Orthopedics

Review Article 

Risk Factors for Perimegaprosthetic Infections After Tumor Resection

Marco De Gori, MD; Giorgio Gasparini, MD; Rodolfo Capanna, MD

Abstract

Periprosthetic joint infection remains one of the most challenging and pervasive complications following megaprosthetic replacement after tumor resection. The authors conducted a systematic review of the literature for clinical studies that reported a risk factor analysis for perimegaprosthetic joint infections. The search included English-language studies published up to July 2015. Eight studies fulfilled the inclusion criteria. Identified factors mostly related to both surgical procedure and hospitalization. Physicians should consider these results when discussing the outcomes of limb salvage surgery with patients and trying to reduce the overall burden of perimegaprosthetic joint infections. [Orthopedics. 2017; 40(1):e11–e16.]

Abstract

Periprosthetic joint infection remains one of the most challenging and pervasive complications following megaprosthetic replacement after tumor resection. The authors conducted a systematic review of the literature for clinical studies that reported a risk factor analysis for perimegaprosthetic joint infections. The search included English-language studies published up to July 2015. Eight studies fulfilled the inclusion criteria. Identified factors mostly related to both surgical procedure and hospitalization. Physicians should consider these results when discussing the outcomes of limb salvage surgery with patients and trying to reduce the overall burden of perimegaprosthetic joint infections. [Orthopedics. 2017; 40(1):e11–e16.]

Periprosthetic joint infection remains one of the most challenging complications following joint replacement and a leading cause of early implant failure.1 Although the overall infection rate is relatively low, being approximately 1% following hip and knee arthroplasties,2 it might dramatically increase in the presence of factors such as patients' immunosuppression, extensive soft tissue dissection, long operating times,3 and neoplastic diseases.4

A deep infection may be a devastating complication following megaprosthetic replacement after tumor resection, leading to challenges in treatment decisions5 and posing a high risk for repeated surgical procedures, prolonged hospital stay and rehabilitation, pain, poor functional outcome, and failed limb salvage.3,6,7 Overall, a recent systematic review8 reported a mean rate of perimegaprosthetic infection (PMI) of 10%; notably, a PMI rate as high as 43% may follow revision surgery.9 It has been suggested that long-term antibiotic prophylaxis decreases the risk of PMIs,8 but controversy remains about the role of other factors in the development of PMIs, thus supporting the need for a comprehensive literature review.

The purpose of this study was to systematically evaluate published clinical studies determining which variables predict the PMI rate after tumor resection.

Materials and Methods

The authors conducted a systematic literature search using the MEDLINE/PubMed and Cochrane Register of Controlled Trials databases. They wanted to identify and include in the search all English-language studies addressing septic complications of the use of megaprostheses in the treatment of bone tumors including an analysis of risk factors for PMIs. Level V studies were excluded from the search.

The MEDLINE/PubMed search was performed as follows: 1: “megaprosth* infect*” AND “English”[Language] NOT “case reports”[Publication Type] NOT “comment”[Publication Type] NOT “congresses”[Publication Type] NOT “editorial”[Publication Type] NOT “technical report”[Publication Type]; 2: “(tumor* OR tumour*) endoprosth* infect*” AND “English”[Language] NOT “case reports”[Publication Type] NOT “comment”[Publication Type] NOT “congresses”[Publication Type] NOT “editorial”[Publication Type] NOT “technical report”[Publication Type]; and 3: 1 OR 2. The search of the Cochrane Register of Controlled Trials database was performed using the terms “megaprosth*” OR “tumor* endoprosth*” AND “infect*”.

This search identified 249 pertinent records. These records were reviewed and cross-referenced to exclude repeated references, leaving 236 articles for review. Overall, 212 articles were excluded on the basis of titles or abstracts. Full-text articles were then retrieved and reviewed, in full, for the remaining 24 studies. Reference sections of all articles were searched for undetected studies, thus adding 9 studies to the review. Of the 33 studies, 25 were further excluded on the basis of the full-text review. The remaining 8 articles10–17 met the inclusion criteria and were analyzed in this systematic review (Figure).


Flowchart for the literature search.

Figure:

Flowchart for the literature search.

