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J Orthop Surg Res
J Orthop Surg Res
Journal of Orthopaedic Surgery and Research
1749-799X
BioMed Central London

39261944
5070
10.1186/s13018-024-05070-7
Systematic Review
The prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip: a systematic review and meta-analysis
Xinling Miao 1
Qingsong Tang 2
Xiahui Li lixiahui@cdu.edu.cn

1
Yi Xu 786281997@qq.com

1
Kai Li 1
Liu Yang 1
Yuli Long 1
1 https://ror.org/034z67559 grid.411292.d 0000 0004 1798 8975 School of Nursing, Chengdu University, Chengdu, China
2 grid.54549.39 0000 0004 0369 4060 Chengdu Women’s and Children’s Central Hospital, School of Medicine, University of Electronic Science and Technology of China, Chengdu, 611731 China
11 9 2024
11 9 2024
2024
19 56031 7 2024
8 9 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Background

Transient synovitis of the hip is the most common cause of limping in paediatric emergency departments. There is no consensus regarding routine follow-up after hip synovitis among children, and there are no standardized criteria for selecting cases that warrant follow-up due to persistent or recurring symptoms to rule out the possibility of Legg-Calvé-Perthes disease. Delayed treatment of Legg-Calvé-Perthes disease may increase the risk of developing early secondary coxarthrosis. Understanding the prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip is of paramount importance and could empower both parents and paediatricians to make well-informed decisions when selecting follow-up care for children, thus ensuring that no cases of Legg-Calvé-Perthes disease are missed among diagnosis paediatric patients with transient synovitis of the hip. The aim of this review was to estimate the prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip.

Methods

This study was conducted in strict accordance with the PRISMA guidelines and was registered with PROSPERO. The PubMed, Embase, and Cochrane Library databases were comprehensively searched up to July 2024 to identify relevant studies. The inclusion criteria were as follows: patients diagnosed with transient synovitis of the hip; patients aged up to 18 years; and studies with a minimum of 10 cases of paediatric transient synovitis of the hip. To pool the prevalence rates from individual studies, we utilized a random-effects meta-analysis. To assess the quality of the included studies in detail, we employed the Joanna Briggs Institute’s quality assessment checklist.

Results

A total of 19 studies were ultimately included for the final analysis, with 2,617 paediatric cases of transient synovitis of the hip. The results of meta-analysis revealed that the pooled prevalence estimate of Legg-Calvé-Perthes disease among all paediatric patients with transient synovitis of the hip was 2.7% (95% CI 1.4–5.1). Significant heterogeneity was observed across the studies included in this analysis (I2 = 79.990%; P = 0.000). The pooled prevalence estimate of Legg-Calvé-Perthes disease among paediatric patients with recurrent or persistent transient synovitis of the hip was 36.3% (95% CI 21.6–54.2). Significant heterogeneity was also observed across the studies included in this analysis (I2 = 51.519%; P = 0.036). Furthermore, the follow-up period varied from 6 weeks to 24 months. The primary diagnostic imaging modality utilized for identifying Perthes disease was X-ray.

Conclusion

Our study revealed that among paediatric patients with transient synovitis of the hip, routine X-ray follow-up of the hips after 6 weeks to rule out Legg-Calvé-Perthes disease is warranted only in patients who exhibit persistent or recurrent symptoms.

Keywords

Legg-Calvé-Perthes disease
Paediatric
Transient synovitis of the hip
Systematic review
Meta-analysis
issue-copyright-statement© BioMed Central Ltd., part of Springer Nature 2024
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pmcIntroduction

Paediatric transient synovitis of the hip is a self-limiting, noninfectious inflammation of the synovial membrane, with an average annual incidence of approximately 0.2% in the general population [1]. The average age at onset of paediatric transient synovitis of the hip is six years, with a range between three and eight years [2]. The symptoms of this condition include hip pain, restricted movement, and a notable refusal to bear weight [3]. Treatment for paediatric transient synovitis of the hip primarily involves rest and the administration of anti-inflammatory agents [4], and it is generally considered a benign condition with a good prognosis, as it typically resolves within 2 weeks [5]. As the most common cause of limping in paediatric emergency departments [3], paediatric transient synovitis of the hip has attracted the attention of health care providers.

