Pediatr Radio! (1997) 27: 106-110© Springer-Verlag 1997

Stephen Chapman Non-accidental injury or brittle bones

Christine M. Hall

Received: 18 June 1996Accepted: 8 November 1996

S. Chapman (®)The Birmingham Children's Hospital NHSTrust, Ladywood Middleway,Birmingham B16 8ET, UK

C. M. HallThe Hospital for Sick Children NHS Trust,Great Ormond Street, LondonWC1N 3JH, UK

Abstract When a child presentswith one or more unexplained frac-tures, non-accidental injury (NAI)should be considered in the differ-ential diagnosis. This article reviewssome of the other differential diag-noses, particularly osteogenesis im-perfecta and the alleged "temporarybrittle bone disease".

Introduction

When faced with an infant who may have one or morefractures, the radiologist must help his clinical colleagueto decide:

1.If there truly is an injury and not one of the many de-velopmental variants which are so common in chil-dren [1].

2.Whether the explanation is appropriate for the injurysustained, i.e., an accident.

3.Whether the explanation is inappropriate in terms ofmechanism, force or dating of the injury, i.e., theremust be a suspicion of NAI or fragile bones.

4. If there is evidence of an underlying skeletal abnor-mality which has predisposed to the fracture, i.e.,there are fragile bones.

The majority of older children will have fractures whichare the result of accidents. Certain fractures in infancyare strongly suggestive of NAI, e.g., hand fractures inthe non-ambulant child, acromial fractures, fractures ofthe outer end of the clavicle, and spinal, posterior riband metaphyseal fractures. In the vast majority of casesthe clinical findings, family history and radiological ap-pearances will differentiate between NAI, accidental

trauma and fractures resulting from inappropriate trau-ma because of fragile bones. In a minority there will bea totally inexplicable fracture or fractures where abusewould appear to be unlikely. Much has been written onthe type and severity of accidental trauma necessary toproduce different injuries at different ages, and this in-formation will not be reiterated here. This article will re-view some of the more frequently asked questionsregarding the possibility of unduly fragile bones, re-membering, of course, that children with medical condi-tions can be and have been abused and this includeschildren with osteogenesis imperfecta [2]. Indeed, a na-tionwide survey of child abuse in Japan revealed that10 % of victims were from multiple births and that abuseof one twin was associated with that child's medicalproblems or non-home care [3]. Comparisons of theabused twin with the non-abused twin, and examinationof the abuser's attitude to the victim suggested thatmedical and non-medical factors encouraged favourit-ism. A review of the wider issues involved in the abuseof disabled children is provided by Westcott [4].

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Are the fractures due to osteogenesis imperlecta?

Osteogenesis imperfecta (01) is an inherited disorder ofconnective tissue resulting from abnormal quantity and/or quality of type I collagen, the major protein of bone[5, 6]. The phenotypic presentation is enormously var-ied, ranging from perinatal death to normal life spancomplicated by only a few fractures [7]. Because frac-tures are a feature of the condition it must be given seri-ous consideration in any child with unexplainedfractures. There are four major types in the Sillence clas-sification [6] but it should be noted that there are nostrict boundaries:

I This is the most common form of the disorder. Os-seous fragility is associated with blue sclerae and a posi-tive family history, although new mutations do occur. Itshould be easy to diagnose.

II This form is lethal in the fetal or perinatal periodand does not warrant consideration in this clinical set-ting. As well as fractures the skeleton is grossly abnor-mal.

III This is a progressively deforming type of 01 and,again, should not cause confusion with the "normal"child with fractures. Fractures at birth are common.

IV This is a rare type of 01. It is a heterogeneousgroup with mild to severe bone disease, nearly alwayswith a positive family history, but because of white scle-rae may be considered in the child with unexplainedfractures.

