Infection: Long Bone Osteomyelitis in Adults: Fundamental Concepts and Current Techniques

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■ trauma update

Section Editors: David J. Hak, MD, MBA & Philip F. Stahel, MD

infection
S P OT L I G H T O N
ERRATUM

This article has been amended to include a factual correction. An error was identified subsequent to its original
printing (2013; 36[5]:368-375), which was acknowledged in an erratum printed in 2014; 37(1):16. The online
article and its erratum are considered the version of record.

Long Bone Osteomyelitis in Adults:


Fundamental Concepts and Current
Techniques
Julia Sanders, MD; Cyril Mauffrey, MD, FRCS

to retained humor.2 Warfare behind the disease process are


Abstract: Osteomyelitis is challenging for orthopedic sur- in the 20th century spurred reviewed and the current tech-
geons. The fundamental basis of osteomyelitis treatment is
advances in plastic and ortho- niques for the management of
wide surgical debridement. A variety of operative techniques
pedic surgery and, along with osteomyelitis are discussed.
exist for soft tissue coverage and segmental bony stabilization;
the introduction of penicillin An algorithm for treatment
however, extensive resection remains the crucial starting point
in the 1940s, pointed the treat- based on these concepts and
in a comprehensive treatment plan. Antibiotic therapy con-
ment of osteomyelitis in the techniques is presented and
tinues to be a cornerstone of adjuvant therapy; nevertheless,
the length of treatment is still debated. With ever-increasing direction that has taken today.3 illustrated using clinical ex-
antimicrobial resistance rates, targeted therapy based on ac- Unfortunately, the man- amples.
curate cultures has become imperative. Osteomyelitis requires agement of osteomyelitis has
a multidisciplinary team prepared to formulate an individual- been given too little attention EPIDEMIOLOGY
ized surgical and medical plan for each patient. The aim of to date, and quality clinical Although many break-
the current article is to highlight and summarize the current trials to support treatment throughs have been made in
concepts in the management of long bone osteomyelitis. practice are scarce. The vari- the field of infectious disease
ability in practice and lack of over the past decades, osteo-
standardization highlights the myelitis remains a difficult

O steomyelitis is a chal-
lenge for orthopedic sur-
geons. Bone provides a unique
ated by both pathophysiol-
ogy and treatment algorithms.
Hippocrates first described the
latter statement. A treatment
algorithm that is based on a
classification scheme with a
problem for the orthopedic
community, particularly in
busy trauma centers that care
harbor for microorganisms disease, recommending splint- poor interobserver variability for open and complex frac-
that produce biofilms, allow- ing and clean dressings for can contribute to this difficul- tures. Infection rates in open
ing them to attach resiliently open fractures and highlight- ty. Furthermore, few centers long bone fractures range from
to biologic and implanted ing the risk of bone infection.1 treat a high volume of patients 4% to 64%.4 A recent study
surfaces while remaining in- Ambroise Paré, a French sur- that would be sufficient to showed that even in patients
susceptible to host defenses. geon, described his own open develop evidence-based algo- receiving state-of-the-art or-
Acute and chronic phases of tibia fracture that developed an rithms. Finally, surgical meth- thopedic and plastic surgical
osteomyelitis are differenti- infection, and attributed this ods aimed at local excision of care, 23% of patients devel-
the lesion are bound to failure; oped infections after an aver-
The authors are from the Department of Orthopaedics, Denver Health the infected tissue within bone age of 3 procedures per limb.5
Medical Center, Denver, Colorado. has the potential to spread, Chronic infections are both
The authors have no relevant financial relationships to disclose.
and wide excision with clear expensive and challenging to
Correspondence should be addressed to: Cyril Mauffrey, MD, FRCS,
Department of Orthopedics, Denver Health Medical Center, 777 Bannock St, margins is the most valid treat- treat and cure rates are still
Denver, CO 80204 (cyril.mauffrey@dhha.org) ment philosophy. In this arti- not optimal. Ideally, treatment
doi: 10.3928/01477447-20130426-07 cle, the fundamental concepts methods should offer complete

