1. Pediatr Radiol
DOI 10.1007/s00247-008-1001-z
COMMENTARY
Rickets vs. abuse: a national and international epidemic
Kathy A. Keller & Patrick D. Barnes
Received: 4 November 2007 / Revised: 28 July 2008 / Accepted: 18 August 2008
# Springer-Verlag 2008
Keywords Rickets . Child abuse . Metabolic bone disease . women 18 to 29 years of age in Boston. A recent study of
Nonaccidental injury healthy infants and toddlers aged 8 to 24 months in Boston
found an insufficiency rate of 40% and a deficiency rate of
12.1% [4].
In the May 2007 issue of Pediatric Radiology, the article In September 2007, a number of articles about congen-
“Can classic metaphyseal lesions follow uncomplicated ital rickets were published in the Archives of Diseases in
caesarean section?” [1] suggested that enough trauma could Childhood including an international perspective of mother
occur under these circumstances to produce fractures previ- and newborn DD reported from around the world [5].
ously described as “highly specific for child abuse” [2]. Concentrations of 25-hydroxyvitamin D [25(OH)D] less
However, the question of whether the metaphyses were normal than 25 nmol/l (10 ng/ml) were found in 18%, 25%, 80%,
to begin with was not raised. Why should this be an issue? 42% and 61% of pregnant women in the UK, UAE, Iran,
Vitamin D deficiency (DD), initially believed to primarily northern India and New Zealand, respectively, and in 60 to
affect the elderly and dark-skinned populations in the US, is 84% of non-western women in the Netherlands. Currently,
now being demonstrated in otherwise healthy young adults, most experts in the US define DD as a 25(OH)D level less
children, and infants of all races. In a review article on than 50 nmol/l (20 ng/ml). Levels between 20 and 30 ng/ml
vitamin D published in the New England Journal of are considered to indicate insufficiency, reflecting increas-
Medicine last year [3], Holick reviewed some of the recent ing parathyroid hormone (PTH) levels and decreasing
literature, showing deficiency and insufficiency rates of calcium absorption [3]. With such high prevalence of DD
52% among Hispanic and African-American adolescents in in our healthy young women, congenital deficiency is
Boston, 48% among white preadolescent females in Maine, inevitable, since neonatal 25(OH)D concentrations are
42% among African American females between 15 and approximately two-thirds the maternal level [6].
49 years of age, and 32% among healthy white men and Bodnar et al. [7] at the University of Pittsburgh, in the
largest US study of mother and newborn infant vitamin D
Editor’s note: See related articles in this issue: Slovis TL, Chapman S levels, found deficient or insufficient levels in 83% of black
doi:10.1007/s00247-008-0997-4; Chesney RW doi:10.1007/s00247- women and 92% of their newborns, as well as in 47% of
008-0993-8; Jenny C doi:10.1007/s00247-008-0995-6; Slovis TL,
Chapman S doi:10.1007/s00247-008-0994-7 white women and 66% of their newborns. The deficiencies
were worse in the winter than in the summer. Over 90% of
K. A. Keller
these women were on prenatal vitamins. Research is
Pediatric Radiology of America,
Stanford, CA 94305, USA currently underway to formulate more appropriate recom-
mendations for vitamin D supplementation during pregnan-
P. D. Barnes (*) cy (http://clinicaltrials.gov, ID: R01 HD043921).
Department of Radiology, Lucile Packard Children’s Hospital,
The obvious question is, “Why has DD once again
725 Welch Road,
Palo Alto, CA 94304, USA become so common?” Multiple events have led to the high
e-mail: pbarnes@stanford.edu rates of DD. In the past, many foods were fortified with

2. Pediatr Radiol
vitamin D. At present, milk is the only product required to best location to search for radiographic evidence of congenital
be fortified in the US, although studies have shown that up rickets and nutritional rickets in infants less than 3 months
to 70% of sampled milk does not contain the required of age is in the cranium [19]. The skull, as a reflection of
amount of vitamin D. There are few other natural food rapid brain growth in early life, is the most affected bone at
sources of vitamin D. While exposure to the sun’s UVB this age. Softening of the skull (craniotabes), especially in
rays remains the best natural source of vitamin D, during the occipital region with palpable enlargement of the sutures
the winter months, above the 35° latitude (at the level of and fontanelles, was a common clinical finding with
Atlanta, Georgia) there is a loss of UVB rays that are congenital rickets in the past, and is once again being
necessary for skin synthesis of vitamin D. In addition, described in association with newborn DD [20]. Demineral-
along with the concern for skin cancer and skin aging, there ized sutures create a diastatic appearance with poorly defined
has been a significant increase in the use of sunscreen and margins on radiographs (pseudodiastasis). The skull is better
protective clothing. A sun protection factor of 8 blocks evaluated on the head CT scan, which should be done to
about 95% of the UVB rays, and with regard to vitamin D, exclude sutural diastasis from increased intracranial pressure.
