteoporosis. J Clin
Endocrinol Metab 1999; 84: 1839-1843.