Musculoskeletal disorders are a leading cause of severe chronic pain and physical disability for millions of people around the globe. It is anticipated that their prevalence will increase dramatically in the future because of extended life expectancies and lifestyle changes toward more mobility and recreation1. Epidemiologic studies have linked population aging with future increases in the prevalence of age-related musculoskeletal conditions, such as fragility fractures and osteoarthritis2-8. The number of primary and revision total hip and total knee arthroplasties has increased steadily between 1990 and 2002, and these numbers are anticipated to further escalate over the next two decades9,10. The rate of deep infection following total hip arthroplasty and total knee arthroplasty has been reported to range between 1% and 4%11, and the rate of deep infection as a reason for revision is projected to increase at a faster rate for total knee arthroplasty than for total hip arthroplasty. Kurtz et al. used the U.S. Nationwide Inpatient Sample (1990-2003) to demonstrate that the number of infections after revision total hip arthroplasty is projected to increase from 3400 in 2005 to 46,000 in 2030, while infections after revision total knee arthroplasty are projected to increase from 6400 in 2005 to 175,500 in 203012.
Infections with resistant pathogens, such as the community-acquired and the health-care-acquired methicillin-resistant Staphylococcus aureus, have become increasingly common over the past two decades13. Soft-tissue infections such as cellulitis, abscesses, and pyomyositis from community-acquired methicillin-resistant Staphylococcus aureus occur with increasing frequency in athletes, especially in those engaged in team sports14-16. Health-care-acquired methicillin-resistant Staphylococcus aureus generally affects acutely and chronically ill patients with central lines, indwelling catheters, and internal fixation devices, causing septic arthritis, osteomyelitis, and bacteremia17. In addition, the contemporary management of fractures frequently uses implantable hardware for internal fixation. The overall infection rate following internal fixation is approximately 5%, with open fractures being disproportionately affected18. Moreover, the number of elderly patients with hip fractures treated operatively is growing, and this has resulted in increased rates of methicillin-resistant Staphylococcus aureus infection18.
Nosocomial infections are also becoming more common; this is attributed to overcrowding, understaffing, inadequate hand-hygiene compliance by health-care workers, and increased movement of patients and staff between hospital wards19,20. In addition, the growing number of high-risk, immunocompromised patients undergoing surgery further increases the severity of septic complications and other adverse outcomes21,22. As well as being life-threatening23, these infections can often lead to functional impairment, long-lasting disability, or even permanent handicap with an inevitable social and economic burden24-26.
Musculoskeletal infections place an additional cost burden on total health-care expenditures, which are already rising faster than the gross domestic product in the United States27. However, both in the United States and Europe, bone and joint disorders have not been addressed as a health-care priority1. The latest economic developments impose the need for an open forum discussion of this subject that might increase awareness among health-care professionals and policy makers, for the benefit of our patients and the medical community in general. In this review, we analyze the available evidence on the growing socioeconomic consequences of musculoskeletal infections on the patient and the health-care system, including the unavoidable impact on the treating physician.
An unrestricted computerized search of OVID SP and MEDLINE for studies published between 1950 and 2010 was conducted, and additional searches of the reference lists of retrieved articles in any language were done. The following terms were used in various combinations: "biofilm infections," "treatment cost," "infected joint arthroplasties," "socioeconomic burden," "economics," "necrotizing fasciitis," "soft tissue infections," "musculoskeletal wound infections," "staphylococcal infections," "osteomyelitis," "prosthesis-related infection," "periprosthetic joint infection," "joint replacement infections," and "cost." Although abstracts of English, French, and German-language publications were read, only English-language works were selected for a final review. Data from abstracts and correspondence were included as long as the data were not subsequently duplicated in published articles. The terms related to costs and social and economic burden were, in most cases, "hidden" inside the reports rather than addressed as main issues of the studies.
Health-care-associated infections are second only to medication errors as a cause of adverse events in hospitalized patients28. The acquisition of a nosocomial bacterial pathogen by a susceptible patient may occur by means of the hands of health-care workers, as hand-washing policies are seldom adhered to, especially during periods of understaffing and high workload29-34. The chain of transmission of nosocomial or community-acquired pathogens, such as the health-care-associated methicillin-resistant Staphylococcus aureus or the community-acquired methicillin-resistant Staphylococcus aureus strains by means of the hands of health-care workers or escorts of the patients, underlines the importance of hand hygiene in the development or the transmissibility of infection35. As a consequence of the magnitude of the health-care-associated infection burden worldwide, the World Health Organization28 recently adopted guidelines on hand hygiene in health care. Methods to assess the size and nature of the problem exist and can contribute to correct monitoring and discovery of solutions.
