Rickets, edited by Francis H. Glorieux.
Nestle Nutrition Workshop Series. Vol. 21.
Nestec Ltd.. Vevey/Raven Press. Ltd..
New York© 1991.
Vitamin D-Deficiency Rickets
in Saudi Arabia
Abdel-Wahab T. H. Elidrissy
College of Medicine, Omdurman Islamic University, P.O. Box 3453, Khartoum, Sudan
Rickets was primarily a disease of temperate countries but after a long period of
eradication it has reappeared among the immigrants in these countries (1-5). In sunny
countries, rickets is being seen in such a magnitude as to be considered a community
health problem (6-14). The natural and main source of vitamin D even in temperate
countries is still through exposure to sunshine (15-17). This chapter reviews the
factors associated with development of rickets in a country, Saudi Arabia, where
there is abundance of sunshine.
EFFECTS OF VITAMIN D DEFICIENCY
The initial outcome of vitamin D deficiency is hypocalcemia, followed by hypophosphatemia, and a rise of alkaline phosphatase, these findings are termed biochemical rickets or osteomalacia. The hypophosphatemia, although an invariable
finding in vitamin D-deficiency rickets, might not be as striking as is the hypocalcemia
in the early stage of the disease (18). The hypocalcemia stimulates the parathormone
which in turn leads to bone resorption in an attempt to maintain normal serum calcium
(19). In growing bones, bone matrix continues to be produced but due to impaired
calcification its accumulation becomes irregular leading to widening at the epiphyseal
ends of the bones which manifests clinically in areas of fast bone growth like the
wrist and costochondral junction. In weight-bearing long bones, inadequate mineralization may induce deformities of varying severity.
PATHOGENESIS OF RICKETS
In Riyadh, the level of ultraviolet rays available in the atmosphere is consistent
with what is expected at such an altitude (20) and the amount that reaches the usually
exposed human skin is enough to maintain adequate circulating levels of 25(OH)D
(21). Then why do we see rickets in such a place? In trying to answer this question
I will first discuss the interrelations of vitamin D status between mother and infant
and then the factors affecting it.
223
224
RICKETS IN SA UDI ARABIA
Maternal Vitamin D Deficiency as a Cause of Rickets
in Infants
In Riyadh, rickets commonly occurs in the first year of life with a mean age of
ten months (6,22). Although congenital rickets has been reported (23,24) the youngest
infant seen with clinical rickets in our series was two months old and presented with
hypocalcemic convulsions associated with minimal bony changes (22). The mothers
of rachitic infants were found to be vitamin D deficient (25) and paired maternal and
cord blood vitamin D status proved to be low (26,27). In spite of this low 25(OH)D,
calcium levels in cord blood were maintained within normal levels, and were even
higher than the corresponding maternal levels (28,29). These findings conform with
the active transplacental transport of calcium (30,31), which could be linked to the
high levels of 1,25(OH)2D during pregnancy (32,33) especially since the placenta (34)
and the fetus (35) can act as additional sites for the synthesis of 1,25(OH)2D. Indeed
our data show normal to high levels of 1,25(OH)2D in pregnancy in spite of the low
levels of 25(OH)D. A lack of correlation between the two metabolites was also shown
(36).
The active transplacental calcium transfer in spite of the poor vitamin D status of
the mother was found to maintain adequate fetal bone mineralization and prevent
congenital rickets except in states of severe maternal osteomalacia (37).
The maternal vitamin D deficiency state during pregnancy leads to delivery of
infants with poor vitamin D stores, but marginally adequate calcification. After birth
these infants are unable to maintain normal calcium levels due to the loss of the
active transplacental calcium pump and lack of vitamin D reserves. This might manifest as neonatal hypocalcemia in some (30,38) or later manifestations in others,
depending on vitamin D content of the milk and environmental exposure to the sun
(39). The evidence available supports the hypothesis that maternal vitamin D deficiency contributes to rickets in the offspring (6) (Fig. 1). Infantile rickets in Libya
was attributed to similar low maternal and cord blood 25(OH)D levels (40).
