An Orthopedic Approach to a Child with a Limp: A Step-by-Step Review Article ()
1. Background
Definition: Limping in a child is defined as a child with abnormal walking pattern [1] . It is one the chief complaints in children referred to orthopedics and requires specific attention. Limping may be the sign of a wide range of etiologies from minor disorders to life-threatening causes. Some limping causes like Legg-Calvé-Perthes disease, slipped capital femoral epiphysis, developmental dysplasia of the hip, septic arthritis, and malignancies could lead to long-term complications if not diagnosed and treated early [2] [3] . Since many of these etiologies can overlap with other minor diseases, such as transient synovitis and overuse injury, and their clinical signs can resemble each other; thus, diagnosing a child with a limp needs a systematic approach to prevent misdiagnosis [4] .
Age levels: Toddlers, children of 1 - 3 years of age, when able to walk independently, usually take wide short steps. Asymmetrical steps with foot slaps, and sometimes falling, are expected in this age group. Children of 3 - 5 years of age usually walk with smoother and more symmetrical steps. Better arm movement and overall coordination of the body are observed in them compared with the younger age group. Finally, by the age of 7, most children walk in a pattern similar to that of their adults, which includes longer and slower strides [3] [4] [5] .Therefore, it is important to consider the age of the child in order to differentiate normal variations from gait abnormalities [5] .
Categories: Antalgic and non-antalgic gait are the two main categories of limping. Pain in the spine, hip, knee, or ankle induces a shortened stance phase on the affected side for the weight-bearing situation which is seen in antalgic limping. Non-antalgic limping includes excessive flexion of the hip or knee joint during swing phase of the gait resulting in toe walking which may be a sign of other etiologies such as clubfoot, limb length difference, or even neurological disabilities such as cerebral palsy [6] [7] [8] .The differential diagnoses for limping are provided in Table 1 based on age and pain.
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Table 1. Most common limping causes in children in each age group.
2. History
Obtaining exact history helps the doctor shorten a long list of possible diagnoses. First, whether the limping is painful or not? Then, whether the child can bear the weight? Any history of acute trauma is prone to the diagnoses of fractures, intra-articular injury, strain, and sprains. Gradual worsening of the symptoms without a history of trauma, in the presence of fever or chills, indicates infection and inflammatory process, and without fever or chills is suspicious to stress fractures [9] [10] [11] [12] [13] .
History of recent viral or bacterial infection must also be considered. Recent occurrence of conditions such as rash or diarrhea may be indicative of reactive arthritis. Preceding history of pharyngitis could indicate transient synovitis, acute rheumatic fever or migratory polyarthralgia as probable causes of limping. History of insect bites or travelling to rural areas indicates the possibility of Lyme disease [10] [11] .
An obvious fracture without a history of trauma indicates the possibility of a pathological fracture or child abuse. Children that are susceptible to abuse must be examined separately from their parents [12] [13] .
Questions about the type of pain can also be helpful. Burning pain is more common in nerve involvement, whereas constant pain is more prevalent in infections and malignancies. Moreover, the presence of focal pain strengthens the probability of fractures, infections, and malignancies. Morning stiffness and pain relief with activity guides the physician toward rheumatologic disorder. Pain worsening with activity or any recent physical activity indicates overuse injury and stress fractures [14] [15] .
Persistent limb pain is suggestive of interosseous disorders affecting the fibrous tissue between the tibia and fibula, such as a tumor or infection. Recent significant weight loss, anorexia, night sweats and night pain can be associated with malignant etiologies. Serious etiologies usually are more accompanied by night pain instead of pain after physical activity [16] .
A detailed history of birth and development, past medical history, immunization status and family history of rheumatological, metabolic, neuromuscular or immunodeficiency disease can be assessed at history overall. To exemplify, a history of bleeding disorder could be associated with hemarthrosis. Displays of sexual behaviors in children or being sexually active should be considered for gonococcal arthritis and reactive arthritis. Limping associated with neck pain, photophobia, or fever that ends in neck stiffness in the clinical exam is a strong indicator of meningitis [12] . Table 2 shows the important points of inquiry into patients’ medical history considering the red flags.
