Pediatr RadiolDOI 10.1007/s00247-008-1001-z COMMENTARYRickets vs. abuse: a national and international epidemicKathy A. Kel...
Pediatr Radiolvitamin D. At present, milk is the only product required to      best location to search for radiographic ev...
Pediatr Radiol   It is also important to remember when searching for                    have shown that adults with osteop...
Pediatr Radiolbeen documented in young infants with osteogenesis                         right knee swelling. A metaphysea...
Pediatr Radiol a                                                                          c b                             ...
Pediatr Radiol a                                                                                    b                     ...
Pediatr Radiolpresence of abuse should not preclude the diagnosis and                  13. Kefah AS, Saleh AA, Abbas AA et...
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Rickets Abuse Kathy Keller


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Rickets Abuse Kathy Keller

  1. 1. Pediatr RadiolDOI 10.1007/s00247-008-1001-z COMMENTARYRickets vs. abuse: a national and international epidemicKathy A. Keller & Patrick D. BarnesReceived: 4 November 2007 / Revised: 28 July 2008 / Accepted: 18 August 2008# Springer-Verlag 2008Keywords Rickets . Child abuse . Metabolic bone disease . women 18 to 29 years of age in Boston. A recent study ofNonaccidental 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 incaesarean section?” [1] suggested that enough trauma could Childhood including an international perspective of motheroccur 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] lessHowever, 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 toaffect 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 lesschildren, and infants of all races. In a review article on than 50 nmol/l (20 ng/ml). Levels between 20 and 30 ng/mlvitamin 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 decreasingliterature, showing deficiency and insufficiency rates of calcium absorption [3]. With such high prevalence of DD52% among Hispanic and African-American adolescents in in our healthy young women, congenital deficiency isBoston, 48% among white preadolescent females in Maine, inevitable, since neonatal 25(OH)D concentrations are42% 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 DEditor’s note: See related articles in this issue: Slovis TL, Chapman S levels, found deficient or insufficient levels in 83% of blackdoi:10.1007/s00247-008-0997-4; Chesney RW doi:10.1007/s00247- women and 92% of their newborns, as well as in 47% of008-0993-8; 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% ofK. A. Keller these women were on prenatal vitamins. Research isPediatric 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 (, ID: R01 HD043921).Department of Radiology, Lucile Packard Children’s Hospital, The obvious question is, “Why has DD once again725 Welch Road,Palo Alto, CA 94304, USA become so common?” Multiple events have led to the highe-mail: rates of DD. In the past, many foods were fortified with
  2. 2. Pediatr Radiolvitamin D. At present, milk is the only product required to best location to search for radiographic evidence of congenitalbe fortified in the US, although studies have shown that up rickets and nutritional rickets in infants less than 3 monthsto 70% of sampled milk does not contain the required of age is in the cranium [19]. The skull, as a reflection ofamount of vitamin D. There are few other natural food rapid brain growth in early life, is the most affected bone atsources of vitamin D. While exposure to the sun’s UVB this age. Softening of the skull (craniotabes), especially inrays remains the best natural source of vitamin D, during the occipital region with palpable enlargement of the suturesthe winter months, above the 35° latitude (at the level of and fontanelles, was a common clinical finding withAtlanta, Georgia) there is a loss of UVB rays that are congenital rickets in the past, and is once again beingnecessary 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 definedhas been a significant increase in the use of sunscreen and margins on radiographs (pseudodiastasis). The skull is betterprotective clothing. A sun protection factor of 8 blocks evaluated on the head CT scan, which should be done toabout 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 makecertain Islamic women, who, even in the sunny climate of the teeth and petrous bones appear relatively dense onthe 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 atstorage 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 usuallystatus of neonates born to obese mothers was found to be symmetric, and will occur first in the fastest-growing longpoorer than the vitamin D status of neonates born to lean bones (the femurs, tibiae and fibulae). The metaphysealmothers [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 metaphysealincrease in the frequency and the duration of breast-feeding, changes in the distal ulnar can be found even when theboth of which are risk factors for infant nutritional DD. In distal radial metaphyses appear normal [23]. While the2003, the American Academy of Pediatrics published physeal and metaphyseal changes can be subtle in earlyguidelines recommending that all breast-fed infants receive infancy, with treatment, the metaphyses may become100% of their daily vitamin D requirement from supple- increasingly sclerotic and deformed [23]. While these earlymentation. 