Results

Study Characteristics

All included studies (Table 1) retrospectively reviewed a series of patients having undergone a megaprosthetic replacement after tumor resection (level IV studies). These studies reported on a total of 2136 patients (range, 62–1161 per study); the mean patient age was 33.3 years (range, 5–90 years). In 2 studies,10,13 megaprostheses were used to treat lesions located in either the femur, tibia, humerus, or pelvis; 2 studies14,17 included only lesions of the proximal tibia; 2 studies11,12 included only lesions of the femur and tibia; 1 study15 included only lesions of the proximal femur; and 1 study16 included lesions located in either the distal femur or the proximal tibia. The mean PMI rate was 14.2% (range, 7.2%–25.8%), with PMIs having occurred from 9 days to 240 months postoperatively.


Details of Included Studies

Table 1:

Details of Included Studies

Statistical analysis of risk factors for PMIs was performed through Kaplan-Meier survival curve comparisons (ie, using the Mantel-Cox log-rank test) in 5 studies,11,12,14–16 logistic regression analysis (ie, using the Hosmer-Lemeshow goodness-of-fit test) in 1 study,13 comparative statistics (ie, using the chi-square test) in 1 study,17 and preliminary comparative statistics (ie, using the chi-square test, Fisher's exact test, the Student's t test, or the Mann-Whitney U test, when appropriate) followed by stepwise logistic regression analysis in 1 study.10

Patient-Related Factors

All of the evaluated risk factors are summarized in Table 2. Patients' sex and age at surgery were not found to influence PMI rate.10,13,14,16 Increasing body mass index was associated with a significantly higher risk of PMI.13 Overall, the presence of comorbidities was also associated with PMIs,10 but neither a higher American Society of Anesthesiologists score10 nor the presence of diabetes mellitus13 specifically increased the risk. Perimegaprosthetic infections were also found to be more frequent with a coexisting skin necrosis or a superficial surgical site infection.16 Preoperative white blood cell count,14 febrile neutropenia,13,14 bacteremia,13 and the use of an indwelling port system14 were not associated with the development of a PMI.


Risk Factors for Perimegaprosthetic Infection
Risk Factors for Perimegaprosthetic Infection

Table 2:

Risk Factors for Perimegaprosthetic Infection

Disease-Related Factors

Six studies10,11,13–16 explored the role of lesion histology and tumor characteristics in determining PMI rate. Controversy remains regarding whether primary or metastatic lesions have a higher risk of PMI.11,15 Among primary tumors, no significant differences in PMI rates were found according to histological features10,11,14 and metastatic spread at diagnosis.10,13 No significant effects of chemotherapy10,11,13,14,16 and radiotherapy10,11,15 were found for the development of a PMI.

Five studies10–12,15,16 explored the role of localization of lesions in determining PMI rate. Proximal tibial and pelvic locations were identified as strong risk factors for PMIs10; in particular, pelvic extension of proximal femoral disease has led to a higher PMI rate than that following reconstruction of the proximal femur alone.15 Conversely, distal femoral location of the lesion appears to be a protective factor for PMI.10

Procedure-Related Factors

A preoperative hospitalization of more than 48 hours has been found to predict a higher risk of PMI.10 Overall, features of perioperative antibiotic prophylaxis do not act as risk factors for PMIs; indeed, no significant differences in PMI rates have been found according to the choice of antibiotic used,13 the intraoperative dosing,13 the number of postoperative antibiotics used,16 and the length of postoperative prophylaxis.13,14

Specific operative features have been widely explored. No significant effects of the use of a clean air operating room were found for the development of a PMI.16 Two studies11,15 have shown that the use of a cemented megaprosthesis has led to a higher PMI rate than that following the use of an uncemented megaprosthesis; conversely, there were no statistical differences in PMI rates according to prosthesis type10,16 or hinge movement.11 Overall, width of resection margins,10 bone resection length,10,14,16 and extracapsular resection of knee tumors16 do not affect PMI rate; however, resection of greater than 37% of the proximal tibia was found to be related to a higher PMI rate.14 In distal femoral lesions, resection of 3 or 4 heads of the quadriceps muscle was associated with a significantly higher PMI rate than resection of 2 or fewer heads.16 The need for additional surgical procedures after the megaprosthesis implantation was associated with a higher risk of PMI.10 Two10,13 of 3 studies10,13,14 agreed that increasing surgical times statistically correlated with PMI rate; in particular, an operation lasting longer than 2.5 hours is a strong risk factor for the development of a PMI.10 One17 of 3 studies13,16,17 indicated that the routine use of a gastrocnemius flap for anterior reconstruction and megaprosthesis coverage following a proximal tibial resection led to a significant reduction of PMI rate. On the other hand, the PMI rate following megaprosthetic replacement of the proximal tibia was not found to increase with the use of synthetic material to fix the patellar tendon.14

