Bone Scintigraphy After a Negative Radiological Skeletal Survey Improves the Detection Rate of Inflicted Skeletal Injury in Children

Background: Timely diagnosis of child physical abuse is of paramount importance. The added value of bone scintigraphy (BS) after a negative radiological skeletal survey (RSS) in children with suspected physical abuse has never been evaluated.

Objective: The objective of this study was to assess the extent to which BS could improve the detection rate of skeletal injury in children with suspected physical abuse with an initial negative RSS.

Methods: We used discharge codes to retrospectively identify children evaluated for suspected physical abuse in a university hospital (Nantes, France). We included all consecutive children younger than 3 years old who underwent both RSS and BS, with an interval of ≤96 h between tests, from 2013 to 2019. BS and RSS results were interpreted independently during the study period. We specifically analyzed BS results for children with a negative RSS to assess the value of BS as an add-on test.

Results: Among the 268 children ≤3 years old with suspected physical abuse who underwent RSS, 140 (52%) also underwent BS within 96 h and were included in the analysis. The median age was 6 months old (interquartile range: 3–8). The detection rate of ≥1 skeletal injury with RSS alone was 49% (n = 69/140, 95% CI: 41–58%) vs. 58% (n = 81/140, 50–66%) with RSS followed by add-on BS, for an absolute increase in the detection rate of 9% points (95% CI: 4–14%). The number of children with a negative RSS who would need to undergo BS to detect one additional child with ≥1 skeletal injury was 6 (95% CI: 4–11).

Conclusion: In young children with suspected physical abuse with a negative RSS, add-on BS would allow for a clinically significant improvement in the detection rate of skeletal injuries for a limited number of BS procedures required. Prospective multicenter studies are needed to confirm these findings.

Evidence Before This Study

Uncertainty about the extent of the added value of bone scintigraphy (BS) after a negative radiological skeletal survey (RSS) impedes harmonized guidelines on the role of BS in the diagnostic pathway of young children with suspected physical abuse.

Added Value of This Study

Performing BS in young children with suspected physical abuse after a negative RSS would allow for a clinically significant improvement in the detection rate of skeletal injuries for a limited number of BS procedures required.

Introduction

Physical abuse is estimated to occur in 4–16% of the population younger than 18 years old in high-income countries (1). Timely diagnosis of child physical abuse is of paramount importance because failure to identify an inflicted injury and to intervene appropriately may put the child at risk for further abuse and precludes treatment of injuries and rehabilitation (2–5). After cutaneous injuries, inflicted skeletal injuries are the second most common finding in children with suspected physical abuse (3, 6–10) and are an indicator of severe assault (8–13).

Radiological skeletal survey (RSS) is the currently recommended test for the diagnosis of inflicted skeletal injuries in all children under 2 years old with suspected physical abuse (6, 13–16). However, RSS cannot be considered a reference standard because skeletal injuries of the ribs, hands, and feet, which are reliable indicators of child physical abuse (8–13, 17), may be inconspicuous or invisible on initial RSS (18–21). Thus, follow-up RSS after 2 weeks may help detect skeletal injuries missed on the initial RSS (14, 18, 19, 21) and are recommended (6, 13–16). Several reports have underscored the lack of adherence to follow-up RSS, mainly because of concerns about delaying the diagnosis (22–25). Any alternative approach that would enhance the detection rate of inflicted skeletal injuries without causing a 2-weeks delay would be clinically highly relevant.