368 ORTHOPEDICS | Healio.com/Orthopedics


■ trauma update

resolution of infection and op- The Cierny-Mader system


timized function and mobil- identifies 4 anatomic types of
ity of the affected extremity. osteomyelitis (Figure 1): med-
Currently, despite advances ullary (type I), superficial (type
in both surgical and chemical II), localized (type III), and
treatment, recurrence rates fol- diffuse (type IV). Medullary
lowing bony infection are be- disease involves the internal
tween 20% and 30%.6 surface of the bone only, often
associated with intramedul-
CLASSIFICATION lary hardware. Superficial os- 1A 1B
Several classification sys- teomyelitis is often associated
tems have been devised for with soft tissue infections that
osteomyelitis, but the Cierny- spread down to bone, such as
Mader system remains the most the base of an open pressure
clinically relevant. This system ulcer. Localized disease in-
stratifies hosts into 3 categories volves the full thickness of the
(A-C) based on physiologic cortex and is essentially a deep
comorbidities and designates 4 extension of a superficial pro-
anatomic stages of infection (1- cess. These lesions are limited
4), which are combined to pro- enough that surgical resec-
1C 1D
duce 12 classifications.7 This tion of involved bone leaves Figure 1: Cierny and Mader classification showing the 4 anatomic types
of osteomyelitis known as medullary (A), superficial (B), localized (C), and
system assists in clinical deci- a stable segment. In contrast, diffuse (D).
sion making for the extent of diffuse osteomyelitis is a full-
surgical debridement, as well thickness infection extensive
as antibiotic therapy. enough to require fixation Contiguous spread of infection negative bacilli are also iso-
Host factors are impor- following debridement due can be caused by surgery, partic- lated. Antimicrobial-resistant
tant in determining treat- to instability.7 This classifica- ularly the placement of prosthe- organisms have become more
ment algorithms. According tion system still guides treat- ses or hardware, and trauma or common, and a recent study
to the Cierny-Mader system, ment despite having a poor other foreign body introduction. of approximately 200 patients
a type A host is a healthy pa- interobserver variability. It is Osteomyelitis can also arise sec- noted that no single antibiotic
tient without comorbidities often difficult to differentiate ondary to vascular insufficiency, regimen would adequately
that might affect their ability between a medullary and a su- commonly from a soft tissue in- treat the infections.11 Rarely,
to heal. Type B hosts have 1 perficial or localized infection. fection in patients with diabetes tuberculosis, other atypical
or more comorbidities that Magnetic resonance imaging mellitus. mycobacterium, and fungi
increase their risk of treat- often shows a diffuse appear- In the hematogenous form, may also cause osteomyelitis.
ment failure, including local ance, which is a more accurate a single pathogen is usu-
(eg, vascular disease, chronic and realistic representation of ally isolated, with the most PATHOGENESIS
edema, fibrosis from radiation the infectious process. common organism being At the onset of infection
or scarring, and obesity) and Staphylococcus aureus.10 In in osteomyelitis, immediate
systemic factors (eg, drug use, ETIOLOGY contrast, osteomyelitis sec- vascular changes occur that
age, diabetes mellitus, malig- Osteomyelitis can arise sec- ondary to contiguous spread compromise blood flow to the
nancy, immune deficiencies, ondary to hematogenous spread or direct inoculation is usu- bone. If the infection is not
and malnutrition).8 Type C or from a contiguous source of ally caused by multiple organ- eradicated before the bone
hosts are compromised to the infection. Hematogenous infec- isms. Polymicrobial infection dies, a sequestrum develops
point that the benefits of treat- tion is more common in those was responsible for approxi- and provides a base for the
ment are outweighed by the younger than 20 years and older mately 30% of infections in formation of a microbial bio-
possible risks. These patients than 60 years and is the least one series.11 Staphylococcus film. Biofilms are comprised
are offered palliation or treated common form of the disease. aureus is the most common of exopolysaccharide poly-
expectantly while their comor- It rarely causes osteomyelitis isolate in polymicrobial infec- mers forming a protective
bidities are addressed. of the long bones in adults.9 tions, but anaerobes and gram- fibrous matrix around host

