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Journal of Forensic and Legal Medicine 60 (2018) 9–14

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Journal of Forensic and Legal Medicine


journal homepage: www.elsevier.com/locate/yjflm

The detection of significant fractures in suspected infant abuse T


a,∗ b c
Emma Raynor , Praveen Konala , Anthony Freemont
a
University of Manchester, School of Medical Sciences, Stopford Building, Oxford Road, Manchester, M13 9PT, United Kingdom
b
Manchester Royal Infirmary, Oxford Road, Manchester, M13 9WL, United Kingdom
c
Manchester Molecular Pathology Innovation Centre, 3rd floor Citylabs, Nelson Street, Manchester, M13 9NQ, United Kingdom

A R T I C LE I N FO A B S T R A C T

Keywords: Objective: Skeletal survey is a commonly used means of detecting fractures in infants, and is used as a screen in
Child abuse suspected cases of physical abuse. It is recognised that in live infants, a repeat survey some days after a suspected
Infant episode of injury will detect more fractures than one taken shortly after the suspected injury, indicating that the
Rib fracture latter lacks sensitivity. In infants who die soon after a suspected episode of physical abuse, the managing
Histopathology
clinicians do not have the option of a second survey; however there is the opportunity for the microscopic
examination of bones removed at autopsy. Increasingly Osteoarticular Pathology at the Manchester University
NHS Foundation Trust (MFT) is being sent samples of bones from infants suspected of inflicted injury for his-
tological examination, both from bones with fractures detected at autopsy or skeletal survey and from posterior
ribs and long bone metaphyses (sites of significance in assessing for abusive injury) when there is no evidence of
fracture on skeletal survey or autopsy. Here we report the results of an audit of the anonymised data from a series
of such cases, to establish the sensitivity of skeletal survey (SS) to detect fractures and to define the medico-legal
value of submitting bones for histological examination.
Methods: This was an audit of skeletal injuries in 38 infants aged < 18 months presenting to MFT for specialist
histopathological evaluation of suspected non-accidental fractures between January 2011 and June 2017.
Histopathological examination was performed on all bones submitted and compared with contact radiography of
isolated bones and post-mortem skeletal surveys undertaken by specialist paediatric or musculoskeletal radi-
ologists for the presence of fracture.
Results: A total of 318 fractures were detected histologically; of these, 178 (56%) were of the ribs, 119 (37.5%)
were of major limb long bones, 10 (3%) were of the skull, and 11 (3.5%) were recorded as ‘other’. Excluding
refractures, skeletal survey detected 54% of the fractures recorded histologically. No fractures were detected
radiologically that were not seen histologically. Generally, for skeletal survey, detection rates improved with the
age of the lesion, and rib fractures were more difficult to detect than long bone fractures. Ribs 5–8 were the most
frequently fractured ribs, and metaphyses around the knee accounted for most metaphyseal limb long bone
fractures undetected by SS.
Conclusion: In infants coming to post-mortem, histopathology is more sensitive than SS for the detection of
clinically significant fractures. In children suspected of non-accidental injuries but with negative or equivocal SS,
sampling of the anterior and posterior end of ribs 5–8 and the bones around the knee for histological ex-
amination could reveal clinically unsuspected fractures and significant evidence of physical abuse. 71% of in-
fants showed evidence of old fractures typical of non-accidental injury.

1. Introduction second most common presentation of physical abuse, with classic me-
taphyseal lesion (CML) and posterior rib fractures being particularly
Since Caffey first established a relationship between unexplained specific.2–16 The consequence of overlooking such injuries could prove
subdural haematoma and long bone fractures in 1946,1 studies ex- fatal4,5; fractures indicative of inflicted injury that antedate death by
amining links between skeletal injury and physical abuse in infants days or weeks are, in our experience, often first recognised only after
have grown in number. Most of these are radiological. Fractures are the death.