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 resolvemust feed her infant 8 l (about 89 three-ounce bottles) of without the interval stages of fracture healing (subperiostealbreast milk per day to provide the recommended daily new bone formation, callous, and remodeling) within a fewvitamin D intake of 200 IU [9]. Even infants born to weeks. When subperiosteal changes are present, particularlymothers who are replete with vitamin D demonstrate in the tibiae, a lateral view may reveal early bowingdecreasing 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, theystudy 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 thewith severe DD common in the winter. Recent literature Achilles tendon on the calcaneus causes the tibiae to bowsuggests 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 beof 400 IU per day) is required to provide both the mother subtle on radiographs in the acute stage at this age, but mayand 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 longnutritional rickets in infants younger than 6 months old, the bone diaphyses, insufficiency fractures and Looser zonesage at which we typically first see the fraying and cupping (i.e. pseudofractures) of the ribs and forearms have all beenassociated with rickets? The appearance of DD in early described in infants [19, 23, 24]. It may be particularlyinfancy will vary with many factors, including age at difficult to distinguish rib fractures from Looser zones inpresentation, prenatal maternal DD, nutritional history, infants on radiographs alone. Timing of fractures in childrengeographic location, sun exposure, skin color, and season. with rickets is not possible since published parametersPast case reports of congenital rickets range from normal- assume normal underlying bone. The only assumption thatappearing bones to diffuse bone rarefaction, fractures at can be made of fractures in an infant with DD is that thebirth, and metaphyseal fraying and cupping [13–18]. The healing will be delayed.
  3. 3. Pediatr Radiol 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 densityappearance 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 byseasonal 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 referenceabout the bone health in these infants. Prior studies on the range and not significantly different until after 6 months ofaccuracy of radiographs in determining bone mineralization age. However, differences in bone mineral density have a b c d Right LeftFig. 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 lucencysutures with poorly defined margins (arrows). Brain CT scan showed with sclerotic borders of the right distal radial metadiaphysis andno intracranial abnormality, and there were no clinical findings for transverse sclerotic changes in the same location of the left distalincreased intracranial pressure, confirming the pseudodiastatic appear- radius (i.e. Looser zones-arrows). d AP views of the lower extremitiesance of craniotabes. b Chest radiographs. The lateral view shows a show mild irregular sclerotic changes of the tibial and fibularflared appearance of the anterior rib ends (white outlined arrows) with metaphyses, distal more than proximal (arrows). The oblique fracturea compression fracture of T8 that is confirmed on the AP and oblique of the right tibia was asymptomatic on presentation and was neverviews (black outlined arrows). Also, notice the healing right posterior noted on multiple prior visits to the pediatrician
  4. 4. Pediatr Radiolbeen documented in young infants with osteogenesis right knee swelling. A metaphyseal fracture of the rightimperfecta using quantitative CT [26], which may be a distal femur was diagnosed by radiograph and a follow-upmore accurate modality in early infancy. Quantitative US skeletal survey was interpreted as up to 28 fractures highlyfor bone strength may be a useful adjunct to CT to give us a specific for nonaccidental trauma. The mother’s vitamin Dbetter 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 vitaminin 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 bestmodality for evaluating physeal abnormalities. MRI has Case 3 A 4-month-old Caucasian boy (Fig. 3) had leftalready 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 skeletalpersistence of cartilage into the metaphysis. The physeal surveys were interpreted as seven or eight fractures thatwidth of the distal femur showed little variability (0.9 to were nonspecific. The mother was found to have a vitamin D1.9 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/mlcorrelates 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 ahealing oblique right tibial fracture was found on the viral respiratory illness. A chest radiograph demonstratedradiograph. 