sunscreen use produces the same effect as a burka worn by Indistinctness of the facial bones and the orbital roof make
certain Islamic women, who, even in the sunny climate of the teeth and petrous bones appear relatively dense on
the Middle East, continue to have high rates of DD. The radiographs [21].
increase in obesity is another important factor since fat Metaphyseal changes of the long bones appear first at
storage of this vitamin decreases its availability to the rest the most recently formed metaphyseal margin, the Laval-
of the body. In a recently published study, the vitamin D Jeantet ring. These metaphyseal changes are usually
status of neonates born to obese mothers was found to be symmetric, and will occur first in the fastest-growing long
poorer than the vitamin D status of neonates born to lean bones (the femurs, tibiae and fibulae). The metaphyseal
mothers [8]. changes in the distal femurs and proximal tibiae occur first
Over the past few decades, there has been a significant along the medial aspects [22], and the early metaphyseal
increase in the frequency and the duration of breast-feeding, changes in the distal ulnar can be found even when the
both of which are risk factors for infant nutritional DD. In distal radial metaphyses appear normal [23]. While the
2003, the American Academy of Pediatrics published physeal and metaphyseal changes can be subtle in early
guidelines recommending that all breast-fed infants receive infancy, with treatment, the metaphyses may become
100% of their daily vitamin D requirement from supple- increasingly sclerotic and deformed [23]. While these early
mentation. Research has demonstrated breast milk to be so metaphyseal changes may mimic Salter-Harris II fractures,
deficient in vitamin D that the average lactating woman they are asymptomatic and, with treatment, usually resolve
must feed her infant 8 l (about 89 three-ounce bottles) of without the interval stages of fracture healing (subperiosteal
breast milk per day to provide the recommended daily new bone formation, callous, and remodeling) within a few
vitamin D intake of 200 IU [9]. Even infants born to weeks. When subperiosteal changes are present, particularly
mothers who are replete with vitamin D demonstrate in the tibiae, a lateral view may reveal early bowing
decreasing levels within 8 weeks if not supplemented deformity. Bowing deformities of the long bones prior to
[10]. Ziegler et al. [11] at the University of Iowa, during a weight bearing are not common, but when present, they
study of iron levels in breast-fed infants, incidentally found reflect positional stresses or musculotendinous forces,
that the majority of their unsupplemented infants had DD, such as the “saber shin deformity” where the pull of the
with severe DD common in the winter. Recent literature Achilles tendon on the calcaneus causes the tibiae to bow
suggests that supplementing lactating women with 2,000 to anteriorly [19].
4,000 IU per day (rather than the current recommendation Rachitic flaring of the anterior rib ends will also be
of 400 IU per day) is required to provide both the mother subtle on radiographs in the acute stage at this age, but may
and her breast-fed infant with adequate vitamin D [12]. become more pronounced with healing. Loss of cortical
What are the radiographic findings of congenital and distinction, subperiosteal new bone formation in the long
nutritional rickets in infants younger than 6 months old, the bone diaphyses, insufficiency fractures and Looser zones
age at which we typically first see the fraying and cupping (i.e. pseudofractures) of the ribs and forearms have all been
associated with rickets? The appearance of DD in early described in infants [19, 23, 24]. It may be particularly
infancy will vary with many factors, including age at difficult to distinguish rib fractures from Looser zones in
presentation, prenatal maternal DD, nutritional history, infants on radiographs alone. Timing of fractures in children
geographic location, sun exposure, skin color, and season. with rickets is not possible since published parameters
Past case reports of congenital rickets range from normal- assume normal underlying bone. The only assumption that
appearing bones to diffuse bone rarefaction, fractures at can be made of fractures in an infant with DD is that the
birth, and metaphyseal fraying and cupping [13–18]. The healing will be delayed.