Hand-cleansing is an imperfect process, the efficacy of which depends on the product used, the technique employed, and the duration of the process. Thus, it is likely that it will not remove all of the microorganisms from the hands of health-care workers. Bottone et al.36 reported that washing the hands with a nonantiseptic lotion soap five times for thirty seconds each time did not reliably remove all of the nosocomial pathogens applied to the fingertips; therefore, a single hand-washing, even assuming a bacterial contamination of 100 colony-forming units, as shown by fingertip transfer experiments, is not sufficient to remove all bacteria between patient contacts. Girou et al.37, for example, found that rubbing hands with a 75% alcohol-based solution resulted in a median percentage reduction in bacterial contamination of 83% compared with a reduction of only 58% when washing with medicated soap. Similarly, Zaragoza et al.38 found that the use of an alcohol-based solution resulted in an average reduction in colony-forming units of 88.2% compared with only 49.6% when soap and water was used. In this direction, Mody et al.39, using a nationally representative sample of hospitals in the United States, revealed that the use of an alcohol-based hand-rubbing solution for hand hygiene has been widely adopted with little discussion or controversy, regardless of academic or Veterans Affairs affiliation, participation in a collaborative, presence of a hospital epidemiologist, or the number of infection control professionals at a given hospital. They reported also that the use of an alcohol-based hand-rubbing solution appears to have a clear and unambiguous advantage in enhancing hand-hygiene practices among health-care workers, a practice previously plagued by poor compliance. Thus, hand-washing and/or hand-rubbing with an alcohol-based solution should be a crucial action recommended to prevent and control the transmission of pathogens within health-care settings.
Monitoring the compliance of health-care workers with the guidelines for hand hygiene showed that the frequency of hand-washing decreases as the rate of indications for hand-washing increases30-33,40. Mody et al.39 reported that the alcohol-based hand-rubbing solution is a relatively simple innovation and perceived as a time-saver. Moreover, its use is straightforward to implement and apparently poses little risk to users. Furthermore, it has been shown that alcohol hand gels cause less skin irritation and dryness than soap-and-water hand-washing41.
From an economic point of view, noncompliance with hand-hygiene practices is associated with considerable attributable hospital costs, and minimal improvements in compliance can lead to substantial savings42. Although full adherence to hand-hygiene recommendations may not have yet been attained at some institutions, Pittet et al.43 reported that the promotion of hand hygiene is probably cost-saving from a hospital perspective as the total costs associated with a successful alcohol-based hand-hygiene promotion campaign corresponded to <1% of the costs attributable to nosocomial infections. In this direction, hand hygiene has been identified as and proven an effective preventive measure that is often simple to implement.
The use of gloves is also an essential action when it can be anticipated that contact with blood or other potentially infectious materials, mucous membranes, or nonintact skin will occur44. However, in no way does glove use modify or replace hand hygiene by either hand-rubbing or hand-washing45-48. Health-care workers should never wear the same pair of gloves for the care of more than one patient45-48 or during patient care if they are moving from a contaminated body site to either another body site within the same patient or the environment46,48. The reuse of gloves is not recommended49. Gloves represent a risk for pathogen transmission and infection if used inappropriately28.
Health-care workers’ attitudes and compliance with hand hygiene are extremely complex50, and available data indicate that a successful program would have to be multidisciplinary and multifaceted50. It has been reported that hand-hygiene monitoring through observation of the behavior of caregivers and recording of the actions taken can lead to higher rates of hygiene compliance and consequently to a real decrease in the number of hospital-acquired methicillin-resistant Staphylococcus aureus infections51. Leadership support and commitment to adopting and implementing evidence-based recommendations are crucial, particularly for innovations that require organization-wide deployment. Consistent with this observation, the probability of a facility adopting the use of an alcohol-based hand-rubbing solution was positively associated with increased agreement that leadership is supportive and rewards clinical innovation39. Nevertheless, culture change is frequently required as the level of compliance often depends on staff beliefs and attitudes, while the importance of role models and senior mentors should always be underlined52.
