Orthopedics

Feature Article 

Characteristics of Pyogenic Musculoskeletal Infections in Older Children and Adolescents

Sarah N. Pierrie, MD; Brian P. Scannell, MD; Brian K. Brighton, MD, MPH; Kelly L. Vanderhave, MD

Abstract

The characteristics and clinical consequences of pyogenic bone and joint infections in older children and adolescents have received little attention. This study evaluated the presentation and complications of musculoskeletal infections involving the pelvis and extremities in children older than 10 years. Thirty patients 10 to 17 years old (mean, 12.7 years old) were treated for musculoskeletal infections. Mean time to diagnosis was 9.2 days. Prior to correct diagnosis, 83% were assessed by at least 1 outpatient provider. At the time of admission, 55% were weight bearing and 93% were afebrile. Twenty-eight percent had a multifocal infection. More than one-third had serious medical complications or orthopedic sequelae; compared with patients without complications, this group had a significantly higher admission C-reactive protein and longer hospital stay. Symptoms of musculoskeletal infection common among young children may be absent in adolescents. Axial imaging is recommended to identify adjacent or multifocal disease. The Kocher criteria are less sensitive for septic hip arthritis in the adolescent population. Prompt recognition and treatment are critical to avoid medical and musculoskeletal complications. [Orthopedics. 2020;43(4):e291–e298.]

Abstract

The characteristics and clinical consequences of pyogenic bone and joint infections in older children and adolescents have received little attention. This study evaluated the presentation and complications of musculoskeletal infections involving the pelvis and extremities in children older than 10 years. Thirty patients 10 to 17 years old (mean, 12.7 years old) were treated for musculoskeletal infections. Mean time to diagnosis was 9.2 days. Prior to correct diagnosis, 83% were assessed by at least 1 outpatient provider. At the time of admission, 55% were weight bearing and 93% were afebrile. Twenty-eight percent had a multifocal infection. More than one-third had serious medical complications or orthopedic sequelae; compared with patients without complications, this group had a significantly higher admission C-reactive protein and longer hospital stay. Symptoms of musculoskeletal infection common among young children may be absent in adolescents. Axial imaging is recommended to identify adjacent or multifocal disease. The Kocher criteria are less sensitive for septic hip arthritis in the adolescent population. Prompt recognition and treatment are critical to avoid medical and musculoskeletal complications. [Orthopedics. 2020;43(4):e291–e298.]

Musculoskeletal infection in children involves a wide spectrum of diagnoses, including hematogenous osteomyelitis, periosteal abscesses, septic arthritis, soft tissue abscesses, myositis, fasciitis, diskitis, and paraspinous infections. In this population, infectious conditions commonly present with fever, focal pain, and some degree of local irritability or extremity disuse in the absence of major trauma. Potential consequences of missed or delayed diagnoses of pyogenic bone and joint infections include osteonecrosis, fracture, remote infection, and sepsis, making prompt diagnosis imperative.

Several diagnostic algorithms for evaluating suspected pyogenic hip infections in young children using clinical parameters and blood tests have been proposed.1–4 The most widely used algorithm, described by Kocher et al1 in 1999, was devised to distinguish between septic hip arthritis and transient synovitis and was validated clinically in a cohort of elementary-aged children.2 Recent studies have shown marked variation in these algorithms' ability to correctly diagnose patients with intra-articular infections and similar criteria have not been validated for conditions other than septic arthritis of the hip.2,3,5–8 Furthermore, there is a paucity of literature regarding disease characteristics and the application of these clinical guidelines in older children and adolescents. The purpose of this study was to evaluate the presentation and complications of musculoskeletal infections involving the pelvis and extremities in children 10 to 17 years old. The authors' hypothesis was that older children and adolescents with musculoskeletal infection exhibit more subtle symptoms than those previously described in younger children and respond to treatment differently than do their younger counterparts.

Materials and Methods

This was a retrospective case series of patients treated at a tertiary care pediatric hospital between 2008 and 2013. Following institutional review board approval, consecutive patients aged 10 to 17 years were identified using International Classification of Diseases, Ninth Edition codes for bony and soft tissue infections. Demographic and clinical data were extracted from the medical record. A musculoskeletal radiologist and 2 board-certified pediatric orthopedic surgeons (B.P.S., K.L.V.) independently reviewed the imaging studies.