However, Legg-Calvé-Perthes disease is a relatively rare cause of limping in paediatric emergency departments. Early diagnosis is necessary due to the varying treatment options and prognoses, which depend on the duration of symptoms and the stage of the disease [6]. Delayed intervention can lead to an increased risk of developing early secondary coxarthrosis [7, 8]. The onset of symptoms among patients with Legg-Calvé-Perthes disease is often insidious and can lead to confusion as they may resemble the symptoms of paediatric transient synovitis of the hip [8].Current recommendations in Belgium suggest conducting a control X-ray of the pelvis six weeks after an episode of paediatric transient synovitis of the hip to rule out the possibility of Legg-Calvé-Perthes disease [6]. Furthermore, Lenoir et al. [9] demonstrated that among the children who remained symptom-free following an episode of transient synovitis, none were subsequently diagnosed with Legg-Calvé-Perthes disease. A follow-up X-ray to rule out Legg-Calvé-Perthes disease after a diagnosis of transient hip synovitis seems necessary only for patients exhibiting persistent or recurrent symptoms. Currently, there is no consensus regarding routine follow-up after hip synovitis or the criteria for selecting patients who warrant follow-up due to persistent or recurring symptoms. Importantly, potential overtreatment can not only be harmful to patients but also places an unnecessary financial strain on the health care system.

Understanding the authentic the prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip is of paramount importance and could empower both parents and paediatricians to make well-informed decisions when selecting follow-up care for children, ensuring that no cases Legg-Calvé-Perthes disease are missed among children with transient synovitis of the hip. Generally, the reported prevalence of Legg-Calvé-Perthes disease among children with paediatric transient synovitis of the hip varies significantly across studies, ranging from 0 to 38% [3, 10–12]. Furthermore, the exact prevalence of Legg-Calvé-Perthes disease in cases of paediatric recurrent or persistent transient synovitis has yet to be determined.Based on the study by Keenan et al. [11], this systematic review defines recurrence of symptoms as the reappearance of symptoms within one month following their initial resolution, whereas persistence is characterized by symptoms that endure for more than one month.The objective of this review is to undertake a comprehensive analysis of existing literature on the prevalence of Legg-Calvé-Perthes disease among children with transient synovitis of the hip by employing both qualitative and quantitative methodologies.

Methods

Research design and method

This study was performed in strict accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. The systematic approach employed for searching, assessing eligibility, evaluating quality, extracting data, and analysing results was executed with precision in accordance with a crafted protocol. Furthermore, the study protocol was officially registered with the International Prospective Register of Systematic Reviews (PROSPERO) prior to the initiation of data extraction, ensuring transparency and rigor in our methodology (Registration CRD42024570712).

Data source and selection process

The PubMed, Embase, and Cochrane Library databases were searched in July 2024. The search strategy employed a combination of MeSH terms and keywords, specifically targeting the following phrases: “transient synovitis” or “coxitis fugax” or “irritable hip” and “child” or “infant” or “newborn” or “pediatric”. Additionally, to ensure that relevant studies were included, the reference lists of the selected eligible studies were reviewed to identify additional eligible studies.

Eligibility criteria and study selection

In this comprehensive review, we included studies that met the following stringent criteria: (i) the participants were children, were diagnosed with transient synovitis of the hip, aged up to 18 years, with a minimum of 10 cases reported of paediatric transient synovitis of the hip; (ii) the study either directly reported the prevalence of Legg-Calvé-Perthes disease among these paediatric cases of transient synovitis of the hip or provided adequate data to enable the calculation of this prevalence; and (iii) the study was published in English. We excluded reviews, commentaries, case reports, and studies involving animal subjects. Furthermore, letters to the editor, conference papers, books, editorials, and notes were not considered in our analysis.

Methods for data extraction and quality assessment

Two independent authors diligently extracted relevant data from the chosen studies. The following data were extracted from each study: the name of the first author(s), the total sample size, the year of publication, follow-up duration, diagnostic imaging modalities for Legg-Calvé-Perthes disease, as well as the sample size and prevalence estimates of persistent or recurrent symptoms.