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 nonaccidentalvitamin 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 increasedCase 2 A 2-month-old Caucasian girl (Fig. 2) was brought intracranial pressure. While on prenatal vitamins during herto the pediatrician for her regular well-baby check and for second pregnancy, the mother’s vitamin D level was 17 ng/ml a b cFig. 2 Case 2, a 2-month-old Caucasian girl. a AP skull radiographs. deformity (arrow). c AP views of the lower extremities show mildOn presentation the sagittal suture appears widened (top image, fibular bowing deformities with a metaphyseal fracture of the rightarrow) but this has resolved after 5 months of formula feeding (bottom distal femoral metaphysis (white arrow) and left proximal tibia (whiteimage, arrow). Brain CT and MRI showed no intracranial abnormality outlined arrow). Metaphyseal irregularities of the right proximal andand there were no clinical findings for increased intracranial pressure. distal tibia and fibula are also noted (thin black arrows). The left distalb AP spine view shows asymmetric T8 vertebral body height tibia and fibula are partially obscured
  5. 5. Pediatr Radiol a c b dFig. 3 Case 3, a 4-month-old Caucasian male. a Skull imaging. AP white arrows), which also show early cupping, while the distal radialplain radiograph demonstrates a diastatic-appearing sagittal suture metaphyses are still well defined. The early metaphyseal changes inwith poorly defined margins (small arrow). Axial CT image (bone the wrist typically present in the ulna before the radius. c Lateral viewsalgorithm) demonstrates that the demineralization along the sagittal of the lower extremities show symmetric anterior bowing andsuture (large arrow) and not diastasis is causing this radiographic broadening of the tibiae consistent with the saber shin deformity. Thisappearance (i.e. pseudodiastasis). Brain CT scan showed no intracra- bowing occurs before weight bearing begins, and is due to the tractionnial abnormality and there were no clinical signs of increased pressure. of the Achilles tendon on the calcaneus. d A rickets survey wasb AP views of the forearms demonstrate a transverse lucency through performed 8 months after the initial presentation, when it wasthe distal radial diaphysis with surrounding sclerosis (thin black documented that the vitamin D level was 19.6 ng/ml and the alkalinearrow). A lack of symptoms, angulation or displacement is important phosphatase level was 2,386 U/l (normal range 145–320 U/l). Duringin differentiating fractures from Looser zones. There is a buckle these 6 months, the infant had been formula fed. The radialfracture in the right distal radial metadiaphysis (white outlined arrow). metaphyses are deformed (arrows)Note the indistinct appearance of the distal ulnar metaphyses (longat 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 infantmother’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] revealand the Caucasian girl with a vitamin D level of 8.7 ng/ml a similar pattern to the above cases. Of the 104 infants withdelivered in the summer). They were born north of the 35° confirmed rickets, 94% under 1 year of age were breast-fedlatitude. 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 firstseen by physicians, nurses, home health visitors, lactation 3 weeks of life). No supplemented, breast-fed infantconsultants, day-care workers, audiologists, ultrasonogra- showed DD (Canadian recommendations are 400 IU/day).
  6. 6. Pediatr Radiol a b cFig. 4 Case 4, a 2-month-old Caucasian/African-American girl. a AP left demonstrates early fraying (thick arrow). These were allviews of the shoulders demonstrate symmetric irregular metaphyseal asymptomatic on presentation and historically. c AP view of themineralization along the lateral aspects that were asymptomatic (top knees demonstrate metaphyseal flaring and fragmentation that appeararrows) and had resolved after a month of formula feeding without to represent classic metaphyseal lesions (top, arrows) although theysubperiosteal new bone formation or callus. b AP views of the wrists were asymptomatic and resolved without subperiosteal new bonedemonstrate the distal ulnar metaphyseal changes (thin arrows). While formation, callus, or remodeling after 16 days of formula feedingthe 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 haveMay was double the cases reported per month from June to vitamin D levels less than 10 ng/ml. In the UK foodDecember. 