Diagnoses of osteomyelitis and soft tissue infection were assigned based on radiographic and clinical findings. The diagnosis of septic arthritis was assigned to patients with 1 or more of the following criteria: a synovial white blood cell (WBC) count greater than 50,000 cells/mm3; a positive synovial Gram stain or culture; a joint effusion in the setting of contiguous abscess or documented bacteremia; frank intracapsular purulence found at the time of surgery; or a documented history of septic arthritis in the setting of concerning laboratory and clinical examination findings. Patients with hip or knee irritability who did not fulfill these diagnostic criteria were presumed to have noninfectious transient synovitis unless an alternative etiology (eg, osteomyelitis, inflammatory arthritis) was identified by imaging and laboratory studies. A subgroup of patients with septic arthritis of the hip was reviewed separately.

Infectious disease consultants determined the type and duration of antibiotic therapy. Patients were transitioned to oral antibiotics at the infectious disease physician's discretion based on clinical, laboratory, and imaging findings.

Descriptive statistics were calculated as means and standard deviations for continuous variables and as percentages for categorical variables. To evaluate the strength of predictors, univariate and multivariate analyses were performed. To compare continuous variables, t tests were used; the chi-square test or Fisher's exact test was used to compare categorical variables. P<.05 was considered significant.

Results

Thirty patients (21 male and 9 female) with an average age of 12.7 years (range, 10 to 17 years) were treated for musculoskeletal infections, including osteomyelitis (n=15), septic arthritis of the hip (n=14) and knee (n=3), deep soft tissue infections (n=8), and sacroiliitis (n=3) (Table 1). Mean time from onset of symptoms to diagnosis was 9.3 days (range, 1 to 30 days). Twenty-five (83%) of 30 patients were assessed by at least 1 outpatient provider prior to diagnosis of musculoskeletal infection. Of these, 44% had seen 2 or more providers before receiving the appropriate diagnosis.

Presentation, Management, and Orthopedic Complications of Musculoskeletal Infections in 30 Older Children and AdolescentsPresentation, Management, and Orthopedic Complications of Musculoskeletal Infections in 30 Older Children and Adolescents

Table 1:

Presentation, Management, and Orthopedic Complications of Musculoskeletal Infections in 30 Older Children and Adolescents

Prior to admission, the most common complaint was localized pain at the site of infection (93%) and subjective fever (80%). Only 2 (7%) patients had a measured temperature greater than 38.5°C at the time of orthopedic evaluation. More than half (55%) of the patients were full or partial weight bearing. Mean admission laboratory values included WBC count of 11.6×103 cells/mm3 (range, 5.1 to 33.1×103 cells/mm3), absolute neutro-phil count of 8.4×103 cells/mm3 (range, 2.3 to 30.5×103 cells/mm3), erythrocyte sedimentation rate (ESR) of 50.6 mm/h (range, 1 to >140 mm/h), and C-reactive protein of 15.5 mg/dL (range, 1.3 to 38.7 mg/dL; normal is <0.5 mg/dL at the authors' institution).

Only 15% of patients had abnormal findings on plain radiograph. Twenty-nine (97%) of 30 patients subsequently underwent magnetic resonance imaging (MRI); noncontiguous or multifocal infections were identified in 8 (28%) patients. Seven (41%) of 17 patients with septic arthritis had adjacent osteomyelitis identified on MRI.

The decision to proceed with surgery was made at the attending surgeon's discretion. Twenty-four (80%) patients underwent surgery, for a total of 46 procedures (range, 1 to 9 procedures). All patients with septic arthritis were treated surgically. A high infection burden at the time of index surgery and failure to respond to medical management were indications for additional surgery. Repeat MRI was not routinely performed.

A pathogenic organism was isolated from fluid, blood, or tissue cultures in 73% (22 of 30) of patients. Organisms were identified from 12 (48%) of 25 blood cultures, 8 (62%) of 13 tissue samples, and 12 (63%) of 19 fluid samples. Eighty-two percent of isolated species were Staphylococcus species. The most common isolates were oxacillin-sensitive Staphylococcus aureus (methicillin-sensitive Staphylococcus aureus; 15 [68%] of 22 patients), followed by oxacillin-resistant Staphylococcus aureus (methicillin-resistant Staphylococcus aureus) and Streptococcus species (2 patients [9.1% each] of 22). Other species isolated from this cohort included coagulase-negative Staphylococcus, Salmonella, and Fusobacterium species in 1 patient each. Two patients received antibiotics before blood or tissue samples were obtained; 1 of these patients had negative cultures.