3. Clinical Exam: Physiologic or Pathologic Gait
Do not forget to undress the child completely during the examination. It is important to pay attention to the child’s upper body posture and evaluate for scoliosis, kyphosis, and lordosis abnormalities. Sitting position is recommended for spondylodiscitis assessment [14] . The presence of tenderness in the spinal muscles
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Table 2. Limping child checklist.
and the spinous processes on palpation of the child’s back is suggestive of causes related to spinal issues, such as trauma, discitis, vertebral osteomyelitis, or spinal cord tumors, all of which can be confirmed by a positive history of back pain [17] [18] .
Gait observation in a free space could be vastly enlightening. Monitoring a child when he/she is not paying attention can give the doctor information about the possibility of malingering. Any deviation from the normal state is considered limping. Signs of limping may be found in lumpy, asymmetrical, laborious, or irregular gait, which can be painful or painless. It is necessary to determine whether the child prefers one foot or moves asymmetrically [19] [20] .Moreover, considering varus and valgus deformities can narrow the differential diagnosis [21] .
As previously mentioned, it is necessary to have a correct understanding of normal gait based on the age of the child to identify deviations from the normal state at the onset of physical examination. Gait is usually immature before 18 months. At this age, the legs are extended to support the body which is called “toddler’s gait” characterized by a wide-based stance and short, unsteady steps. Although the movements of the joints are similar, the knees and ankles are more flexed, and the child cannot maintain the position of the single leg for a long time. The amplitude of the knee flexion decreases during the swing phase and the steps are short, the rhythm of walking is faster, but the overall velocity is slower. The more mature the gait is, the slower the cadence is and the longer the strides are. This developmental change is for a higher energy efficiency and more stable walking [22] .
Painful Limping: To examine an antalgic gait, first, we should be alert that some children are unable to express pain and, in some cases, just a reduction in standing time on the disabled side, a decrease in weight-bearing time, or a shortening in the stride length of the opposite limb are signs of antalgic gait. In addition, we should take into consideration that sometimes the painful zone is not the same as the provoking area, like knee pain which could be caused by hip disorders [14] [23] .
Protected, slow, and shuffling gait (having difficulty lifting the feet off the ground) is observed in antalgia originating from spinal pathologies. Touch the whole limb and pay attention to the baby’s face for grimacing. Prominent distress or disturbance, inability or refusal to bear weight on the affected limb, inconsolable pain, and fixing the limb position for comfort are some warning signs of potentially more serious problems such as compartment syndrome or musculoskeletal sepsis [24] .
It is best to start with the evaluation of the painless limb, and then, move on to the painful limb. In this way, we can compare the intensity of the child’s reaction. If the child can bear weight on the limping limb, subsequently, both limbs should be carefully evaluated. For toddlers, it is recommended that this evaluation be performed slowly and gently on the lap of the parents [25] .
Skin findings, including erythema, ecchymosis, swelling, laceration, and tenderness in the upper and lower anterior iliac spine during the pelvic examination, may indicate avulsion fractures of the anterior superior iliac spine due to the contraction of the sartorius and tensor fasciae lata muscles [26] [27] . racture of the direct head of the rectus has similar manifestations. Mutual symmetry should be considered when assessing the range of motion in the pelvis, knees, and ankles. Evidence of masses and effusions, or maximal tenderness points during the palpation of joints and muscles, could be aroused from the infectious causes or fractures [12] [28] .
Internal Rotation of the hip in a simulated prone position is a beneficial test for younger children. In this examination, the child is placed in the parent’s arms on his/her chest and the hips are fully stretched to increase the joint pressure by reducing the volume of the joint capsule [3] .This position allows a more accurate measurement of the internal rotation of the pelvis compared to the prone and internal rotation position, as the pelvis is stabilized in this position [29] . For babies of older age range, it could be performed in a lying down prone position. Lack of internal rotation of the hip is a sensitive indicator of intra-articular etiologies such as Legg disease in 4 - 10 years old and Slipped Capital Femoral Epiphysis (SCFE) in older ages, and some subacute disorders also should be considered such as synovitis and arthritis [4] [24] .
