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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Osseointegrated Titanium Implants for Limb Prostheses Attachments: Infectious Complications</title><author><name sortKey="Tillander, Jonatan" sort="Tillander, Jonatan" uniqKey="Tillander J" first="Jonatan" last="Tillander">Jonatan Tillander</name><affiliation><nlm:aff id="Aff1">Department of Infectious Diseases, University of Gothenburg, SE-416 85 Göteborg, Sweden</nlm:aff></affiliation></author><author><name sortKey="Hagberg, Kerstin" sort="Hagberg, Kerstin" uniqKey="Hagberg K" first="Kerstin" last="Hagberg">Kerstin Hagberg</name><affiliation><nlm:aff id="Aff2">Department of Orthopedics, University of Gothenburg, Göteborg, Sweden</nlm:aff></affiliation></author><author><name sortKey="Hagberg, Lars" sort="Hagberg, Lars" uniqKey="Hagberg L" first="Lars" last="Hagberg">Lars Hagberg</name><affiliation><nlm:aff id="Aff1">Department of Infectious Diseases, University of Gothenburg, SE-416 85 Göteborg, Sweden</nlm:aff></affiliation></author><author><name sortKey="Br Nemark, Rickard" sort="Br Nemark, Rickard" uniqKey="Br Nemark R" first="Rickard" last="Br Nemark">Rickard Br Nemark</name><affiliation><nlm:aff id="Aff2">Department of Orthopedics, University of Gothenburg, Göteborg, Sweden</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">20473597</idno><idno type="pmc">2939339</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2939339</idno><idno type="RBID">PMC:2939339</idno><idno type="doi">10.1007/s11999-010-1370-0</idno><date when="2010">2010</date><idno type="wicri:Area/Pmc/Corpus">000C41</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000C41</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Osseointegrated Titanium Implants for Limb Prostheses Attachments: Infectious Complications</title><author><name sortKey="Tillander, Jonatan" sort="Tillander, Jonatan" uniqKey="Tillander J" first="Jonatan" last="Tillander">Jonatan Tillander</name><affiliation><nlm:aff id="Aff1">Department of Infectious Diseases, University of Gothenburg, SE-416 85 Göteborg, Sweden</nlm:aff></affiliation></author><author><name sortKey="Hagberg, Kerstin" sort="Hagberg, Kerstin" uniqKey="Hagberg K" first="Kerstin" last="Hagberg">Kerstin Hagberg</name><affiliation><nlm:aff id="Aff2">Department of Orthopedics, University of Gothenburg, Göteborg, Sweden</nlm:aff></affiliation></author><author><name sortKey="Hagberg, Lars" sort="Hagberg, Lars" uniqKey="Hagberg L" first="Lars" last="Hagberg">Lars Hagberg</name><affiliation><nlm:aff id="Aff1">Department of Infectious Diseases, University of Gothenburg, SE-416 85 Göteborg, Sweden</nlm:aff></affiliation></author><author><name sortKey="Br Nemark, Rickard" sort="Br Nemark, Rickard" uniqKey="Br Nemark R" first="Rickard" last="Br Nemark">Rickard Br Nemark</name><affiliation><nlm:aff id="Aff2">Department of Orthopedics, University of Gothenburg, Göteborg, Sweden</nlm:aff></affiliation></author></analytic><series><title level="j">Clinical Orthopaedics and Related Research</title><idno type="ISSN">0009-921X</idno><idno type="eISSN">1528-1132</idno><imprint><date when="2010">2010</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p> The concept of osseointegration involves direct contact between titanium implant and bone. This transcutaneous prosthetic system for amputees is intended to assure stable long-term fixation. Most metal transcutaneous implants have failed, primarily owing to infection.</p></sec><sec><title>Questions/purposes</title><p>We determined the frequency and describe the presentation of infectious complications with this novel method. We also evaluated the bacterial flora at the skin-penetration area and its relation to the development of local and implant-related infection.</p></sec><sec><title>Patients and Methods</title><p>We prospectively followed 39 patients with arm and leg amputations fitted with transcutaneous osseointegrated titanium implants a mean of 56 months earlier (range, 132–133 months). There were 33 femoral, one tibial, four ulnar, four radial, and three humeral implants. Patients were selected during a 6-month period in 2005 and identically reevaluated after 3 years. Implant infection was defined as definite, probable, or possible based on clinical, radiologic, and microbiologic evidence.</p></sec><sec><title>Results</title><p>The frequency of implant infection was 5% at inclusion and 18% at followup. One patient with infection recovered owing to antibiotic treatment and another patient had the implant removed. Most implant infections had low infectious activity, and in five of the seven patients with infections, prosthetic use was not affected. The most common bacteria in superficial and deep cultures were Staphylococcus aureus and coagulase-negative staphylococci.</p></sec><sec><title>Conclusions</title><p>Despite frequent colonization around the skin-implant interface by potentially virulent bacteria such as Staphylococcus aureus and bacteria associated with biomedical device infections such as coagulase-negative staphylococci, this titanium implant system for bone-anchored prostheses caused few infections leading to disability or implant removal.