Eighty-three percent of patients required both intravenous (mean, 11.3 days; range, 1 to 49 days) and oral (mean, 24.7 days; range, 7 to 59 days) antibiotic therapy. Three (10%) patients received exclusively intravenous antibiotics, and 1 patient was treated only with oral antibiotics.

Five (17%) patients had medical complications, including deep venous thrombosis (DVT), pneumonia, pulmonary embolism, Clostridium difficile infection, and wound complications (Table 2). Four (13%) patients required readmission within 30 days of discharge for recurrent symptoms. The average length of readmission stay was 4.8 days (range, 1 to 8 days). No patients required reoperation during the second admission.

Frequency of Medical Complications of Infection in a Cohort of 30 Older Children and Adolescents

Table 2:

Frequency of Medical Complications of Infection in a Cohort of 30 Older Children and Adolescents

Musculoskeletal sequelae of infection were detected at follow-up in one-third of patients. Findings included loss of full joint motion, recurrent joint effusion (in the setting of normal results on rheumato-logic workup), chronic osteomyelitis, heterotopic ossification, avascular necrosis of the hip, persistent limp, and end-stage hip or sacroiliac arthrosis (Table 3). One 16-year-old female adolescent with left hip septic arthritis, psoas abscess, and osteomyelitis of the ilium had severe joint destruction with subluxation of the femoral head and eventually required total hip arthroplasty (Figure 1). One 14-year-old female adolescent with Salmonella sacroiliitis initially treated nonoperatively with intravenous antibiotics developed painful arthritis and underwent elective sacroiliac fusion 26 months later (Figure 2).

Frequency of Musculoskeletal Complications of Infection in a Cohort of 30 Older Children and Adolescents

Table 3:

Frequency of Musculoskeletal Complications of Infection in a Cohort of 30 Older Children and Adolescents

A 16-year-old girl presented with insidious onset of left hip and flank pain. After 3 weeks of symptoms, she was diagnosed with a complicated pelvic abscess (asterisk), osteomyelitis of the ilium, and a left hip effusion (arrowhead) (A, coronal computed tomography scan; B, axial computed tomography scan). She ultimately underwent 4 surgeries, including irrigation and debridement of a left thigh abscess identified 3 weeks after her initial surgery (C, axial T2-weighted magnetic resonance image). She developed early femoral head avascular necrosis (D, anteroposterior pelvic radiograph 3 weeks postoperatively) that rapidly progressed (E, anteroposterior pelvic radiograph 3 months postoperatively). Left total hip arthroplasty was performed 4 months later (F, anteroposterior pelvic radiograph).

Figure 1:

A 16-year-old girl presented with insidious onset of left hip and flank pain. After 3 weeks of symptoms, she was diagnosed with a complicated pelvic abscess (asterisk), osteomyelitis of the ilium, and a left hip effusion (arrowhead) (A, coronal computed tomography scan; B, axial computed tomography scan). She ultimately underwent 4 surgeries, including irrigation and debridement of a left thigh abscess identified 3 weeks after her initial surgery (C, axial T2-weighted magnetic resonance image). She developed early femoral head avascular necrosis (D, anteroposterior pelvic radiograph 3 weeks postoperatively) that rapidly progressed (E, anteroposterior pelvic radiograph 3 months postoperatively). Left total hip arthroplasty was performed 4 months later (F, anteroposterior pelvic radiograph).

A 14-year-old otherwise healthy girl presented with progressive left hip pain. Magnetic resonance imaging revealed left sacroiliitis (A, axial T2-weighted magnetic resonance image). She underwent fluoroscopic aspiration (B). Cultures were positive for Salmonella species, and she was treated with 4 weeks of intravenous antibiotics. Her pain persisted, and pelvic imaging (C, anteroposterior radiograph; D, axial computed tomography scan) demonstrated end-stage arthrosis. Three years after initial presentation, she underwent left sacroiliac fusion (E, anteroposterior pelvic radiograph).