Corresponding author.
E-mail addresses: emma.raynor@student.manchester.ac.uk (E. Raynor), Praveen.Konala@mft.nhs.uk (P. Konala),
tony.freemont@manchester.ac.uk (A. Freemont).

https://doi.org/10.1016/j.jflm.2018.09.002
Received 12 February 2018; Received in revised form 5 July 2018; Accepted 3 September 2018
Available online 05 September 2018
1752-928X/ © 2018 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/BY-NC-ND/4.0/).
E. Raynor et al. Journal of Forensic and Legal Medicine 60 (2018) 9–14

Imaging techniques are the mainstay of fracture recognition in live Histology is regarded as the most accurate means of demonstrating
and dead infants. The skeletal survey (SS) is the first-line investigation and ageing fractures,3,4,14,33 especially those that are radiographically
for suspected physical abuse,5,8 the Royal College of Radiologists re- subtle.3,14,33 For instance, it is reported that: histology confirmed 6 CML
commends 22 different views17 to adequately visualise the entire ske- identified as ‘abnormal’ on SS3; four from five rib fractures ‘suspected’,
leton. For instance, SS identified 1029 fractures in 313 of 567 infants but not diagnosable, on SS33 and metaphyseal fractures in two speci-
aged < 12 months.9 789 fractures (77%) were clinically unsuspected, mens that appeared normal radiographically.3 However selecting tissue
thus highlighting the role of skeletal survey in detecting occult inflicted for histological examination is key, as it is not practical to sample the
fractures, particularly ribs,18 that would otherwise go undetected. whole skeleton histologically. For this the histopathologist relies on the
In addition to identifying fractures, SSs can provide information on radiologist and autopsy pathologist to guide sampling.
the age of skeletal injuries and the presence of any underlying bone There are no large studies that have systematically described the
disease17 which may prove particularly useful where an explanation different fracture detection rates of post-mortem SS, CR and histo-
provided by the care-giver does not match the type or extent of injuries pathology and related them to histological age of fracture, bone, and
sustained.19 region of bone; and yet the evidence above suggests the right balance of
CT scanning7 has proven useful in confirming skeletal injuries these techniques could be extremely important in optimising the de-
otherwise subtle on skeletal survey in both living and dead children. tection of abusive injuries. This is the rationale for our study.
High-detail CT scans can identify CMLs,14 and create 3D reconstruc-
tions that effectively demonstrate the extent of an injury to a lay jury.7
One drawback of CT scanning is the radiation dose20–22; potentially 2. Methods
outweighing its value as a screening test in live infants.
MRI scanning has also been used to supplement SS. When used to This was a retrospective audit of anonymised data from all cases of
assess non-cerebral injuries (including CMLs and rib fractures), whole- suspected non-accidental injuries referred to the histology department
body MRI has a ‘high specificity but low sensitivity’ when compared to of the Manchester Royal Infirmary for specialist histopathological
SS.23 For instance when whole-body MRI was compared to SS in 16 evaluation of skeletal injuries between 2011 and June 2017 (226 cases).
infants, 5.4% of CMLs were identified by MRI vs 64.8% by SS alone.23 Inclusion criteria were:
MRI identified only 54% of rib fractures.
In live infants bone scintigraphy has a high sensitivity for radio- • Child < 18 months old at the time of death.
graphically subtle lesions, such as rib fractures, with 50% in one study • Recorded data from a post-mortem skeletal survey reported by a
being identified by bone scintigraphy alone.24,25 One drawback is the specialist paediatric or musculoskeletal radiologist.
low sensitivity of detection of CMLs because of high uptake of scinti- • Archived contact radiographs of all the bones. Only cases with CR in
graphic medium by normal growth plates.24 2 planes for all bones examined were included.
There is broad agreement that outside the skull, certain skeletal
injuries carry a high likelihood of being abusive. The most significant in A total of 38 infants met these criteria. The median age was 12
this respect are metaphyseal and posterior rib fractures26 particularly in weeks (range: 19 days–14 months).