All the search results were aggregated and subsequently subjected to an independent eligibility screening by two of the authors. In cases of disagreement, a third author intervened to mediate and resolve conflicts during a meeting with the screening authors. This resolution process involved attentively listening to the arguments presented and fostering discussions until a consensus was reached. The screening process entailed a thorough review of the abstracts for each result. After the initial screening and removal of duplicates, the studies identified as potentially relevant underwent a comprehensive full-text review to determine their eligibility for inclusion.

To evaluate the quality of the studies included in our final analysis, we utilized the Joanna Briggs Institute Quality Assessment Tool. This comprehensive tool assesses individual studies through a frequency scale, where responses are classified as “yes”, “no”, “not clear” or “not applicable”. The overall quality score for each study was carefully computed by aggregating the number of affirmative responses, thus ensuring a thorough evaluation process.

Data synthesis and analysis

In this study, all the statistical analyses were conducted via Comprehensive Meta-Analysis Software, version 3.0. The prevalence rates obtained from the individual studies were combined via a random-effects meta-analysis model [13]. To assess the degree of heterogeneity among the studies, the I2 statistic was utilized. The interpretation of the I2 values is as follows: a value of 75% indicates high heterogeneity, 50% signifies moderate heterogeneity, and 25% denotes low heterogeneity [14]. To further investigate the potential sources of heterogeneity among the studies included in our analysis, we conducted sensitivity analysis via the leave-one-out method. To assess the risk of publication bias, we utilized Egger’s regression tests alongside funnel plots. In all our statistical analyses, we adhered to a P value threshold of 0.05 to determine statistical significance.

Results

Identification of relevant studies

The literature search initially yielded a total of 972 studies. We excluded 258 duplicates. Then, 657 records were excluded after title and abstract screening—including 321 based on their titles and 336 based on their abstracts—as they failed to meet our stringent inclusion criteria. Therefore, a total of 57 publications were included for full-text screening. Ultimately, 19 of these publications were deemed appropriate and qualified for inclusion in our current systematic review and meta-analysis (Fig. 1).Fig. 1 PRISMA flowchart of the review search

Characteristics of the included studies

The fundamental attributes of the studies included in this systematic review and meta-analysis are delineated in Table 1. A total of 19 articles [1, 3, 6, 9–12, 15–26] were included in the final analysis, collectively encompassing 2617 cases of paediatric transient synovitis of the hip. The included studies reviewed were published over an extensive period, spanning from 1956 to 2021. The sample sizes of these studies varied significantly, ranging from as few as 13 paediatric cases to as many as 383. Furthermore, the follow-up period varied from 6 weeks to 24 months. A total of 11 articles [1, 3, 6, 9, 11, 15, 17, 22, 23, 25, 26] were included in the symptom analysis, accounting for 100 cases of paediatric transient synovitis of the hip. The primary diagnostic imaging modality utilized for identifying Legg-Calvé-Perthes disease was X-ray.Table 1 Baseline characteristics of included studies

Study name	Total	Follow-up time	Symptom (persistenc or recurrence)	Diagnostic imaging modalities (Perthes disease)	
Sample size	Prevalence, cases (n)	Sample size	Prevalence, cases (n)	
Caravias DE 1956	48	2.1%, 1	18 months	–	X-ray	
Jacobs BW 1960	25	12%, 3	18 months	7	42.9%, 3	X-ray	
Jacobs B W 1971	62	16.9%, 11	7 months	18	61.1%, 11	X-ray	
Calver R 1981	50	10.0%, 5	6 months	–	99mTc radionuclide and X	
Sharwood PF 1981	101	1.0%, 1	6 months	12	8.3%, 1	X-ray	
Mukamel M 1985	41	2.4%, 1	4 months	1	100%, 1	X-ray	
Haueisen DC 1986	118	2.5%, 3	6 months	–	X-ray	
Egund N 1987	49	2.0%, 1	6.5 (5–9) months	–	CT	
Landin LA 1987	258	3.9%, 10	5 months	9	100%, 9	X-ray	
Hasegawa Y 1988	55	1.8%, 1	4–9 months	–	99mTc-MDP	
Briggs RD 1990	286	0.3%, 1	–	–	X-ray	
Gopakumar TS 1992	181	2.2%, 4	7 (6–24) months	–	99mTc-MDP and X-ray	
Taylor GR 1995	358	0.3%, 1	–	4	25%, 1	Isotope scans and MRI	
Keenan WN 1996	13	38.5%, 5	3 months	13	38.5%, 5	X-ray	
Fischer SU 1999	65	1.5%, 1	18–21 months	–	X-ray	
Dubois-Ferrière V 2015	383	0.3%, 1	6 weeks	1	100%, 1	X-ray	
Lenoir U 2017	198	2%, 4	3 months	20	20%, 4	X-ray	
Lázaro Carreño MI 2018	84	1.2%, 1	6 months	3	33.3%, 1	X-ray	
Heylen CE 2021	242	1.2%, 3	6 weeks	12	25%, 3	X-ray	