</p></sec><sec><title>Level of Evidence</title><p>Level IV, therapeutic study. See the Guidelines for Authors for a complete description of levels of evidence.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Adell, R" uniqKey="Adell R">R Adell</name></author><author><name sortKey="Eriksson, B" uniqKey="Eriksson B">B Eriksson</name></author><author><name sortKey="Lekholm, U" uniqKey="Lekholm U">U Lekholm</name></author><author><name sortKey="Br Nemark, Pi" uniqKey="Br Nemark P">PI Brånemark</name></author><author><name sortKey="Jemt, T" uniqKey="Jemt T">T Jemt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Arens, S" uniqKey="Arens S">S Arens</name></author><author><name sortKey="Schlegel, U" uniqKey="Schlegel U">U Schlegel</name></author><author><name sortKey="Printzen, G" uniqKey="Printzen G">G Printzen</name></author><author><name sortKey="Ziegler, Wj" uniqKey="Ziegler W">WJ Ziegler</name></author><author><name sortKey="Perren, Sm" uniqKey="Perren S">SM 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Clin Orthop Relat Res</journal-id><journal-title-group><journal-title>Clinical Orthopaedics and Related Research</journal-title></journal-title-group><issn pub-type="ppub">0009-921X</issn><issn pub-type="epub">1528-1132</issn><publisher><publisher-name>Springer-Verlag</publisher-name><publisher-loc>New York</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">20473597</article-id><article-id pub-id-type="pmc">2939339</article-id><article-id pub-id-type="publisher-id">1370</article-id><article-id pub-id-type="doi">10.1007/s11999-010-1370-0</article-id><article-categories><subj-group subj-group-type="heading"><subject>Clinical Research</subject></subj-group></article-categories><title-group><article-title>Osseointegrated Titanium Implants for Limb Prostheses Attachments: Infectious Complications</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Tillander</surname><given-names>Jonatan</given-names></name><degrees>MD</degrees><address><email>jonatan.tillander@vgregion.se</email></address><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Hagberg</surname><given-names>Kerstin</given-names></name><degrees>RPT, PhD</degrees><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Hagberg</surname><given-names>Lars</given-names></name><degrees>MD, PhD</degrees><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Brånemark</surname><given-names>Rickard</given-names></name><degrees>MD, PhD</degrees><xref ref-type="aff" rid="Aff2">2</xref></contrib><aff id="Aff1"><label>1</label>Department of Infectious Diseases, University of Gothenburg, SE-416 85 Göteborg, Sweden</aff><aff id="Aff2"><label>2</label>Department of Orthopedics, University of Gothenburg, Göteborg, Sweden</aff></contrib-group><pub-date pub-type="epub"><day>15</day><month>5</month><year>2010</year></pub-date><pub-date pub-type="pmc-release"><day>15</day><month>5</month><year>2010</year></pub-date><pub-date pub-type="ppub"><month>10</month><year>2010</year></pub-date><volume>468</volume><issue>10</issue><fpage>2781</fpage><lpage>2788</lpage><history><date date-type="received"><day>2</day><month>9</month><year>2009</year></date><date date-type="accepted"><day>19</day><month>4</month><year>2010</year></date></history><permissions><copyright-statement>© The Author(s) 2010</copyright-statement></permissions><abstract id="Abs1"><sec><title>Background</title><p> The concept of osseointegration involves direct contact between titanium implant and bone. This transcutaneous prosthetic system for amputees is intended to assure stable long-term fixation. Most metal transcutaneous implants have failed, primarily owing to infection.</p></sec><sec><title>Questions/purposes</title><p>We determined the frequency and describe the presentation of infectious complications with this novel method. We also evaluated the bacterial flora at the skin-penetration area and its relation to the development of local and implant-related infection.</p></sec><sec><title>Patients and Methods</title><p>We prospectively followed 39 patients with arm and leg amputations fitted with transcutaneous osseointegrated titanium implants a mean of 56 months earlier (range, 132–133 months). There were 33 femoral, one tibial, four ulnar, four radial, and three humeral implants. Patients were selected during a 6-month period in 2005 and identically reevaluated after 3 years. Implant infection was defined as definite, probable, or possible based on clinical, radiologic, and microbiologic evidence.</p></sec><sec><title>Results</title><p>The frequency of implant infection was 5% at inclusion and 18% at followup. One patient with infection recovered owing to antibiotic treatment and another patient had the implant removed. Most implant infections had low infectious activity, and in five of the seven patients with infections, prosthetic use was not affected. The most common bacteria in superficial and deep cultures were Staphylococcus aureus and coagulase-negative staphylococci.</p></sec><sec><title>Conclusions</title><p>Despite frequent colonization around the skin-implant interface by potentially virulent bacteria such as Staphylococcus aureus and bacteria associated with biomedical device infections such as coagulase-negative staphylococci, this titanium implant system for bone-anchored prostheses caused few infections leading to disability or implant removal.