679704

research-article2016
FASXXX10.1177/1938640016679704Foot & Ankle SpecialistFoot & Ankle Specialist

vol. XX / no. X Foot & Ankle Specialist 1

〈 Review 〉
Hematogenous Calcaneal
Osteomyelitis in Children Megan L. Mooney, BS, Kirk Haidet, MD,
Jiayong Liu, MD, and Nabil A. Ebraheim,

A Systematic Review of the

MD

Literature
Abstract: Osteomyelitis in children 79% to 97% of cases. Methicillin- puncture wound or hematogenous
commonly affects long bones such as sensitive Staphylococcus aureus was spread.1-3 Systemic bacteremia can
the femur, tibia, and humerus. There the most common cultured organism. result in hematogenous seeding of long
have been relatively few documented Treatment involved either antibiotics bones, most commonly the femur, tibia,
studies of osteomyelitis at unusual alone or in combination with surgical and humerus, but can also involve
locations, such as the calcaneus. debridement/evacuation. Penicillin, unusual sites such as the clavicle, ribs,
The objective of this study is to penicillin derivatives, cephalosporins, talus, and calcaneus.4-7 Previous
systematically review information on clindamycin, and chloramphenicol literature has reported the rate of
the diagnostic and treatment methods were the most commonly used occurrence of calcaneal osteomyelitis
of calcaneal osteomyelitis as well as antibiotics, with duration varying from to be between 3% and 10%.2,3,5,8-10
associated complications. Methods 5 days to 10 weeks. The most common Acute hematogenous calcaneal

“
included research database searches complication was
using primarily PubMed and EMBASE recurrent osteomyelitis.
databases. Results of the review show
Levels of Evidence: Heel pain in children has a vast array
no clear approach to diagnosis and
III
treatment of calcaneal osteomyelitis of differential diagnoses, which can
in children. Clinical presentation Keywords:
of refusal to bear weight was the hematogenous; delay diagnosis and treatment of
most common clinical symptom. osteomyelitis;
Magnetic resonance imaging was calcaneus; children calcaneal osteomyelitis.”
100% diagnostic in studies that used
this modality, compared with X-rays,
which were 14%-71.4% diagnostic. Introduction
Blood cultures were diagnostic in Osteomyelitis is a relatively common osteomyelitis origin has been reported
27% to 55% of cases, and erythrocyte infection among the pediatric to occur in 43% to 63% of calcaneal
sedimentation rate was elevated in population and can result from a direct osteomyelitis cases.1

DOI: 10.1177/1938640016679704. From the University of Toledo Medical Center, Toledo, Ohio. Address correspondence to: Jiayong Liu, MD, Department of Orthopaedic
Surgery, University of Toledo Medical Center, 3065 Arlington Avenue, Toledo, OH 43614; e-mail: jiayong.liu@utoledo.edu.
For reprints and permissions queries, please visit SAGE’s Web site at http://www.sagepub.com/journalsPermissions.nav.
Copyright © 2016 The Author(s)