Preliminary reports have suggested that bone scintigraphy (BS) with technetium-99m diphosphonate can increase the detection rate with RSS (26–31). Indeed, BS presents a functional evaluation of total skeletal metabolism, which allows for detecting a skeletal injury within hours of its occurrence, and has shown high diagnostic performance in the assessment of various bone disorders (32). BS has poor sensitivity for “classical metaphyseal injuries” and other frequent skeletal injuries considered typical of child physical abuse (29, 31) because of physiological hypermetabolism in these regions, thereby capturing the radiotracer. Therefore, BS cannot replace RSS. Moreover, BS implies exposure to more radiation than does RSS (2.3 vs. 0.1–0.5 mSv on average) (33), is available only in hospitals with nuclear medicine departments, and adds costs. Positioning BS as an add-on test (34) after a negative RSS would allow for using the reclassification potential of BS while limiting the number of BS procedures performed. The benefit of this strategy has never been evaluated.

The objective of this study was to assess the extent to which BS could improve the detection rate of skeletal injury in children with suspected physical abuse with an initial negative RSS.

Methods

Study Design

We conducted a retrospective study in a tertiary university pediatric hospital. The protocol was approved by the ethics committee of Nantes University Hospital, allowing for this observational study with information for parents available on billboards placed in all public places of the hospital. We used the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines (35) to report this study (Appendix 1).

Participants

We used the following ICD-10 discharge codes to retrospectively identify, among all children evaluated by RSS, those potentially evaluated for a suspicion of physical abuse: abuse syndromes (codes beginning with T74), intracranial traumatic injuries (codes beginning with S06), intra-abdominal traumatic injuries (codes beginning with S36), and skeletal injuries (codes beginning with S02, S12, S22, S32, S42, S52, S62, S72, S82, S92, M84). We included the medical files of all consecutive children younger than 3 years old who underwent both RSS and BS, from January 2013 to July 2019, a period during which the local protocol encouraged clinicians to perform both tests in children with suspected physical abuse. We included children for whom tests were performed with an interval of ≤96 h to limit bias related to time.

Imaging Tests

During the study period, the local protocol for RSS agreed with international guidelines (6, 15, 16, 36) with performance of frontal and profile skull views, frontal chest view, profile whole spine views, frontal unprepared abdominal view, frontal upper-limb (arms, forearms, hands) views, frontal lower-limb (thighs, legs, feet) views, and frontal pelvis views. A profile incidence of the chest was added with suspected rib injuries. The local protocol for BS also agreed with international guidelines (32). The acquisition was carried out in the “whole body” twice after the injection of the radiotracer (99m-Tc diphosphonate): first, the tissue acquisition at 5 min after the injection and, second, the bone acquisition at 3–4 h after the injection. The doses of the radiotracer were adapted to the child's weight, with a baseline activity of 35.0 MBq (32). BS was performed in situ without sedation.

BS and RSS results were interpreted independently during the study period. All RSS results were analyzed by a senior pediatric radiologist, and all BS results were analyzed by a senior physician in nuclear medicine, with strong expertise in RSS and BS, respectively. In our study, we used the results of the routine interpretation of both tests. Positivity of the RSS or BS was defined as the detection of one or more skeletal injuries (i.e., fracture, periosteal apposition, displacement) in a child, including any index skeletal injury(ies), that is, the skeletal injury(ies) detected before RSS, which were at the origin of the suspected physical abuse and its diagnostic workup. A negative RSS or BS was defined as no skeletal injury detected. When the BS result was considered doubtful, new radiographs were obtained 7–10 days later on the doubtful region. No muscle injury was reported.

Data Extraction and Analyses

Two of the authors (FB and CP) reviewed the medical files and extracted the children's characteristics (age at the time of the imaging investigation, sex, reason for suspecting physical abuse), the imaging protocol followed, and the number of skeletal injuries detected by RSS and BS and their location. We calculated the detection rates of children with ≥1 skeletal injury with RSS alone and with add-on BS (i.e., after a negative RSS), the absolute increase in the detection rate of children with ≥1 skeletal injury with the add-on strategy, and the number needed to test (NNT) (i.e., the number of children with a negative RSS who would need to undergo a BS to detect one additional child with ≥1 skeletal injury; formula in Appendix 2). We also evaluated the number of additional skeletal injuries detected by BS, their location, and whether they led to an orthopedic or surgical treatment. Finally, we described the number of additional skeletal injuries detected by BS for children after a positive RSS.