Environmental Factors Leading to Vitamin D Deficiency
Housing
Most of the rachitic infants were living either in flats or traditional mud houses
(6,24). The traditional mud house is high walled with small high windows. In both
types of dwellings there is no direct access to sunshine in contrast to rural houses
that have courtyards where mothers and their children can be exposed to sunlight
in privacy (6). The lowest levels of vitamin D among the pregnant mothers were
found to be associated with traditional houses and flats (29).
Location
The location of the house may also contribute to vitamin D deficiency. This is
supported by the finding that almost all the rachitic infants came from the crowded
RICKETS IN SAUDI ARABIA
225
JMofrmol Vitamin D Dftci«ncy|
V
I Infant boni with poor Vitonwi D > t o r » |
- 6 - S Month*
*
— Doa net pcmnt
m Ricfcm
PMrMfAQI OOfiQf
-Bowing of teg*
RG. 1. Sequelae of maternal vitamin D deficiency.
parts of the city (27). In these areas, mothers and their infants remain indoors with
no chance of being exposed to sunshine. This simulates what used to be seen in
Europe following the industrial revolution when rickets was endemic in the slums
of the industrial cities (2), although in Riyadh there is no lack of ultraviolet rays
(21,22) but only lack of exposure to it.
Customs
Female dressing
Since the purdah observed by some immigrants in Europe was considered to be
a major factor in the prevalence of rickets and osteomalacia among them we studied
the pattern of dressing and its relation to the occurrence of rickets. The traditional
dressing of women in Riyadh was found not to affect their vitamin D status as the
25(OH)D levels of female students were found to be similar to male students (41).
Also, school girls from the age of six to nineteen years did not show a drop in
25(OH)D levels coinciding with the change to traditional dress taking place at puberty
(42). In rural areas, where women wear similar traditional dress, rickets is not a
problem (6,43). This could easily be explained by the fact that houses have courtyards
where sun exposure can be achieved while carrying out home duties. From the
available evidence it can thus be stated that the women's way of dressing per se is
not what causes vitamin D deficiency.
226
RICKETS IN SAUDI ARABIA
\ Poorly illuminated flats with no "open
"• areas inbetween the buildings
FIG. 2.
Urbanization umbrella.
Mothers and infants having no access
to direct sunlight
Wrapping the infants
Although we have reported this custom as a causal factor of rickets in our original
communication (6), subsequently we did not find evidence to support this, especially
since the period of wrapping is up to four months of age. In this period of life mothers
do not usually expose their infants to direct sunshine guided by the belief that the
sun will hurt them (39).
The Umbrella Phenomenon
The sunshine is abundant in Riyadh but an umbrella is formed depriving the infants
and their mothers from getting access to sunshine (44). Urbanization forms the main
pillar on which this umbrella is pivoted as shown in Figure 2. Urbanization is associated with living in flats that are devoid of sunshine especially since ultraviolet
light does not penetrate glass. Rickets is seen due to man-made factors preventing
access to the available ultraviolet rays and accordingly synthesis of vitamin D. The
statement by Park (45) before the discovery of vitamin D that rickets is a disease of
artificial ways of living and never associated with natural life still holds true in sunny
countries.
EPIDEMIOLOGY
As rickets is seen in Riyadh at a mean age often months and the usual presentation
is by symptoms not directly related to the disease (Fig. 3), its diagnosis might be
missed and, accordingly, the true incidence is difficult to elicit (6). The diagnosed
RICKETS IN SA UDI ARABIA
0
10
20
227
30
FIG. 3. Clinical presentation of rickets.
cases formed less than 1% of the admission in Riyadh childrens' hospitals (unpublished data). The majority of the rachitic infants have normal protein and caloric
nutritional status (24). This makes it sometimes difficult to elicit the physical signs
of rickets like swollen wrists and costochondral beading. In an epidemiological and
clinical study of the patients seen by the author, 52% were living in flats with a
majority of illiterate mothers. Fifty-seven percent of the mothers thought that exposure to the sun was harmful to their infants and only 12% realized that sunlight
was good for the infant. Eighty-six percent of the mothers never exposed their infants
to the sun. Parents were first degree cousins in 46% which is not different from the
general community. Eighty-nine percent of rachitic children were breast-fed. These
facts confirm our previous observations (6).