Figure 2:

A 14-year-old otherwise healthy girl presented with progressive left hip pain. Magnetic resonance imaging revealed left sacroiliitis (A, axial T2-weighted magnetic resonance image). She underwent fluoroscopic aspiration (B). Cultures were positive for Salmonella species, and she was treated with 4 weeks of intravenous antibiotics. Her pain persisted, and pelvic imaging (C, anteroposterior radiograph; D, axial computed tomography scan) demonstrated end-stage arthrosis. Three years after initial presentation, she underwent left sacroiliac fusion (E, anteroposterior pelvic radiograph).

When compared with patients without identifiable post-infection sequelae, the 12 patients with medical or musculoskeletal complications of infection had a significantly higher C-reactive protein on admission (22.7 vs 10.7 mg/dL, P=.003) and longer hospital stay (15.1 vs 5.1 days, P=.002). However, patients with complications were not significantly more likely to be readmitted (P=.27) or to have been seen by more than 1 provider prior to diagnosis (P=.36) than those without complications. Both groups had a substantial delay in diagnosis (11.5 days in the complication group and 7.9 days in the group without complications), but the difference was not statistically significant (P=.28).

Septic Hip Subgroup Analysis

A subgroup of 14 patients with confirmed septic arthritis of the hip (average age, 12.8 years) was reviewed separately. When the Kocher criteria were applied to this cohort, 7 patients presented with 1 positive criterion, 6 with 2 positive criteria, and 1 with 3 positive criteria. No patient demonstrated 4 positive criteria at the time of admission. Elevated ESR was the most common positive finding (n=9), followed by refusal to bear weight (n=6), elevated WBC count (n=4), and subjective fever in the week prior to admission (n=2). None of the patients with septic hip had a documented temperature greater than 38.5°C. The mean C-reactive protein for this subgroup was 16.8 mg/dL (range, 1.5 to 32.6 mg/dL) and 13 of 14 patients had a C-reactive protein greater than 2.0 mg/dL.

Discussion

Musculoskeletal infections have significant morbidity in pediatric patients of all ages. Despite abundant literature regarding the diagnosis and treatment of bone and joint infections in young children, there is little existing literature about the management of these problems in older children and adolescents. This study described the presentation and complications of bone, joint, and soft tissue infections in this group.

The results of this study suggest that the presenting signs and symptoms of musculoskeletal infections in older children differ from those encountered in younger children. Young children with bone or joint infections commonly present with irritability, fever, and refusal to bear weight. In this cohort of children 10 years or older, patients nearly universally presented with focal joint or extremity pain; however, the majority were able to partially or fully weight bear and were afebrile. This may in part explain the prolonged interval from symptom onset to diagnosis (mean, 9.3 days). Additionally, 83% of patients were assessed by at least 1 out-patient provider, and nearly half of these were seen by at least 2 providers prior to diagnosis. These findings suggest that the diagnosis of infection may be more difficult in the outpatient setting when older children do not present with the classic symptoms of musculoskeletal infection.

Kocher et al1,2 previously described an algorithm using 4 specific criteria to differentiate septic hip arthritis from transient synovitis. These criteria were initially defined in a population of children with a mean age of 6 years but, in practice, have been applied clinically to children of all ages. Unlike the patients in the initial study by Kocher et al,1 where the presence of a fever was associated with the highest odds ratio of septic arthritis (as opposed to transient synovitis), none of the patients in the current septic hip cohort had a documented temperature greater than 38.5°C. In the current study, an elevated ESR was the most consistent finding among adolescents with septic arthritis of the hip; however, diminished weight bearing, elevated WBC count, and a subjective history of fever each affected fewer than half the patients in this group. Importantly, C-reactive protein was almost uniformly elevated in this cohort of patients, mirroring the findings of Caird et al.3 Because the pretest probability of transient synovitis in the adolescent population is low and these patients often do not conform to the predictive algorithm available for younger patients, septic arthritis should be at the forefront of the differential diagnosis for adolescents with joint irritability and elevated inflammatory markers such as ESR and C-reactive protein.

Historically, the evaluation of musculoskeletal infections started with radiography and was followed by bone scintigraphy if necessary. The sensitivity of plain radiographs and bone scans in detecting infections caused by Staphylococcus aureus is only 20% and 53%, respectively, compared with 99% for MRI.9 Magnetic resonance imaging is particularly useful for its ability to identify multifocal infection and extraosseous disease, including DVT.9–12 The current findings support the routine use of MRI, which diagnosed multifocal infection in 28% of patients, in the adolescent population.