MAY 2013 369


■ trauma update

ism responsible for deep infec- scans (Figure 3). Often, more
tion.14 Cierny8 recommended than 1 type of imaging is needed
using polymerase chain reac- for adequate diagnosis and sur-
tion DNA pyrosequencing to gical planning. Radiographic
detect and characterize micro- changes are visible approxi-
organisms. Prolonged culture mately 2 weeks after the physi-
(up to 14 days) has also been ologic process of infection be-
recommended to increased gins. The classic signs on plain
sensitivity for low-virulence radiographs include periosteal
organisms because 7-day cul- reaction and osteopenia.10 As
tures only provided evidence the infection progresses, radio-
2A 2B of infection in 64% of patients graphic signs (in order of ap-
Figure 2: Anteroposterior (A) and lateral (B) radiographs of a distal femur in a recent series.11 pearance) are soft tissue swell-
highlighting the features of diffuse osteomyelitis, which include regional os- Surprisingly, leukocyte ing, solid periostitis, lysis and
teopenia, periosteal reaction with aggressive features (including Codman’s
triangle), peripheral sclerosis, sequestrum, and involucrum.
count may be normal; how- lucencies, surrounding sclero-
ever, elevated erythrocyte sis, and sinus tracts.15
sedimentation rate and noncar- Computed tomography scan
cells, as well as bacteria.12 Swelling, skin changes, and diac C-reactive protein are key can assist in visualizing soft tis-
Necrotic bone is resorbed, drainage over the site may be signs of infection. The eryth- sue changes surrounding a bony
with cancellous bone requir- present. Acute infection in rocyte sedimentation rate and infection but is impractical to
ing a few weeks to disappear. adults and particularly chil- C-reactive protein will both use for infections with local
Cortical bone may take longer, dren may present with more decrease with successful treat- hardware due to resultant arti-
even up to months, to erode. systemic signs, such as chills, ment; therefore, their values fact. It is best used for detailed
Inflammatory cells in granu- night sweats, erythema, and should be followed closely dur- surgical planning because it
lation tissue are responsible severe pain.13 Sinus tracts are ing the pre- and postoperative clearly identifies sequestra and
for the destruction of infected often present over the area of phases. C-reactive protein is devascularized bone. Magnetic
bone. Microorganisms freely chronically infected bone. If known to increase and decrease resonance imaging offers high-
propagate, and the biofilm ex- these become obstructed, they faster in response to physio- er resolution and easily dif-
pands within the cavity formed may form abscesses. logic changes than erythrocyte ferentiates between bone and
by this resorption. As osteo- sedimentation rate. In addition soft tissue involvement. It has
myelitis progresses, new bone LABORATORY to inflammatory markers, labo- high sensitivity and specificity
forms around the sequestrum Initial workup should in- ratory studies, including albu- for diagnosing osteomyelitis,
from the neighboring pieces clude basic complete blood min, prealbumin, creatinine, which typically appears as a
of intact periosteum and end- count, inflammatory markers, and blood glucose should be decreased local marrow signal
osteum. As it begins to sur- cultures, and gram stain. Gram followed to ensure optimiza- on T1 and an increased local
round the area of infection, it stain is a reflexive addition to tion of host factors.10 Blood marrow signal on T2.16 Sinus
is known as the involucrum. any workup but may not lend cultures are positive only in tracts are also well visualized
The involucrum is often ir- any diagnostic value except the acute hematogenous form on magnetic resonance imag-
regular with perforating sinus to potentially guide early tai- of osteomyelitis and generally ing but often require gadolini-
tracts and may increase in den- loring of antibiotic therapy. do not assist with the diagno- um enhancement.15
sity and thickness with time.13 Cultures are necessary to iden- sis of chronic infection in long Radionuclide labeled scans
tify the microbial offender bones.1 are useful, especially in clini-
DIAGNOSIS responsible for the infection. cal situations where a clear
Diagnosis is based on clini- Bone biopsies should be taken IMAGING diagnosis has not been made
cal examination, tissue cul- at the time of surgical debride- Common imaging tech- and in acute settings when
tures, laboratory studies, and ment and should be carefully niques for detecting osteomy- radiographs are not helpful.
imaging. Symptoms of chron- evaluated for sensitivities. elitis include plain radiography However, they do not offer
ic osteomyelitis are not always Cultures taken from sinus tract (Figure 2), computed tomogra- high-resolution delineation of
obvious and may include low- drainage are not reliable for phy, magnetic resonance imag- anatomical involvement. Bone
grade fever and chronic pain. determining the microorgan- ing, and radionuclide labeled scans with methylene diphos-