</p></sec><sec><title>Level of Evidence</title><p>Level IV, therapeutic study. See the Guidelines for Authors for a complete description of levels of evidence.</p></sec></abstract><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Association of Bone and Joint Surgeons® 2010</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Introduction</title><p>In high-income countries, chronic vascular disease is the leading cause of limb loss [<xref ref-type="bibr" rid="CR22">22</xref>]. However, many previously healthy individuals undergo amputation secondary to trauma, neoplasia, infection, and arterial embolism [<xref ref-type="bibr" rid="CR12">12</xref>]. The conventional way to suspend a prosthetic limb to the body is with a prosthetic socket [<xref ref-type="bibr" rid="CR20">20</xref>]. Users of socket prostheses commonly report impaired quality of life [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR13">13</xref>, <xref ref-type="bibr" rid="CR26">26</xref>, <xref ref-type="bibr" rid="CR27">27</xref>] and complications including dermatitis and infected sores [<xref ref-type="bibr" rid="CR10">10</xref>, <xref ref-type="bibr" rid="CR21">21</xref>].</p><p>Prosthetic bone anchorage is intended to eliminate or minimize these problems. Our novel method is based on the principles of osseointegration (Fig. <xref rid="Fig1" ref-type="fig">1</xref>), which has been in clinical use in prosthetic teeth replacement since 1965 [<xref ref-type="bibr" rid="CR4">4</xref>]. One report suggests a 15-year implant survival rate of approximately 90% in mandibular bone [<xref ref-type="bibr" rid="CR1">1</xref>]. With osseointegration, direct contact between fixture and bone tissue is intended, assuring a stable, long-term attachment for the external prosthesis [<xref ref-type="bibr" rid="CR5">5</xref>]. This technique results in easy prosthesis handling, improved limb control, and eliminates socket-impaired ROM and socket-caused skin disorders [<xref ref-type="bibr" rid="CR15">15</xref>, <xref ref-type="bibr" rid="CR16">16</xref>, <xref ref-type="bibr" rid="CR30">30</xref>] (Fig. <xref rid="Fig2" ref-type="fig">2</xref>). During the years, various attempts to anchor prosthetic limbs with transcutaneous metal implants other than titanium [<xref ref-type="bibr" rid="CR17">17</xref>, <xref ref-type="bibr" rid="CR18">18</xref>, <xref ref-type="bibr" rid="CR25">25</xref>] have failed, primarily owing to infection. Currently, our center has treated more than 100 patients with femoral titanium implants (Fig. <xref rid="Fig3" ref-type="fig">3</xref>), three with tibial implants, 15 with humeral implants, and 20 with ulnar and/or radial implants. Treatment failures were more common before we introduced a standardized treatment protocol in 1999 [<xref ref-type="bibr" rid="CR14">14</xref>, <xref ref-type="bibr" rid="CR28">28</xref>].<fig id="Fig1"><label>Fig. 1</label><caption><p>This schematic drawing shows the implant components and surrounding tissues.</p></caption><graphic xlink:href="11999_2010_1370_Fig1_HTML" id="MO1"></graphic></fig><fig id="Fig2"><label>Fig. 2</label><caption><p>This is a ventral view of the transcutaneous component (abutment) in a patient with a transfemoral amputation. (Published with permission from Nigel Jarvis, the University of Gothenburg, The Sahlgrenska Academy, Gothenburg, Sweden.)</p></caption><graphic xlink:href="11999_2010_1370_Fig2_HTML" id="MO2"></graphic></fig><fig id="Fig3"><label>Fig. 3</label><caption><p>A lateral view is shown of a patient securing an external prosthesis to the abutment. (Published with permission from Nigel Jarvis, the University of Gothenburg, The Sahlgrenska Academy, Gothenburg, Sweden.)</p></caption><graphic xlink:href="11999_2010_1370_Fig3_HTML" id="MO3"></graphic></fig></p><p>Clinical observations have led us to believe that poor primary osseointegration increases the risk of subsequent infection. However, this is not substantiated. Experimental evidence supports antiinfectious properties of titanium compared with other biomaterials when implanted in bone and in soft tissues [<xref ref-type="bibr" rid="CR2">2</xref>, <xref ref-type="bibr" rid="CR7">7</xref>]. Medical device infection is caused predominantly by staphylococci, with coagulase-negative staphylococci being the most common [<xref ref-type="bibr" rid="CR32">32</xref>, <xref ref-type="bibr" rid="CR33">33</xref>]. However, as the definitive diagnosis of infection is sometimes a problem, culture-based algorithms have been developed to increase diagnostic sensitivity [<xref ref-type="bibr" rid="CR3">3</xref>, <xref ref-type="bibr" rid="CR19">19</xref>, <xref ref-type="bibr" rid="CR23">23</xref>, <xref ref-type="bibr" rid="CR32">32</xref>, <xref ref-type="bibr" rid="CR33">33</xref>]. We therefore base our definitions of infection on clinical, radiographic, and bacteriologic findings. Although current titanium transcutaneous implants are intended to reduce infections compared with previously used metals and transcutaneous techniques, there are little data regarding infections with these implants. In the related but incomparable setting of dental osseointegration, infection is well characterized [<xref ref-type="bibr" rid="CR31">31</xref>], but less has been published regarding infection in bone-anchored hearing aids [<xref ref-type="bibr" rid="CR29">29</xref>].