We conducted two sensitivity analyses. In the first, we included only children with an interval between tests of ≤24 h. In the second, we included children with an interval between tests of ≤96 h, but outcomes were recalculated considering the RSS as negative if it detected no skeletal injury or only an index skeletal injury (i.e., those already known before RSS and at the origin of the suspected physical abuse and its diagnostic workup). We used R v3.5.2 for the analyses (R foundation for Statistical Computing, Vienna, Austria).

Results

Population

During the study period, among the 268 children ≤3 years old with suspected physical abuse who underwent RSS, 140 (52%) also underwent BS within 96 h (Figure 1) and were included in the analysis. The median age was 6 months (interquartile range: 3–8), and 54% (n = 75) were boys. The main reasons for suspecting physical abuse were index skeletal injuries (44%, n = 61), bruises (35%, n = 49), and/or intracranial injuries (24%, n = 34) (Appendix 3). Children who underwent BS differed significantly from those who did not only in the reason for suspecting physical abuse: they had significantly more intracranial injuries than those who did not undergo BS (24%, n = 34, vs. 10%, n = 12, p = 0.01) (Appendix 3).

FIGURE 1

Figure 1. Flow chart of inclusion of children and results of radiological skeletal survey (RSS) and add-on bone scintigraphy (BS). *Among the 69 children with positive RSS, BS detected 48 supplementary skeletal injury in 34 children (34/69, 49%).

Imaging Tests

RSS and BS were performed within 72 h for 97% (n = 136/140) of the children and within 24 h for 76% (n = 106/140) of the children. The detection rate of ≥1 skeletal injury with RSS alone was 49% (n = 69/140; 95% confidence interval [CI] 41–58%) and revealed a total of 132 skeletal injuries (range: 1–12) (Figure 1 and Table 1). The detection rate of children with ≥1 skeletal injury with the add-on BS strategy was 58% (n = 81/140; 50–66%), revealing skeletal injuries in 12 children among those with negative RSS and 23 new skeletal injuries (range: 1–4 skeletal injuries). The absolute increase in the detection rate with add-on BS was 9% points (95% CI: 4–14%) and was statistically significant (McNemar test, p = 0.001). The NNT to detect one additional child with ≥1 skeletal injury was 6 (95% CI: 4–11). Among the 23 skeletal injuries not detected by RSS, the most frequent locations were the foot (17%, n = 4) and tibia (17%, n = 4) (Table 1). New skeletal injuries were revealed by BS after a negative RSS in 12 children. In 11 of these 12 children, the diagnosis of skeletal injury was definitively made on BS alone (Figure 1). For one child, BS was inconclusive, which led to obtaining new radiographs of the doubtful region 10 days after the initial RSS. These new radiographs confirmed one skeletal injury. Among these 12 children, the additional injuries identified did not lead to any orthopedic or surgical treatment.

TABLE 1

Table 1. Location of the skeletal injuries detected by radiological skeletal survey and add-on bone scintigraphy in the 140 included children.

Sensitivity Analyses

On sensitivity analysis including only children with an interval between tests of ≤24 h (76%, n = 106), the RSS detection rate of children with ≥1 skeletal injury was 52% (n = 55/106; 42–62%), with an absolute increase in the detection rate of 8% points (95% CI: 4–16%) with add-on BS and an NNT of 6 (95% CI: 3–12) (Appendix 4).

For 44% (n = 61) of the children, physical abuse was initially suspected on the basis of ≥1 index skeletal injury(ies). By defining a positive RSS when it detected ≥1 skeletal injury different from the index skeletal injury(ies), the RSS detection rate of children with ≥1 skeletal injury(ies) was 22% (n = 31/140; 16–30%), with an absolute increase in the detection rate of 14% points (95% CI: 8–20%) with add-on BS and an NNT of 6 (95% CI: 4–9) (Appendix 4).