non-ambulatory infants.3–5,7,10,12 Grasping by the chest, squeezing, Fractures detected for each of the 3 tests, SS, CR and histology, were
violent shaking and pulling and twisting of the limbs are implicated in tabulated and compared. The data for skeletal surveys was as reported
these injuries.5,7,8 Caution is required in neonates as obstetric trauma, by the specialist radiologists. Contact radiographs are used by specialist
including traumatic vaginal births and uncomplicated Caesarean sec- histopathologists to aid sampling for histological analysis. For this study
tions,27–29 has been causally implicated in these types of fracture. however, in addition to being reviewed by AF and ER, all CR radio-
CMLs, particularly when acute, can be difficult to detect with con- graphs in which: no fracture could be seen; the appearances were felt to
ventional radiography.5,7 One study reported 15 healing metaphyseal be equivocal; or where a fracture was seen histologically but not
lesions visible on follow-up SS as ‘indeterminate’ initially.4 radiographically by the pathologists, were reviewed by a specialist
Whilst posterior rib fractures5–7,9,11 are highly specific for non- consultant musculoskeletal radiologist (PK). All fractures identified on
accidental injury,2,4–6,9–12 carrying a 95% positive predictive value for CR by AF, ER or PK were tabulated as positive. Histological recognition
physical abuse in children aged < 3 years,18 because of the anatomy, of fractures was made by AF, an osteoarticular pathologist specialising
with bone and soft tissue overlay, and a frequent lack of displacement, in the histological recognition and interpretation of fracture healing, in
they may be overlooked by conventional radiography, particularly if the biopsy diagnosis of paediatric metabolic bone disease, and 27 years
acute.5,6,9,17,30 In life, follow-up SS increases detection rates. In one medicolegal experience in recognising and aging fractures in infants.
study,30 94% of fractures first diagnosed at follow-up were either me- Specimens of bone were received from Home Office and forensic
taphyseal or rib fractures, and in another,9 64% of 98 new definite pathologists from across the UK as samples of bone in formalin. A short
fractures identified at follow-up in 41 infants were rib fractures. clinical history and the results of SS were included in all cases used in
In fatally abused infants follow-up SS is not possible6; necessitating this paper. Contact radiography was performed on a Faxitron [Faxitron
a different approach for detecting skeletal injuries after death. Bioptics, LLC 3440 E Britannia Drive, Suite 150, Tucson, Arizona USA
Skeletal survey, palpation at autopsy, and visualised peri-osseous 85706]. Images were taken in 2 planes. Following this, bones were
bruising alert pathologists to the possibility of fractures. In addition, decalcified and then widely sampled to include known and suspected
forensic and paediatric pathologists in the UK are increasingly taking fracture sites from SS, autopsy findings, CR, and sites at which identi-
key bones (e.g. posterior ribs) that might have occult fractures for fying a fracture might be of significance in assessing abusive injuries
histological examination by an experienced Osteoarticular Pathologist. (mainly metaphyses and posterior elements of the ribs). The tissue was
Prior to histological analysis it is common practice for the laboratory taken into paraffin using conventional methods and then sectioned at
dealing with the bone samples to undertake ‘contact’ (specimen) x-rays 4 μm. Serial sections were stained with haematoxylin and eosin (H&E)
using a high dose, high resolution system. These are rarely, if ever, and Martius scarlet blue (MSB). Two sections were examined from most
reported by radiologists, but guide experienced histopathologists in tissue blocks but equivocal microscopic findings always resulted in
sample selection. “deeper” sections being taken.
In one study comparing contact radiography (CR) with SS, fracture Fractures were aged histologically in a manner similar to that de-
detection increased from 58% to 92%, the additional skeletal injuries scribed by Klotzbach et al.33 supplemented with our own data derived
including high-specificity type injuries, of metaphyses and posterior from previously published studies examining the in-situ molecular
ribs.4 Evidence indicates it may also improve fracture aging.4,7,31,32 biology of fractures.34–36 Briefly:

