Ultrasound techniques for the detection of developmental dysplasia of the hip: a systematic review and meta-analysis

ABSTRACT BACKGROUND: Developmental dysplasia of the hip (DDH) encompasses a broad spectrum of hip pathologies, including femoral or acetabular dysplasia, hip instability, or both. According to the medical literature, ultrasonography is the most reliable diagnostic method for DDH. Several techniques for the assessment of hips in newborns and infants, using ultrasonography, have been described. OBJECTIVE: To compare the accuracy of the Graf technique and other diagnostic techniques for DDH. DESIGN AND SETTING: A systematic review of studies that analyzed ultrasound techniques for the diagnosis of DDH within an evidence-based health program of a federal university in São Paulo (SP), Brazil. METHODS: A systematic search of relevant literature was conducted in the PubMed, EMBASE, Cochrane Library, CINAHL, and LILACS databases for articles published up to May 5, 2020, relating to studies evaluating the diagnostic accuracy of different ultrasound techniques for diagnosing DDH. The QUADAS 2 tool was used for methodological quality evaluation. RESULTS: All hips were analyzed using the Graf method as a reference standard. The Morin technique had the highest rate of sensitivity, at 81.12–89.47%. The Suzuki and Stress tests showed 100% specificity. The Harcke technique showed a sensibility of 18.21% and specificity of 99.32%. CONCLUSION: All the techniques demonstrated at least one rate (sensibility and specificity) lower than 90.00% when compared to the Graf method. The Morin technique, as evaluated in this systematic review, is recommended after the Graf method because it has the highest sensitivity, especially with the three-pattern classification of 89.47%. REGISTRATION NUMBER: Identifier: CRD42020189686 at the International Prospective Register of Systematic Reviews (identifier: CRD42020189686).

of age and in 25% in those under 40 years of age who develop premature arthrosis. 4,8,11,17,18 In cases in which DDH is treated inappropriately, the main complication is avascular necrosis of the femoral head. 5,11,19 In such cases, the diagnostic method of choice is magnetic resonance imaging. 20 The risk factors for DDH include the following: 1,19 • Family history • Female sex (4-6 times higher risk) • First-born status Despite being operator-dependent, ultrasonography is considered as the most reliable method for the diagnosis of DDH in the neonatal period. 12,17,21,22 It is a noninvasive method that does not involve the use of radiation, and is portable and easy to use.
However, a physician must perform more than 100 ultrasound examinations to be considered as qualified. 13,15,[23][24][25][26] Ultrasonography of the hip detects 52% more pathological hips than the Ortolani and Barlow tests. 14 In addition, ultrasonography makes it possible to perform a dynamic study and the Ortolani and Barlow maneuvers simultaneously. 14, 15 Various techniques have been described for the ultrasound assessment of hips in newborns and infants, although there is no consensus as to which technique is the best. 27,28 OBJECTIVE The objective of this study was to determine the detection rates and accuracy of different two-dimensional ultrasound techniques for the diagnosis of DDH using the Graf method as a reference. To this end, we conducted a systematic review of the literature on this topic.

Study model
The study design followed the model outlined in the Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy, version 5.1. 29 The review was registered with the International Prospective Register of Systematic Reviews (identifier: CRD42020189686).

Inclusion criteria
This review was performed in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement. 30 We included comparative studies on the diagnostic accuracy of the Graf   technique and at least one other technique for diagnosing DDH   in the first year of life, among patients with or without risk factors for   the condition. The other techniques included the Finnbogason, Harcke,   Morin, Rosendahl, stress test, Suzuki, Terjesen, and Tréguier techniques. We did not impose any restrictions with respect to the patient origin, article language, sample size, or publication status of the studies.

Patients
Among the selected studies, all patients were of age ≤ 12 months.
The study sample included infants who underwent ultrasound for routine screening or were considered to be at a high risk for DDH.

Study selection and data extraction
The selected studies were those potentially eligible for inclusion in terms of the relevance of the abstracts or full texts. Two authors, working independently, determined their eligibility.
Disagreements were resolved through a consensus. Data extraction was performed using a standardized form. The selection process was carried out on the Rayyan platform. 31 In case of missing data, we contacted the authors of the study by e-mail.