Discussion

Key Results

The stakes of identifying skeletal injuries in a child with suspected physical abuse are critical, with major impact on the early decision for child protection and subsequent consequences for the early and long-term health of the child. Thus, our objective was to evaluate the added value of BS after a negative RSS to detect skeletal injuries in children with suspected physical abuse. The absolute increase in the detection rate was 9% points and was statistically significant. This increase in the detection rate was obtained by performing BS in only half of the children with suspected physical abuse. The add-on strategy allowed for limiting the number of BS procedures performed, with an NNT of 6. The extent of the increase in the detection rate was similar to or higher on both sensitivity analyses performed with a more stringent maximal interval between the two tests (≤24 h) or by defining a positive RSS when it detected ≥1 skeletal injury different from the index skeletal injury(ies). Regarding the benefit–inconvenience balance, this low number of necessary BS procedures seems compatible with the burden of this procedure, which involves added radiation exposure (2.3 mSv on average) and requires intravenous access and sometimes a transfer to another hospital with a nuclear medicine department.

Limitations

Our study had limitations. First, it was retrospective and performed in a single tertiary hospital with a referral center for abused children. This design could have led to a biased selection of children more seriously affected. Only 55% of the eligible children underwent both RSS and BS in the study period, which suggests a higher medical worry for those children and was confirmed by the higher rate of intracranial injuries than in children with RSS alone (Appendix 3). Subsequently, the NNT calculated in the present population could be biased and would be higher with a less selected population. However, the general characteristics of the study population were close to those reported in the literature (37–41) in terms of age, sex ratio, and frequency of skeletal injuries.

The interpretation of the RSS may be difficult, and a new interpretation by one or more independent experts may have led to the detection of more skeletal injuries. However, the choice not to reanalyze the RSS allowed for evaluating the impact of BS in “real life,” not in an experimental situation.

We could not estimate the exact added value of BS to reclassify child physical abuse. Indeed, the final diagnosis of child physical abuse relies on a combination of social and clinical evaluations and medical tests (42), so the detection of additional skeletal injuries by BS may have limited impact when cutaneous, neurological, or ophthalmologic findings suggesting physical abuse have already been detected. However, the additional skeletal injuries detected by BS may confirm the diagnosis of abuse in doubtful cases, and their location brings additional information to adapt treatment (43) and evaluate the potential mechanisms involved in the inflicted injury (20, 42).

Finally, we focused on an add-on strategy among children with a negative RSS and did not emphasize the 69 children with a positive RSS in whom BS detected supplementary skeletal injury(ies) in 34 children (Figure 1). The added value of BS after a positive RS was already reported in the literature (26–31), and its clinical usefulness may be less obvious than the added value of BS after a negative RSS. Furthermore, performing BS in children with a negative RSS and in all children with suspected physical abuse would increase the number of BS procedures required and the NNT.

Conclusions

Despite several original studies (26–31) and one narrative review (18) concluding that RSS and BS are complementary tests, discrepancies remain between international guidelines for the indication of BS in the diagnostic work-up of suspected physical abuse in children (15, 16, 36). There is a consensus that BS should not replace RSS given its lack of sensitivity for classical metaphyseal injuries. A strategy of no BS is highly arguable given the available data on its potential for reclassifying inflicted skeletal injury and the high stakes of missing child physical abuse in relation to the risk of recidivism (estimated at 35% to 50% in the literature) (44–46) and an overall increased risk of morbi-mortality (2–5). A strategy of systematic BS after RSS, whatever the RSS results, would lead to many useless BS procedures with doubtful clinical consequences and additional invasiveness, irradiation, and costs. The add-on strategy that we evaluated for the first time in this study would benefit the reclassification potential of BS while keeping the number of children exposed to the negative effects of BS (pain, additional radiation exposure, and costs) as low as possible. Prospective multicenter studies are needed to confirm these findings.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Ethics Statement

The studies involving human participants were reviewed and approved by Direction de la Recherche, Département promotion, cellule recherche non-interventionnelle of Nantes University Hospital. Written informed consent from the participants' legal guardian/next of kin was not required to participate in this study in accordance with the national legislation and the institutional requirements.