Patrick’s Test is performed while the child is lying on his/her back with the examiner flexing, abducting, and rotating the hip externally, and examining the sacroiliac joint for any pathology. Pelvic compression test is also used for similar cases. The child lies on his/her back and the examiner presses the iliac wings together. Pain in this maneuver again indicates sacroiliac joint pathology [1] .
The crawl test can be used to localize pathology in children who do not stand on their feet. The child should be encouraged to crawl with the help of the parents. If cross-crawling is done, the pathology is probably in the distal knee [26] . Pelvic osteomyelitis and pelvic and knee sepsis disable a child from crawling. Therefore, physical examination and subsequent imaging studies should be limited to the legs and feet in the presence of a normal crawl test. Possible pathologies in this area include distal tibial osteomyelitis, tibial fracture, osteochondritis of the foot (like Kohler’s disease), foot fracture, and the presence of a foreign body in the foot [30] .
Non-painful Limping: In non-painful limping, considering the type of abnormal gait could be enormously helpful. Steppage gait is when the hip and knee joints are flexed more than normal during the swing phase and toes clear the ground, which is experienced in neurologic conditions that make the child unable to dorsiflex the foot. Trendelenburg gait is another type of abnormal gait in which the pelvis is unable to remain in the neutral position, exhibiting a downward tilt toward the normal side during the swing phase. A positive Trendelenburg test signifies developmental dysplasia of the hip (DDH) or any other disorder in hip abductor mechanism [31] . Circumduction gait is when excessive extension is seen in the knee and it locks at the end of the stance phase. The affected limb is circumducted or abducted during the swing phase and clears the ground with the toe due to difficulty lifting the foot off the ground. This finding is common in neurologic or mechanical disorders which lead to stiffness of the knee or ankle. We should also consider limb-length discrepancy in this pattern. The Galeazzi test could be employed for this purpose, explained in the tests section. Note that Short-limb gait is also seen in milder degrees of discrepancy in which the child equalizes the length of the limbs through knee flexion in the longer limb without plantar flexion or with plantar flexion in the shorter limb and standing on the toes. Hand-to-thigh gait can be found in children suffering from quadriceps paralysis due to spinal cord injury, neuro-muscular dystrophy, or polio. This gait is easy to discover; the child pushes the thigh backward manually to stabilize the knee [19] . The last gait type in the non-antalgic group is the equinus gait which is typical in congenital talipes equinovarus (CTEV), cerebral palsy, idiopathic tight Achilles tendon, and limb-length discrepancy. In equinus gait, the child walks on the toes painlessly; however, sometimes, it can be the result of calcaneal fracture or a foreign body in the foot as antalgic etiologies [32] [33] [34] . More explanations are provided in Table 3.
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Table 3. Abnormal gaits.
Evaluation of hip abduction is performed in the supine position with flexed hips and knees while the soles of the feet are together. Any limitation in this area is in the interest of DDH. The Galeazzi test, also known as the Allis sign, is used to check the difference in length between the two lower limbs, with the child lying down and the knees bent so that the soles of the feet touch the ground and the ankles touch the buttocks. The test is positive when the knees are not level [35] Any range of motion limitation or length difference detected may be an indication of DDH, Legg-Calvé-Perthes disease, proximal femoral focal deficiency (PFFD), focal hypertrophy, etc [12] [34] [36] [37] [38] .
To evaluate neuromuscular causes of limping, a complete neuromuscular examination is needed. Presence of spastic muscles in the affected limb may be suggestive of upper motor neuron (UMN) lesions such as cerebral palsy; however, hypotonia is suggestive of lower motor neuron (LMN) disorders, including polio and spina bifida. Findings such as muscle atrophy and muscle twitching (fasciculations) may have LMN causes. Additionally, reflexes and tone are decreased, Babinski sign is down, and flaccid paralysis can be detected In LMN disorders. Other subgroups of LMN include hereditary motor and sensory neuropathies (Charcot-Marie-Tooth disease) and myopathies such as Duchenne muscular dystrophy (DMD) [28] [39] .