Evaluation of the methodological quality
For all the eligible studies, we employed the Quality Assessment of Diagnostic Accuracy Studies 2 tool, 32 which focuses on the evaluation of bias and accuracy. All analyses were performed and all diagrams were created using the Review Manager program (version 5.3, RevMan; Cochrane Collaboration, Oxford, United Kingdom). The Review Manager program was used to calculate the sensitivity and specificity, as well as the corresponding 95% confidence intervals (CIs), for the previously mentioned criteria.

Search strategies
We performed a thorough systematic search for original articles in the following databases (from inception to May 5, 2020): PubMed, Excerpta Medica, Cochrane Library, Cumulative Index to Nursing and Allied Health Literature, and Latin-American and Caribbean Health Sciences Literature. We used the National Library of Medicine Medical Subject Headings "Hip Dislocation, Congenital" and "Ultrasonography, " together with the term "Graf. " Additionally, we performed manual searches of the reference lists of the included studies and evaluated the main reviews of the subject. Appendix 1 provides the full search strategy.

Graf
The Graf method consists of the evaluation of a conventional coronal view with the patient in the lateral position, providing qualitative and quantitative assessments of the hip. 17,[33][34][35] The Graf method classifies the degree of coverage of the bony acetabular roof (alpha angle) and cartilaginous acetabular roof (beta angle).
For the meta-analysis, we considered that following the guidance provided by Graf, 36 a type IIA−hip was an indication for treatment.

Morin
In the Morin technique, 37 a coronal image of the flexed hip was evaluated to estimate the percentage of the femoral head that was medial to the lateral iliac margin (the "iliac line, " resembling the Graf "baseline") and consequently covered by the bony acetabulum. The studies analyzed used different classifications of normal test results. Therefore, each study was evaluated individually.

Suzuki
In the Suzuki technique, 14,38 the hips of the patient were maintained in abduction (in flexion or extension) and a long linear probe was positioned transversely over the lower pelvis in the region of the pubic bones. The purpose was to delineate the location of the femoral head. In the meta-analysis, we considered that a slight dislocation should not be classified as a normal test result and was an indication for treatment.

Stress test
For the ultrasound stress test, 43 the patient was placed in the lateral position, and a dynamic stress test was performed in the coronal plane, with the hip in flexion. For the meta-analysis, a lax hip was classified as abnormal.

Rosendahl
In the Rosendahl technique, 44 the patient was placed in the lateral position, the ultrasound probe was positioned laterally, and the physician performed a stress test (adjusted Barlow maneuver) with one hand while using the other hand to maintain the ultrasound probe in the correct position. In this meta-analysis, an elastic hip was classified as abnormal.

Selected studies
We conducted a systematic review of 494 studies. At the end of the selection process, 15 studies were deemed to meet the inclusion criteria and present acceptable quality, as determined using the Quality Assessment of Diagnostic Accuracy Studies 2 tool. Therefore, all 15 studies were included in the systematic review (Figure 1), as well as in the meta-analysis.

Analysis on the studies
In one study, there was a concern of bias in patient selection because the study sample included only male patients. Two other studies did not describe the patient-selection process. In two studies, the comparative technique was performed after the results of the Graf method were known, and in five studies, the order of application of the methodologies was not noted. In three studies, there were concerns regarding the application of the Graf method because only the alpha angle was evaluated. All the patients were younger than 12 months of age. In most studies, the Graf method and comparative technique were performed on the same day (Figures 2 and 3).  41,42 with the stress test in one study, 43 and with the Rosendahl technique in one study. 44 As shown in Table 1A, Gunay et al. 45    As detailed in Table 6, the Finnbogason technique was evaluated in two separate studies. 41,42 Collectively, the two studies showed that the technique had a sensitivity of 39.48% and specificity of 96.83% (P < 0.05), with an overall accuracy of 83.73%. Two studies evaluated a collective total of 1,186 hips.
Poul et al. 43 applied the stress test technique to the evaluation of 1,744 hips ( Table 7). The authors found that the technique had a sensitivity and specificity of 39.48% and 96.83%, respectively (P < 0.05), with an overall accuracy of 97.94%.    Table 9. The sensitivity and specificity data were also analyzed in forest plots (Figure 4), along with summary receiver operating characteristic curves (Figure 5).

DISCUSSION
In the studies selected for review, the Graf method was used as a reference for the diagnosis of DDH. Among the other analyzed techniques, the Morin technique had the highest sensitivity (81.12%) when the proportion of acetabular coverage of the femoral head was divided into two categories and 89.47% when it was divided into three categories, whereas the specificity was 83.95% and 82.70%, respectively. In terms of the