Author's Note

Some results were presented orally on June 18, 2019 at the Second National Congress of the French Society of Pediatric Forensic Pathology in Nantes, France.

Author Contributions

FB, EL, CG-L, and MC: conception of study. FB, EL, NV, FS, TE, CG-L, JC, and MC: design of study. FB, CP, and CG-L: data management. FB, JC, and MC: data analysis. FB and MC: drafting of the manuscript. EL, CP, NV, FS, TE, JC, and CG-L: revising of the manuscript. FB, CP, EL, NV, FS, TE, MC, and CG-L: final approval of the version to be published. All authors contributed to the article and approved the submitted version.

Funding

FB and CG-L had external funding for this study (Hôpitaux Universitaires du Grand Ouest—HUGO, Mustela Foundation, and the Véronique-Roualet prizes). The authors had no financial relationships with any organizations that might have an interest in the submitted work in the previous 3 years and there were no other relationships or activities that could appear to have influenced the submitted work. The funders had no role in the design and conduct of the study, the analysis and interpretation of the data, preparation, review, or approval of the manuscript.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fped.2020.00498/full#supplementary-material

References

1. Gilbert R, Widom CS, Browne K, Fergusson D, Webb E, Janson S. Burden and consequences of child maltreatment in high-income countries. Lancet. (2009) 373:68–81. doi: 10.1016/S0140-6736(08)61706-7

PubMed Abstract | CrossRef Full Text | Google Scholar

2. Krug E, Dahlberg L, Mercy J, Zwi A, Lozano R. World Report on Violence and Health. Geneva: World Health Organization (2002).

Google Scholar

3. Berkowitz CD. Physical abuse of children. N Engl J Med. (2017) 376:1659–66. doi: 10.1056/NEJMcp1701446

PubMed Abstract | CrossRef Full Text | Google Scholar

4. Norman R, Byambaa M, De R, Butchart A, Scott J, Vos T. The long-term health consequences of child physical abuse, emotional abuse, and neglect: a systematic review and meta-analysis. PLoS Med. (2012) 9:e1001349. doi: 10.1371/journal.pmed.1001349

PubMed Abstract | CrossRef Full Text | Google Scholar

5. Afifi T, Mather A, Boman J, Fleisher W, Enns M, Macmillan H. Childhood adversity and personality disorders: results from a nationally representative population-based study. J Psychiatr Res. (2011) 45:814–22. doi: 10.1016/j.jpsychires.2010.11.008

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Christian CW, Committee on Child Abuse and Neglect. The evaluation of suspected child physical abuse. Pediatrics. (2015) 135:e1337–54. doi: 10.1542/peds.2015-0356

CrossRef Full Text | Google Scholar

7. Loder RT, Bookout C. Fracture patterns in battered children. J Orthop Trauma. (1991) 5:428–33. doi: 10.1097/00005131-199112000-00007

PubMed Abstract | CrossRef Full Text | Google Scholar

8. Kemp AM, Dunstan F, Harrison S, Morris S, Mann M, Rolfe K, et al. Patterns of skeletal fractures in child abuse: systematic review. BMJ. (2008) 337: a1518. doi: 10.1136/bmj.a1518

CrossRef Full Text | Google Scholar

9. Loder RT, Feinberg JR. Orthopaedic injuries in children with nonaccidental trauma: demographics and incidence from the 2000 kids' inpatient database. J Pediatr Orthop. (2007) 27:421–6. doi: 10.1097/01.bpb.0000271328.79481.07