The examination can provide some other clues for non-orthopedic etiologies. For instance, the presence of any skin rash can indicate Lyme disease, reactive arthritis, or viral causes. Abdominal pain or tenderness along with limping is common in appendicitis and psoas abscess. Finding an abdominal mass is expected in neuroblastoma. Psoas sign can be used to check these causes. In this test, the child lies on the side and the examiner extends the hip passively. If the child has pain during the hip extension, the test is positive [4] [23] . The list of related tests is provided in Table 4.
4. Para-Clinical
Laboratory tests. The performance of paraclinical tests should be based on history and examination. In this way, the cause of limping can be investigated as precisely as possible. If malignancy, infection, or inflammatory arthritis is
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Table 4. Clinical exam tests.
suspected, a blood analysis should be performed, including a complete blood count with differential measurement of erythrocyte sedimentation rate (ESR) and C-reactive protein (CRP). Increased WBCs and platelets are common in infections and inflammatory diseases versus malignancies, which are accompanied by cytopenia. ESR and CRP are high in all of them [40] [41] .
In case of septic arthritis, joint fluid aspiration and Gram staining, and culture and cell count are necessary. Based on the Kocher Criteria, a non-weight-bearing condition associated with high temperature (>38.5), Serum ESR > 40 mm/h, and Serum WBC > 12,000 cells/mm3 are strongly susceptible to the diagnosis of septic arthritis. Turbid synovial fluid, WBC count of more than 50,000 to 100,000 per/mm3 with PMNs > 75%, is pathognomonic of septic arthritis; however, in transient synovitis, clear yellow synovial fluid is observed with lower WBC count (5000 to 15,000 per/mm3) and PMNs < 25% [10] . Moreover, using real-time PCR-based method to evaluate acute arthritis and determine its cause can be helpful in Kingella kingae cases [42] .
Culturing of body specimens would be differentiating in the diagnosis of septic arthritis. For instance, synovial fluid culture is positive in septic arthritis, but transient synovitis demonstrates a negative result. A positive bone culture from the suspected area confirms osteomyelitis. Blood culture sometimes could help in finding the specific source of the infection [40] . To consider some microorganisms specifically, Neisseria gonorrhoeae in urethral, cervical, pharyngeal, and rectal cultures is specific to gonococcal arthritis. Application of urethral and stool culture in patients with positive history of Neisseria gonorrhoeae could be helpful. Salmonella, Campylobacter, Shigella, and Yersinia in stool cultures and Chlamydia in urethral cultures are important findings in reactive arthritis. A positive Group A hemolytic streptococcus in throat culture is suggestive of acute rheumatic fever. Anti-streptolysin O (ASO) titer elevation is also probable in this disease [40] [43] .
To evaluate fewer common etiologies, antinuclear antibody (ANA) test is helpful for the primary assessment of systemic lupus erythematosus (SLE)-inducing arthritis. Checking coagulation profile in known hemophilia cases or positive familial histories may show increased activated partial thromboplastin time (aPTT) which suggests hemorrhagic effusion or hematoma. Lyme titer should be checked for suspected patients with history of travelling to endemic areas of Lyme disease [41] . Leukemia should be regarded as a potential cause in children who have a limp, constitutional symptoms, and an elevated white blood cell count (ranging from 10,000 to 100,000) or Cytopenia [44] . Further detail on paraclinical tests is presented in Table 5.
Imaging. Imaging is the most important paraclinical evaluation. Plain radiographs of the localized part of the suspected limb are both sensitive and specific for the diagnosis of prevalent causes [3] ; however, if pain is not localized, a more generalized X-ray view could be enlightening through comparative evaluation of the contralateral side [45] . There are some common radiographic views in limping evaluation imaging. Anteroposterior (AP) and frog-leg lateral pelvis radiographs are helpful in the consideration of fracture, missed DDH, and congenital Coxa vara [21] [43] . These views are not required in patients with normal hip motion with regular crawling. It must be noted that the frog pelvis view should be avoided in suspected acute unstable slipped capital femoral epiphysis since it can exacerbate the slip. Alternatively, a true lateral hip view could be applied [46] [47] [48] [49] .