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2 Foot & Ankle Specialist
Figure 1.
Flow chart of article selection.
Heel pain in children has a vast array
of differential diagnoses, which can delay
diagnosis and treatment of calcaneal
osteomyelitis.1,3,6,9,11-14 Systemic
symptoms such as fever and leukocytosis
are present in most cases of long-bone
osteomyelitis but are often absent in
calcaneal osteomyelitis, which can
prolong correct diagnosis.4,10,11,12,15
Delays in diagnosis can result in several
complications, such as growth
disturbances, contiguous spread of
infection to surrounding joints, and
additional surgical interventions.2,10,16
Osteomyelitis of the calcaneus is a
relatively rare occurrence, with few
documented case reports and minimal,
small retrospective reviews completed on
the topic. No standard protocol for
diagnosis or treatment has been
established. There has been no
systematic review completed on this
topic. The aim of this review is to
provide a systematic review of diagnosis,
treatment, and outcomes of osteomyelitis
involving the calcaneus.
Methods
A comprehensive literature review was
completed. All types of studies were
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considered, including retrospective
studies, prospective studies, and case
reports. The literature review was
completed primarily using PubMed and
EMBASE research databases. The
references listed in the obtained articles
were also reviewed in efforts to include
all applicable articles. Keywords included
hematogenous, osteomyelitis, calcaneus,
and children.
The inclusion criterion for this study
was based on information provided
within the case report or study. Required
information included the following:
number of participants, age, method of
diagnosis, and method(s) of treatment.
Articles were excluded from the review if
the required information, as noted above,
was not reported. Publishing dates did
not exclude articles from the review.
Only articles available in English, or with
English summaries, were considered for
review; see Figure 1.
The articles were reviewed, and
information was collected and compiled
into tables. Information of interest
included the following: number of cases,
number of male and female patients,
average age, clinical symptoms, time to
diagnosis, method of diagnosis,
organisms cultured, treatments given,
Mon XXXX
including antibiotic and surgical options,
and complications.
Results
In total, there were 18 articles fitting
the inclusion criteria and were included
within the review. There were a total of
243 cases of calcaneal osteomyelitis that
were reviewed; see Table 1. In total, 142
were male and 97 female. Cases reported
by Morrey et al12 did not include gender
and, therefore, did not contribute to the
gender distribution. The average age was
7.6 years. Average time to presentation
was 17.1 days. Previous injury was
reported in 72 of the 243 reported cases
(26.9%), and recent illness was reported
in 35 of 243 cases (14.4%).
Approximately 136 of the 234 (56%)
cases did not report a history of a
previous illness or injury.
Several methods of diagnosing
calcaneal osteomyelitis were reported,
including clinical symptoms and
laboratory testing. Such methods
included the following: blood culture,
tissue/wound culture, bone biopsy,
aspiration, plain X-ray, ultrasound,
magnetic resonance imaging (MRI), bone
scan, laboratory findings of elevated
erythrocyte sedimentation rate (ESR),
C-reactive protein, white blood cell
count, and clinical presentation. Many of
these methods were used in combination
to establish a diagnosis.
Of the cases reporting blood culture,
tissue/wound culture, and bone biopsy,
there were several bacteria found; see
Table 2. Methicillin-sensitive
Staphylococcus aureus was the most
common organism reported. There was 1
documented case of methicillin-resistant
S aureus (MRSA).
Diagnostic modalities reported in the
studies varied significantly; refer to Table
3. ESR elevations were noted in 79% to
97% of cases when considering studies
that included more than 10 cases.2,13,14
Blood culture results varied among
studies and were positive in 27% to 55%
of cases when cultures were obtained.2,14
Magnetic resonance imaging was not
available as a diagnostic tool in earlier
studies but was used in recent
vol. XX / no. X Foot & Ankle Specialist 3

Table 1.
Below are the 18 articles fitting inclusion criteria listed alphabetically by Author.

Reference Number Title Author Number of Cases

4 Osteomyelitis of the calcaneus and talus Antoniou and Conner 13
11 An unusual cause of refusal to walk Clark et al 1
8 Group B β-hemolytic streptococcal osteomyelitis of the Doberstein et al 1
heel. a case report
5 Unusual sites of acute osteomyelitis in childhood Donovan and Shah 5
18 Osteomyelitis of the calcaneus: report of eight cases Feigin et al 8
6 Hematogenous osteomyelitis of the calcaneus Fox and Aponte 1
1 Hematogenous calcaneal osteomyelitis in children Jaakkola and Kehl 21
9 Hematogenous osteomyelitis of the calcaneus in children: Jenzri et al 26
26 cases
15 Calcaneus osteomyelitis from community-acquired MRSA Lee et al 1
2 Pediatric calcaneal osteomyelitis Leigh et al 60
16 Delayed recognition of pediatric calcaneal osteomyelitis: Mallia et al 1
a case report
12 Hematogenous osteomyelitis at uncommon sites in Morrey et al 4
children
3 Osteomyelitis of the calcaneus in children Puffinbarger et al 11
10 Hematogenous osteomyelitis of the calcaneus in children Rasool 14
17 Primary acute and subacute localized osteomyelitis and Robertson 3
osteochondritis in children
7 Acute hematogenous osteomyelitis of the os calcis Schweitzer 1
13 Osteomyelitis of the calcaneum Wang et al 52
14 Hematogenous calcaneal osteomyelitis in children Winiker and Schärli 20
243 Cases in total