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It is also important to remember when searching for have shown that adults with osteoporosis have 30–40%
radiographic evidence of vitamin deficiencies that multiple bone mineral loss before it becomes evident on radio-
deficiencies are the rule and may modify the radiographic graphs. Unfortunately, the value of DXA bone density
appearance of the skeletal response. In addition, the studies at this age may be limited. Bishop and Plotkin [25]
appearance of rickets will be altered by factors such as studied the bone mineral density of the lumbar spine by
seasonal and dietary changes that cause waxing and waning DXA in infants with fractures due to osteogenesis imper-
of the deficiency [23]. fecta and in infants with fractures thought to be non-
Radiographs alone may not give us enough information accidental, and found both groups within the reference
about the bone health in these infants. Prior studies on the range and not significantly different until after 6 months of
accuracy of radiographs in determining bone mineralization age. However, differences in bone mineral density have
a b
c d
Right Left
Fig. 1 Case 1, a 2-month-old Caucasian girl. a Axial CT images fracture of the tenth rib vs. pseudofracture (Looser zone, small black
(bone algorithm) demonstrate diastatic-appearing coronal and sagittal arrows). c AP views of the forearms demonstrate transverse lucency
sutures with poorly defined margins (arrows). Brain CT scan showed with sclerotic borders of the right distal radial metadiaphysis and
no intracranial abnormality, and there were no clinical findings for transverse sclerotic changes in the same location of the left distal
increased intracranial pressure, confirming the pseudodiastatic appear- radius (i.e. Looser zones-arrows). d AP views of the lower extremities
ance of craniotabes. b Chest radiographs. The lateral view shows a show mild irregular sclerotic changes of the tibial and fibular
flared appearance of the anterior rib ends (white outlined arrows) with metaphyses, distal more than proximal (arrows). The oblique fracture
a compression fracture of T8 that is confirmed on the AP and oblique of the right tibia was asymptomatic on presentation and was never
views (black outlined arrows). Also, notice the healing right posterior noted on multiple prior visits to the pediatrician

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been documented in young infants with osteogenesis right knee swelling. A metaphyseal fracture of the right
imperfecta using quantitative CT [26], which may be a distal femur was diagnosed by radiograph and a follow-up
more accurate modality in early infancy. Quantitative US skeletal survey was interpreted as up to 28 fractures highly
for bone strength may be a useful adjunct to CT to give us a specific for nonaccidental trauma. The mother’s vitamin D
better understanding of bone health [27]. level, checked in the summer, was <4 ng/ml. Two months
While MRI is unnecessary in detecting physeal widening after being changed to formula feeding, the infant’s vitamin
in older infants and children, in younger infants, when the D level, in the summer, was 17.8 ng/ml.
epiphyses are minimally, if at all, ossified, it is the best
modality for evaluating physeal abnormalities. MRI has Case 3 A 4-month-old Caucasian boy (Fig. 3) had left
already been used to describe rickets in older children [28], lower leg swelling after an accident at day care. Radio-
with the failure of ossification in the hypertrophic zone and graphs demonstrated a fracture and follow-up skeletal
persistence of cartilage into the metaphysis. The physeal surveys were interpreted as seven or eight fractures that
width of the distal femur showed little variability (0.9 to were nonspecific. The mother was found to have a vitamin D
1.9 mm) in a study of MRI in normal children, which level of 14 ng/ml and a PTH of 120 pg/ml (levels >72 pg/ml
correlates with a prior histologic study [29]. indicative of hyperparathyroidism). After 6 months of formula
feeding, the infant’s vitamin D level was 19.6 ng/ml, and the
alkaline phosphatase level was 2,386 U/l (normal range 145–
Case reports 320 U/l).