</p><p>Our aims were (1) to describe the frequency and (2) the bacterial flora at the skin-penetration area and its relation to the development of local and implant-related infection in this novel method. The various clinical presentations of implant infections also are described.</p></sec><sec id="Sec2" sec-type="methods"><title>Patients and Methods</title><p>We prospectively studied bacterial colonization and infectious complications in 39 patients with arm and leg amputations previously treated with 45 transcutaneous osseointegrated titanium implants. All patients attending the osseointegration outpatient clinic at Sahlgrenska University Hospital, Göteborg, Sweden, for scheduled or emergency visits between January and June 2005 were included. No patients refused to participate. At least 3 months had elapsed since the second surgical procedure (abutment insertion). This cohort was followed longitudinally for an average of 3 years to identify implant infections and cross sectionally surveyed twice (at inclusion and after approximately 3 years) for bacterial presence, local infection, and antibiotic use. All skin-penetrating loci were subjected to separate clinical, bacteriologic, and radiographic assessment. There were 18 women and 21 men with a mean age of 49.3 years (range, 28–74 years). Amputations were the result of either trauma or neoplasia. Thirty-three of the implants were femoral (bilateral in one), four each were ulnar and radial (bilateral in one), three were humeral, and one was tibial. The patients had been living with the implant(s) a mean of 54 months (range, 3–132 months). Indications for these implants were severe discomfort when using conventional socket prostheses or poor stump conditions [<xref ref-type="bibr" rid="CR13">13</xref>].</p><p>The treatment involves two separate surgical procedures. A titanium screw (fixture) is inserted into the residual bone and allowed to integrate for 6 months before the skin-penetrating extension (abutment) is inserted [<xref ref-type="bibr" rid="CR28">28</xref>]. Based on the experience of successful skin-penetrating implants in the head and neck regions [<xref ref-type="bibr" rid="CR29">29</xref>], the skin is attached directly to the distal end of the residual bone to reduce soft tissue mobility and risk of infection. We consider the implant osseointegrated when it is stable on clinical examination, pain free when loaded [<xref ref-type="bibr" rid="CR28">28</xref>], and there are no signs of loosening seen on radiographs, ie, no radiolucent zone around the implant. Postoperative followup includes clinical examination (pain evaluation, implant stability, skin and soft tissue condition), a rehabilitation protocol [<xref ref-type="bibr" rid="CR14">14</xref>], and radiographs at 6 months and 1, 2, 3, 5, 7, 10, and 15 years after surgery.</p><p>We used the following five definitions for implant infection and required all stated criteria for the given diagnosis<bold>:</bold> (1) definite implant infection: (a) clinical symptoms of implant-related infection, (b) radiographic signs consistent with periimplant bone infection, and (c) at least three of five intraoperatively obtained cultures yielding identical pathogens; (2) probable implant infection: (a) clinical symptoms of implant-related infection, (b) radiographic signs consistent with periimplant bone infection, and (c) positive relevant culture not as defined previously; (3) possible implant infection: (a) clinical symptoms of implant-related infection, (b) radiographic signs consistent with periimplant bone infection, and (c) no relevant cultures; (4) local infection in the skin penetration area: (a) local signs/symptoms of infection (inflammation with or without secretion) in the skin penetration area but no symptoms of deep infection, (b) no radiographic signs consistent with periimplant bone infection, and (c) with or without relevant cultures; (5) bacterial colonization around the skin-implant interface: (a) neither local inflammatory signs nor other clinical symptoms of infection, with or without secretion, at the skin-implant interface, (b) no radiographic signs consistent with periimplant bone infection, and (c) positive bacterial culture from the skin-implant interface. We considered radiographic evidence of osteolysis with or without periosteal sclerosis around a previously integrated implant to be consistent with implant infection. The definitions also were based on previously proposed culture diagnostics in infected hip and knee arthroplasties [<xref ref-type="bibr" rid="CR19">19</xref>, <xref ref-type="bibr" rid="CR23">23</xref>].