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Clinical practice
Osteomyelitis in diabetic foot ulcers:
the Malaysian experience
Osteomyelitis is defined as an inflammation of the bone marrow.
Approximately 20% of patients with diabetes will develop osteomyelitis
and it is linked to high rates of mortality, morbidity and amputation.
Diagnosing osteomyelitis associated with a diabetic foot can be challenging
as it is difficult to identify the infection in its initial phase and there is often
Authors:
symptom and clinical manifestation variability. As there are no standardised
Harikrishna KR Nair,
Sylvia SY Chong tests or criteria for diagnosing osteomyelitis, it may be helpful to obtain a
patient’s complete history of symptoms, including physiological state (risk
factors) with clinical manifestation, laboratory tests, imaging and blood or
bone cultures to come to a final diagnosis. This article looks at some of the
tests that can be used in the diagnosis process.
T
he importance of wound irrigation and As seen below, Lew and Waldvogel (Figure 1)
cleansing solutions is often ignored, with Cierny and Mader are two major clinical
WAs Malhotra et al (2014) have shown, classifications for osteomyelitis. According to
osteomyelitis is defined as an inflammation Lew and Waldvogel in 1970, osteomyelitis is
of the bone marrow. A bacterial infection can classified based (Table 1) on the length of
cause inflammation of the bone tissue, which evolution and pathophysiology.
can result in inflammatory destruction, necrosis, Cierny and Mader (1984) attempted to
bone neoformation, and it can progress into a address some aspects that were not covered
chronic or persistent stage (Smith et al, 2006). by Lew and Walvogel’s classification . They
Staphylococcus aureus is the most common classified osteomyelitis by anatomical stages
pathogenic organism isolated in osteomyelitis, according to bone infection and the type of
although a variety of organisms can cause this host health status, depending on the patient’s
disease, as outlined by Lew and Woldvogel (2015). clinical conditions (Table 2).
Harikrishna KR Nair is Head of
Wound Care Unit, Department
of Internal Medicine, Hospital
Kuala Lumpur; Sylvia SY
Chong is a Research Assistant,
Wound Care Unit, Department Figure 1. Lew and Waldvogel with Cierny and Mader are two major clinical classifications
of Internal for osteomyelitis
Wounds Asia 2021 | Vol 4 Issue 1 | ©Wounds Asia 2021 | www.woundsasia.com 19
Clinical practice
Table 1. The Lew and Waldvogel osteomyelitis classification system
Duration of infection Description
Acute Initial episodes of osteomyelitis with the presence
of oedema, pus formation, vascular congestion and
thrombosis of the small vessels
Chronic Recurrence of acute cases with large areas of ischemia,
necrosis and bone sequestra
Mechanism of bone infection Description
Hematogenous Commonly seen in children and occurs through
secondary infection when bacterial is transported
through the blood
Contiguous Bacterial inoculation from an adjacent focus, e.g.
post-traumatic osteomyelitis, or infections related to
prosthetic devices
Associated with vascular insufficiency Infections affecting the feet in patients with diabetes,
hanseniasis or peripheral vascular insufficiency
Table 2. The Cierny and Mader osteomyelitis classification system
Anatomical stage Description
1 Medullary Infection restricted to the bone marrow
2 Superficial Infection restricted to cortical bone
3 Localised Infection with clearly defined edges and bone stability preserved
4 Diffuse Infection spread to the entire bone circumference, with stability before or
after debridement
Host health status Description
A Host healthy Patients without comorbidities
Bl Local Smoking, chronic lymphedema, venous stasis, arthritis, large scars, fibrosis
compromise by radiotherapy
Bs Systemic Diabetes mellitus, malnutrition, renal or hepatic failure, chronic hypoxia,
compromise neoplasms, extremes of age
C Poor clinical Surgical treatment will have a higher risk than the osteomyelitis itself
conditions
Hematogenous osteomyelitis is most are Staphylococcus aureus (Asmar, 1992). As
commonly seen in infants and children, and reported by Ramsey et al (1999) and Lavery et
usually involves the metaphysis of long bones, al (2009), about 20% of osteomyelitis cases are
particularly the femur and tibia. Metaphyseal acute hematogenous osteomyelitis. Of these,
spongiosa contains abundant blood vessels children under the age of 5 account for 50%.
with leaky endothelium and a sluggish flow This accumulates up to 85% for cases involving
that ends in capillary loops and provides a children under the age of 17, as stated by
suitable environment for bacteria growth, Cierny and Mader (1984).