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E. Raynor et al. Journal of Forensic and Legal Medicine 60 (2018) 9–14

• Fractures were recognised as deficiencies in bone with a distinct Table 2


Limb long bone fracture distribution within each bone.
fracture gap and some associated reaction. All the metaphyseal
fractures extended into adjacent bone and were aged from the Proximal metaphysis Shaft Distal metaphysis
changes within the bone.
• < 2 days – Haemorrhage in and around the fracture site with os- Femur
Tibia
4
17
10
5
17
7
teocyte necrosis in bone abutting the fracture line and, in some,
Humerus 9 8 11
more polymorphs in areas of haemorrhage than one would expect to Radius 5 3 6
have resulted from haemorrhage alone. Ulna 3 4 4
• < 7 days – Formation of granulation tissue, evidence of chronic Fibula 3 0 3
inflammation and formation of early fracture callus with con-
densation of connective tissue into primitive bone and cartilage like
structures. decision was made to assess the detection rate of the imaging techni-
• < 14 days – Obvious trabeculae of woven bone and nodules of ques based on site alone, giving a total of 100 fracture sites.
46 long bone fractures were detected by both SS and CR (46%); 14
cartilage in the medulla and on periosteum typical of “primary
callus”. by CR only (14%); 15 by SS only (15%); and 25 were not detected by
• About 14 days – Almost all cases show widespread more intense either (25%). 48 fractures were aged ≤14 days; of these, SS failed to
identify 15 (31%), and CR 14 (29%). 52 fractures were aged > 14 days;
haematoxyphilia of the matrix indicative of mineralisation. Callus
bridges the fracture site. of these, SS failed to identify 24 lesions (46%), and CR failed to identify
• > 14 days – Onset of remodelling of primary callus. 26 lesions (50%).
• > 28 days – Formation of lamellar bone on the surface of existing Of the 119 long bone fractures, 46 (39%) were defined as meta-
physeal histologically. Generally, the detection rate of metaphyseal
woven bone and cartilage nodules.
• > 2 months – Progressive matrix reorganisation. fractures by SS and CR increased as the age of the lesion increased. 36
fractures were aged ≤14 days; of these, SS and CR each failed to
In the context of this paper, fractures “≤14 days old” are those identify 9 (25%), but they were not the same 25%. 10 fractures were
showing neither widespread matrix colour change typical of miner- aged > 14 days; of these, SS identified all, and CR 9 of the 10. This data
alisation nor bridging callus formation. This time point was chosen is presented in Table 3.
because it corresponds to defined radiological events. Rib Fractures: The total number of rib fractures was 178 (56% of
Histologically detected fractures were tabulated by bone, site within total number fractures). These were distributed among 21 infants, the
the bone and histological age. number of fractures per infant ranging from 2 to 26 (median: 6). Rib
fractures were identified in at least two adjacent ribs in 19 of the 21
infants.
3. Results There were generally more fractures of the left ribcage than of the
right ribcage. The seventh rib was the most frequently fractured rib of
General findings: In no case did SS or CR detect a fracture that was both the left and the right ribcage (Graph 1).
not identified histologically. Comparative analyses given below are 25 fractures were refractures. Again SS and CR failed to identify any
therefore described relative to the fractures identified histologically. of the refractures, therefore, as for the limb long bones, comparative
Histologically, 318 fractures were identified in the 38 infants. Of studies were based on 153 fracture sites rather than 178 fractures. 72
these, 178 (56%) affected ribs, 119 (37.5%) limb long bones, 10 (3%) rib fractures (47%) were detected by SS and 83 (54%) by CR. 52
skull and 11 (3.5%) were classified as ‘other’ fractures (3 clavicle, 4 fractures (34%) were not detected by either SS or CR. The position in
cervical spine, 2 lumbar spine, 1 ankle not otherwise specified, 1 first the rib of the fractures and the number detected by SS and CR are given
metacarpal). in Table 4.
Limb Long Bone Fractures: The 119 limb bone fractures were found This analysis showed: 38 fractures of the anterior metaphyses, 14
in 20/38 infants (53%); the number of fractures identified in a single shaft, and 18 posterior metaphyses 14 days old or less at the time of
infant ranged from 1 to 19 (median: 4). The number and distribution by death; and 26 anterior metaphyseal, 11 shaft, and 46 posterior meta-
bone are presented in Table 1. physeal fractures aged > 14 days.
The most common locations for limb long bone fractures were of, or For those fractures dated ≤14 days, SS detected 8 (21%) of the
involved, the proximal tibial and the distal femoral metaphyses (17 anterior metaphyseal fractures, 1 (7%) of the shaft fractures and 5
fractures [14%] each). Thus 28% of all long bone fractures affected the (28%) of the posterior metaphyseal fractures. CR increased the detec-
metaphyses around the knee. tion rate of anterior metaphyseal fractures to 37%, shaft fractures to
Histologically, 19 of the limb long bone fractures were new frac- 79% and posterior metaphyseal fractures to 44%.
tures through the site of an existing, older fracture (refractures). SS Of the fractures more than 14 days old at the time of death: SS
detected 13 of the older fractures and CR 16, however neither SS nor CR detected 69% of the anterior metaphyseal fractures, 82% of shaft
distinguished refracture from the older fracture. With this in mind a fractures and 67% of posterior metaphyseal fractures, with CR