CLINICAL PICTURE
The clinical presentation of rickets in cases seen by the author in a period of three
years is shown in Figure 3. These infants present with respiratory and gastrointestinal
symptoms and signs of rickets may pass unnoticed. Craniotabes is elicited only in
early life. During the first six months of life, rickets may present with hypotonia and
hypocalcemic convulsions. At this stage, rickets is subclinical, and radiology of the
bones of the forearm may reveal either minor changes or no changes at all. The
hypocalcemic convulsions may be precipitated by fever. In the second year of life
delayed walking and eruption of teeth may warrant seeking medical advice. It is only
when the child starts to walk that bowing of the legs and a waddling gait becomes
an obvious cause of concern. Excessive sweating may be noticed by some parents.
228
RICKETS IN SA UDI ARABIA
DIAGNOSIS
Diagnosis of rickets in infants depends mainly on suspecting the condition and
accordingly looking for its signs among children presenting with the common pediatric ailments such as chest infection and gastroenteritis.
PREVENTION
In such sunny countries, exposure to the sun is the natural and best method of
preventing rickets. This can be achieved by alleviating the factors forming the umbrella. Houses need to be designed in a way to allow for exposure to sun in privacy.
When exposure to the sun is impractical vitamin D supplementation in the form of
medication is essential, 400 IU daily is enough to prevent rickets. Improvement of
maternal vitamin D status will prevent neonatal hypocalcemia (39) and will render
breast-fed infants not needing further supplementation and maintain bone mineralization for at least the first six months of life without vitamin D supplementation
(46). For complete discussion of this important topic see chapter by L. Paunier.
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8. Salimpour R. Rickets in Tehran. Arch Dis Child 1975^0:63-6.
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14. Hojer B, Medhin MG, Sterky G, Zetterstrom R, Daniel K. Combined vitamin D deficiency rickets
and protein-energy malnutrition in Ethiopian infants. Environmental Child Health 1977:73-9.
15. Haddad JG, Hahn TJ. Natural and synthetic sources of circulating 25-hydroxyvitamin D in man.
Nature 1973244:515.
16. Lawson DEM, Paul AA, Black AE, Cole TJ, Mandal AR, Davie M. Relative contribution of diet
and sunlight to vitamin D status in the elderly. Br Med J 1979^:303.
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18. Harrison HE, Harrison HC. Vitamin D and phosphate homeostasis. In: Norman AW, ed. vitamin
D molecular biology and clinical nutrition. New York: Marcel Dekker, 1980;378.
19. DeLuca HF. Vitamin D metabolism and function. New York: Springer-Verlag, 1979;44.
20. Hannan MH, El-Yazigi A, Al-Watban FAH, Feteih N. Solar ultraviolet-B in Riyadh: its significance
in studies on vitamin D deficiency in Saudi Arabia. King Faisal Specialist Hospital Journal
1983;4(4):307-12.
21. Sedrani SH. Low 25-hydroxyvitamin D and normal calcium concentration in Saudi Arabia: Riyadh
region. Ann NutrMetab 1984^28:181-5.
22. Elidrissy ATH. Protein-calorie nutritional status of infants with deficiency rickets in Riyadh. Annals
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23. Ford JA, Davidson DC, Mclntosh WB, Fyfe WM, Dunnigan MG. Neonatal rickets in Asian immigrant
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24. Moncrieff M, Fadahunsi TO. Congenital rickets due to maternal vitamin D deficiency. Arch Dis Child
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25. Elidrissy ATH, Sedrani S, Lawson DEM. Vitamin D deficiency in mothers of rachitic infants. Calcif
Tissue Int 1984^6:266-8.