Chu et al.53 investigated the clinical outcome, use of health-care resources, and infection-associated costs of Staphylococcus aureus bacteremia in hospitalized patients with all types of prosthetic devices between 1994 and 2002. The orthopaedic device group comprised 24% of all patients with bacteremia and included deep-tissue abscesses (10%), septic arthritis (8%), and osteomyelitis (5%). The mean total costs in the orthopaedic group, including initial hospitalization, outpatient visits, and rehospitalizations of up to twelve weeks after an episode of Staphylococcus aureus bacteremia, were the second highest following cardiovascular devices. A hospital-acquired infection was 15% more costly compared with a community-acquired infection and required the highest mean number of procedures (2.4) per patient53. Similarly underscoring the gravity of bone and joint infections, a study by Rubin et al.54 revealed that the direct medical costs, including the mean hospital charges, professional fees, and expenses after hospital discharge, for the treatment of osteomyelitis (US$35,000) and septic arthritis ($35,100) were similar to those for pneumonia ($35,400) and were higher than those for bacteremia ($31,300) or surgical site infections ($21,800). Likewise, in twelve patients with biopsy-confirmed chronic pelvic osteomyelitis from neglected truncal pressure ulcers over an eighteen-month period (six months prior to the initial positive bone biopsy to one year following the bone biopsy), the costs of treatment reached a mean of $59,600 per patient, including hospital, professional, and pharmacy charges but excluding surgery charges55.
Whitehouse et al.56 studied surgical site infections after orthopaedic surgery and reported dramatically greater costs for the patients with an infection, with twice as many hospitalizations and operative procedures as those for matched uninfected control patients and median hospital costs that were four times higher. Patients with an infection also reported greater physical limitation and a greater reduction in health-related quality of life. Clinical outcomes following either a single-stage or a two-stage revision joint arthroplasty because of sepsis have been less favorable than those after aseptic revision arthroplasty57.
Revision for an infection at the site of a total knee arthroplasty required an average of 2.4 additional hospitalizations and 3.4 additional operations, with a hospital stay that was 3.7 times longer than that required for a primary arthroplasty and 2.7 times longer than was necessary for an aseptic revision58. The total operative time required for a two-stage revision for an infection at the site of a knee arthroplasty was 3.4 times greater than that required for a primary total knee arthroplasty and 1.8 times greater than that for an aseptic revision; patients with an infection also received more blood transfusions59,60. Furthermore, satisfaction rates for patients undergoing revision total knee arthroplasty are <50%, an undeniably dismal number61.
With use of a single surgeon's database (100 nonconsecutive septic and aseptic revision total knee arthroplasties from 1992 to 2000)62, it was demonstrated that resource consumption for patients with an infection was more than double compared with the average aseptic revision. Some of this difference was from the increased length of stay (2.5 times longer) and a higher complication rate (21.2% for the septic group compared with 9% for the aseptic group). The implant type also made a big difference in overall resource consumption in the infection subgroup. Single component exchange, based on early detection and aggressive treatment, necessitated 50% less resource consumption compared with two-stage procedures as a result of late intervention (mean, US$56,746 compared with $109,805) and resulted in less morbidity as well. This finding underscores, from a cost-effectiveness perspective, the importance of rapid detection and timely and efficient treatment of acute postoperative or hematogenous periprosthetic infections, in which implant stability is preserved. Additionally, isolated removal and isolated reimplantation resulted in much higher morbidity and greater resource consumption. Isolated reimplantations were technically more challenging and consumed substantial resources ($116,831). Isolated removals were done in patients whose severity of illness was so great they could not undergo reimplantation; their poor medical status also explained the considerable resource consumption ($99,045) in these cases.
The impact of an infection at the site of a hip arthroplasty on morbidity, costs, and length of stay was examined by Bozic and Ries11. They found that the total direct medical costs associated with revision total hip arthroplasty because of infection are 2.8 times higher than those associated with revision because of aseptic loosening and 4.8 times higher than the direct medical costs associated with a primary total hip arthroplasty.