A pathogenic organism was identified in 73% of cases in the current study. This is comparable to or slightly better than the isolation rate (55% to 64%) found in other studies of pediatric musculoskeletal infections13–15 and may speak to the evolution of pyogenic infection in the adolescent population related to delay in diagnosis. In the current older child and adolescent cohort, Staphylococcus species were responsible for the majority (82%) of infections in which a pathogen was identified. Methicillin- or oxacillin-resistant Staphylococcus aureus infection was implicated in less than 10% of these infections, a smaller proportion than in previous reports.13–16

Numerous musculoskeletal complications, including damage to adjacent physes, joint destruction or ankylosis, osteonecrosis, and pathologic fracture, have been reported in the literature.17–19 In the current study, one-third of patients experienced long-term morbidity related to infection. Avascular necrosis, joint contracture, and heterotopic ossification were the most common sequelae observed in this series of adolescent patients. Two patients required additional orthopedic procedures to address pain associated with end-stage arthrosis.

The authors observed a trend toward longer duration of symptoms prior to definitive treatment among patients who experienced complications, emphasizing the importance of prompt detection. Haas and Wenger20 retrospectively studied a series of 36 patients with septic arthritis of the hip with particular attention to continuing problems following resolution of infection. Seven (19%) of these patients were 9 to 13 years old. They reported that although all patients had seen a physician within 7 days of onset of symptoms, infection was not considered or diagnosed at the first encounter. Excluding 1 patient with a 14-month delay in diagnosis, the average time from presentation to initiation of treatment was 18 days (range, 7 to 24 days). Although no direct correlation between time to treatment and complications could be established in the current small series, the trend toward prolonged time to diagnosis in older patients places them at high risk for complications.

Medical complications occurred in two-fifths of the patients in the current study. The prolonged hospital stay noted among patients experiencing complications likely reflects a high infection burden that increases the risk for complications. Deep venous thrombosis is a recognized sequelae of pediatric musculoskeletal infection, particularly methicillin-resistant Staphylococcus aureus, affecting nearly one-third of patients.21 In a retrospective study of 212 pediatric patients with osteomyelitis, Hollmig et al22 noted that patients with DVT were significantly older on average than patients without DVT (10.9 vs 7.4 years). Deep venous thrombosis has been associated with disseminated infection23 and can be accompanied by pulmonary embolism, particularly in patients with severe methicillin-resistant Staphylococcus aureus infection.19,24,25 The current authors found no difference in complications between patients with methicillin-sensitive Staphylococcus aureus and methicillin-resistant Staphylococcus aureus infections.

An inherent weakness of this study was its small size. All eligible patients treated by 7 pediatric orthopedic surgeons during a 5-year period at a regional children's hospital and referral center (whose emergency department manages more than 29,000 pediatric visits annually—an estimated 145,000 visits during the study period) were included. Nevertheless, the relative infrequency of serious musculoskeletal infection among older children and teenagers resulted in a limited sample. Additionally, the retrospective nature of this study allows the authors to demonstrate trends but prevented them from drawing firm conclusions about causation from the available data.

Conclusion

Musculoskeletal infections can be difficult to diagnose and treat in older children and adolescents. A strong index of suspicion is critical because symptoms common among younger children, such as fever and failure to bear weight, may be absent in the adolescent. An elevated C-reactive protein was almost uniformly correlated with intraarticular infection. Advanced imaging with MRI is recommended to help identify adjacent or multifocal disease. Although the trend toward delay in diagnosis and long-term morbidity did not reach statistical significance, prompt recognition and treatment remain imperative because complications and sequelae can be severe.