Case 1 A 2-month-old Caucasian girl (Fig. 1) was brought Case 4 A 2-month-old girl (Fig. 4) with an African-
to the pediatrician for an asymptomatic leg bump. A American mother and Caucasian father presented with a
healing oblique right tibial fracture was found on the viral respiratory illness. A chest radiograph demonstrated
radiograph. The skeletal survey was interpreted as 16 healing rib fractures. Skeletal survey was interpreted as six,
fractures suspicious for inflicted injury. The mother’s possibly eight, fractures highly specific for nonaccidental
vitamin D level was 8.7 ng/ml (insufficiency 20–30 ng/ml, trauma. The baby had skull and cervical spine fractures.
deficiency <20 ng/ml). The infant was not checked for DD. MRI demonstrated small old subdural hemorrhages. She
had no clinical or imaging findings to suggest increased
Case 2 A 2-month-old Caucasian girl (Fig. 2) was brought intracranial pressure. While on prenatal vitamins during her
to the pediatrician for her regular well-baby check and for second pregnancy, the mother’s vitamin D level was 17 ng/ml
a b c
Fig. 2 Case 2, a 2-month-old Caucasian girl. a AP skull radiographs. deformity (arrow). c AP views of the lower extremities show mild
On presentation the sagittal suture appears widened (top image, fibular bowing deformities with a metaphyseal fracture of the right
arrow) but this has resolved after 5 months of formula feeding (bottom distal femoral metaphysis (white arrow) and left proximal tibia (white
image, arrow). Brain CT and MRI showed no intracranial abnormality outlined arrow). Metaphyseal irregularities of the right proximal and
and there were no clinical findings for increased intracranial pressure. distal tibia and fibula are also noted (thin black arrows). The left distal
b AP spine view shows asymmetric T8 vertebral body height tibia and fibula are partially obscured

5. Pediatr Radiol
a c
b
d
Fig. 3 Case 3, a 4-month-old Caucasian male. a Skull imaging. AP white arrows), which also show early cupping, while the distal radial
plain radiograph demonstrates a diastatic-appearing sagittal suture metaphyses are still well defined. The early metaphyseal changes in
with poorly defined margins (small arrow). Axial CT image (bone the wrist typically present in the ulna before the radius. c Lateral views
algorithm) demonstrates that the demineralization along the sagittal of the lower extremities show symmetric anterior bowing and
suture (large arrow) and not diastasis is causing this radiographic broadening of the tibiae consistent with the saber shin deformity. This
appearance (i.e. pseudodiastasis). Brain CT scan showed no intracra- bowing occurs before weight bearing begins, and is due to the traction
nial abnormality and there were no clinical signs of increased pressure. of the Achilles tendon on the calcaneus. d A rickets survey was
b AP views of the forearms demonstrate a transverse lucency through performed 8 months after the initial presentation, when it was
the distal radial diaphysis with surrounding sclerosis (thin black documented that the vitamin D level was 19.6 ng/ml and the alkaline
arrow). A lack of symptoms, angulation or displacement is important phosphatase level was 2,386 U/l (normal range 145–320 U/l). During
in differentiating fractures from Looser zones. There is a buckle these 6 months, the infant had been formula fed. The radial
fracture in the right distal radial metadiaphysis (white outlined arrow). metaphyses are deformed (arrows)
Note the indistinct appearance of the distal ulnar metaphyses (long
at the beginning of the winter. The infant was not checked for phers, family and friends. At this level of inflicted injury,
DD. Even her second child, born several months after the should there not be evidence of the battered infant
mother’s DD was documented, was not checked for DD. syndrome? Should infants with so many inflicted fractures
These were all term infants, with two born in the winter not be in severe pain or distress?
and two born in the summer (the African-American mother Recently published rickets data from Canada [30] reveal
and the Caucasian girl with a vitamin D level of 8.7 ng/ml a similar pattern to the above cases. Of the 104 infants with
delivered in the summer). They were born north of the 35° confirmed rickets, 94% under 1 year of age were breast-fed
latitude. There was no indication of suspected abuse in any without vitamin D supplementation (three were on formula,
of these infants prior to their first radiograph despite being but developed hypocalcemic seizures within the first
seen by physicians, nurses, home health visitors, lactation 3 weeks of life). No supplemented, breast-fed infant
consultants, day-care workers, audiologists, ultrasonogra- showed DD (Canadian recommendations are 400 IU/day).