</p><p>At inclusion patients were examined clinically and asked to answer a questionnaire (Appendix 1) regarding infectious complications and antibiotic use during the 6 months preceding the visit. Without any preparation of the surrounding skin, samples were taken from the skin-implant interface with a sterile cotton swab, transported in a coal-based medium, and cultured on routine agar plates for at least 2 days. A second set of bacterial cultures was performed 3 years later and an identical questionnaire was answered. Patients who were not scheduled for a visit at this time collected bacterial samples (cotton swabs) themselves according to careful written instructions and, if necessary, with the assistance of their attending clinic. These patients were experienced in handling the skin-implant area and we anticipated no methodologic problems with the patients performing their own cultures. Cultures and questionnaires were sent to Sahlgrenska University Hospital by mail. Sampled cultures transported in a coal-based medium are expected to survive a 2-day transport by mail. Culturing the samples then was performed at our certified laboratory.</p><p>All cultures were examined by one (SK) experienced bacteriologic analyst. The number of colony forming units (CFU) was defined as +++ (> 100 CFU), ++ (10–100 CFU), or + (< 10 CFU). A routine disk method was used to determine antibiotic resistance.</p><p>The latest scheduled or symptom-prompted radiographs at inclusion and followup were checked for signs of bone infection. All patients had radiographs performed within 6 months of inclusion. Followup radiographs were obtained for 31 patients. Of the remaining eight patients, two already had osteomyelitic changes at the beginning of the study, four were excluded, and two were without infectious symptoms.</p><p>Four patients were lost to followup. In one, the implant was extracted owing to mechanical loosening in a previously radiated femur (October 2006). In another patient, chronic skin infection led to abutment removal (February 2007). Complete skin healing over the retained implant followed. Two patients (one Swedish) did not complete the followup protocol for nonmedical reasons. Their admitting medical centers were contacted and no implant infections were reported. The study was approved by the ethical committee at the University of Gothenburg.</p></sec><sec id="Sec3"><title>Results</title><p>The frequencies for patients with definite/probable/possible implant infections were 5% (two of 39) at inclusion and 18% (seven of 39) at followup (Table <xref rid="Tab1" ref-type="table">1</xref>). Seven patients had a history of local infection at the skin penetration area during the 6-month period before inclusion and 11 patients had local infections during the 6-month period before followup (Table <xref rid="Tab1" ref-type="table">1</xref>). Four and six patients, respectively, had been treated with short-term oral antibiotics. Fourteen patients had secretion from the skin pocket. In 10 patients, the secretion was purulent.<table-wrap id="Tab1"><label>Table 1</label><caption><p>Bacterial colonization and infection at the beginning of the study and at followup</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Type of infection</th><th align="left">Initial assessment</th><th align="left">Followup (2-3 years)</th></tr></thead><tbody><tr><td align="left">Possible/probable/definite implant infection</td><td align="left">2</td><td align="left">6<sup>‡</sup></td></tr><tr><td align="left">Local soft tissue infection in the skin penetration area*</td><td align="left">7</td><td align="left">11</td></tr><tr><td align="left">Superficial colonization without signs of infection</td><td align="left">23 (24)<sup>†</sup></td><td align="left">16 (17)</td></tr><tr><td align="left">No growth of bacteria or signs of infection</td><td align="left">7 (12)</td><td align="left">2 (4)</td></tr><tr><td align="left">Lost for followup<sup>§</sup></td><td align="left"></td><td align="left">4</td></tr></tbody></table><table-wrap-foot><p>* Including all episodes of infection during 6 months before first and second assessments; <sup>†</sup>figures in parentheses correspond to total number of clinical sites, which exceed the number of patients; three patients had more than one implant; <sup>‡</sup>total number of implant infections during the 3-year study was seven; one patient had been treated successfully at followup; <sup>§</sup>contact with admitting clinic indicated no implant infection.</p></table-wrap-foot></table-wrap></p><p>The most common bacteria found around the skin-implant interface were Staphylococcus aureus, coagulase-negative staphylococci, and streptococci group A, B, or G. In three of seven patients with implant infections at followup, inclusion cultures from the skin-implant interface yielded the same species as the suspected infectious agent (Table <xref rid="Tab2" ref-type="table">2</xref>). Staphylococcus aureus was cultured from specimens from 16 patients (17 implants), coagulase-negative staphylococci from 10, streptococcus group B, G, or nontypable from nine, beta-hemolytic streptococcus group A from one, Enterococcus sp. from three, alfa streptococci from one, and Gram-negative rods from four (Table <xref rid="Tab2" ref-type="table">2</xref>) at inclusion. No Staphylococcus aureus strain was methicillin-resistant.