One of the limitations of the previously described studies is that clinical and economic data were obtained from a subset of patients from either a single institution or a single surgical practice11,53-56,58-60,62,63, which may or may not reflect national or international revision costs related to infection. The Nationwide Inpatient Sample is particularly well suited for epidemiological studies of rare procedures or diseases, such as deep infection, in the United States population. Kurtz et al.64, by using data from the Nationwide Inpatient Sample (1990-2004), showed that the rate of infection was 0.92% after a total knee arthroplasty and 0.88% after a total hip arthroplasty. The length of stay was significantly longer for patients with an infection at the site of a hip arthroplasty (9.7 days) and for those with an infection at the site of a knee arthroplasty (7.6 days) compared with procedures in patients without an infection (4.3 days for hip procedures and 3.9 days for knee procedures). Hospitalization charges were also significantly greater for arthroplasties in patients who had an infection develop (1.76 times greater for hip procedures and 1.52 times greater for knee procedures) than for patients who did not have an infection. Urban nonteaching hospitals experienced the highest burden of infection (1.18% for hip procedures and 1.26% for knee procedures) compared with rural (0.61% and 0.69%, respectively) and urban teaching hospitals (0.73% and 0.77%, respectively). An important limitation of the study is that the authors did not capture the second stage of a two-stage revision for infection. This resulted in an underestimation of the overall economic burden for infection.
Kurtz et al.65, using the same database, also demonstrated that the economic burden of infections is expected to exceed 50% of the inpatient resources available for revisions by 2025 for total hip arthroplasty and by 2016 for total knee arthroplasty. The overall prevalence of deep infection (the infection burden) is projected to increase at a comparable rate for both primary and revision total hip arthroplasty and total knee arthroplasty, with the infection burden increasing between 2005 and 2030 from 1.4% to 6.5% for total hip arthroplasty and from 1.4% to 6.8% for total knee arthroplasty.
In an another study by the same group12, the length of stay for patients who had an infection after revision arthroplasty was shown to be, on the average, 1.6 times greater than that for patients who had a revision without infection, and the hospital charges for patients who had an infection after a revision were, on the average, 1.5 times greater than those for patients who had a revision without an infection. However, there was no significant difference in the length-of-stay ratio or in the charge ratio for hip compared with knee revision procedures. The same authors also demonstrated that the hospital setting (rural, urban nonteaching, or urban teaching) did not significantly influence the length-of-stay ratio or the charge ratio, but it had a substantial effect on the infection burden; the greatest proportion of the infections were diagnosed in urban teaching hospitals, as they serve as referral centers although the primary operations were done elsewhere.
Bozic et al.66, on the basis of the Healthcare Cost and Utilization Project Nationwide Inpatient Sample database, analyzed the clinical, demographic, and economic data from 51,345 revision total hip arthroplasties in the United States over a fifteen-month period. Infection (14.8%) was the third most common cause of revision, following instability and/or dislocation (22.5%) and mechanical loosening (19.7%). Infection was by far the most common reason for arthrotomy and removal of the prosthesis (74.3%), followed by dislocation (11.7%). The highest average billed charges ($69,380) were associated with arthrotomy and prosthesis removal, underlining the greater resource consumption for revision total hip replacements in patients with an infection.
Although single-stage exchange revision has been proposed as a means to decrease costs and rehabilitation time, and possibly to reduce the mechanical complications following surgery for infection at the site of an arthroplasty, this method is less likely to be more cost-effective than the two-stage exchange because of its inherent higher probability for reinfection67. Furthermore, the emotional burden and suffering should never be underestimated because, even in patients whose treatment is successful, six to eighteen months of rehabilitation are necessary in order to regain function comparable with the preinfection state68; however, this state is rarely achieved.
Periprosthetic infections may also become lethal, although it is rare, with an overall mortality rate reported to range from 1% to 2.7% for patients around sixty-five years of age and increasing to 7% for patients who are more than eighty-five years old69. In the first three months after resection arthroplasty, the probability of death increases twofold in patients with infection at the site of a hip arthroplasty. In cases of life-threatening systemic sepsis and when local tissue conditions or the patient's general health status becomes severely impaired, disarticulation may be necessary to reduce the probability of death70.