6. Pediatr Radiol
a b
c
Fig. 4 Case 4, a 2-month-old Caucasian/African-American girl. a AP left demonstrates early fraying (thick arrow). These were all
views of the shoulders demonstrate symmetric irregular metaphyseal asymptomatic on presentation and historically. c AP view of the
mineralization along the lateral aspects that were asymptomatic (top knees demonstrate metaphyseal flaring and fragmentation that appear
arrows) and had resolved after a month of formula feeding without to represent classic metaphyseal lesions (top, arrows) although they
subperiosteal new bone formation or callus. b AP views of the wrists were asymptomatic and resolved without subperiosteal new bone
demonstrate the distal ulnar metaphyseal changes (thin arrows). While formation, callus, or remodeling after 16 days of formula feeding
the right distal radial metaphysis remains normal in appearance, the (bottom)
The number of cases reported per month from February to has been demonstrated that 18% of pregnant women have
May was double the cases reported per month from June to vitamin D levels less than 10 ng/ml. In the UK food
December. The clinical and radiographic findings in the products are not required to be fortified, including milk.
infants less than 1 year of age were skeletal deformities, Should we assume that these deliveries were not as
fractures, hypocalcemic seizures, delayed development and “uncomplicated” as reported, or should we consider the
failure to thrive. This is similar to the findings from the US possible effects of the normal trauma of delivery (even in
in a review of rickets cases from 1986 to 2003, although the uncomplicated cesarean sections) on infants born with
authors also reported three infants with rickets who were congenital rickets?
breast-fed with supplementation [31]. The current US In summary, in infants less than 6 months of age with
recommendation of 200 IU/day is a recent reduction from multiple asymptomatic metaphyseal lesions (particularly
the previous recommendation of 400 IU/day. along the medial aspect of the distal femurs and proximal
Early detection and treatment of DD is important as tibiae as well as in the distal tibiae and fibulae), pseudodia-
serious long-term effects are now being reported and stasis of the sutures, transverse lucencies through the
adequate vitamin D levels are important beyond bone and forearms and ribs, and compression fractures of the spine
dental health. DD has been linked to increased rates of type should alert the radiologist to the possibility of osteomala-
I diabetes (with a recent study suggesting a level relation- cia with early metaphyseal changes, insufficiency fractures
ship), schizophrenia, depression, autoimmune diseases, and Looser zones. Clinical correlation is important, as most
cancer, and asthma. In fact, nearly every tissue in the body of these lesions are asymptomatic both at presentation and
has been found to have vitamin D receptors [3]. It is clear historically. With documentation of DD, 2 week follow-up
we are only beginning to understand what vitamin D does, radiographs may identify metaphyseal lesions that are
and more importantly, what its deficiency implies. resolving at an accelerated rate without interval subperios-
Regarding the issue of classic metaphyseal lesions teal new bone, callus or remodeling. While concomitant
occurring in infants following uncomplicated cesarean nonaccidental injury should never be excluded from the
section, these cases were diagnosed in the UK, where it differential, it goes without saying that the suspicion or

7. Pediatr Radiol
presence of abuse should not preclude the diagnosis and 13. Kefah AS, Saleh AA, Abbas AA et al (2001) Congenital rickets
secondary to untreated maternal renal failure. J Perinatol 21:473–
treatment of DD. With subclinical DD being reported at such
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high prevalences, the radiologists’ attention to these meta- 14. Moncrieff M, Fadahunsi TO (1974) Congenital rickets due to
bolic changes on radiographs will provide valuable input to maternal vitamin D deficiency. Arch Dis Child 49:810–811
help promote improvement in the vitamin D status of 15. Zeidan S, Bamford M (1984) Congenital rickets with maternal
pre-eclampsia. J R Soc Med 77:426–427
pregnant women and their newborn infants.
16. Kirk J (1982) Congenital rickets: a case report. Aust Paediatr J
18:291–293
17. Mohapatra A, Sankaranarayanan K, Kadam SS et al (2003)
Congenital rickets. J Trop Pediatr 49:126–127
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