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Table 5. Laboratory tests.
In non-localized examination or in young children who are unable to cooperate in presenting history, the entire lower leg view is recommended [45] An AP view of both tibias together is beneficial in evaluating knee-related causes such as genu varus and genu varum, or metaphyseal fractures. The lateral view of each tibia including the knee and entire foot demonstrates any possible lesions or misalignments. The AP view of both feet together should be applied for microfractures or foreign bodies [43] .
Ultrasonography (US) is another sensitive imaging method for effusion detection in joints, especially in the hip. When it is not possible to distinguish different fluids via the US, ultrasound-guided aspiration should be performed urgently. For alteration of ultrasound-guided aspiration, the synovial fluid aspiration can be performed under fluoroscopic guidance or even blinded by an expert [47] . The synovial fluid analysis has been previously explained. The US is beneficial for detecting cartilaginous joint fracture, radiolucent foreign bodies (such as splinters, plastic, and glass), soft tissue swelling, and abscessess [48] [49] [50] .
When pathology cannot be identified through medical history, physical examination, and radiographic and ultrasound findings, bone scintigraphy is an appropriate test for the evaluation of stress fractures, osteomyelitis, tumors, and metastatic lesions in the child. This test has low specificity, but has a high sensitivity [51] .
CT scans are less commonly used in the primary investigation steps of limping causes due to the high dose of radiation, nevertheless, the modern CT scan techniques offer much lower radiation dose. Sometimes, a three-dimensional CT scan is performed for a more detailed imaging of bone abnormalities including occult fractures, benign lesions such as simple bone cysts, non-ossifying fibromas, and osteoid osteomas, visualization of the cortical bone, and intra-abdominal causes like neuroblastoma or hepatosplenomegaly [52] [53] .
Magnetic resonance imaging (MRI) with high sensitivity and specificity is a great option for the examination of joints, cartilage, medullary bone, muscles, and vascular abnormalities and can be used in the form of localized or whole-body MRI. This imaging method is suitable for confirming osteomyelitis, identifying stress fractures, early diagnosis of Legg disease and avascular necrosis of the femoral head due to sickle cell disease, and determining the extension of malignancies. Initial radiographs are commonly used in acute hematogenous osteomyelitis, but MRI could be helpful in earlier diagnosis and prevention of further sequels. Comparison of the images of two hips is also used to detect pre-slip. Spinal disorders such as discitis are best evaluated through MRI [54] [55] . The application of different types of imaging is presented in Table 6 and the radiographies of some etiologies are shown in Figure 1.
5. Diagnostic Algorithm
Figures 2-4 show the practical algorithms for the diagnosis of the causes of limping in a child.
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Table 6. Imaging and the proper X-ray views for different limping causes.
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Figure 2. The approach to antalgic gait.
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Figure 3. The approach to non-antalgic gait (Steppage gait, Hand-to-thigh gait and Short-limb gait).
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Figure 4. The approach to Equinus gait, Circumduction gait and Trendelenburg gait.
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Table 7. The abstract of treatment and follow-up for different limping causes.
6. Treatment/Follow-Up
Table 7 presents the abstract of treatment and follow-up for different limping causes.
7. Conclusion
Limping is a common complaint in children referring to orthopedic surgeons. There are many differential diagnoses for limping. It is important, therefore, to have a systematic approach in order not to miss any case or dangerous etiology. In this article, we provided a comprehensive and inclusive view of pediatric limping based on antalgic and non-antalgic limping, acute trauma history, systemic symptoms, and different abnormal gaits. Although the symptoms of many causes of limping overlap, especially as children are sometimes unable to provide information, the related algorithms help the physician not to miss any serious diseases and consider all possible conditions.
NOTES
*Co-corresponding author.