Hip fractures requiring a revision operation, especially revision for infection or failure of fixation, result in a twofold to threefold increase in cost compared with the uncomplicated cases71. In one study, prospective data on early infection (diagnosed two to eighty-four days postoperatively) after hip fracture surgery72 demonstrated that 1.2% of the patients developed a deep wound infection and 1.1% developed a superficial one. Staphylococcus aureus was the causative agent in 71.3% and methicillin-resistant Staphylococcus aureus, in 48.8% of the patients. Length of stay, cost of treatment, and predischarge mortality all substantially increased with deep infection of a hip fracture wound. The one-year mortality was 50% compared with 30% for those who did not have an infection develop. A deep infection doubled the operative costs, tripled the investigation costs, and quadrupled the ward costs. Methicillin-resistant Staphylococcus aureus infection increased costs, length of stay, and predischarge mortality compared with infection with non-methicillin-resistant Staphylococcus aureus.
Necrotizing fasciitis is a life-threatening emergency with mortality rates reported to range from 6.1% to 43% when it affects the extremities73 and as high as 76% when it affects the abdominal wall and perineum23,74-80. Specifically, Ogilvie and Miclau23 retrospectively analyzed the cases of 150 patients with necrotizing soft-tissue infections of the extremities and reported an overall mortality of 9.3%, which was lower than the 26% rate reported in a meta-analysis of mixed anatomic sites76. Patients presenting with clinical evidence of necrotizing fasciitis need specific multidisciplinary intervention including surgical, intensive care, infectious disease, and hyperbaric oxygen specialists81. Making a timely diagnosis soon after presentation requires a high index of suspicion by the orthopaedic surgeons who are often the first to treat such patients referred for "treatment of cellulitis" after a fracture or soft-tissue injury. Early diagnosis and treatment is associated with lower mortality rates77,78. The treatment of patients with necrotizing fasciitis incurs direct hospital inpatient costs resulting from critical morbidity and tissue loss as well as postdischarge costs for the survivors because of the need for extensive rehabilitation and, in some cases, long-term disability.
Faucher et al.79 collected data from cases of patients admitted for acute care with the diagnosis of necrotizing fasciitis (thirty-nine patients) or Fournier's gangrene (eighteen) and demonstrated an in-hospital mortality rate of 12%. The mean length of stay (and standard deviation) for the survivors was 26.3 ± 2.2 days (range, one to seventy days), and charges ranged from US$20,000 to $866,000 (mean, $154,000 ± $22,700). The daily charges for those who died were twice as high as those of the survivors, illustrating the greater resources needed for these more seriously ill patients.
Widjaja et al.80 analyzed the cost of treating necrotizing fasciitis at an Australian tertiary-care referral hospital with extensive experience with these infections and a well-developed financial expenditure system and compared the cost with the current case-mix-based government funding arrangements applied in Victoria, Australia. Clinical costing data quoted in Australian dollars were provided with a breakdown into the following cost groupings: medical, surgical, nursing, allied health, operating room, emergency department, intensive care unit, imaging, pathology, pharmacy, and hyperbaric therapy. The lower limb was involved in 77% of the cases, and the upper limb, in 23%. Approximately 90% of the cases were referrals, and one-third of the patients were receiving respiratory support with ventilation at the time of transfer. Two-thirds of the patients required intensive care admission for a mean of eleven days (range, one to forty-nine days). Overall, 11% of the patients died; half of them died in the first week after admission, and half died as a result of late complications. The mean hospital stay was thirty-six days for survivors and sixty-eight days for those who died. For the ninety-two patients studied, the total funding dollar value reached AU$3,208,664, but the true costs of inpatient care were nearly twice that amount at $5,935,545 (a mean cost of $64,517 per patient). Only ten patients received funding that exceeded the hospital costs, and the average shortfall per case was $33,891. One of the patients in this study incurred a total cost of $514,889 with forty-six days in the intensive care unit and 474 in-hospital days. The mean cost of treating necrotizing fasciitis in this series exceeded that reported in the literature for a number of other medical conditions such as endarterectomy82, coronary artery bypass surgery83, one year of hemodialysis84, or surgical treatment of cerebral arteriovenous malformations85. The limitation of the study was that it did not evaluate the costs of rehabilitation after discharge, transfer to other institutions for reconstructive surgery, or the lost productivity of the patient. Furthermore, the authors did not attempt to calculate the cost of initial hospitalizations elsewhere or patient transfer by ambulance, often including a medical escort. It is clear that necrotizing fasciitis infections are expensive conditions to treat, both in terms of dollars as well as in terms of mortality, morbidity, and residual disability.