Although many regard 01 type IV as rare (only 5 %of the patients in the Sillence study) one group of au-thors in particular has suggested a higher prevalence[8], including those with normal teeth, type IVA [9].The study of 78 patients with 01 subtype IV A [9] has,however, been criticised by others [10, 11], who haveraised the possibility that the population includes indi-viduals with NAI mistakenly diagnosed as 01. Criti-cisms of the paper include the facts that the featureswere evaluated via questionnaires, radiographs wereavailable for review in only 17 patients and only 12 skullradiographs were examined. Only 9 % of the skull ra-diographs had a significant number of wormian bones(as defined by Cremin et al. [12] ). There was a high inci-dence of skull and metaphyseal fractures, which is atvariance with other published data on the radiologicalfeatures of 01. Joint laxity in family members has beenused to support the contention that a collagen disorderis present in a child [13], but in Paterson et al.'s 1987 pa-per [9] even in the control group 7 % of children had dis-located joints and 6 % were `double-jointed' suggestingthat these signs are over-interpreted.

New genetic mutations for Ol have been docu-mented, so is it possible for a child to have a new muta-tion for type IV 01, i.e., have no relevant familyhistory and no other signs of 01 such as osteoporosisand multiple wormian bones in the skull? Taitz [14]

showed that the incidence of type IV OI with fracturesunder 1 year of age, with no family history and other-wise normal radiological findings, including no wormianbones, and normal teeth is between 1 in 1 million and 1in 3 million. Thus, in a city of 500 000 people with 6000births per annum the incidence would be one case every100-300 years. The number of NAI cases with fractureswould be expected to be 15 per year. Metaphyseal frac-tures do occur in Ol, but only in the presence of obviousbone disease with radiologically abnormal bones [15].

Collagen abnormalities can be found after skin fibro-blast culture in approximately 85 % of patients with Ol[16, 17]. There have been no studies on normal subjects,but Byers has studied hundreds of family members of af-fected individuals. Only the affected individuals andfamily members who are mosaic have biochemical ab-normalities [16]. The true prevalence of biochemicalcollagen abnormalities in the paediatric age group isnot known, and until this information is available the re-sults of skin fibroblast culture can only be one piece ofthe jigsaw. Furthermore, the abnormalities detected inskin fibroblasts may have nothing to do with alterationsin bone and increased bone fragility. Recent courtjudgements in the UK have upheld the diagnosis ofNAI, even in the presence of abnormal collagen, whenthe radiological evidence has been strongly in favour ofabuse. So which children should undergo skin biopsyand fibroblast culture? Three difficult situations inwhich it may be appropriate are (a) when the fracturesite is consistent with the history but the force involvedin the injury seems too minor to have caused the frac-ture; (b) when fractures recur in a protected environ-ment; and (c) when there are no external signs ofabuse. Fibroblast culture takes at least 3 months, and itis important that the child is protected during this pe-riod. This test is currently not provided as a routine ser-vice in the UK.

There are reports of cases of 01 initially misdiag-nosed as NAI [18-20]. However, these cases have exhib-ited either clinical and/or radiological abnormalitiessuggestive of 01 or a missed positive family historywhich should have enabled the correct diagnosis tohave been made. Other reports have failed to providefull and detailed clinical and radiological descriptions,preventing others from making an independent judge-ment on the correctness of the authors' opinions [13,21, 22]. Gahagan and Rimsza described three patientswhere skin fibroblast culture was claimed to alter the di-agnosis from NAI to 01 [23]. However, one of these pa-tients had blue sclerae, one was investigated formultiple fractures at the age of 9 years (an unusuallylate age for fractures due to NAI) and one had a positivefamily history for 01. In this last case there was still con-cern that abuse coexisted with 01. Thus, the sporadiccase reports do not provide significant evidence for theview that there is a large group of infants with clinically

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and radiologically occult bone fragility. The differentia-tion of child abuse from OI has been the subject of re-cent reviews [11, 24, 25].

Are the fractures due to copper deficiency?