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 asfractures, hypocalcemic seizures, delayed development and “uncomplicated” as reported, or should we consider thefailure to thrive. This is similar to the findings from the US possible effects of the normal trauma of delivery (even inin a review of rickets cases from 1986 to 2003, although the uncomplicated cesarean sections) on infants born withauthors 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 withrecommendation of 200 IU/day is a recent reduction from multiple asymptomatic metaphyseal lesions (particularlythe 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 theadequate vitamin D levels are important beyond bone and forearms and ribs, and compression fractures of the spinedental 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 fracturesship), schizophrenia, depression, autoimmune diseases, and Looser zones. Clinical correlation is important, as mostcancer, and asthma. In fact, nearly every tissue in the body of these lesions are asymptomatic both at presentation andhas been found to have vitamin D receptors [3]. It is clear historically. With documentation of DD, 2 week follow-upwe are only beginning to understand what vitamin D does, radiographs may identify metaphyseal lesions that areand 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 concomitantoccurring in infants following uncomplicated cesarean nonaccidental injury should never be excluded from thesection, these cases were diagnosed in the UK, where it differential, it goes without saying that the suspicion or
  7. 7. Pediatr Radiolpresence 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 475high prevalences, the radiologists’ attention to these meta- 14. Moncrieff M, Fadahunsi TO (1974) Congenital rickets due tobolic changes on radiographs will provide valuable input to maternal vitamin D deficiency. Arch Dis Child 49:810–811help promote improvement in the vitamin D status of 15. Zeidan S, Bamford M (1984) Congenital rickets with maternal pre-eclampsia. J R Soc Med 77:426–427pregnant 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 49:126–127References 18. Ford JA, Davidson DC, McIntosh WB et al (1973) Neonatal rickets in Asian immigrant population. Br Med J 3:211–212 1. O’Connell A, Donoghue V (2007) Can classic metaphyseal 19. Resnick D (1996) Bone and joint imaging, 2nd edn. Saunders, lesions follow uncomplicated caesarean section? Pediatr Radiol Philadelphia, pp 511–524 37:488–491 20. Yorifuji J, Yorifuji T, Tachibana K et al (2008) Craniotabes in 2. Kleinman PK, Marks SC, Blackbourne B (1986) The metaphyseal normal newborns: the earliest sign of subclinical vitamin D lesion in abused infants: radiologic-histopathologic study. AJR deficiency. J Clin Endocrinol Metab 93:1784–1788 146:895–905 21. Swischuk LE, Hayden CK (1977) Seizures and demineralization 3. Holick MF (2007) Vitamin D deficiency. N Engl J Med 357:266–281 of the skull. A diagnostic presentation of rickets. Pediatr Radiol 4. Gordon CM, Feldman HA, Sinclair L et al (2008) Prevalence of 6:65–67 vitamin D deficiency among healthy infants and toddlers. Arch 22. Tatcher TD, Fischer PR, Pettifor JM et al (2000) Radiographic Pediatr Adolesc Med 162:505–512 scoring method for the assessment of the severity of nutritional 5. Dawodu A, Wagner CL (2007) Mother-child vitamin D deficiency: rickets. J Trop Pediatr 46:132–139 an international perspective. Arch Dis Child 92:737–740 23. Silverman FS, Kuhn JP (1993) Caffey’s pediatric x-ray diagnosis, 6. Hillman LS, Haddad JG (1974) Human perinatal vitamin D 9th edn. Mosby, St. Louis, pp 1746–1751 metabolism. I. 25-Hydroxyvitamin D in maternal and cord blood. 24. Kirks DR (1998) Practical pediatric imaging, 3rd edn. Lippincott- J Pediatr 84:742–749 Raven, Philadelphia, pp 447–453 7. Bodnar LM, Simhan HN, Powers RW et al (2007) High 25. Bishop NJ, Plotkin H (1998) When is a fracture child abuse? Bone prevalence of vitamin D insufficiency in black and white pregnant 23:S458 women residing in the northern United States and their neonates. J 26. Miller ME, Hangartner TN (1999) Bone density measurements by Nutr 137:447–452 computed tomography in osteogenesis imperfect-type I. Osteoporos 8. Bodnar LM, Catov JM, Roberts JM et al (2007) Prepregnancy Int 9:427–432 obesity predicts poor vitamin D status in mothers and their 27. Xiang-peng L, Wei-Li Z, Jiamin H et al (2005) Bone measure- neonates. J Nutr 137:2437–2442 ments of infants in the first 3 months of life by quantitative 9. Gartner LM, Greer FR (2003) Prevention of rickets and vitamin D ultrasound: the influence of gestational age, season, and postnatal deficiency: new guidelines for vitamin D intake. Pediatrics age. Pediatr Radiol 35:847–853 111:908–910 28. Ecklund K, Doria AS, Jaramillo D (1999) Rickets on MR images.10. Hoogenboezam T, Degenhart JH, de Muinck Keizer-schrama SM Pediatr Radiol 29:673–675 et al (1989) Vitamin D metabolism in breast-fed infants and their 29. Kemper NF, Sissons HA (1976) Quantitative histology of the mothers. Pediatr Res 25:623–628 human growth plate. J Bone Joint Surg Br 58:426–43511. Ziegler EE, Hollis BW, Nelson SE et al (2006) Vitamin D 30. Ward LM, Gaboury I, Ladhani M et al (2007) Vitamin D deficiency in breastfed infants in Iowa. Pediatrics 118:603–610 deficiency rickets among children in Canada. CMAJ 177:161–12. Hollis BW, Wagner CL (2004) Vitamin D requirements during 166 lactation: high-dose maternal supplementation as therapy to 31. Weisberg P, Kelley SS, Ruowei L et al (2003) Nutritional rickets prevent hypovitaminosis D in both mother and nursing infant. among children in the United States: review of cases reported Am J Clin Nutr 80:1752S–1758S between 1986 and 2003. Am J Clin Nutr 80:1697S–1705S