Skin and soft-tissue infections of the extremities are causes of frequent visits to health-care providers. Most of them are superficial and are readily treated with local care and oral antibiotics. However, they may affect deeper structures including fascia and muscle16. Charalambous et al.86 reported on 142 consecutive hospital admissions to treat acute soft-tissue infections of the extremities between 1996 and 2001; half of the infections were cellulitis and a substantial proportion (forty-three) were abscesses. The 142 soft-tissue infection episodes required 143 operations and accounted for 748 hospital inpatient days and a total of 194 follow-up clinic appointments. The average stay was four days (range, one to forty-four days), comparable with the postoperative stay following elective hip and knee joint replacement at the same institution.
The costs are even higher in cases in which methicillin-resistant Staphylococcus aureus infection of the skin and soft tissues either complicates a surgical incision or causes an infected skin ulcer or abscess. Rosner et al.87 reviewed the charts of all eighty-nine patients with methicillin-resistant Staphylococcus aureus infections admitted to a teaching hospital and treated with either intravenous administration of vancomycin or linezolid. The total hospital and nonhospital costs were higher in the vancomycin-treated group (Can$8444 per patient) compared with the linezolid-treated group ($7693 per patient), which had a one-day shorter length of stay with the patients discharged on oral linezolid. Hospitalization represented approximately 80% of the total cost. Similarly, examining the outcome and economic consequences of methicillin-resistant Staphylococcus aureus infections, Resch et al.88 presented a retrospective matched-pairs analysis of routine administrative data from eleven German hospitals (ranging from small specialized clinics to large maximum care and university hospitals). On the basis of 313,942 cases, which represented 1.9% of all the cases reported in German hospitals in 2004, the results showed that patients with methicillin-resistant Staphylococcus aureus stay in the hospital eleven days longer, exhibit a 7% higher mortality, are 7% more likely to undergo mechanical ventilation, and incur substantially higher total costs (mean difference, €8198) compared with patients without methicillin-resistant Staphylococcus aureus infection. The higher cost was attributed mainly to longer stays in the hospital, as the cost per day was only marginally higher.
Moreover, Anderson et al.89 conducted a multicenter matched-outcomes study in order to estimate the impact attributed to Staphylococcus aureus and methicillin resistance on the outcomes of 659 surgical patients (46% of the orthopaedic procedures). They compared patients with surgical site infections due to methicillin-resistant Staphylococcus aureus with matched control patients without infection and with patients with surgical site infections due to methicillin-sensitive Staphylococcus aureus. Patients with a surgical site infection because of methicillin-resistant Staphylococcus aureus were thirtyfold more likely to be readmitted and sevenfold more likely to die within ninety days compared with controls without infection. Similarly, patients with a surgical site infection due to methicillin-resistant Staphylococcus aureus stayed in the hospital for sixteen more days and accrued more than US$40,000 of additional charges compared with controls without infection. Concerning the impact of methicillin resistance, patients with a surgical site infection due to methicillin-resistant Staphylococcus aureus compared with patients with surgical site infection due to methicillin-sensitive Staphylococcus aureus were 2.6-fold more likely to die within ninety days following surgery, and they stayed in the hospital six more days and accrued >$23,000 of additional charges.
Extending the length of hospital stay for individuals with an infection further aggravates the problem of hospital bed shortage under the pressure for new admissions. When the incidence of methicillin-resistant Staphylococcus aureus exceeds the capacity of the hospital's isolation facilities, multibed rooms might be used for isolation, preventing the use of both occupied and unoccupied beds90, a phenomenon termed bed blocking. A blocked bed represents a lost opportunity to provide services to another patient (opportunity cost), which in public health care can be difficult to quantify in economic terms. Herr et al.91 calculated that >80% of the excess costs associated with control of methicillin-resistant Staphylococcus aureus were related to bed blocking. Hospital administrators attempt to alleviate pressure on bed use by increasing the number of beds in a fixed-area ward. Unfortunately, this strategy has been shown to actually increase methicillin-resistant Staphylococcus aureus transmission and cross-infection92 by means of an increase in the number of possible contact routes.