Abused infants will cease to sustain fractures when re-moved from a dangerous environment to a place of safe-ty. It may be suggested that the child was, during theperiod in which fractures were sustained, sufferingfrom a condition in which the bones were temporarilyprone to fracture. Copper deficiency, a rare conditionwhich may, even less commonly, be complicated by frac-tures, has been invoked as an explanation for "tempo-rary brittle bones" [26, 27]. From our knowledge of thesmall number of cases of copper deficiency which havebeen complicated by fractures (approximately 20 in theworld literature) we can conclude that it is unlikely:

1.In a full-term infant less than 6 months of age who hasbeen breast-fed or has received a modern infant for-mula of the sort commonly available in the UK, be-cause the body's stores of copper are high and themilks contain sufficient copper

2. In a preterm infant less than 2.5 months of age, be-cause fetal copper stores are sufficient for this lengthof time

3. In a term infant with rib fractures or any child with askull fracture, because this clinical setting has not yetbeen reported

4. In the absence of one of the predisposing factors (pro-longed total parenteral nutrition, feeding with copper-deficient milk including ordinary cows' milk, malnu-trition and malabsorption) which have been presentin all of the previously reported cases

5. In the absence of anaemia and neutropenia, which areclinical features of copper deficiency

6.Without other radiological abnormalities (osteoporo-sis, abnormal metaphyses and retarded bone age)

7.When recovery occurs without a change of diet ortreatment with copper supplementation

8.With normal plasma copper and caeruloplasminlevels

Fractures have never been reported as a late sequelaof proven copper deficiency. The Lord Chief Justice ofEngland and Wales has rejected the argument that cop-per deficiency may be an important cause of unex-plained fractures [28].

Are the fractures due to "temporary brittle bonedisease"?

Paterson et al. recently described 39 children, over a 10-year period, with fractures only in the first year of life[29-31]. In the majority of cases the diagnoses weremade retrospectively. The authors speculated that thedisorder reflects a temporary collagen defect due totransient copper deficiency or another metalloenzymedeficiency, but this remains unproved [32, 33]. The fea-tures of this condition can be itemised as follows, andwe have added, in italics, the similarity with NAI and/or normal infants:

— Fractures in the first year of life. This is the peak agefor fractures due to NAI.

— A preponderance of rib and metaphyseal fractures.As in NAI.

— Fractures found "by accident" when radiographs aretaken. There is a discrepancy between the radiologicalevidence of injury and the superficial evidence oftrauma. This is typical of rib and metaphyseal injuriesin NAI. There is the assumption that in the absence ofbruising the injuries must have occurred with minimalforce, implying the presence of brittle bones.

— Periosteal reactions without fractures are commonand sometimes almost symmetrical. Shopfner de-scribed symmetrical physiological periosteal reactionsin the first 6 months of life in 30 % of children [34].

— Fractures occurring in hospital. It is well recognisedthat fractures may first become evident in hospital asthe callus develops, and this applies particularly to pos-terior rib fractures [35]. Caretakers may also abusechildren while they are in hospital.

— Delay in bone age. This is notoriously difficult to as-sess in the first year of life.

— Osteopenia in 30 %. Again difficult to assess radiolog-ically, and there are no radiologists as authors on thePaterson et al. paper.

— Expanded costochondral junctions. A frequent nor-mal finding in infancy, and fractures at this site arealso well-described.

— Metaphyseal abnormalities which resemble fractures.There is no proof that they are not fractures, and theillustrations are certainly consistent with fractures.Kleinman et al. have conclusively shown that these ra-diological abnormalities are fractures [36].

— A high incidence of vomiting and diarrhoea. Theseare common, and some may say normal, events in in-fancy; in this group of patients the severity is not quan-tified, or related to failure to thrive. Furthermore, thesesymptoms are not only non-specific but may also bepresenting symptoms in NAI.

— Apnoeic attacks in 32 % of cases. No information isgiven as to whether subdural haemorrhages were ex-cluded.

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— Hepatomegaly. Not quantified, and a palpable liver isa recognised normal feature in infancy.

— Anaemia. A physiological anaemia in this age group iswell recognised and may be exacerbated in childrenwith multiple fractures.