Quality of the included studies

Table 2 presents a detailed analysis of the quality and potential biases inherent among the included studies. Notably, 18 studies, representing 94.7% of the total, utilized an adequate sample frame to accurately determine the prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip. Furthermore, approximately ten studies, accounting for 52.6% of the total, received positive evaluations concerning their response rates. Based on the Joanna Briggs Institute’s quality evaluation checklist, the articles selected for the final analysis presented a mean quality score of 7.2, with scores for individual articles ranging from five to nine. Notably, nine studies, constituting 47.4% of the total, were classified as high-quality, each achieving a score of 7.2 or above. The remaining articles, which had scores ranging from 5 to 7.2, were deemed to be of fair quality.Table 2 Qualities of included studies (7.2)

Study name	Response	
Q1	Q2	Q3	Q4	Q5	Q6	Q7	Q8	Q9	Total	
Caravias DE 1956	Y	Y	N	Y	Y	Y	Y	N	U	6	
Jacobs BW 1960	Y	N	N	Y	Y	Y	Y	Y	U	6	
Jacobs B W 1971	Y	Y	N	Y	Y	Y	Y	Y	U	7	
Calver R 1981	Y	Y	N	Y	Y	Y	Y	Y	U	7	
Sharwood PF 1981	Y	Y	Y	Y	Y	Y	Y	N	Y	8	
Mukamel M 1985	Y	N	N	Y	Y	Y	Y	N	U	5	
Haueisen DC 1986	Y	Y	Y	Y	Y	Y	Y	Y	Y	9	
Egund N 1987	Y	N	N	Y	Y	Y	Y	N	U	5	
Landin LA 1987	Y	Y	Y	Y	Y	Y	Y	Y	Y	9	
Hasegawa Y 1988	Y	Y	N	Y	Y	Y	Y	N	U	6	
Briggs RD 1990	Y	Y	Y	Y	Y	Y	Y	N	Y	8	
Gopakumar TS 1992	Y	Y	Y	Y	Y	Y	Y	Y	Y	9	
Taylor GR 1995	Y	Y	Y	Y	Y	Y	Y	N	Y	8	
Keenan WN 1996	N	N	N	Y	Y	Y	Y	Y	U	5	
Fischer SU 1999	Y	Y	N	Y	Y	Y	Y	N	Y	7	
Dubois-Ferrière V 2015	Y	Y	Y	Y	Y	Y	Y	N	Y	8	
Lenoir U 2017	Y	Y	Y	Y	Y	Y	Y	Y	Y	9	
Lázaro Carreño MI 2018	Y	Y	N	Y	Y	Y	Y	N	U	6	
Heylen CE 2021	Y	Y	Y	Y	Y	Y	Y	Y	Y	9	
Keys:

Q1–Q9 represents questions used to assess the quality of included studies, which are listed below

Q1. Was the sample frame appropriate to address the target populations?

Q2. Were the study participants sampled appropriately?

Q3. Was the sample size adequate?

Q4. Were the study subjects and setting described in detail?

Q5. Was the data analysis conducted with suffcient coverage of the identifed sample?

Q6. Was a valid method used in the identification of conditions?

Q7. Was the condition measured in a standard, reliable way for all participants?

Q8. Was there an appropriate statistical analysis?