26. Behon NR, Elidrissy ATH, Gaafer TH, et al. Maternal vitamin D deficiency as a factor in the
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24,25 dihydroxyvitamin D in vitro synthesis by human deddua and placenta. Nature 1979i281:317.
35. Kuoppala T. Can the fetus regulate its calcium uptake? BrJ Obstet Gynaec 1984;91:1192-6.
36. Mograhby SAS, Al-Shawaf T, Akiel A, Sedrani SH, Elidrissy ATH, AI-Meshari AA. The effect of
parity on vitamin D metabolites. Ann Trop Paediatr. (In press.)
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born to Asian and white mothers. Br MedJ 1983^86:1233-5.
38. Brooke OG, Brown IRF, Bone CDM, et al. Vitamin D supplements in pregnant Asian women: effects
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39. Elidrissy ATH, El-Swailem AR, Belton NR, Aldrees A, Forfar JO. 25 Hydroxy-vitamin D in children
with rickets in Riyadh. In: Norman AW, et al., eds. Chemical, biochemical and clinicai endocrinology
of calcium metabolism. Berlin: de Gruyter, 1982;735-7.
40. Elzouki A, Legnain M, Markstead T. Vitamin D nutritional status of neonates and pregnant women
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41. Sedrani S, Elidrissy ATH, El Arabi KM. Sunlight and vitamin D status in normal Saudi subjects.
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42. Elidrissy ATH, Abdullah MA, Sedrani SH, Karrar ZA, Arabi KM. Vitamin D in school girls in
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43. Abdullah MA, Swailem A, Taha SA. Nutritional status of preschool children in central Saudi Arabia.
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DISCUSSION
Dr. Holick: You made a very good point regarding the role of breast-feeding in vitamin D
nutrition. It may be worthwhile to mention that the mechanism by which transfer from mother
to child is not specifically by secreting vitamin D into the milk, but rather by passive transport
in the milk of both albumin and the vitamin-D-binding protein that carries with it principally
25(OH)D, which is then the principal source of vitamin D for the infant.
Dr. Coates: Malnourished babies usually don't have a regular medical follow-up, and they
come to the hospital with an infection such as pneumonia or acute diarrhea which gets
prolonged because of secondary lactase deficiency. Nutritional rickets is diagnosed at the
hospital. We often see hypocalcemia with convulsion after fasting, in first and third stage
rickets. What is your experience regarding rickets with malnutrition after prolonged diarrhea?
Dr. Elidrissy: Most cases of rickets occur among breast-fed, well nourished infants. I have
also seen cases of malabsorption and celiac disease who developed rickets. But as a whole,
in our community, the nutrition status of infants is good. And they might develop rickets as
part of chronic diarrhea, yes, but this is not the general case. The incidence of rickets is
about 2 to 3% in a hospital population so that we see about 500 children with rickets per
year. The other problem is hypocalcemia in the first months of life. I have seen one or two
cases of hypocalcemic convulsions with florid rickets, but most of the cases occur at an early
stage and with high fever. Thus, as a rule, every patient admitted for febrile convulsions
ought to have a work-up to eliminate a disturbance in calcium homeostasis.
Dr. Pettifor: I have two comments. The first is over the term vitamin D deficiency. It
should be reserved for those individuals that have other biochemical evidence of inadequate
vitamin D supply, in other words, not only low 25(OH)D but also hypocalcemia, elevated
PTH levels, and perhaps hypophosphatemia; and that we should reserve for those who have
just low 25(OH)D levels the term low vitamin D status rather than vitamin D deficiency. I
think this may help us to differentiate the problem in various countries, for instance Saudi
Arabia. Do your mothers actually have clinical symptoms or biochemical evidence of vitamin
D deficiency or do they not rather just suffer from low vitamin D status? I think this makes
a difference. Secondly, I believe that there is no harm in suggesting that we should give
vitamin D supplements not only to all breast-fed infants, but to all infants under the age of
one year. As pediatricians, the majority of us are attempting to encourage breast-feeding.