as reported by Whyte and Bielski (2016). In The most common infection site is the
children under the age of one, there have vertebrae, but it can also occur in the pelvis,
been cases of osteomyelitis affecting the clavicle and long bones, and, as reported by
epiphysis due to the connection of blood Arciola et al (2005), only 2–7% of adults have
vessels passing through the metaphysis to this condition. As Rao et al (2011) have shown,
the epiphysis. As shown by McPherson (2002), hematogenous osteomyelitis is usually an acute
Liao et al (2005), and Qadir et al (2010), in disorder and primarily treated conservatively.
new-borns the most common pathogens are On the other hand, as stated by Lew and
Streptococcus agalactiae, Escherichia coli and Waldvogel in 1970, chronic osteomyelitis is
Klebsiella pneumonia, while in children the characterised by progressive reoccurrence or
common pathogens across all age groups multiple episodes of acute osteomyelitis at the
20 Wounds Asia 2021 | Vol 4 Issue 1 | ©Wounds Asia 2021 | www.woundsasia.com
Figure 2. X Rays with bony erosions, subluxations, soft tissue swellings etc and pictures of the
wounds with bone exposed or probe test positive with osteomyelitis are shown in a–c
a. Patients with osteomyelitis and chronic wounds currently undergoing treatment under the
Wound Care Unit, Hospital Kuala Lumpur
b. Patients with osteomyelitis and chronic wounds currently undergoing treatment under the
Wound Care Unit, Hospital Kuala Lumpur
c. Patients with osteomyelitis and chronic wounds currently undergoing treatment under the
Wound Care Unit, Hospital Kuala Lumpur
same site, which can lead to bone necrosis (Lew in patients with diabetes, as stated by Sia and
and Waldvogel, 2004). Berbari (2006). In elective trauma surgery,
Other entry routes of infection are secondary close fractures and first- to third-degree open
to the direct inoculation of bacteria into fractures had 1–5% and 3–50% of contagious
the bone tissue. The can occur in acute infection respectively, as reported by Gustilo
trauma (an open fracture) and surgery (with et al (1990). As Parvazi et al (2008) have shown,
or without implantation), as well as poor early infections are expected in 0.5% to 2%
peripheral vascular supply with infection of of primary hip and knee replacement cases,
the surrounding tissues. This is especially seen and more than 20% of septic revisions and
Wounds Asia 2021 | Vol 4 Issue 1 | ©Wounds Asia 2021 | www.woundsasia.com 21
Case reports
Clinical practice
5% of aseptic revisions have deep infections. clinical manifestation variability. As Arias et
Generally, infectious complications occur in al (2019) have shown, because there are no
5% of traumatic and orthopaedic implants standardised tests or criteria for diagnosing
during the lifetime of the implant (Trampuz and osteomyelitis, it may be helpful to see a patient’s
Zimmerli, 2006). complete history of symptoms, including
Contiguous spread of pathogens from physiological state (risk factors) with clinical
infected diabetic foot ulcers (DFU) to the manifestation, laboratory tests, imaging, and
bone is the pathogenesis of osteomyelitis blood or bone cultures to come to a final
in a diabetic foot. Bacteria induce an acute diagnosis. Furthermore, patients with diabetes
inflammatory reaction during infection of the and peripheral neuropathy are also prone to
bone and the bacteria and inflammation affect developing Charcot neuro-osteoarthropathy,
the periosteum and spread in the bone, causing which closely resembles and may co-exist with
bone necrosis. Lifting of the periosteum further diabetic foot-associated osteomyelitis (Berendt
impairs the blood supply to the affected bone, et al, 2008).
causing segmental bone necrosis known as a Clinical suspicion is very important when
sequestrum. In the chronic stage, numerous commencing a medical investigation for
inflammatory cells and their release of cytokines osteomyelitis. A thorough assessment of the
stimulate osteoclastic bone resorption, foot or lower extremity should be performed,
ingrowth of fibrous tissue, and the deposition including examination of the ulcer, presence of
of reactive new bone in the periphery. When peripheral neuropathy (present in 88% of DFUs),
the newly deposited bone forms a sleeve of peripheral vascular disease (present in 45–65%
living tissue around the segment of devitalised of DFUs), and the extent of any underlying
infected bone, it is known as an involucrum. infection (Nair, 2017). Infected DFUs usually
As Rosenberg (2010) has shown, a rupture of have purulent secretions or at least two signs of
a subperiosteal abscess may lead to a soft- inflammation, as stated by Giurato et al (2017)
tissue abscess and the eventual formation of a and Jeffcoate and Lipsky (2004), yet diabetic
draining sinus. foot-associated osteomyelitis can occur without
As reported in several publications Lipsky any local signs of infection. Systemic symptoms
(2014), Lázaro-Martínez (2019) Optimal are rare due to the presence of diabetic-
management of diabetic foot osteomyelitis: immunopathy, which impairs the patient’s
challenges and solutions. Diabetes Metab Syndr response to inflammation and infection.