PubMed Abstract | CrossRef Full Text | Google Scholar

10. Offiah A, van Rijn RR, Perez-Rossello JM, Kleinman PK. Skeletal imaging of child abuse (non-accidental injury). Pediatr Radiol. (2009) 39:461–70. doi: 10.1007/s00247-009-1157-1

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Nimkin K, Spevak MR, Kleinman PK. Fractures of the hands and feet in child abuse: imaging and pathologic features. Radiology. (1997) 203:233–6. doi: 10.1148/radiology.203.1.9122400

PubMed Abstract | CrossRef Full Text | Google Scholar

12. Kleinman PK, Blackbourne BD, Marks SC, Karellas A, Belanger PL. Radiologic contributions to the investigation and prosecution of cases of fatal infant abuse. N Engl J Med. (1989) 320:507–11. doi: 10.1056/NEJM198902233200807

PubMed Abstract | CrossRef Full Text | Google Scholar

13. Flaherty E, Perez-Rossello J, Levine M, Hennrikus W, American Academy of Pediatrics Committee on Child Abuse and Neglect. Evaluating children with fractures for child physical abuse. Pediatrics. (2014) 133:e477–89. doi: 10.1542/peds.2013-3793

PubMed Abstract | CrossRef Full Text | Google Scholar

14. Section on Radiology, American Academy of Pediatrics. Diagnostic imaging of child abuse. Pediatrics. (2009) 123:1430–5. doi: 10.1542/peds.2009-0558

PubMed Abstract | CrossRef Full Text | Google Scholar

15. Halstead S, Scott G, Thust S, Hann G. Review of the new RCR guidelines 2017: the radiological investigation of suspected physical abuse in children. Arch Dis Child Educ Pract Ed. (2018) 104:309–12. doi: 10.1136/archdischild-2017-314591

PubMed Abstract | CrossRef Full Text | Google Scholar

16. Expert Panel on Pediatric Imaging, Wootton-Gorges SL, Soares BP, Alazraki AL, Anupindi SA, Blount JP, et al. ACR appropriateness criteria^® suspected physical abuse—child. J Am Coll Radiol. (2017) 14: S338–49. doi: 10.1016/j.jacr.2017.01.036

PubMed Abstract | CrossRef Full Text | Google Scholar

17. Adamsbaum C, De Boissieu P, Teglas JP, Rey-Salmon C. Classic metaphyseal lesions among victims of abuse. J Pediatr. (2019) 209:154–9.e2. doi: 10.1016/j.jpeds.2019.02.013

PubMed Abstract | CrossRef Full Text | Google Scholar

18. Kemp AM, Butler A, Morris S, Mann M, Kemp KW, Rolfe K, et al. Which radiological investigations should be performed to identify fractures in suspected child abuse? Clin Radiol. (2006) 61:723–36. doi: 10.1016/j.crad.2006.03.017

PubMed Abstract | CrossRef Full Text | Google Scholar

19. Kleinman PK, Nimkin K, Spevak MR, Rayder SM, Madansky DL, Shelton YA, et al. Follow-up skeletal surveys in suspected child abuse. AJR Am J Roentgenol. (1996) 167:893–6. doi: 10.2214/ajr.167.4.8819377

PubMed Abstract | CrossRef Full Text | Google Scholar

20. Kleinman PK, Marks SC, Adams VI, Blackbourne BD. Factors affecting visualization of posterior rib fractures in abused infants. Am J Roentgenol. (1988) 150:635–8. doi: 10.2214/ajr.150.3.635

PubMed Abstract | CrossRef Full Text | Google Scholar

21. Zimmerman S, Makoroff K, Care M, Thomas A, Shapiro R. Utility of follow-up skeletal surveys in suspected child physical abuse evaluations. Child Abuse Negl. (2005) 29:1075–83. doi: 10.1016/j.chiabu.2004.08.012