<table-wrap id="Tab2"><label>Table 2</label><caption><p>Bacterial findings at the skin-implant interface at first observation and second observations 2.5 to 3 years later*</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="3">Bacteria</th><th align="left" colspan="4">First observation (n = 39)</th><th align="left" colspan="4">Second observation (n = 30)</th><th align="left" rowspan="3">Not quantified</th></tr><tr><th align="left" rowspan="2">Number of patients<sup>§</sup></th><th align="left" rowspan="2">+++</th><th align="left" colspan="2">Bacterial colonies</th><th align="left" rowspan="2">Number of patients<sup>§</sup></th><th align="left" rowspan="2">+++</th><th align="left" colspan="2">Bacterial colonies</th></tr><tr><th align="left">++</th><th align="left">+</th><th align="left">++</th><th align="left">+</th></tr></thead><tbody><tr><td align="left">S. aureus</td><td char="." align="char">16<sup>†</sup></td><td char="." align="char">9</td><td char="." align="char">3</td><td char="." align="char">4</td><td char="." align="char">19</td><td char="." align="char">11</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">7</td></tr><tr><td align="left">CoNS</td><td char="." align="char">10</td><td char="." align="char">0</td><td char="." align="char">5</td><td char="." align="char">5</td><td char="." align="char">11</td><td char="." align="char">4</td><td char="." align="char">1</td><td char="." align="char">4</td><td char="." align="char">2</td></tr><tr><td align="left">Streptococcus group B</td><td char="." align="char">6</td><td char="." align="char">2</td><td char="." align="char">1</td><td char="." align="char">3</td><td char="." align="char">3</td><td char="." align="char">3</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">0</td></tr><tr><td align="left">Streptococcus group G</td><td char="." align="char">2</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td></tr><tr><td align="left">Streptococcus group A</td><td char="." align="char">1</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td></tr><tr><td align="left">Enterococci 3</td><td char="." align="char">2</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">1</td><td align="left"></td></tr><tr><td align="left">Citrobacter sp. 2</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td><td align="left"></td></tr><tr><td align="left">Proteus mirabilis</td><td char="." align="char">1</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td></tr><tr><td align="left">Serratia sp.</td><td char="." align="char">1</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">2</td><td char="." align="char">2</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">0</td></tr><tr><td align="left">P. aeruginosa</td><td char="." align="char">2</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">1</td><td char="." align="char">1</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">0</td></tr><tr><td align="left">Other Gram-negative rods </td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">2</td><td char="." align="char">1</td><td char="." align="char">1</td><td char="." align="char">—</td><td char="." align="char">0</td></tr><tr><td align="left">Aerobic streptococci nontypable</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td></tr><tr><td align="left">Alfa streptococci</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">—</td><td char="." align="char">1</td></tr><tr><td align="left">Coryneforms</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">1</td><td char="." align="char">1</td><td char="." align="char">0</td><td char="." align="char">0</td><td char="." align="char">0</td></tr><tr><td align="left">No growth</td><td char="." align="char">8</td><td align="left"></td><td align="left"></td><td align="left"></td><td char="." align="char">0</td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td></tr><tr><td align="left">Excluded/no culture</td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td><td char="." align="char">9</td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td></tr></tbody></table><table-wrap-foot><p>* Several patients had more than one bacterial species isolated; <sup>†</sup>one patient had a positive S. aureus culture from two loci; CoNS = coagulase-negative staphylococci; <sup>§</sup>several patients had growth of two or more bacteria at the same site.</p></table-wrap-foot></table-wrap></p><p>Followup culture specimens were obtained from 30 patients, as five patients did not send specimens as instructed. Staphylococcus aureus was still the most common finding (19) followed by coagulase-negative staphylococci (11), streptococcus group B (3), Serratia sp. (2) Enterococcus sp., alfa streptococcus, coryneforms, and Pseudomonas aeruginosa (one each) (Table <xref rid="Tab2" ref-type="table">2</xref>). No Staphylococcus aureus strain was methicillin-resistant. Eight of 13 patients with recultured specimens with Staphylococcus aureus at inclusion also had Staphylococcus aureus isolated at followup.