A high prevalence of methicillin-resistant Staphylococcus aureus infection leads to a high rate of bed occupancy, overcrowding, and overburdening of the isolation facilities with a subsequent increased workload of the nursing staff, impeding their effectiveness. This can directly lead to organizational fatigue, which exhausts the health-care personnel93. Factors such as staff turnover rate, staff burnout, frequent movement of patients and staff between hospital areas, increased intermixing of specialties within wards and subsequently increased rates of absenteeism—from understaffing—have been associated with higher prevalences of hospital-acquired infections. These conditions also lead to a negative psychological component in the quality of care and an emotional burden on the staff94,95. Nursing workloads have been shown to rise as a result of an increase in both patient length of stay and severity of illness96. Multiresistant organisms further increase the need for infection control practices and therapeutic activities97. However, such situations are seldom accompanied by an increase in staff numbers and represent, therefore, an additional work burden on nursing staff, ever feeding the vicious circle98.
With regard to total joint arthroplasty, several studies have documented the direct association between surgical procedure volume in a particular hospital and better clinical outcomes in terms of reducing readmissions, reoperations, complications, and mortality rates99,100. The economic burden resulting from disproportionate resource consumption and the lack of incremental reimbursement for revision arthroplasty contributes to the financial problems of many tertiary-care referral centers99. The strong financial disincentives from current reimbursement policies have led certain high-volume joint replacement centers to restrict access to patients with an infection around an implant. This defensive policy may have a detrimental impact on the care and clinical outcomes of such patients.
The growing concern about avoidable complications that patients acquire in the hospital, especially hospital-acquired infections, forced the U.S. Congress in October 2008 to enact legislation providing hospitals with financial incentives to improve patient care. From that date on, Medicare payments to hospitals for the additional care that patients require after contracting certain "hospital-acquired conditions" would be withheld, including catheter-associated urinary-tract infections, vascular catheter-associated bloodstream infections, and certain types of surgical site infections101. Among the unintended consequences of payment withholding for care related to hospital-acquired infections are unnecessary screening tests at the time of admission and overprescription of antibiotics, which only worsen the problem of antibiotic-resistant infections101.
In the era of restricted financing of the health-care systems, many hospitals tried to decrease health-care costs by replacing registered nurses with nursing assistants and by reducing the proportion of full-time staff102,103. However, these procedures had an immediate negative effect on outcomes. Fridkin et al.104 and Stegenga et al.105 reported that cost savings in hospitals, achieved by workforce reengineering, might be offset by increased costs arising from the more frequent occurrence of hospital-acquired infections and other hospital-related adverse events. Additionally, the proportion of experienced staff or the skill-mix of the nursing staff, defined by the ratio of regular nurses to agency, or so-called pool or float, staff (i.e., staff not normally assigned to a particular hospital unit, but who are moved between units or hospitals in response to staffing requirements), have both also been associated with the prevalence of hospital-acquired infections106-108.
Revision surgical procedures per se already pose substantially higher requirements for the surgeon than do primary procedures, in terms of total time spent, mental effort, judgment, technical skills, physical effort, stress, preoperative planning, and exposure to liability59. The human labor and the system resources required for the treatment of an infection at the site of an arthroplasty have been estimated to be three to four times higher compared with those of a primary total joint replacement and two to three times more than the work and resources needed for an aseptic revision arthroplasty57,59,60.
However, this difference is not reflected in the reimbursements received by the surgeon. Hebert et al.58, in a retrospective review of clinical and economic data for primary total knee replacement and aseptic and septic revision total knee replacements, demonstrated that the surgeon's charge for operative treatment of an infection at the site of a knee replacement was 1.5 times that for an aseptic revision and 1.7 times that for a primary total knee implant. The surgeons were reimbursed only 54% of the charges for operative treatment of the infection around the total knee implant and 58% of the aseptic revision charges. Finally, the surgeon's reimbursement constituted 11% of the total fees collected for the treatment of an infection at the site of a total knee implant compared with 21% collected for a primary arthroplasty and 18%, for an aseptic revision arthroplasty. In the United States, under the current Medicare sustained growth rate formula, physicians should expect an overall 37% decrease in reimbursements from 2007 to 2015 without congressional intervention109. Furthermore, physicians should be rewarded for forgoing income for the additional training time needed for the management of musculoskeletal infections110, but instead Congress dropped this opportunity cost component from the equation of the reimbursement rates111. Technical errors or problems with physician-patient communication may lead to malpractice claims. Malpractice insurance is most often obligatory and also contributes to increasing treatment costs109. Upadhyay et al.112 described the results of a survey on the most frequently reported adverse events that led to malpractice litigation among members of the American Association of Hip and Knee Surgeons. Infection was the third most commonly cited source of litigation in the survey (6.9% of the respondents had been defendants in a malpractice action related to this adverse outcome), following nerve injury (13%) and limb-length discrepancy (7.9%). Financial considerations are an important driver of malpractice suits in certain populations or in areas with high concentrations of attorneys113. Strong physician-patient interactions and the best possible preoperative oral and written communication with the patient and the patient's relatives provide the best protection against unwarranted litigation112,114,115.