Table 1
Limb Long Bone Fracture Distribution. The detailed distribution of long bone Table 3
fractures by bone and by site within the bone is given in Table 2. Detection of metaphyseal lesions in limb long bones by age.
Number of fractures Number of infants in which fracture was Metaphyseal fractures aged Metaphyseal fractures aged
detected ≤14 days (N = 46) > 14 days (N = 10)

Femur 31 (26%) 14 Both 22 (61%) 9 (90%)


Tibia 29 (24%) 10 SS only 5 (14%) 1 (10%)
Humerus 28 (24%) 8 CR only 5 (14%) 0 (0%)
Radius 14 (12%) 8 Total by SS 27 (75%) 10 (100%)
Ulna 11 (9%) 7 Total by CR 27 (75%) 9 (90%)
Fibula 6 (5%) 5 Neither 4 (11%) 0 (0%)
Total 119 (100%) 20 Total 36 (of 46 [78%]) 10 (of 10 [100%])

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E. Raynor et al. Journal of Forensic and Legal Medicine 60 (2018) 9–14

we have presented all our data on SS and CR as a proportion of histo-


logically detected fractures. In very general terms skeletal survey, the
mainstay of fracture detection in infants suspected of abusive injury,
failed to detect 39% of all long limb bone fractures and 34% of all rib
fractures. In early fractures (defined here as fractures occurring 14 days
or less prior to death, as assessed histologically) SS failed to detect 31%
of long limb bone fractures and 80% of rib fractures.
In this study neither radiological technique could detect a re-
fracture. 44 of the 318 fractures (14%) were refractures and, as such,
each was evidence of 2 fracturing events at different times, a char-
acteristic of non-accidental injury. We have not included refractures in
the data analyses in this study, but had we done so their inclusion
would have further reduced the ability of SS to detect fractures im-
portant in identifying abusive injuries.
That histology identified all the fractures in specific parts of a bone,
whilst SS (even supplemented by CR) did not, evidences that histology
Graph. 1. Distribution of Rib Fractures by bone. should be considered the definitive test by which to identify fractures.
However, because it is impossible to sample the entire skeleton histo-
Table 4 logically, selection of bone for histological examination is entirely re-
The position of rib fractures by site within the ribs. liant on skeletal survey and post mortem examination findings to target
Anterior metaphysis Shaft Posterior metaphysis bone for histological assessment. Therefore within the context of
identifying fractures, skeletal survey, post mortem examination and
Both 20 (31%) 8 (32%) 26 (41%) histological examination are complimentary and, as such, all are es-
SS only 6 (9%) 2 (8%) 10 (16%)
sential for investigation of an infant suspected of having sustained non-
CR only 11 (17%) 10 (40%) 8 (13%)
Total by SS 26 (41%) 10 (40%) 36 (56%)
accidental injury.
Total by CR 31 (48%) 18 (72%) 34 (53%) From this study we were able to show that, in addition to radi-
Neither 27 (42%) 5 (20%) 20 (31%) ologically suspicious and autopsy findings, there are areas of the ske-
Total 64 (42%) 25 (16%) 64 (42%) leton that warrant sampling for histology (or more detailed imaging
studies in live infants) in all cases of suspected non-accidental injury in
infants, even when SS fails to identify a fracture. They are the anterior
increasing the detection rate of anterior metaphyseal fracture to 88%,
and posterior metaphyses of the 5th, 6th, 7th and 8th ribs bilaterally
shaft fractures to 82% and posterior metaphyseal fractures to 78%.
and the metaphyses around the knees. These are important sites as
Skull Fractures: The total number of skull fractures identified was
metaphyseal and posterior rib fractures are highly correlated with a
10 (3%). One fracture was dated > 14 days. All were detected by both
non-accidental cause.2–16 In our study, these are also areas of the ske-
SS and CR.
leton in which histology detected fractures unrecognised by skeletal
Other Fractures: The total number of ‘other’ fractures identified was
survey, particularly recent fractures. Our recommendation of focused
11 (3.5%; 3 clavicle, 4 cervical spine, 2 lumbar spine, 1 condylar ankle,
sampling of these areas of the skeleton in all cases of suspected non-
1 first metacarpal). SS and CR detected fractures in the peripheral bones
accidental injury is based on the following findings from this study:
but neither detected the spinal fractures all of which were metaphyseal
and predominantly of the transverse processes.
• Skeletal survey detected limb long bone metaphyseal fractures in
75% of cases in which histology dated the fracture as 14 days old or
4. Discussion less. This compares with 100% at fractures older than 14 days.