Yet, to suggest that only breast-fed infants need vitamin D supplementation is probably going
to have a negative effect on our efforts. Even if infants receive vitamin D enriched formulas,
there is no evidence that an extra 400IU vitamin D/day as a supplement is going to produce
vitamin D toxicity. Thus to recommend vitamin D supplementation to all infants would
simplify the message and the public health strategies. To ensure that mothers and their infants
receive adequate sunlight to prevent vitamin D deficiency without vitamin D supplementation
may be a major problem in certain areas where social customs strongly prevent going out
of doors during pregnancy.
Dr. Elidrissy: We have just finished a nationwide study on the levels of vitamin D in Saudi
Arabia. Levels of 25(OH)D are very low compared to the levels reported in the United States
or Europe. Thus, as already discussed, in sunny countries levels of vitamin D may be on
the low side depending on environmental factors. We now recommend in Saudi Arabia that
all breast-fed infants be given vitamin D supplementation, and the same is recommended by
the Ministry of Health for all pregnant women.
Dr. Glorieux: In keeping with the title of this particular session, which is "Rickets as a
RICKETS IN SA UDI ARABIA
231
Public Health Problem," could you give us some indication, whether in Saudi Arabia rickets
is a significant factor of morbidity, in terms of admission to hospitals, growth retardation,
residual deformities, and other problems that may arise from having been rachitic at an early
age.
Dr. Elidrissy: There appear to be no long-term effects of rickets, in our community. My
colleagues and I have also asked certain obstetricians about the incidence of the so-called
rachitic pelvis, but no case was noted. Serious problems may be encountered in infants with
rickets who are admitted for convulsions and pulmonary infection. Adequate preventive
measures is the best way to avoid them.
Dr. Heinrich: In terms of public health, where do you put the detection limit of rickets?
Is it a clinical or a biochemical one? When do you have to implement the preventive measures?
You also said that there is no malnourishment. What about calcium intake in these children?
Could they be calcium deprived?
Dr. Elidrissy: All the cases which we have seen were showing evidence of clinical rickets.
With regard to the low calcium intake, all these infants are breast-fed, and I assume that
they receive enough calcium. But of course, in order to absorb that calcium, it is imperative
that they receive enough vitamin D.
Dr. Markestad: It is interesting that the same clinical pattern of rickets is seen in Saudi
Arabia, Lybia, and Norway, although in Norway it is not a major public health problem
except in the immigrant population. In all three countries the disease is almost exclusively
limited to the first 18 months of life, and permanent skeletal deformities appear to be extremely
rare.
Dr. Martinez: At what age does the introduction of beikost take place in your country?
The early dietary use of flours with a high content in phytate causes poor absorption of
calcium as it has been seen in Bedouins, who eat a bread called raghif (1,2).
Dr. Elidrissy: It is a teaching of Koran that breast-feeding should be continued for two
years. So, many mothers are resisting introduction of any other element before one year of
age. I personally don't like introducing solids, and that includes phytate or fiber containing
foodstuff, before the age of six months. They, thus, should not be considered as playing a
significant role in the pathogenesis of rickets.
Dr. Paunier: You said that you recommend that breast-fed infants should receive vitamin
D supplements. I fully agree with that. But what is the percentage of the breast-feeding
mothers who actually comply with this recommendation? And, in your country, do you have
a specific education program for rickets prophylaxis?
Dr. Elidrissy: Earlier on, we recommended that people take advantage of a nice weekend
in the sun. This became increasingly more difficult with urbanization. We now give 400 IU/
d of vitamin D to all breast-fed infants. The advice is included in Health Education programs
but I have no data about compliance in our population.
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1. Beriyne GM, Ben-Hari J, Nord E, Shaikin R. Bedouin osteomalacia due to calcium deprivation caused
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