Abbreviation: MRSA, methicillin-resistant Staphylococcus aureus.

studies.2,9,15,16 Plain radiographs indicated
diagnostic lesions in 14% to 71.4% of
patients, whereas MRI was diagnostic in
100% of patients imaged.1,2,16
Radiographic descriptions of lesions
were fairly uniform, noting soft-tissue
swelling overlying the lesion and
localized bone destruction with
surrounding inflammation.17 Similar
initial radiographic findings were
reported with the presence of soft-tissue
swelling as the most common
radiographic feature.7,10,15,17,18
Treatment with antibiotics and surgery
were the 2 most common treatment
categories. No studies reported methods
of treatment that differed from these 2
categories. Treatment with antibiotics was
reported as a therapeutic modality in all
studies. The use of antibiotic therapy as
the sole treatment modality was seen in
30% to 48% of cases reported in some
reviews.1,14 The choice of antibiotic,
duration of treatment, and route of
administration differed with each study.
Penicillin, penicillin derivatives,
cephalosporins, clindamycin, and
chloramphenicol were the most
commonly used antibiotics. Intravenous
antibiotics were used most often in the
inpatient setting, with patients being
discharged home on oral equivalents.
Duration of antibiotic treatment most

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4 Foot & Ankle Specialist
Table 2.
Below are the organisms reported
within reviewed articles.
Organisms Cultured
Staphylococcus aureus
Group A β-hemolytic Streptococcus
Staphylococcus epidermidis
Kingella kingae
Klebsiella
Escherichia coli
Micrococcus
Undifferentiated gram positives
Group B Streptococcus
Pseudomonas aeruginosa
Streptococcus bovis
Hemophilus influenzae
Bacillus
Staphylococcus albus
Streptococcus faecalis
Fusobacterium
commonly ranged from 10 days to 5
weeks. Information regarding antibiotic
choice, duration, and route was not
reported in references 9 and 12. There
was no standard measurement of
successful treatment with antibiotics alone;
further studies and criteria are needed to
establish successful antibiotic treatment.
Surgical treatments provided varied
greatly and were not performed in all
cases. The lowest rate of surgical
intervention was reported in 20% of
cases, with the highest rate of surgical
intervention reported being 100%.2,10 The
most common surgical procedures are
noted in Table 4. Indications for surgery
varied among studies, but the most
common indications were continued
pain, localized erythema and swelling
despite initial treatment, and the
presence of abscess or osseous
destruction with imaging.
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Table 3.
Summary of the most commonly used diagnostic modalities and the corresponding
diagnostic percentage.
Diagnostic Modalities
Culture results
Erythrocyte sedimentation rate
Radiographic imaging
X-ray
Magnetic resonance imaging
Immobilization was not consistently
used as a treatment modality. Winiker
and Schärli14 reported that 100% of
patients were placed in plaster casts
postoperatively to decrease
mobilization and weight-bearing
activity.14 Splinting was occasionally
preformed prior to diagnosis because
of initial misdiagnosis.12 There have
been no reported benefits to
immobilization with calcaneal
osteomyelitis.
Complications were reported in 9 of
the reviewed articles and are listed in
Table 5. Recurrence of osteomyelitis
was the most common complication
and was found in up to 17% of cases.2
It is unclear based on the information
within the articles if there is an
association between the duration of
antibiotic use and the development of
recurrence. One study found ankle
ankylosis and limited range of motion
in 27% of cases along with chronic
fistula formation in 26% of cases.9
However, these poor outcomes were
only reported in patients with delayed
presentation/diagnosis, with onset of
symptoms on average 17 days before
initial evaluation.9 Growth
abnormalities were reported as
complications, with incidence ranging
from 3.8% to 9%.3,13 Although growth
abnormalities were noted, most were
asymptomatic and noted only on
radiographic imaging.3,13 Complications
were most commonly seen in patients
presenting 6 to 15 days after onset of
symptoms.10
Mon XXXX
Diagnostic Percentage
27%-55%
79%-97%
14%-71.4%
100%
Discussion
Osteomyelitis within the pediatric
population is a common occurrence and
typically involves the metaphysis of long
bones but can involve atypical locations,
such as the calcaneus. The calcaneal
epiphysis demonstrates vascular anatomy
and blood flow that is similar to
metaphyseal vasculature, allowing the
calcaneus to behave similar to the
metaphysis of a long bone.4,9,11 Reduced
blood flow in this area of bone can lead
to hematogenous spread of bacteria,
predisposing the calcaneus to infection
without direct trauma.11
Diagnosis of calcaneal osteomyelitis is
often delayed because of an atypical
presentation.4,10,11,12,15 Among the
literature reviewed, the most common
initial presenting symptoms of
osteomyelitis of the calcaneus were
severe refusal to bear weight, localized
tenderness, pain, and swelling.
Additionally, history of a prior injury
was reported in 26.9% of cases and a
recent illness in 14.4%. This information
suggests that although prior illness and
injury are not present in the majority of
cases, they are not uncommon
occurrences. If a history of recent
illness or injury is present, osteomyelitis
of the calcaneus should be considered.
The average age of presentation was
7.6 years, with a 58.4% male
predominance. A high index of
suspicion, given clinical presentation
and patient demographics, must be in
place for identification and early
treatment. The focus must be on an
vol. XX / no. X Foot & Ankle Specialist 5