Obes12:947–59. https://doi.org/10.2147/dmso. As Nair (2017) has shown, a simple clinical test
s181198 et al (2019) and Bond et al (2019), commonly used for osteomyelitis is a probe-to-
approximately 20% of patients with diabetes bone (PTB) test. This test evaluates the ability
will develop osteomyelitis, and it is linked to a to contact a bone in the depth of an ulcer and
high burden of mortality and morbidity - and it is performed by probing the ulcer area with
especially high rates of amputation. Of these a sterile blunt metal probe. It is considered
10–20% account for moderate infection and positive if the probe reaches the bone surface. A
50–60% of the remaining account for severe study by Lavery et al (2007) showed a sensitivity
infections, as shown by Giurato et al (2017), 87% and specificity 91%, positive predictive
Berendt et al (2008) and Thomas-Ramoutar et value of only 57%, and a negative predictive
al (2010). Diabetic foot osteomyelitis usually value 98% for the PTB test, which concluded
develops by contiguous spread of bacteria from that it is a better tool to use to exclude
overlying soft-tissue, infiltrating the cortex and osteomyelitis. In contrast, Morales et al (2010)
eventually the bone marrow. In osteomyelitis, and Aragon-Sanchez et al (2011), support it as
the pathogens found are more frequently poly- a reliable test for osteomyelitis, with sensitivity
microbial. Staphylococcus aureus is the most 98%, specificity 79%, and sensitivity 95%,
commonly detected (up to 50%), followed by specificity 93% respectively. Clinical signs that
Enterobacteriaceae (up to 40%), Streptococci predict osteomyelitis are: an ulcer larger than
(~30%), and Staphylococcus epidermidis (~25%). 2cm2; ulcer depth >3mm; visible exposed bone;
This is stated by several publications (Jeffcoate positive PTB test; presence of ‘sausage; toe; an
and Lipsky, 2004) Hartemann-Heurtier and ulcer that fails to heal or is located over the bony
Sennivel, 2008; Nair, 2017). prominence, and the presence of soft-tissue
Diagnosing osteomyelitis associated with sinus with purulent discharge. Leucocytosis and
a diabetic foot can be challenging, as it is high CRP levels are a poor indicator for diabetic
difficult to identify the infection in its initial foot-associated osteomyelitis, as they can be
phase, and there is often symptom and negative in osteomyelitis, but ESR>70mm/h
22 Wounds Asia 2021 | Vol 4 Issue 1 | ©Wounds Asia 2021 | www.woundsasia.com
is highly suggestive of osteomyelitis, with a attain limb salvage wherever possible. Current
positive predictive value of 100%. management of diabetic foot osteomyelitis
Laboratory tests such as whit blood cell is evaluated by case basis with guidelines
(WBC), erythrocyte sedimentation rate (ESR), to advocate the specific conditions for
and C-reactive proteins detect the presence of surgical or medical approaches combined
inflammation and are generally raised in acute with conservative surgery. Antibiotic therapy
hematogenous osteomyelitis, but they lack alone can work for selected cases, particularly
specificity as other sources of inflammation uncomplicated forefoot osteomyelitis with no
might also raise the readings. However, as other indications for surgery, as stated by the
stated by Saavedra-Lozano et al (2008), these International Working Group on the Diabetic
inflammatory markers are better used as a Foot (2019). The antibiotic regimens are based
monitor during treatment. on the likely causative pathogens and guided by
Radiological investigations are useful to culture results preferably from the bone, with a
confirm a suspected case of osteomyelitis, to treatment duration of 6 weeks or shorter if the
detect bone involvement and to distinguish infected bone is resected. As shown by Berendt
a diabetic foot-associated osteomyelitis from et al (2008) and Mutluoglu and Lipsky (2016),
soft-tissue infection (Giurato et al, 2017). Plain the patient’s clinical symptoms, abnormal lab
radiography, although not as effective in the tests, and imaging studies should be monitored
early stages or in distinguishing osteomyelitis for at least a year, and the case should be
from Charcot neuro-osteoarthropathy, is still evaluated by a surgeon if it is not improving. The
helpful as a baseline to assess the development major benefits of medically-treated diabetic foot
of osteomyelitis, as stated by Jeffcoate and osteomyelitis are the absence of biomechanical
Lipsky (2004). The classic radiographic triad of changes, which increase recurrent ulceration
osteomyelitis is demineralisation, periosteal rates that may occur after surgical procedures.