When the anterior and posterior rib metaphyses are taken together,
Despite the large number of cases received in our laboratory over SS detected 23% of fractures ≤14 days old and 68% > 14 days old.
the study period, only 38 met all the inclusion criteria. The largest • Fractures of the distal femoral and proximal tibial metaphyses ac-
single cause of non-inclusion was an absence of a comprehensive ske- counted for 28% of all limb long bone fractures.
letal survey report by a specialist radiologist. We deliberately chose • Fractures of the anterior and posterior ends of the 5th, 6th, 7th and
only cases reported by specialist radiologists to minimise the known 8th ribs accounted for two thirds of all rib fractures not detected by
inter-observer variation in skeletal survey reporting,37 and to try to SS.
provide a method by which maximum comparability could be brought
between radiological and specialist histological analyses. We also re- We have used a cut off of 14 days to distinguish “recent” and “old”
cognise that as our samples are taken by Forensic/Home Office Pa- fractures. Aging of the fractures comes from a histological assessment
thologists from around the UK, and that the sampling did not conform based upon a synthesis of the literature and our own published ex-
to a set protocol, bone sampling and post-mortem fracture detection perience. It must be acknowledged that there are no definitive pub-
therefore include selection bias. In the setting, statistical analysis would lished studies of the appearances of fractures of known ages in infants,
not have had validity and was not performed. an issue that needs to be urgently addressed. However there is a re-
Nevertheless, because we have made a detailed analysis comparing cognised sequence of events in fracture healing that enables the histo-
the detection by SS, CR and histology of the same 318 fractures, we pathologist to say whereabouts in the healing process a fracture has
believe the data are of considerable value to forensic pathologists, reached. Even if one were to ignore giving a specific age to a fracture
forensic/paediatric/musculoskeletal radiologists examining images in there is no doubt that early fractures, particularly non-displaced frac-
cases of potential child abuse, and all those considering the legal im- tures in which there is no mineralised matrix, are more difficult to
plications of differences between fractures detected by skeletal survey detect by skeletal survey.
and histological examination of bone in infants. Our study may help radiologists to focus on specific areas of the
Because of the design of this study, histology was the referent for skeleton for detailed analysis in live infants with existing or future in-
detecting fractures, an approach not used previously. As both SS and CR vestigative techniques. It also flags up the number of “old” fractures in
failed to demonstrate any fractures that were not detected by histology, infants later dying from a death suspected of being non-accidental. In

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E. Raynor et al. Journal of Forensic and Legal Medicine 60 (2018) 9–14

our study 27 of the 38 infants (71%) had at least one fracture > 14 days Declarations of interest
old. This emphasises the proportion of cases of infants suspected as
having died an abusive death who have evidence of previous, probably Miss Emma Raynor: None
inflicted, skeletal injuries. Praveen Konala: None
We have included contact/specimen radiography here because of a Professor Anthony Freemont: None
previously reported study comparing SS, CR and histology in 3 in- Professor Freemont is supported by the MRC and EPSRC (MRC
fants.33 In that study CR was the referent and it noted that all fractures Grant MR/N00583X/1) for work on molecular biomarkers and is part of
detected by CR were also detected by histology. If histopathology was the Musculoskeletal Division of the Manchester NIHR BRC.
superior to CR in detecting fractures the study design would not have
allowed this to become apparent. Equally the study design would have Acknowledgements
meant that if there were any discrepant findings between CR and SS, SS
would inevitably have been found to be inferior to CR. Our study shows This research did not receive any specific grant from funding
that SS and CR detect similar numbers of fractures but that the 2 agencies in the public, commercial, or not-for-profit sectors.
techniques are complimentary, together recognising a greater number
of fractures that either technique alone. However, even in combination, References
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