Comparative analysis of hip joint development abnormalities and risk factors in preterm and term infants

Abstract

Objective

To investigate the risk factors affecting hip joint development in infants and to compare abnormalities in hip joint development between preterm and term infants.

Methods

This retrospective cohort study reviewed the medical records of newborns admitted to the neonatology department of our hospital between January 2019 and January 2020. Hip joint ultrasound screening and follow-up data were collected for each newborn. The enrolled newborns were categorized into two groups: preterm (<37 weeks) and term (≥37 weeks). Hip joint ultrasounds were assessed using the Graf classification criteria.

Results

A total of 955 newborns were included in the study, comprising 393 preterm and 562 term infants. All preterm infants were born at a gestational age over 28 weeks. Among term infants, the proportion of abnormal hip joints during the first and second screenings was significantly higher in singletons than twins (p < 0.05), in non-small for gestational age (non-SGA) infants than SGA infants (p < 0.05), and in females than males (p < 0.0001). By the third screening, the proportion of abnormal hip joints remained significantly higher in females than in males (p < 0.01). In newborns with birth weight percentiles above the 50th percentile (P50), term infants showed a significantly higher proportion of abnormal hip joints than preterm infants during the first screening (P50–P75: 32.1 vs. 15.8%, P75–P90: 36.0 vs. 16.7%, p < 0.01; >P90: 32.1 vs. 15.8%, p < 0.05). During the second screening, term infants in the P50–P75 and P75–P90 percentiles exhibited abnormal hip joint proportions of 27.6 and 34.8%, respectively, which were significantly higher than those in preterm infants (13.9%, p < 0.05; 12.1%, p < 0.01). By the third screening, the proportion of abnormal hip joints in term infants within the P75-P90 percentile was 11.2%, which was significantly higher than that of preterm infants (1.5%, p < 0.05). Overall, preterm infants demonstrated a significantly lower proportion of abnormal hip joints compared to term infants across all four screening time points. By the fourth screening, all abnormal hips in preterm infants had evolved into normal ones according to Graf classification criteria. In contrast, although most abnormal hips in term infants had also resolved, with only 6 of them persisted.

Conclusion

Term singletons, female, and non-SGA infants demonstrated a higher proportion of abnormal hip joints during the early postnatal period. Among neonates born after 28 weeks of gestation, there is no difference in hip development between preterm infants with a birth weight percentile <P50 and term infants. Most abnormal hip joints in both preterm and term infants are due to physiological immaturity and tend to resolve by themselves as natural growth and development. The timing of hip ultrasound screening for preterm infants born after 28 weeks of gestation may not require correction for gestational age.

Introduction

Developmental Dysplasia of the Hip (DDH) refers to structural abnormalities of the hip joint present at birth, encompassing a spectrum of conditions ranging from hip immaturity to complete hip dislocation [1, 2]. With the widespread adoption of hip ultrasound screening, the definition of DDH has been broadened to include a variety of conditions, such as immature hips, hips with mild acetabular dysplasia, unstable hips, subluxated hips, and fully dislocated hips [3]. The prevalence of DDH ranges from 0.06 to 76.1‰, with significant variation across regions and populations [4]. The prevalence might also be potentially attributable to differences in screening methods [5,6,7]. It was reported in a meta-analysis study that the overall estimated prevalence of DDH to be approximately 14.0‰ [8]. Without timely diagnosis and intervention, DDH can lead to joint pain, functional impairments, and early joint degeneration, ultimately impacting an individual’s mobility and quality of life [9]. Therefore, early diagnosis and intervention are critical for improving the prognosis of patients with DDH [10].

In recent years, there has been a growing number of researches on the risk factors for DDH. Currently, the most widely recognized risk factors include a history of breech delivery, female sex, firstborn status, and a family history of DDH [11,12,13]. However, consensus has yet to be reached regarding certain potential risk factors, such as preterm birth and birth weight. Some evidence suggests that preterm birth may be associated with an increased risk of DDH [14, 15]. On the contrary, other studies have found no significant association between preterm birth and DDH [16, 17]. Similarly, Hanratty et al. [18] reported no correlation between birth weight and DDH risk. While Sewell et al. [14] identified macrosomia as a significant risk factor for DDH, emphasizing the importance of targeted screening for these infants. These discrepancies underscore the need for further research to clarify the risk factors associated with DDH.