</p><p>The clinical presentation varied. Two patients had chronic skin fistulas to the implant with occasional secretion but without pain, fever, or implant loosening. Fistulas were present more than 5 years before inclusion and were not treated with antibiotics during the observation time. They were registered as implant infections at inclusion and at followup. Staphylococcus aureus and coagulase-negative staphylococci were suspected etiologic agents. Two patients had implant infections with poor primary osseointegration. One had an infected femoral implant extracted. Preoperative cultures showed coagulase-negative staphylococci, alfa streptococci, and Peptostreptococcus sp. The other patient had a humeral implant infection caused by Escherichia coli. It was verified by biopsies of the culture specimens and treated with ciprofloxacin for 6 months. One year later, there were no signs of relapse. Distal infection involving bone and soft tissue was seen in two patients with good primary osseointegration. The etiology was mixed with Staphylococcus aureus/coagulase-negative staphylococci and Staphylococcus aureus/Enterococcus faecalis being suspected. Both patients underwent surgical revision and prolonged antibiotic treatment. Acute osteomyelitis occurred in one patient who had no fever but had acute pain develop in an osseointegrated femur. Radiography revealed signs of osteomyelitis at the midfixture level. Intraoperative cultures yielded Staphylococcus aureus and coagulase-negative staphylococci (Table <xref rid="Tab3" ref-type="table">3</xref>). In two of seven patients with implant infections at followup, prosthetic use was not affected at any time, three patients were affected only briefly during the time around surgical intervention, and for the patient with acute osteomyelitis, the treatment outcome is still pending.<table-wrap id="Tab3"><label>Table 3</label><caption><p>Etiology and outcome of patients with implant infections at followup</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Age of patient (years)</th><th align="left">Months since surgical session 2 at inclusion</th><th align="left">Months to infection after surgical session 2</th><th align="left">Locus</th><th align="left">Suspected bacterial etiology*</th><th align="left">Culture at skin penetration area<sup>†</sup></th><th align="left">Treatment given at followup</th><th align="left">Outcome</th></tr></thead><tbody><tr><td align="left">36</td><td char="." align="char">3</td><td char="." align="char">35</td><td align="left">Femur</td><td align="left">S. aureus, CoNS</td><td align="left">No growth</td><td align="left">Débridement/clindamycin + rifampicin</td><td align="left">Ongoing</td></tr><tr><td align="left">40</td><td char="." align="char">24</td><td char="." align="char">36</td><td align="left">Humerus</td><td align="left">E. coli</td><td align="left">CoNS</td><td align="left">Completed 6 months ciprofloxacin</td><td align="left">Recovered</td></tr><tr><td align="left">45</td><td char="." align="char">84</td><td char="." align="char">31</td><td align="left">Femur</td><td align="left">S. aureus, E. faecalis</td><td align="left">S. aureus, GBS</td><td align="left">Revision/teicoplanin</td><td align="left">Ongoing</td></tr><tr><td align="left">49</td><td char="." align="char">18</td><td char="." align="char">36</td><td align="left">Femur</td><td align="left">CoNS</td><td align="left">CoNS</td><td align="left">Clindamycin/extraction</td><td align="left">Implant extraction</td></tr><tr><td align="left">54</td><td char="." align="char">24</td><td char="." align="char">32</td><td align="left">Femur</td><td align="left">S. aureus, GBS</td><td align="left">CoNS</td><td align="left">Flucloxacillin/revision/ clindamycin</td><td align="left">Ongoing</td></tr><tr><td align="left">65</td><td char="." align="char">96</td><td char="." align="char">60</td><td align="left">Femur</td><td align="left">GBS</td><td align="left">GBS, P. mirabilis</td><td align="left">No treatment</td><td align="left">Ongoing, fistulas</td></tr><tr><td align="left">77</td><td char="." align="char">120</td><td char="." align="char">11</td><td align="left">Femur</td><td align="left">CoNS</td><td align="left">S. aureus</td><td align="left">No treatment</td><td align="left">Ongoing, fistulas</td></tr></tbody></table><table-wrap-foot><p>* Cultures taken from tissue specimens or from fistulas; <sup>†</sup>bacterial swab taken at initial assessment from the area where the implant system penetrates the skin; CoNS = coagulase-negative staphylococci; GBS = group B streptococci.</p></table-wrap-foot></table-wrap></p></sec><sec id="Sec4"><title>Discussion</title><p>Transcutaneous osseointegrated titanium implants for prosthetic systems in patients with amputations provide improved performance and less socket-caused complications in selected patients [<xref ref-type="bibr" rid="CR15">15</xref>, <xref ref-type="bibr" rid="CR16">16</xref>]. Our aim was to describe the frequency, clinical presentation, and bacterial occurrence in local and implant-related infections.</p><p>We acknowledge several limitations. First is the relatively short followup, although some patients had been living with the implant for more than 10 years. Most patients were young or middle-aged and probably will require use of their implants or other prostheses for numerous decades. We cannot predict the long-term durability of these implants. Second, we included some patients initially treated during a learning phase. The enrolled patients represent all phases of method development. We presume with experience the infection rates will diminish. Third, we did not review all patients. Rather, we studied a subgroup of 39 patients recruited during a 6-month period. As all patients attending (regular and emergency visits) the clinic during the inclusion period agreed to participate, we presume this cohort represents the entire population. A retrospective analysis of implant infection and risk factors in 100 patients treated with femoral osseointegrated implants and a prospective analysis of patients treated with the refined protocol are in progress.