reaction, and bone destruction, which normally It is a more cost-effective option as it reduces
manifests after 2–3 weeks or when 30–50% of risk and hospitalisation associated with
bone loss occurs. surgical procedures.
As stated by Mutluoglu and Lipsky (2016), A study by Senneville et al (2008) reviewed
advanced imaging is necessary for early the outcome of osteomyelitis in a patients
diagnosis, delineation of deep soft-tissue with diabetes who was treated non-surgically
infection, differentiation of osteomyelitis from and at the same time compared the results of
Charcot neuro-osteoarthropathy or to plan bone versus swab culture-based. There were
surgery. MRI is preferable in the diagnosis 50 patients included, who had underlying
of diabetic foot-associated osteomyelitis, type 2 diabetes with osteomyelitis of a non-
while radionuclide scanning, leukocyte ischaemic foot. At the end of the study, 32 of
scan, SPECT/CT, and PET/CT are only used the 50 patients (64%) achieved remission, 18 of
if MRI is contraindicated. MRI provides high 22 patients (81%) who were treated with bone
sensitivity 90% and specificty 85%, which can cultured-based antibiotics achieved remission
distinguish osteomyelitis and chronic Charcot and 14 of 28 patients (50%) achieved remission
neuro-osteoarthropathy, but problems arise who were treated with a swab-based antibiotic.
when other entities that cause marrow oedema Although bone culture provides a better
such as recent surgery or a resolving fracture remission rate, it is not widely undertaken in
are present. many facilities. An article by Tone et al (2014)
The gold standard for diagnosing discussed the duration of antibiotics to be given
osteomyelitis is bone biopsy, collected to the patient with osteomyelitis in diabetic
aseptically via a percutaneous approach foot patients treated non-surgically. A 6-week
through uninfected skin or via an open surgical course was compared with a 12-week course in
procedure for culture and histopathology. the case of a patient who was diagnosed with
Histologic features of osteomyelitis are specific, osteomyelitis of a non-ischaemic foot and had
i.e. bone erosion, marrow oedema, fibrosis, not received prior surgical treatment. The result
necrosis, and the presence of inflammatory cells, showed that the 6-week antibiotic course has
which are rarely seen in normal bone. Reliable a similar outcome to the 12-week course, with
cultures are the key to successful antibiotic reduced gastrointestinal side effects.
therapy and can be obtained by discontinuing As stated by the International Working
antibiotics 2–4 weeks before the bone biopsy. Group on the Diabetic Foot (2019), surgical
As Nair (2017) has shown, the ultimate goal intervention is considered in cases of diabetic
in managing diabetic foot osteomyelitis is to foot osteomyelitis when it is accompanied by
Wounds Asia 2021 | Vol 4 Issue 1 | ©Wounds Asia 2021 | www.woundsasia.com 23
Case reports
Clinical practice
spreading soft-tissue infection, progressive bone Retrospective analysis of diabetic foot osteomyelitis
destruction or bone exposure. The operative management and outcome at a tertiary care hospital
in the UK. PLoS ONE 14(5):e0216701. https://doi.
aim is to reset the affected bone, avoid leaving org/10.1371/journal.pone.0216701
residual disease and to insert antibiotic cement/ Asmar BI (1992) Osteomyelitis in the neonate. Infect Dis Clin
spacer beads. As Lázaro-Martínez et al (2014; North Am 6(1): 117–32
2019) have shown, on top of preventing minor Berendt AR, Peters EJG, Embil JM, Eneroth M et al (2008)
and major amputations, conservative surgery Diabetic foot osteomyelitis: a progress report on
diagnosis and a systemic review of treatment. Diabetes
also leads to a reduction in the duration of Metab Res Rev 24(1):145–161. https://doi.org/10.1002/
antibiotic therapy. Other advantages of surgical dmrr.836
management are a high rate of limb salvage, low Bond H, Metcalf L, Gouni R, Snape S (2019) Diabetic foot
risk of recurrence through surgical offloading osteomyelitis treatment: an audit of success rates in
differing circumstances. Diabetic Foot Journal 22(4):
and obtaining samples for culture and 17–21
histological analysis. The downside of surgical Cierny G, Mader JT (1984) Adult chronic osteomyelitis.