Furthermore, the early natural progression of hip joint development over time in preterm infants compared to term infants deserves closer attention. Gaining a deeper understanding of the natural history of neonatal hip development can help inform the design of more precise screening strategies and targeted intervention measures.

To address the aforementioned issues, this study aims to review the hip ultrasound screening data of neonates in our hospital, investigate the risk factors affecting neonatal hip development, and compare the abnormalities in hip development between preterm and term infants. Furthermore, we examine the early developmental progression of the hip joint in both preterm and term infants, with the goal of providing more scientifically grounded guidance for the early screening of DDH.

Methods and materials

Study design

This study is a retrospective study. By reviewing medical records from the neonatal department of our hospital between January 2019 and January 2020, we gathered data on hip ultrasound screenings and corresponding follow-up information for each newborn.

Study population

Inclusion Criteria: (1) Preterm and term neonates admitted to the neonatal department of our hospital during the same period after birth; (2) Guardians provided informed consent for participation in ultrasound screening and demonstrated compliance in completing all four scheduled hip ultrasound screenings (at 1, 7, 42, and 90 days after birth).

Exclusion Criteria: (1) Presence of other congenital abnormalities, such as torticollis, clubfoot, spinal deformities, or meningomyelocele; (2) Conditions that may interfere with hip joint development, such as arthrogryposis, hypoxic-ischemic encephalopathy, or intracranial hemorrhage; (3) Extremely preterm infants with unstable vital signs, for whom initial hip examinations may pose potential risks.

Data collection

The collected data included the newborn’s gender, birth weight, gestational age at birth, singleton or twin status, parity, family history of DDH, fetal position at birth, mode of delivery, and the results from four scheduled hip ultrasound screenings (conducted on days 1, 7, 42, and 90 after birth). The SIUI Color Doppler Ultrasound Diagnostic System (model Apogee 3100) with a 7.5–10 MHz linear probe was used for all examinations. Each screening was independently performed by two professionally trained pediatric orthopedic attending physicians, and the final hip joint classification was determined through a comprehensive review of their findings (Fig. 1).

Fig. 1

Images of Type I and Type IIa hips in preterm infants during the four screening sessions. A shows the Type I hip in a preterm infant on the first day after birth. B and C demonstrates the screenings at 7 and 42 days, respectively. D shows the 90-day screening, where the hip remains as Type I. E shows the Type IIa hip in a preterm infant on the first day after birth. F and G demonstrates the screenings at 7 and 42 days, respectively. H shows the 90-day screening, where the hip has transitioned to Type I

Study groups

Based on the definition of preterm birth, the enrolled newborns were categorized into two groups: the preterm group (<37 weeks) and the term group (≥37 weeks) [19]. For further stratified analysis, the birth weights of both preterm and term newborns were classified into six groups according to the Standards for Growth Assessment of Newborns at Different Gestational Ages (a health industry standard of the People’s Republic of China, which could be traced online: http://www.nhc.gov.cn/wjw/fyjk/202208/d6dcc281e9b74db88dc972b34cbd3ec7.shtml): <P10 (infants with birth weight percentiles less than 10th percentile), P10–P25, P25–P50, P50–P75, P75–P90, and >P90. Among these, infants classified as <P10 was defined as small for gestational age (SGA), while those ≥P10 was classified as non-SGA [20].

Hip joint ultrasound classification

The classification criteria for hip ultrasound using the Graf method are as follows: Type I is defined as normal hip joints. Types IIa+, IIa−, and IIb indicate immature hips, where: Type IIa refers to those <6 weeks of age, Types IIa+ and IIa− apply to 6–12 weeks, and Type IIb corresponds to >12 weeks. Type IIc indicates hip dysplasia. Types D, III, and IV represent hip dislocation [21, 22]. In this study, Type I was defined as a normal hip joint, while Type II and above were classified as abnormal. If ultrasound examination revealed abnormalities in both hips, the side with the more severe abnormality was used to determine the classification diagnosis for the study subject.