An increased risk of PMIs was found for patients who needed a postoperative admission to the intensive care unit and for those having experienced a postoperative hematoma.13 Despite the fact that the estimated blood loss was not higher in patients with a PMI,10 two10,13 of 3 studies10,13,14 detected that an increased postoperative blood transfusion requirement posed a higher risk of PMI; in particular, transfusion of 2 or more units of allogeneic packed cells emerged as a predictor of PMI.10

Discussion

Due to improved imaging modalities, understanding of tumor biology, and advances in adjuvant treatments, limb amputation is now used selectively in the treatment of bone tumors.18 Indeed, limb salvage surgery has become the standard of care for bone tumors, being applicable for up to 85% of patients18 and resulting in limb salvage for up to 90% of them.19 Because the use of megaprostheses is currently gaining momentum as the most common reconstructive technique after tumor resection,12,20 the goal of this systematic review was to identify factors affecting the risk of PMIs. Notably, the presence of several conflicting results together with the lack of comprehensive reviews to date exploring the exact causative factors for PMIs has often led to extending to megaprostheses previous information on risk factors for periprosthetic joint infections resulting from the analysis of primary arthroplasties.5

Both the presence of comorbidities and a higher body mass index at surgery have been reported as significant patient-related risk factors for PMIs. Of interest, the direct association between body mass index and infection rate is well established in conventional arthroplasties, as obesity increases both the morbidity from osteoarthritis and the risk of periprosthetic joint infections21; conversely, caution should be exercised in applying this risk factor to the tumor megaprosthesis population, as up to 18% of previous cohorts13 were underweight.

Localization of lesions was found to be an important risk factor for PMIs, with higher rates expected following megaprosthetic replacement of both pelvic and proximal tibial tumors. As previously argued,10 long operating times because of the complex anatomy, large bone defects after tumor resection, and difficulty in achieving wide surgical margins are all factors accounting for challenges in pelvic surgery. On the other hand, the high PMI rate following proximal tibial tumor resection may correlate with the difficulty in achieving a good soft tissue coverage, thus being confirmed by the marked reduction in PMI rate following the routine use of gastrocnemius flaps as part of the reconstruction.17 Notably, soft tissue condition has been shown to be a strong predictor of PMI and the most important risk factor for failed limb salvage.7

The most important finding of this systematic review was that the majority of factors accounting for a higher PMI rate are related to both surgical procedure and hospitalization. Of interest, prolonged preoperative hospital stay and operative time,22–24 the presence of postoperative hematoma,25 and the increasing number of allogeneic blood transfusions26 are all proven risk factors for periprosthetic joint infections, and their role has been confirmed following megaprosthetic replacement after tumor resection. The results of the current review indicate that the features of perioperative antibiotic prophylaxis do not act as risk factors for PMIs, thus contradicting a previously published systematic review.8 However, evidence and guidelines directing the prescription of prophylactic antibiotic regimens in musculoskeletal tumor surgery are lacking, so considerable variation in strategies exists.27

Of interest, this review found agreement that a higher PMI rate can be expected in cemented than in cementless megaprostheses,11–15 thus contradicting information regarding conventional arthroplasties.28 However, factors such as the antibiotic loading of acrylic cement,29 megaprosthesis alloy system,30 and surface treatments31 are all pertinent to consider.

This systematic review had limitations. First, the lack of randomized controlled trials (level I or II) on the role of specific factors in the development of PMIs impeded the performance of a strict meta-analysis to draw firm and univocal conclusions. In addition, there is wide variability in the reporting of risk factors for PMIs. Notably, none of the studies considered included all of the factors studied. Moreover, there is variability in the statistical measures used. These issues combined make it difficult to compare the results for all of the factors important to the surgeon and the patient.

Conclusion

This systematic review identified the role of several factors in the development of PMIs after tumor resection. Identified factors mostly relate to both surgical procedure and hospitalization. Therefore, there are several modifiable risk factors for PMIs. Physicians should consider these results when discussing the outcomes of limb salvage surgery with patients and trying to reduce the overall burden of PMIs.