PubMed Abstract | CrossRef Full Text | Google Scholar

22. Offiah AC, Hall CM. Observational study of skeletal surveys in suspected non-accidental injury. Clin Radiol. (2003) 58:702–5. doi: 10.1016/S0009-9260(03)00226-5

PubMed Abstract | CrossRef Full Text | Google Scholar

23. van Rijn RR, Kieviet N, Hoekstra R, Nijs HGT, Bilo RaC. Radiology in suspected non-accidental injury: theory and practice in The Netherlands. Eur J Radiol. (2009) 71:147–51. doi: 10.1016/j.ejrad.2008.02.014

PubMed Abstract | CrossRef Full Text | Google Scholar

24. Hulson OS, van Rijn RR, Offiah AC. European survey of imaging in non-accidental injury demonstrates a need for a consensus protocol. Pediatr Radiol. (2014) 44:1557–63. doi: 10.1007/s00247-014-3063-4

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Swinson S, Tapp M, Brindley R, Chapman S, Offiah A, Johnson K. An audit of skeletal surveys for suspected non-accidental injury following publication of the British Society of Paediatric Radiology guidelines. Clin Radiol. (2008) 63:651–6. doi: 10.1016/j.crad.2007.11.010

PubMed Abstract | CrossRef Full Text | Google Scholar

26. Haase GM, Ortiz VN, Sfakianakis GN, Morse TS. The value of radionuclide bone scanning in the early recognition of deliberate child abuse. J Trauma. (1980) 20:873–5. doi: 10.1097/00005373-198010000-00009

PubMed Abstract | CrossRef Full Text | Google Scholar

27. Sty JR, Starshak RJ. The role of bone scintigraphy in the evaluation of the suspected abused child. Radiology. (1983) 146:369–75. doi: 10.1148/radiology.146.2.6217487

PubMed Abstract | CrossRef Full Text | Google Scholar

28. Mandelstam SA, Cook D, Fitzgerald M, Ditchfiels MR. Complementary use of radiological skeletal survey and bone scintigraphy in detection of bony injuries in suspected child abuse. Arch Dis Child. (2003) 88:387–90. doi: 10.1136/adc.88.5.387

PubMed Abstract | CrossRef Full Text | Google Scholar

29. Bainbridge JK, Huey BM, Harrison SK. Should bone scintigraphy be used as a routine adjunct to skeletal survey in the imaging of non-accidental injury? A 10 year review of reports in a single centre. Clin Radiol. (2015) 70: e83–9. doi: 10.1016/j.crad.2015.04.012

PubMed Abstract | CrossRef Full Text | Google Scholar

30. Barlucea A, Silva F, Laguna R, Montalvan C. Child abuse patterns: retrospective evaluation of clinical, radiographic and scintigraphic data in a Hispanic population. J Nucl Med. (2010) 51:1655.

Google Scholar

31. Jaudes PK. Comparison of radiography and radionuclide bone scanning in the detection of child abuse. Pediatrics. (1984) 73:166–8.

PubMed Abstract | Google Scholar

32. Van den Wyngaert T, Strobel K, Kampen WU, Kuwert T, van der Bruggen W, Mohan HK, et al. The EANM practice guidelines for bone scintigraphy. Eur J Nucl Med Mol Imaging. (2016) 43:1723–38. doi: 10.1007/s00259-016-3415-4

PubMed Abstract | CrossRef Full Text | Google Scholar

33. Rao R, Browne D, Lunt B, Perry D, Reed P, Kelly P. Radiation doses in diagnostic imaging for suspected physical abuse. Arch Dis Child. (2019) 104:863–8. doi: 10.1136/archdischild-2018-316286

PubMed Abstract | CrossRef Full Text | Google Scholar

34. Bossuyt PM, Irwig L, Craig J, Glasziou P. Comparative accuracy: assessing new tests against existing diagnostic pathways. BMJ. (2006) 332:1089–92. doi: 10.1136/bmj.332.7549.1089