Statistical analysis

Data analysis was performed using SPSS 25.0 software. Normally distributed measurement data were expressed as mean ± standard deviation (x̄ ± s). Categorical data were presented as frequencies and percentages [n (%)]. For comparisons between groups, chi-squared tests, Fisher’s exact tests, or continuity correction tests were used for categorical variables. A significance level of α = 0.05 was applied, with p < 0.05 considered statistically significant. GraphPad Prism statistical software (Version 8, GraphPad Software, LLC) was used for graphical plotting.

Results

A total of 955 newborns were included in this study, comprising 393 preterm infants (41.2%) and 562 term infants (58.8%) (Fig. 2). Among the preterm infants, the youngest gestational age was 28 weeks and 1 day. There were no cases of extremely preterm infants (<28 weeks), while 32 were classified as very preterm (28–31 weeks), 64 as moderate preterm (32–33 weeks), and 297 as late preterm (34–36 weeks), respectively. None of the newborns had a family history of DDH or were impacted by lifestyle factors such as improper swaddling. The average gestational age for preterm infants was 34.3 ± 1.9 weeks, with an average birth weight of 2357.9 ± 537.3 g. For term infants, the average gestational age was 39.0 ± 1.1 weeks, and the average birth weight was 3369.0 ± 503.2 g. Among term infants, twins had an average gestational age of 37.3 ± 0.6 weeks, with an average birth weight of 2403.0 ± 452.6 g, while singletons had an average gestational age of 39.0 ± 1.1 weeks, with an average birth weight of 3390.0 ± 483.5 g. In terms of parity, the proportion of primiparas was higher in the term infant group (68.5%). Additional details are provided in Table 1.

Fig. 2

Flowchart of subjects’ inclusion of this study. Between January 2019 and January 2020, a total of 1,064 newborns were admitted to the neonatology department. Of these, 27 were excluded due to guardians not consenting to hip joint ultrasound screening, 34 had other associated deformities or diseases, and 48 were lost to follow-up. Ultimately, 955 newborns were included in the study, comprising 393 preterm infants and 562 term infants

Table 1 General Information of Preterm and term Infants Included in the Study

In the comparisons of singleton/twin status, SGA/non-SGA, sex, parity, delivery mode, and fetal position at birth, no statistically significant differences were observed in the results of the four hip ultrasound screenings among preterm infants (Table 2). For term infants, the proportion of abnormal hips was significantly higher in singletons than twins (p < 0.05), in non-SGA infants than SGA infants (p < 0.05), and in females than males (p < 0.0001) during the first and second screenings. During the third screening, females continued to exhibit a higher proportion of abnormal hips compared to males (p < 0.01) (Table 3).

Table 2 Risk factor analysis of abnormal hip rates in four hip screenings among preterm infants

Table 3 Risk factor analysis of abnormal hip rates in four hip screenings among term infants

Among preterm and term infants with birth weight percentiles greater than P50, the proportions of abnormal hips during the first screening in term infants were 32.1% for P50–P75, 36.0% for P75–P90, and 32.1% for those over P90, respectively. These rates were significantly higher than those observed in preterm infants (15.8, 16.7, and 15.8%, respectively; p < 0.01). During the second screening, the rates of abnormal hips in term infants were 27.6% for P50-P75 and 34.8% for P75-P90, both significantly higher than those in preterm infants (13.9%, p < 0.05; 12.1%, p < 0.01). In the third screening, term infants with P75–P90 showed an abnormal hip proportion of 11.2%, which was significantly higher than the 1.5% observed in preterm infants (p < 0.05). By the fourth screening, no significant differences in abnormal hip proportions were found between preterm and term infants across all birth weight percentiles (Fig. 3).