370 ORTHOPEDICS | Healio.com/Orthopedics


■ trauma update

phonate are highly sensitive


and specific for osteomyelitis
when increased activity is seen
on initial and delayed images
but becomes less accurate in
the setting of recent surgery
or trauma. White blood cell la- 3C
beled scans may be performed
with several different labels
and require longer testing time
but offer improved specific-
ity.15 Gallium citrate and in-
dium may also be used as la- 3D
beling compounds to identify Figure 3: Features of diffuse tibial
areas of inflammation but are osteomyelitis as shown on coronal
less popular due to cost and T1- (A) and T2-weighted (B) magnetic
resonance images. Axial computed to-
technical requirements.10
mography scan revealing diffuse proxi-
mal femoral osteomyelitis (C) and axial
TREATMENT magnetic resonance image showing
Definitive management of type II osteomyelitis of the tibia (D).
long bone osteomyelitis re-
quires a multidisciplinary ap-
proach involving aggressive 3A 3B
surgical debridement and re-
construction followed by an-
tibiotic therapy.10 Antibiotic 4 to 6 weeks, based largely Once adequate surgical de- Antibiotics can also be
therapy alone leads to high on animal studies and the bridement has occurred, both delivered locally rather than
failure rates. The current au- knowledge that it takes ap- the offending biofilm and the systemically. Alternate routes
thors believe that osteomyelitis proximately 4 weeks for bone vascular deficiency should of antibiotic delivery include
should be surgically treated as to revascularize after surgical have been addressed, and in- antibiotic-impregnated cement
a malignancy, with wide clear debridement.10 Haidar et al17 travenous antibiotics should beads, which provide both high
margins ensuring adequate soft proposed that a shorter duration be effective. Shorter courses local antibiotic concentrations
tissue coverage. High recur- of antibiotic treatment could be of intravenous antibiotics and dead space management.
rence rates are seen with con- feasible following aggressive would save the health care The effectiveness of this treat-
servative debridement.1 Soft surgical debridement and well- system a significant amount ment, both alone and in con-
tissue coverage and dead space vascularized flap placement. of money considering the cost junction with intravenous anti-
management after extensive Antibiotic therapy alone fails and logistical barriers to out- biotics, has been demonstrated
debridement is paramount be- because the infection site has a patient intravenous therapy. in animal models and human
cause spaces left unmanaged poor vascular supply. Without A recent Cochrane review trials.17 However, local anti-
may contribute to ongoing in- adequate blood flow to the area, attempted to summarize the biotic strategies have not been
fection. All efforts should be adequate concentrations of an- evidence for systemic anti- proven superior to intravenous
made to optimize the host prior timicrobials cannot be attained. biotic treatment after surgi- administration and require sur-
to treatment, such as smoking Levels of antibiotics in bone cal debridement for chronic gical removal.
cessation and close control of are less than 20% of serum lev- osteomyelitis.6 The authors Biodegradable antibiotic
blood glucose in patients with els, even in healthy bone,1 and found few quality studies, but delivery systems obviate the
diabetes mellitus.9 are theoretically even lower in those chosen demonstrated no need for a second surgical pro-
diseased tissue. The biofilms significant difference between cedure for removal and several
Antibiotics formed in osteomyelitis may recurrence rates 12 months systems are being developed.
Tradition has dictated that further decrease the penetration after oral and parenteral anti- Collagen fleece is a nontoxic,
antibiotic therapy should last of antimicrobials. biotic treatment.6 biocompatible antibiotic car-