References

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  11. Pugmire BS, Shailam R, Gee MS. Role of MRI in the diagnosis and treatment of osteomyelitis in pediatric patients. World J Radiol. 2014;6(8):530–537. doi:10.4329/wjr.v6.i8.530 [CrossRef] PMID:25170391
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Presentation, Management, and Orthopedic Complications of Musculoskeletal Infections in 30 Older Children and Adolescents

Patient No.Age, yTime to Diagnosis, dFeveraWeight BearingbWBC, 103 cells/mm3ESR, mm/hCRP, mg/dLPrevious EvaluationscMRIDiagnosisNo. of Intraoperative ProceduresMusculoskeletal Complications
1104NoNo5.35032.61NoSeptic arthritis hip2None
2101NoYes9.5564.90YesSeptic arthritis hip1None
3104NoUnknown10.8188.11YesSeptic arthritis knee1Recurrent knee effusion
4132NoNo15.32112.80YesSeptic arthritis hip1None
5135NoNo12.98513.82YesSeptic arthritis hip1None
61421NoYes6.212422.32YesSeptic arthritis hip1None
71421NoUnknown33.18830.91YesSeptic arthritis knee1None
81714NoNo13.01127.02YesSeptic arthritis hip1None
9115NoUnknown5.1415.01YesSeptic arthritis hip + inflammatory arthritis1None
10152NoYes8.44213.30YesSeptic arthritis hip + inflammatory arthritis1None
11105NoNo15.08135.11YesSeptic arthritis knee + distal femur OM3Flexion contracture
121211NoYes13.4644.81YesSeptic arthritis hip + pelvic abscess1None
131214NoYes9.1683.42YesSeptic arthritis hip + pelvic OM1AVN
14122NoNo11.04638.71YesSeptic arthritis hip + pelvic OM + gluteal pyomyositis9Persistent limp
15136NoNo8.72029.01YesSeptic arthritis hip + proximal femur OM + ulna OM4AVN; painful HO
161328NoYes12.8>14013.11YesSeptic arthritis hip + proximal femur OM5AVN; decreased hip ROM; persistent limp
171621NoUnknown13.05531.92YesSeptic arthritis hip + pelvic OM + psoas abscess4End-stage hip arthrosis requiring THA; painful HO requiring excision
18105NoNo10.414.91YesPelvis OM0None
191130NoYes10.6325.61YesPelvic OM1None
20137NoUnknown6.429.82YesGreater trochanter OM0None
21137YesNo14.67030.83YesDistal femur OM2Chronic OM
221210NoYes12.9121.52YesPelvic OM + adductor pyomyositis0None
23176NoYes15.04522.93YesPelvic OM + pelvic abscess1None
2411UnknownNoUnknown13.0468.30YesSacroiliitis0End-stage sacroiliac arthrosis requiring sacroiliac fusion
25134YesUnknown11.47612.51YesSacroiliitis0Persistent limp
261614NoUnknown8.44616.53YesSacroiliitis + pelvic abscess1None
27108NoYes7.4792.51YesCalcaneus OM0None
28123NoYes10.72311.33Yes5th metatarsal OM1None
29106NoYes16.17110.70YesThigh abscess1None
30173NoUnknown8.141.30YesFoot abscess1None

Frequency of Medical Complications of Infection in a Cohort of 30 Older Children and Adolescents

Medical ComplicationNo.
Deep venous thrombosis3
Pneumonia2
Pulmonary embolism1
Clostridium difficile infection1
Wound infection1

Frequency of Musculoskeletal Complications of Infection in a Cohort of 30 Older Children and Adolescents

Musculoskeletal ComplicationNo.
Avascular necrosis3
Persistent limp3
End-stage arthrosis2
Heterotopic ossification2
Loss of terminal motion2
Recurrent idiopathic effusion1
Chronic osteomyelitis1
Authors

The authors are from the Department of Orthopaedics (SNP), San Antonio Military Medical Center, JBSA Ft Sam Houston, Texas; and OrthoCarolina and Atrium Musculoskeletal Institute (BPS, BKB) and TeamHealth (KLV), Charlotte, North Carolina.

The authors have no relevant financial relationships to disclose.

The views expressed in this manuscript are those of the authors and do not reflect the official policy of the Department of the Air Force, Department of Defense, or US Government. Dr Pierrie is an employee of the US Government. This work was prepared as part of her official duties and as such, there is no copyright to be transferred.

Correspondence should be addressed to: Brian P. Scannell, MD, OrthoCarolina, 1915 Randolph Rd, Charlotte, NC 28207 ( Brian.Scannell@Orthocarolina.com).

Received: January 07, 2019
Accepted: April 29, 2019
Posted Online: June 05, 2020

10.3928/01477447-20200521-04

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