Fig. 3

The Comparison of Hip Joint Ultrasound Screening Results Between Preterm and Term Infants with Different Birth Weight Percentiles. A During the first screening, the proportion of abnormal hip joints was significantly higher in term infants compared to preterm infants (P50–P75: 32.1 vs. 15.8%, P75–P90: 36.0 vs. 16.7%, p < 0.01; >P90: 32.1 vs. 15.8%, p < 0.05). B In the second screening, the proportions of abnormal hip joints in term infants with P50–P75 and P75–P90 were 27.6 and 34.8%, respectively, significantly exceeding those in preterm infants (13.9%, p < 0.05; 12.1%, p < 0.01). C For the third screening, term infants with P75–P90 had a significantly higher rate of abnormal hip joints at 11.2%, compared to 1.5% in preterm infants (p < 0.05). D By the fourth screening, there was no significant difference in the proportion of abnormal hip joints between preterm and term infants across different birth weight percentiles. ^*: p < 0.05, ^**: p < 0.01, chi-squared test

The first screening results using the Graf method showed that in the preterm group, 318 infants (80.9%) had normal hips, while 75 infants (19.1%) had abnormal hips. Among the abnormal cases, 74 (18.8%) were classified as type IIa and 1 (0.3%) as type IIc, with no other abnormal hip types identified. In the term group, 384 infants (68.3%) had normal hips, while 178 infants (31.7%) had abnormal hips. Among these, 173 (30.8%) were classified as type IIa, 4 (0.7%) as type IIc, and 1 (0.2%) as type D, with no other abnormal types identified. The difference between the two groups was statistically significant (p < 0.0001).

For the second screening using the Graf method, 329 infants (83.7%) in the preterm group had normal hips, while 64 infants (16.3%) had abnormal hips. Among the abnormal cases, 63 (16.0%) were classified as type IIa and 1 (0.3%) as type IIc, with no other abnormal types identified. In the term group, 404 infants (71.9%) had normal hips, while 158 infants (28.1%) had abnormal hips. Of these, 153 (27.2%) were classified as type IIa, 4 (0.7%) as type IIc, and 1 (0.2%) as type D, with no other abnormal types identified. The difference between the two groups remained statistically significant (p < 0.0001).

During the third screening, 383 infants (97.5%) in the preterm group were found to have normal hips, while 10 infants (2.5%) had abnormal hips, all of which were classified as type IIa(+). In the term group, 527 infants (93.8%) had normal hips, while 35 infants (6.2%) had abnormal hips. Among these, 31 (5.5%) were classified as type IIa(+), 3 (0.5%) as type IIa(−), and 1 (0.2%) as type D, with no other abnormal types identified. The difference between the two groups was statistically significant (p < 0.01).

By the fourth screening, all 393 infants (100%) in the preterm group had normal hips, with no abnormal hips detected. In the term group, 556 infants (98.9%) had normal hips, while 6 infants (1.1%) had abnormal hips. Among these, 5 (0.9%) were classified as type IIb and 1 (0.2%) as type D. The difference between the two groups was statistically significant (p < 0.05) (Fig. 4). All these six infants received Pavlik harness treatment after the fourth screening.

Fig. 4

The Comparison of Hip Joint Ultrasound Screening Results Between Preterm and Term Infants Across Four Screenings. A The first screening results showed that the abnormality rates of hip joints in preterm infants (19.1%) were significantly lower than those in term infants (31.7%) (p < 0.0001). B The second screening results indicated that preterm infants (16.3%) continued to have significantly lower abnormality rates compared to term infants (28.1%) (p < 0.0001). C In the third screening, the abnormality rates in preterm infants (2.5%) remained significantly lower than in term infants (6.2%) (p < 0.01). D By the fourth screening, the rates of hip joint abnormalities in preterm infants (0%) were still significantly lower than those in term infants (1.1%) (p < 0.05). ^*: p < 0.05, ^**: p < 0.01, ^****: p < 0.0001, chi-squared test

Discussion

Our study revealed that the abnormal rates observed in all four hip ultrasound screenings were significantly lower in preterm infants compared to term infants. This finding suggests that preterm birth may not be a risk factor for DDH, aligning with the results reported by Ghaseminejad-Raeini et al. and Chan et al. [17, 23]. Although the mechanisms by which preterm birth influences hip development remain unclear, several hypotheses have been proposed. Koob et al. [24] suggested that during early and mid-pregnancy, the fetus has sufficient space within the uterine cavity. However, in late pregnancy, as fetal growth accelerates, the uterus may not expand quickly enough to accommodate this growth, resulting in restricted fetal movement, which could negatively affect hip development. Ishikawa et al. [25] proposed that elevated maternal hormone levels during pregnancy could increase hormone levels in the fetus, with some hormones potentially causing relaxation of fetal muscles and ligaments. Preterm birth may interrupt prolonged exposure to these maternal hormones, thereby promoting better hip development. However, this potential protective effect requires further investigation.