References

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Details of Included Studies

StudyYearLevelNo. of Patients (Cases)Mean Age (Range), yTumor SitePMI RatePMI OnsetRisk Factor Analysis
Dhanoa et al102015IV150 (150)25 (7–89)Femur, tibia, humerus, pelvis12.38%9 d to 63 moComparative statistics, logistic regression
Mavrogenis et al112015IV1161 (1161)31.2 (7–80)Femur, tibia8.6%3.7 y (0.5 mo to 19 y)Kaplan-Meier method
Capanna et al122015IV199 (200)43 (12–90)Femur, tibia9.5%16 (2–51) moKaplan-Meier method
Peel et al132014IV121 (121)38 (14–86)Femur, pelvis, tibia, humerus14%541 (41–952) dLogistic regression
Cho et al142012IV62 (62)26.5 (12–65)Proximal tibia25.8%34 (2–240) moKaplan-Meier method
Funovics et al152011IV166 (166)49.8 (5.9–84.3)Proximal femur7.2%39 (0–167) moKaplan-Meier method
Morii et al162010IV82 (82)31.1 (5–86)Distal femur, proximal tibia17%10.9 (0–48) moKaplan-Meier method
Myers et al172007IV194 (194)21.5 (10–74)Proximal tibia19.5%9 (2–22) moComparative statistics

Risk Factors for Perimegaprosthetic Infection

Risk FactorValue
Patient related
  AgeNS10,13,14,16
  SexNS10,13,14,16
  ASA scoreNS10
  ComorbiditiesOR, 5.13, P=.0210
  Diabetes mellitusNS13
  Increasing BMIOR, 1.12, P=.00913
  Superficial SSI70% vs 9.7%, P<.00116; NS13
  NeutropeniaNS13
  BacteremiaNS13
  Indwelling port systemNS14
  WBC countNS14
  Skin necrosis53.8% vs 10.1%, P<.00116
Disease related
  Primary tumor vs metastasis10% vs 32% (at 10 years), P<.00111; 15.3% vs 1.1%, P<.0115; NS10,16
  Metastatic spreadNS10,13
  Malignant tumorNS10
  OsteosarcomaNS10,14
  Ewing sarcomaNS11
  Preoperative chemotherapyNS10,11,13,14,16
  Preoperative radiotherapyNS10,11,15
  Localization (overall)NS11,12,16
  Proximal tibiaOR, 6.27, P=.03210
  Distal tibiaNS10
  Distal femurOR, 0.216, P=.03810
  PelvisOR, 90.32, P=.00210
  Pelvic extension from proximal femur42.8% vs 3.9%, P<.00115
Procedure related
  Preoperative hospitalization >24 hOR, 6.45, P=.04810
  Vancomycin-containing antibiotic prophylaxisNS13
  Intraoperative antibiotic dosingNS13
  No. of postoperative antibioticsNS16
  Length of postoperative antibiotic prophylaxisNS13,14
  Clean air operating roomNS16
  Cemented vs uncemented prosthesis9.6% vs 8.5%, P=.04611; 25% vs 5.8%, P<.0515
  Prosthesis typeNS10,16
  Hinge movementNS11,14
  Resection marginsNS10
  Extracapsular knee resectionNS16
  Resection length (overall)NS10,14,16
  Tibial resection >37%37.5% vs 10.3%, P=.01614
  3 or 4 vs 1 or 2 quadriceps heads resection23.5% vs 5.7%, P=.0416
  Additional proceduresOR, 11.67, P=.00310
  Surgical time (overall)OR, 1.01, P=.00313
  Surgical time >2.5 hOR, 8.96, P=.00410
  Surgical time >3 hNS14
  Gastrocnemius flap coverage14% vs 31%, P=.01417; NS13,16
  Synthetic material to fix the patellar tendonNS14
  Postoperative ICU admissionOR, 3.82, P=.0213
  Postoperative hematomaOR, 7.21, P=.0213
  Blood lossNS10
  Blood units transfused (overall)OR, 1.15, P=.0213
  >2 blood units transfusedOR, 5.74, P=.01610; NS14
Authors

The authors are from the Department of Orthopedic and Trauma Surgery (MDG, GG), “Magna Graecia University,” “Mater Domini” University Hospital, Catanzaro, and the Department of Orthopedic Oncology and Reconstructive Surgery (MDG, RC), Careggi University Hospital, Florence, Italy.

The authors have no relevant financial relationships to disclose.

Correspondence should be addressed to: Marco De Gori, MD, Department of Orthopedic and Trauma Surgery, “Magna Graecia” University, “Mater Domini” University Hospital, Viale Europa, 88100, Catanzaro, Italy ( madegori@hotmail.it).

Received: February 27, 2016
Accepted: May 02, 2016
Posted Online: December 07, 2016

10.3928/01477447-20161128-01

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