</p><p>Skin-penetrating implants were long regarded as unattainable owing to the high rates of failure caused by infection. The transcutaneous osseointegrated titanium implant challenges this claim. In our cohort, seven of 39 (18%) patients either had an implant infection or one developed within 3 years. The implant-infection/implant-year ratio (7/135) is slightly less (5%) than comparable results from Queen Mary’s Hospital in London where four of 16 patients treated with the same method had an implant-related infection develop during a cumulative 67-year period (6%) (unpublished data, Sooriakumaran S, Robinson KP, Ward DA, D′Arcy R, Chittoor SN, Written communication from 12th ISPO Congress in Vancouver, Canada, July 29, 2007). In our cohort, hematogenous and ascending bacterial spread must be suspected. Poor primary osseointegration may have facilitated an ascending infection as seen in two patients. Only one of seven patients was diagnosed and treated for an implant-related infection earlier than 31 months (mean, 34 months) after the surgical procedure. With arthroplasty, late infection (> 24 months) is considered more indicative of hematogenous seeding compared with early (< 3 months) or delayed (3–24 months) infections [<xref ref-type="bibr" rid="CR33">33</xref>]. In our four cases with more virulent bacteria, late onset of symptoms clearly indicates that intraoperative contamination was not the cause of infection. However, we cannot know whether some of the infections were either of hematogenous or new origin, rather than as a result of residual surgical contamination.</p><p>We assessed the presence of local skin infections twice, with a greater frequency at followup (Table <xref rid="Tab2" ref-type="table">2</xref>). All episodes resolved spontaneously or with oral antibiotics indicating no deeper infectious involvement. These adverse effects must be compared with those of conventional socket prostheses. For patients using conventional prostheses, socket-related problems such as ulcers and rashes on the residual limb and restricted movement have been described [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR13">13</xref>]. In two studies, dermatologic problems were reported to occur among 34% to 41% of those using socket prostheses [<xref ref-type="bibr" rid="CR10">10</xref>, <xref ref-type="bibr" rid="CR21">21</xref>]. Many of these are manageable. With a bone-anchored prostheses however, no socket is needed to suspend the artificial limb and consequently no patient in our study had ulcers or contact dermatitis on the residual limb.</p><p>Although various microorganisms may cause foreign body-related infection, staphylococci are the most frequently isolated pathogens [<xref ref-type="bibr" rid="CR11">11</xref>, <xref ref-type="bibr" rid="CR32">32</xref>]. In our study, approximately ½ of the patients were colonized with potentially virulent Staphylococcus aureus in the skin penetration area. Despite this, only three patients had a Staphylococcus aureus implant infection. Unfortunately, we did not perform genetic typing of the bacteria. The ability to adhere to the implant material and to promote biofilm formation are important pathogenic properties for staphylococci and other bacteria [<xref ref-type="bibr" rid="CR9">9</xref>]. The biocompatibility is greater with titanium [oxide] compared with stainless steel and cobalt-chrome alloys [<xref ref-type="bibr" rid="CR2">2</xref>, <xref ref-type="bibr" rid="CR7">7</xref>]. In osseointegration, the tight junction formed between the titanium and the bone tissue might prevent adhesion, colonization, and subsequent biofilm formation. Osseointegration also can be established and maintained in aggressive inflammatory environments such as experimental arthritis in a rabbit knee model [<xref ref-type="bibr" rid="CR6">6</xref>] and in patients with rheumatoid arthritis [<xref ref-type="bibr" rid="CR24">24</xref>]. The osseointegration might explain why some patients with implant infections have such slow, or even no, progressive destruction of the bone tissue with subsequent loosening. It also may explain why patients with poor primary osseointegration are more susceptible to infectious complications.</p><p>We found the osseointegration method with titanium implants and skin penetration of the titanium system in patients with leg and arm amputations caused few severe infectious complications. However, infectious complications occur in approximately two-fifths of the patients during a 3-year period, mostly as local infections in the skin penetration area and more rarely as low-activity implant-associated infections. Staphylococcus aureus and coagulase-negative staphylococci were the most commonly cultured bacteria in the skin penetration area. In our opinion, the frequency and severity of infections do not appear to be obstacles for use of this method. 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