— Neutropenia < 2.0 x 10 9/1 in 26 % of cases.— Other risk factors were prematurity, multiple preg-

nancy (both of which are also risk factors for NAI)and bottle-feeding as opposed to breast-feeding.

This hypothetical condition, as described, bears a strik-ing similarity to many cases of NAI. It could be arguedthat if the parents offer an inappropriate explanationfor the injuries or, indeed, if there is no explanation,then the currently prevailing opinion is that the childshould be considered as suffering from abuse. If, on theother hand, the caretakers are believed, then theremust be a medical diagnosis and "temporary brittlebone disease" becomes an acceptable label even thoughthere is no proof of its existence. It is suggested thatNAI and "temporary brittle bone disease" are indeedthe same condition but with different labels dependingon the credibility of the caretaker's explanation. Paedi-atric radiologists have correctly described the radiologi-cal features of a condition and called it NAI, but if theyhad more readily accepted the histories offered by thecaretakers then they would have called it "temporarybrittle bone disease"!

If there are further attempts to define this conditionit is important that solid medical evidence is used. It isunfortunate that cases which have been debated in thecourts by medical experts of differing opinions andwhich the courts have found to be proven NAI may beincluded as further cases of "temporary brittle bone dis-ease" [37].

Other, rarer causes of fractures in infancy

There are other rare causes of bone fragility in infancy.They all have recognisable clinical, genetic and/or radio-logical manifestations which facilitate their diagnosisand they should not be confused with the "normal" in-fant with a fracture.

The role of expert witnesses

Both in care proceedings, where the welfare of the childis at issue, and in criminal cases experts are supposed tobe even-handed in their approach. They are in a privi-leged position in being able to provide opinion as wellas the facts as known to them. A number of judgementsin the British courts have sought to clarify the role of ex-perts and to indicate what is acceptable opinion andwhat is untried hypothesis [38]. Experts should (a) pro-

vide a straightforward, not a misleading opinion; (b) beobjective and not omit factors which do not supporttheir opinion; and (c) have researched the case thor-oughly [39]. In his guidelines, Mr Justice Cazalet alsostated that

[If] contrary to the appropriate practice an expert does provide areport which is other than wholly objective — that is one whichseeks to "promote" a particular case — the report must make thisclear. However, such an approach should be avoided because, inmy view, it would: (a) be an abuse of the expert's proper functionand privilege; and (b) render the report an argument, and not anopinion [39].

Experts must not put forward untested or unacceptableviews, and must be prepared to cast aside ideas of loy-alty to one party or another and give evidence with thechild's welfare as the primary aim [40]. Conclusionsmust be reached after considering all the available evi-dence, not just those aspects which support a particularview. In 1995 Wall J emphasised these points: "If themedical evidence points overwhelmingly to NAI, anyexpert who advises the parents and the court that the in-jury has an alternative and innocent causation has aheavy duty to ensure that he has considered carefullyall the available material and is, moreover, expressingan opinion which can be objectively justified" [37]. Thisjudgement followed the case of a child with multiplefractures and brain injury where "temporary brittlebone disease" was offered as an explanation for the frac-tures but the brain injury was not held to be a significantfactor in reaching that diagnosis. The expert who ad-vances a hypothesis to explain the facts must also placebefore the court any material that contradicts the expla-nation [41].

Conclusion

Overdiagnosis of child abuse is a tragedy for the childwho may be taken away from his parents and for thefamily faced with loss of a family member and the ac-companying social stigma, but an incorrect diagnosis ofosteogenesis imperfecta or other brittle bone diseasemay put the child's life at risk. An incorrect diagnosisof a brittle bone disorder reinforces the parents' beliefthat there is an underlying medical condition and leadsto false views and hopes. This may hamper or even pre-clude working in a supportive environment to enableeventual rehabilitation with the child. Osteogenesis im-perfecta is an uncommon disease, and "temporary brit-tle bone disease" is no more than a hypothesis; sadly,child abuse is all too common and an individual is atgreater risk of being murdered in the first year of lifethan at any other age.

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