Q9. Was the response rate adequate, and if not, was the low response rate managed appropriately?

	
Y, Yes; N, No; U, Unclear; NA, Not applicable

The prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip (meta-analysis)

The pooled prevalence estimate of Legg-Calvé-Perthes disease among all paediatric patients with transient synovitis of the hip was 2.7% (95% CI 1.4–5.1). Significant heterogeneity was observed across the studies included in this analysis (I2 = 79.990%; P = 0.000) (Fig. 2). Furthermore, the pooled prevalence estimate of Legg-Calvé-Perthes disease among paediatric patients with recurrent or persistent transient synovitis of the hip was 36.3% (95% CI 21.6–54.2). Significant heterogeneity was also observed across the studies included in this analysis (I2 = 51.519%; P = 0.036) (Fig. 3).Fig. 2 The prevalence of Legg-Calvé-Perthes disease among all paediatric patients with transient synovitis of the hip: A random effects meta-analysis (I2 = 79.990%; P = 0.000; based on a random effects model)

Fig. 3 The prevalence of Legg-Calvé-Perthes disease among paediatric patients with recurrent or persistent transient synovitis of the hip: a random effects meta-analysis (I2 = 51.519%; P = 0.036; based on a random effects model)

Sensitivity analysis

To further investigate the potential sources of heterogeneity among the studies included in our analysis, we conducted sensitivity analysis via the leave-one-out method. The results of sensitivity analysis revealed that the primary findings were robust and were not unduly influenced by any single study. Upon systematically excluding each study one at a time, the pooled estimated prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip varied from 2.3 (95% CI 1.3–4.2) to 3.0% (95% CI 1.6–5.6). Moreover, the pooled estimated prevalence of Legg-Calvé-Perthes disease among paediatric patients with recurrent or persistent transient synovitis of the hip ranged from 31.3 (95% CI 18.0–48.5) to 40.0% (95% CI 24.7–57.6). These findings affirm the stability and robustness of our results.

Publication bias

In our comprehensive systematic review and meta-analysis, we revealed no indications of potential publication bias concerning the prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip and the prevalence of Legg-Calvé-Perthes disease among paediatric patients with recurrent or persistent transient synovitis of the hip. These conclusions are substantiated by the symmetrical appearance of the funnel plots and corroborated by the results of regression tests associated with the funnel plot analyses (Egger’s test) for all paediatric patients with transient synovitis of the hip (B = 1.08, SE = -3.12, P = 0.005) (Fig. 4) and paediatric patients with recurrent or persistent transient synovitis of the hip (B = 1.51, SE = − 0.07, P = 0.481) (Fig. 5).Fig. 4 Funnel plot of the risk of publication bias for the prevalence of Legg-Calvé-Perthes disease among all paediatric patients with transient synovitis of the hip

Fig. 5 Funnel plot of the risk of publication bias for the prevalence of Legg-Calvé-Perthes disease among paediatric patients with recurrent or persistent transient synovitis of the hip

Discussion

Key findings

Our review included 19 studies that investigated the prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip. Our qualitative and quantitative analyses revealed that the existing scientific evidence on the prevalence of Legg-Calvé-Perthes disease among paediatric patients with transient synovitis of the hip exhibits substantial variability depending on whether the patient experiences recurrent or persistent transient synovitis.

Our comprehensive meta-analysis revealed that the pooled prevalence estimate of Legg-Calvé-Perthes disease among all paediatric patients with transient synovitis of the hip was 2.7%. However. the pooled estimated prevalence of Legg-Calvé-Perthes disease among paediatric patients with recurrent or persistent transient synovitis of the hip was 31.3%. The primary diagnostic imaging modality utilized for identifying Legg-Calvé-Perthes disease was X-ray. The follow-up period varied from 6 weeks to 24 months. This study indicates that for paediatric patients with transient synovitis of the hip, a follow-up X-ray to rule out Legg-Calvé-Perthes disease is necessary only for patients who exhibit persistent or recurrent symptoms.