Treatments described in the literature MRI and should be completed in

Table 4. focused on antibiotic therapy and patients if the clinical history and exam
The four most common surgical surgical intervention. A variety of is suggestive of osteomyelitis and/or
procedures described in the surgical techniques were used (see symptoms worsen or do not improve.
reviewed articles. Table 4) in management; however, there Initiating conservative treatment with
is little data to suggest which technique antibiotics early in the disease process
Most Common Surgical provides the best clinical outcome. may prevent the need for surgical
Procedures Further studies are needed to compare interventions and further prevent
operative techniques. It is unclear which complications. Specific guidelines and
Irrigation specific antibiotics should be initiated as protocols for the diagnosis and
Incision and debridement also the duration and route. The management of hematogenous calcaneal
antibiotic choice in many of the studies osteomyelitis cannot be determined
Curettage was initially empirical and then later based on the information gathered in
Abscess evacuation/aspiration switched to a pathogen-specific this study because of the vast variation
antibiotic based on culture results. The of modalities utilized. However, with the
most common organism cultured in all information provided, future prospective
the studies was S aureus and, therefore, studies regarding the diagnosis and
would be appropriate to initiate management of hematogenous calcaneal
treatment with antibiotics to cover osteomyelitis can be completed.
Table 5. methicillin-sensitive S aureus. Local Furthermore, the concepts and
Reported complications described in sensitivities and susceptibilities should principles of hematogenous
9 of the reviewed articles. be considered if S aureus is suspected. osteomyelitis of the calcaneus in
MRSA was found in 1 case, and children can be applied to other regions
Complications therefore, empirical treatment against of the lower limb, including the foot
MRSA should not be initiated.15 In many and ankle.
Recurrent osteomyelitis
cases, intravenous antibiotics were given
Additional surgery while awaiting surgery and
postoperatively, subsequently switching References
Limited range of motion 1. Jaakkola J, Kehl D. Hematogenous
to oral solutions on discharge. No
calcaneal osteomyelitis in children.
Prolonged toe walking standard of care was recognized. J Pediatr Orthop. 1999;19:
Duration of treatment was also variable, 699-704.
Permanent calcaneal defects/ with no specific course reported.
deformity 2. Leigh W, Crawford H, Street M, Huang
Further prospective studies regarding M, Manners S, Puna R. Pediatric
Ankle ankylosis antibiotic regimens need to be calcaneal osteomyelitis. J Pediatr Orthop.
completed in order to assess the most 2010;30:888-892.
Chronic fistulas beneficial treatment options regarding 3. Puffinbarger WR, Gruel CR, Herndon WA,
antibiotics. Sullivan JA. Osteomyelitis of the calcaneus
Arthritis in children. J Pediatr Orthop. 1996;16:
Limitations of the study were reflective
224-230.
Growth abnormality of the nature of the study. This study was
4. Antoniou D, Conner AN. Osteomyelitis of
a literature review, containing mostly
Adverse antibiotic reaction the calcaneus and talus. J Bone Joint Surg
retrospective studies. No randomized Am. 1974;56:338-345.
Clostridium difficile entercolitis controlled studies were found on this 5. Donovan RM, Shah KJ. Unusual sites of
topic. acute osteomyelitis in childhood. Clin
Scar sensitivity Osteomyelitis involving the calcaneus Radiol. 1982;33:222-230.
Calcanectomy/Talectomy has not been well reported in the 6. Fox IM, Aponte JM. Hematogenous
literature, and no standardized approach osteomyelitis of the calcaneus. J Am
Gangrene to diagnosis and treatment exists. Podiatr Med Assoc. 1993;83:681-684.