MAY 2013 371


■ trauma update

absolute stability.20 Stage IV


infections are the most chal-
lenging to treat surgically be-
cause they most often require
multiple staged procedures
and necessitate osseous sta-
bilization. Staged procedures
address the need for eradica-
tion of infection followed by
osseous reconstruction aiming
for union and stability once
the tissue is healthy. In Figure
4, the current authors present
their treatment algorithm.
For extensive involvement
with significant segmental
bone loss, several methods of
4 staged treatment have been
Figure 4: Algorithm of the authors’ preferred treatment methodology for the management of stage 4 osteomyelitis. described, with no current
consensus on a gold standard.
A wide variety of studies ex-
rier that offers a triphasic anti- tracts should be removed.7 to access the canal for curet- ist, with many combinations
biotic release and strong clini- Simpson et al18 prospectively tage, which minimizes effects of early and late stabilization,
cal results to date. Polyesters studied the effect of extent of on bony stability.20 Primary coverage, structural support,
are another alternative for surgical debridement on cure closure can usually be attained and antibiotic delivery. Some
biodegradable delivery, offer- rates and found 100% cure because the dead space is lim- weaknesses in the literature
ing a slower breakdown and rates with wide excision and ited to the intramedullary ca- include a paucity of long-term
some evidence of intracellular 100% recurrence rates with nal.8 Stage II infections can be follow-up data and a lack of a
action. Calcium-based carri- intralesional biopsy and local addressed with soft tissue de- universal definition of cure.
ers, including Plaster of Paris, debulking. Marginal resection bridement and decortication of The Papineau, or open air,
calcium sulphate, and calcium with less than 5-mm margins the bone adjacent to the infec- technique and its various per-
hydroxyapatite, are promis- exhibited a 28% recurrence tion. Coverage with a flap has mutations have been widely
ing because they allow tissue rate, all of which were found been described both simulta- cited in the treatment of os-
and bone ingrowth as they de- in type B hosts.18 neously and during a second- teomyelitis. This method in-
grade. Other potential delivery When debriding, healthy stage procedure,7 either with volves radical debridement,
systems not requiring surgical bleeding tissue should be visu- local or free flap mobilization. staged bone grafting, and de-
removal are polyanhydrides, alized at all boundaries of the Stage III osteomyelitis usually layed soft tissue coverage with
amylose starch, and composite surgical site, followed by thor- requires debridement of soft either natural granulation or
carriers. ough irrigation.19 At this point, tissue, sequestrum, and cortex, skin grafting.21 This technique
the need for stabilization and as well as decompression of is often used in type III infec-
Surgical Intervention soft tissue coverage can be the involved medullary canal. tions following saucerization
The extent of surgical de- assessed. Stage I infections Cierny et al7 referred to this because the bone graft does
bridement should be planned limited to the medullary canal process as saucerization, al- not offer significant structural
to account for the host type, may be treated with intramed- luding to the shape of the bone support.22 Meticulous wound
area of involvement, and likely ullary reaming and occasional- left untouched. Stabilization, care is needed because the de-
need for soft tissue coverage ly very localized unroofing and soft tissue coverage, and brided area is left open with
and stabilization. Adequate curettage.7 If evidence exists grafting may all be necessary the bone graft exposed. This
debridement is the key to of metaphyseal involvement or depending on the extent of technique has somewhat fallen
treatment success, and all dead endosteal scalloping, a longi- involvement, with more than out of favor in light of newer
and ischemic tissues and sinus tudinal trough should be made 70% of the cortex required for plastic surgery techniques for