Comparisons with the existing evidence

The current study’s prevalence estimates for Legg-Calvé-Perthes disease among all paediatric transient synovitis of the hip stand at 2.7%. This finding is similar to the conclusions previously reported by certain scholars. Gopakumar et al. [18] reported that four patients (2.2%) were diagnosed with Legg-Calvé-Perthes disease following an initial presentation of irritable hip syndrome. Similarly, Lenoir et al. [9] reported that 4 patients (2%) were identified as having Legg-Calvé-Perthes disease. Notably, all children who remained symptom-free after experiencing transient synovitis, and who were followed for at least three months had negative results on follow-up X-rays. These findings indicate that the resolution of symptoms following an episode of transient synovitis of the hip is a highly reliable indicator for ruling out Legg-Calvé-Perthes disease. Therefore, routine follow-up is not recommended for all children presenting with hip synovitis.

However, the current study revealed that the prevalence of Legg-Calvé-Perthes disease among children who experienced recurrent or persistent transient synovitis of the hip was 31.3%. Similarly, Keenan et al. [11] reported that 38.5% of patients initially diagnosed with either prolonged or recurrent transient synovitis of the hip eventually progressed to Legg-Calvé-Perthes disease. This significant finding underscores the critical importance of routine follow-ups for all children presenting with recurrent or persistent transient synovitis of the hip, thus ensuring timely diagnosis and appropriate management of Legg-Calvé-Perthes disease.

Strengths and limitations

The present study has several strengths. First, this systematic review and meta-analysis aims to determine the prevalence of Legg-Calvé-Perthes disease among paediatric patient with transient synovitis of the hip. By consolidating existing research, thus study provided a foundational understanding of this medical phenomenon. Second, this study estimated the prevalence rates of Legg-Calvé-Perthes disease among children experiencing recurrent or persistent transient synovitis of the hip. This approach allowed for a more detailed and accurate assessment of the condition across different patient demographics. Thirdly, the study incorporated sensitivity analyses to identify and mitigate potential biases, thus ensuring the reliability and validity of the findings. These methodological strengths collectively enhance the study’s contribution to the field of paediatric orthopaedics, offering valuable insights for clinicians and researchers alike.

Several limitations inherent in this systematic review and meta-analysis warrant careful consideration. Firstly, the majority of the included studies had relatively small sample sizes. This limitation raises concerns that the reported prevalence of Legg-Calvé-Perthes disease among children experiencing recurrent or persistent transient synovitis of the hip in our current analysis may not accurately reflect the true prevalence in the broader population. Secondly, our review exclusively included studies published in the English language. Consequently, relevant studies conducted in other languages may have been overlooked, potentially introducing language bias into our findings.

The implications of the findings

The present study has significant research and clinical implications. First, future studies include larger sample sizes of children with recurrent or persistent transient synovitis of the hip to gain a more comprehensive understanding of Legg-Calvé-Perthes disease. Additionally, it is crucial for future studies on recurrent or persistent transient synovitis of the hip to establish specific intervals for follow-up assessments, ensuring timely diagnosis and appropriate management. Finally, future research should explore early diagnostic imaging modalities for Legg-Calvé-Perthes disease, including X-ray, ultrasound, CT, and MRI.

Conclusion

Our research demonstrated that for paediatric transient synovitis of the hip, routine X-ray follow-up of the hips after 6 weeks to rule out Legg-Calvé-Perthes disease is warranted only in patients who exhibit persistent or recurrent symptoms.

Acknowledgements

The authors thank Dr Ren Xiang from Chengdu Women’s and Children’s Central Hospital for the guidance on the development of this article.

Authors’ contributions

Miaoxinling and Tang qingsong equally to this work as co-first authors.Lixiahui and Xu yi equally to this work as co-corresponding authors.Miao XL conceptualized the study, performed the search conducted analyses, conducted the quality assessment, write-up and approval of the final manuscript. Tang QS was involved in data extraction, read and approved the final manuscript. Li XH, Xu Y, Li K, Yang L, and L YL was participated in discussion and consensus and approved the final manuscript. All authors read and approved the final manuscript.

Funding

The authors declare that there is no funding.

Availability of data and materials

No datasets were generated or analysed during the current study. All data generated or analysed during this study are included in this article.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Miao Xinling and Tang Qingsong have contributed equally to this work as co-first authors.
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