PubMed Abstract | CrossRef Full Text | Google Scholar

35. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, et al. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet. (2007) 370:1453–7. doi: 10.1016/S0140-6736(07)61602-X

PubMed Abstract | CrossRef Full Text | Google Scholar

36. Kellogg ND, American Academy of Pediatrics Committee on Child Abuse and Neglect. Evaluation of suspected child physical abuse. Pediatrics. (2007) 119:1232–41. doi: 10.1542/peds.2007-0883

PubMed Abstract | CrossRef Full Text | Google Scholar

37. Duffy SO, Squires J, Fromkin JB, Berger RP. Use of skeletal surveys to evaluate for physical abuse: analysis of 703 consecutive skeletal surveys. Pediatrics. (2011) 127: e47–52. doi: 10.1542/peds.2010-0298

PubMed Abstract | CrossRef Full Text | Google Scholar

38. Karmazyn B, Lewis ME, Jennings SG, Hibbard RA, Hicks RA. The prevalence of uncommon fractures on skeletal surveys performed to evaluate for suspected abuse in 930 children: should practice guidelines change? Am J Roentgenol. (2011) 197: W159–63. doi: 10.2214/AJR.10.5733

PubMed Abstract | CrossRef Full Text | Google Scholar

39. Harper NS, Feldman KW, Sugar NF, Anderst JD, Lindberg DM. Additional injuries in young infants with concern for abuse and apparently isolated bruises. J Pediatr. (2014) 165:383–8. doi: 10.1016/j.jpeds.2014.04.004

PubMed Abstract | CrossRef Full Text | Google Scholar

40. Barber I, Perez-Rossello JM, Wilson CR, Kleinman PK. The yield of high-detail radiographic skeletal surveys in suspected infant abuse. Pediatr Radiol. (2015) 45:69–80. doi: 10.1007/s00247-014-3064-3

PubMed Abstract | CrossRef Full Text | Google Scholar

41. Wood JN, Henry MK, Berger RP, Lindberg DM, Anderst JD, Song L, et al. Use and utility of skeletal surveys to evaluate for occult fractures in young injured children. Acad Pediatr. (2019) 19:428–37. doi: 10.1016/j.acap.2018.08.007

PubMed Abstract | CrossRef Full Text | Google Scholar

42. Kistin CJ, Tien I, Bauchner H, Parker V, Leventhal JM. Factors that influence the effectiveness of child protection teams. Pediatrics. (2010) 126:94–100. doi: 10.1542/peds.2009-3446

PubMed Abstract | CrossRef Full Text | Google Scholar

43. Drouineau MH, Guenego E, Sebille-Rivain V, Vrignaud B, Balencon M, Blanchais T, et al. Do abused young children feel less pain? Child Abuse Negl. (2017) 65:248–54. doi: 10.1016/j.chiabu.2017.02.002

PubMed Abstract | CrossRef Full Text | Google Scholar

44. Oral R, Blum KL, Johnson C. Fractures in young children: are physicians in the emergency department and orthopedic clinics adequately screening for possible abuse? Pediatr Emerg Care. (2003) 19:148–53. doi: 10.1097/01.pec.0000081234.20228.33

PubMed Abstract | CrossRef Full Text | Google Scholar

45. Deans KJ, Thackeray J, Groner JI, Cooper JN, Minneci PC. Risk factors for recurrent injuries in victims of suspected non-accidental trauma: a retrospective cohort study. BMC Pediatr. (2014) 14:217. doi: 10.1186/1471-2431-14-217

PubMed Abstract | CrossRef Full Text | Google Scholar

46. Thackeray J, Minneci PC, Cooper JN, Groner JI, Deans KJ. Predictors of increasing injury severity across suspected recurrent episodes of non-accidental trauma: a retrospective cohort study. BMC Pediatr. (2016) 16:8. doi: 10.1186/s12887-016-0540-y

PubMed Abstract | CrossRef Full Text | Google Scholar