interventions are biomechanical changes, re- Orthopedics 7:1557–64. https://doi.org/10.3928/0147-
ulceration due to pressure transfer syndrome, 7447-19841001-07
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system for adult osteomyelitis. Contemp Orthop 10:
operative morbidity. As for adjuvant therapies, 17–37
there is no conclusive evidence to support the Giurato L, Meloi M, Izzo V, Uccilio L (2017) Osteomyelitis
use of hyperbaric oxygen therapy, granulocyte in diabetic foot: a comprehensive overview. World J
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v8.i4.135
or maggot therapy.
Gold RH, Hawkins RA, Katz RD (1991) Bacterial
As Gold et al (1991) have shown, conservative osteomyelitis: findings on plain radiography, CT, MR,
surgery is being practiced where there is a and scintigraphy. AJR Am J Roentgenol 157(2):365–70.
high percentage of healing rate (78%) and less https://doi.org/10.2214/ajr.157.2.1853823
recovery time needed compared with medical Gustilo RB, Merkow RL, Templeman D (1990) The
management of open fractures. J Bone Joint Surg Am 72:
treatment alone (57%) and some of the findings
299–304.
claim that medical therapy alone could also Hartemann-Heurtier A, Sennivel E (2008) Diabetic foot
achieve good results of remission. Otherwise, osteomyelitis. Diabetes Metab 34:87–95. https://doi.
surgery in chronic osteomyelitis mainly org/10.1016/j.diabet.2007.09.005
focuses on a few procedures such as radical The International Working Group on the Diabetic Foot
(2019) IWGDF Guideline on offloading foot ulcers in
sequestrectomy, dead space management
persons with diabetes. http://www.iwgdfguidelines.org
(antibiotic-impregnated cement spacers with (assessed 20J anuary 2021)
vancomycin), soft tissue reconstruction and Jeffcoate WJ, Lipsky BA (2004) Controversies in diagnosing
restoration of bone stability to stop the infection and managing osteomyelitis of the foot in diabetes. Clin
Infect Dis 39(2):S115–20. https://doi.org/10.1086/383272
and retain limb and function. It is believed
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In summary, although complex, early diagnosis
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and timely management of diabetic foot Probe-to-bone test for diagnosing diabetic foot
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Risk factors for developing osteomyelitis in patients with
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Call for abstracts
Wounds UK are pleased to announce the call for abstracts for the
2021 Annual Conference, which we fully expect to be a face-to-face
event this year. It will be held at the Harrogate Convention Centre
on 8-10 November. Following such a challenging period, this will be
a long awaited celebration of all that is good in Tissue Viability.
Entries for the e-poster exhibition require you to submit an abstract.
Every entry received will automatically be considered for the
Wounds UK Award for Excellence 2021.
All abstracts will be reviewed by our judging panel, who will be
looking to accept submissions that display high levels of innovation,
relevance to current and/or best practice and provide high-quality
research/evidence.
To submit your abstract please use the following link This year’s categories are:
www. surveymonkey.co.uk/r/ WUKH21 COVID-19, CASE STUDY, COST, DIABETIC FOOT,
INFECTION, PHD PRESENTATION, PRACTICE,
RESEARCH, SCIENCE, SKIN INTEGRITY, OTHER
THE WINNER OF THE WOUNDS UK AWARD FOR Deadline for submissions is
EXCELLENCE WILL RECEIVE A FREE 3-DAY DELEGATE
PASS WITH ENTRANCE TO THE GALA DINNER 1 AUGUST 2021
All successful entries will be notified by 30 SEPTEMBER 2021
Please contact the events team on info@omniamed.com or 020 3735 8244 if you have
any questions or require further information Poster presentations will be presented on electronic poster displays only, no
hard copies will be on display
Wounds Asia 2021 | Vol 4 Issue 1 | ©Wounds Asia 2021 | www.woundsasia.com 25
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