Among term infants, we found that the rate of abnormal hip screening results was significantly higher in singletons compared to twins. This observation aligns with the findings of Doyle et al. and De Pellegrin et al. [26, 27]. Czubak et al. proposed that the limited intrauterine space in twin pregnancies should not be regarded as a risk factor for DDH, as the restricted space can be compensated by reduced fetal growth [28]. Indeed, our data showed that term twins had significantly lower gestational ages and birth weights compared to singletons. This relatively shorter duration of exposure to mechanical stress in utero may explain why twins have a lower rate of hip abnormalities than singletons.

Apart from the singleton/twins factor, we also found that term females exhibited a higher rate of hip abnormalities, which aligns with known risk factors for DDH [11, 29]. Higher estrogen levels in females may contribute to pelvic and ligament laxity, potentially explaining the higher prevalence of abnormal hips in females compared to males [30]. Similarly, Bakti et al. [31] reported comparable findings, suggesting that being female not only serves as a risk factor for DDH but may also play a role in slowing the natural resolution of abnormal hips.

Additionally, we found that term infants classified as SGA had a lower rate of hip abnormalities. Previous studies have reported an association between DDH and higher birth weight [32, 33]. Our further analysis revealed that term infants with a birth weight percentile >P50 showed a higher proportion of abnormal hips in early life compared to preterm infants. However, among neonates born after 28 weeks of gestation, there was no significant difference in the proportion of abnormal hips across the four screening sessions between preterm infants with a birth weight percentile <P50 and their term counterparts.

Our study provides certain clinical significance, specifically: (1) Among neonates born after 28 weeks of gestation, there is no difference in hip development between preterm infants with a birth weight percentile <P50 and term infants; (2) For preterm infants born after 28 weeks of gestation, hip ultrasound screening can be performed at the same time as for term infants, without the need to adjust for corrected gestational age. Graf identified two key time points for early hip ultrasound screening: within the first 2 weeks of life and at 6–8 weeks of age, though no specific recommendations were made for preterm infants [34]. Previous research has shown that, without correcting for gestational age, there are no significant differences in acetabular development or femoral head coverage between preterm and term infants [35]. Our findings similarly demonstrate that preterm infants, without gestational age correction, do not exhibit a higher incidence of abnormal hips. Furthermore, by 42 days of life, the majority of abnormal hips had resolved naturally. Based on these results, we propose that the timing of hip ultrasound screening for preterm infants can be synchronized with that of term infants.

This study has several limitations: (1) Being a retrospective study, it is constrained by a limited sample size and includes an insufficient number of DDH cases. Further research with larger sample sizes is required for more comprehensive analysis; (2) The study was conducted in a single hospital, which may limit the generalizability of the findings and may not fully represent other regions or populations; (3) The follow-up period was limited to 90 days after birth, preventing the observation of long-term outcomes in hip development; (4) While various factors were considered, some maternal, environmental, or genetic factors that may influence hip development could have been overlooked.

Conclusion

In conclusion, this study demonstrates that term singletons, females, and non-SGA newborns have a higher proportion of abnormal hip joints in the early postnatal period. Among neonates born after 28 weeks of gestation, there is no difference in hip development between preterm infants with a birth weight percentile <P50 and term infants. Most abnormal hips in both preterm and term neonates are physiologically immature rather than pathological, and in most cases, they naturally mature during postnatal development, negating the need for early intervention. For preterm infants born after 28 weeks of gestation, hip ultrasound screening can be performed at 42 days after birth without the need for correcting gestational age.