Avascular necrosis
Abscess formation
earlier diagnosis in order to improve
prognosis and prevent potential adverse
complications as outlined in Table 5.
Delaying the diagnosis and treatment 7. Schweitzer G. Acute haematogenous
can put the patient at risk of developing osteomyelitis of the os calcis. Med J Aust.
chronic and debilitating complications. 1967;1:1179-1180.
Diagnosis often involves a high clinical 8. Doberstein C, MacEwen GD,
Lee MS. Group B β-hemolytic
suspicion given the history and physical
streptococcal osteomyelitis of the heel:
exam and can be supported by elevated a case report. Clin Orthop Relat Res.
ESR, positive blood cultures, and 1988;(231):225-228.
abnormalities noted on X-ray and MRI. 9. Jenzri M, Safi H, Nessib MN, et al.
An earlier diagnosis can be made with Hematogenous osteomyelitis of the

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6 Foot & Ankle Specialist
calcaneus in children: 26 cases. Rev Chir
Orthop Reparatrice Appar Mot. 2008;94:
434-442.
10. Rasool MN. Hematogenous osteomyelitis of
the calcaneus in children. J Pediatr Orthop.
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11. Clark JR Jr, Trautwein LM, Campbell JR.
An unusual cause of refusal to walk.
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323-325.
12. Morrey BF, Bianco AJ, Rhodes KH.
Hematogenous osteomyelitis at uncommon
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Osteomyelitis of the calcaneum. J Bone
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14. Winiker H, Schärli AF. Hematogenous
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15. Lee MC, Tashjian RZ, Eberson CP.
Calcaneus osteomyelitis from community-
acquired MRSA. Foot Ankle Int.
2007;28:276-280.
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16. Mallia AJ, Ashwood N, Arealis G, Bindi F, Zamfir
G, Galanopoulos I. Delayed recognition
of pediatric calcaneal osteomyelitis: a case
report. J Med Case Rep. 2015;9:185.
17. Robertson DE. Primary acute and
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osteochondritis in children. Can J S.
1967;10:408-413.
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Middelkamp JN. Osteomyelitis of the
calcaneus: report of eight cases. Am J Dis
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