372 ORTHOPEDICS | Healio.com/Orthopedics


■ trauma update

6A 6B
5A 5B

5C 5D
6C 6D
Figure 5: Photographs showing the first stage of the Masquelet technique
Figure 6: Clinical photograph of the tibial segment affected by the infection
used to excise a large segment of the affected tibia. The skin is marked based
that has been cut in half to show the involvement of both the cortex and the
on magnetic resonance imaging findings and extension of the infectious pro-
medullary cavity (A). Clinical photograph showing that the sinus tract is clearly
cess (A). Photograph showing the application of a monotube external fixator
visible. Anteroposterior (C) and lateral (D) radiographs of the tibia with the
and resection of the affected segment with clear margins on the intraoperative
cement spacer in situ.
frozen section (B). Fluoroscopic imaging showing the affected bony segment
resection (C, D).

tissue transfer and grafting term treatment of bone defects.


but remains a foundational It is both time- and cost-
approach to the surgical treat- intensive but has had success in
ment of osteomyelitis. the treatment of osteomyelitis.
McNally et al23 first de- Marsh et al24 reported a 100%
scribed a staged procedure, cure rate at 1-year follow-up
known as the Belfast tech- using an Ilizarov frame on in-
nique, comprised of radical fected long bones, although
debridement, early soft tissue 3 patients failed to unite their
coverage (with or without an- fractures in this time. This tech-
tibiotic beads) to eliminate nique allows stabilization with
dead space, and delayed bone concurrent soft tissue treatment 7A 7B
grafting, if necessary. This as well as distraction osteo- Figure 7: Anteroposterior (A) and lateral (B) radiographs of the tibia following
the second stage of reconstruction using Masquelet technique. The bone graft
decreased the hospitalization genesis to close a segmental
(30 mL) was harvested using a reamer-irrigator-aspirator from the ipsilateral
time necessary for treatment gap and can be combined with femur and inserted into the defect after removal of the antibiotic spacer.
compared with previous meth- other forms of treatment for op-
ods and led to a cure rate of timal outcomes.
92%. They emphasized wide Vacuum-assisted closure of antibiotic therapy. One cidence of positive cultures
resection of infected areas of soft tissue defects has study compared vacuum- after treatment completion.25
with no attempt to salvage dis- been used in many settings, assisted closure therapy to Vacuum-assisted closure
eased tissue as a key compo- and recent evidence has conventional wound care and therapy has also been imple-
nent of treatment.23 demonstrated its efficacy in found a significant reduction mented in combination with
The Ilizarov technique in- the treatment of stage II, III, in infection recurrence, the the Papineau technique in
volves placing a circular exter- and IV infections after de- rate of necessary subsequent lieu of wet-to-dry dressings
nal fixation device for the long- bridement and the initiation flap treatment, and the in- with good results.26

MAY 2013 373


■ trauma update

Masquelet pioneered a surgical techniques by the trials comparing techniques 12. Gristina AG, Oga M, Webb LX,
Hobgood CD. Adherent bacteri-
technique for the treatment same surgeon. They found and identify a gold standard of al colonization in the pathogen-
of segmental bony defects in- good results with debridement treatment for antibiotic length esis of osteomyelitis. Science.
volving initial wide debride- and muscle flap, bone graft, and delivery. 1985; 228:990-993.

ment and the placement of an bone transport, the Papineau 13. Calhoun JH, Manring MM,
Shirtliff M. Osteomyelitis of the
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374 ORTHOPEDICS | Healio.com/Orthopedics

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