Further investigating the effect of the density of attorneys on this matter, Sakoulas et al.116 showed that in seventeen countries in Europe and North America and in forty-one states in the United States, there is an association between the number of antibiotic prescriptions written per capita and the rate of methicillin-resistant Staphylococcus aureus infections; furthermore, the authors demonstrated that the proportion of methicillin-resistant Staphylococcus aureus among clinical Staphylococcus aureus infections was closely associated with the population density of attorneys but not with the density of physicians. Perhaps physicians believe that antibiotics provide a greater chance of avoiding an adverse clinical event rather than causing one or that the use of antibiotics might avert a lawsuit or provide a better defense in the event of a lawsuit. Although the direct cost of defending medical malpractice claims is extreme, exceeding $6.5 billion in the United States in 2001117, the indirect costs to society incurred by promoting an increase in antimicrobial resistance among virulent pathogens such as Staphylococcus aureus is incalculable.
It is obvious that the treatment of bone, joint, and soft-tissue infections necessitates the cooperation of surgeons specialized in musculoskeletal infections and reconstructive orthopaedic surgery, microbiologists, pathologists, radiologists, and physiotherapists in order to accomplish effective management and achieve a functional outcome. In the process of cost identification, it is imperative that we should not only examine the burden of the patient's pain and suffering, we should also gain deeper insights into the burden of these particular infections on the health-care system, the surgeon, and the other physicians managing bone and joint infections. In this way, the estimation of the true cost of bone, joint, and soft-tissue infections can be used to determine the cost-effectiveness of preventive strategies.
In the last two decades, the number of reports examining the cost of musculoskeletal infections was small, considering their major burden and the devastating impact upon patients. Few studies have adhered to the principles of sound economic analysis118, and most were actually retrospective cost-identification or cost-minimization analyses. As far as revision arthroplasties for the treatment of infection are concerned, none of the published studies have calculated the total costs and especially the nonmedical, or indirect, costs to the patient and the society. There have been no reports in the literature evaluating the cost, even direct, of infection at the site of a total joint replacement in the upper extremity, except for direct medical costs in certain cases of soft-tissue infections80,86,88,89,119. An important limitation of most of the reports we analyzed is the lack of data about prior hospitalizations or patient transfer by ambulance (direct nonmedical costs) and a medical escort, the building opportunity costs, postdischarge rehabilitation, or special needs for reconstructive surgery at other institutions120,121. The intangible costs (pain and suffering) or the indirect cost120,121 to the community in terms of lost productivity and reduction in the workforce (morbidity and mortality costs) are either underestimated or not addressed. However, the suffering from disability, the pain, the reduced self-esteem, and the feelings of non-well-being are all factors that are extremely difficult to quantify.
The opportunity cost for special training for each physician specialized in the management of infectious diseases, although hard to quantify, must be identified and calculated as well. Also, analyzing data from single-institution series or heterogeneous groups of patients with different infection etiologies is an additional limitation of the small number of studies available currently; the exceptions are the ones that are based on the Nationwide Inpatient Sample database12,64-66.
All surgeons must be concerned for quality improvement as an integral part of patient care and should never hesitate to diagnose an infectious complication and proceed with the appropriate management. Early intervention is the best way to reduce the likelihood of the infection spreading to deeper structures. From the patient's perspective, delays and negligence have particular implications for the cost of care. Surgical teams dedicated to primary joint replacement help to decrease infection rates, which have been higher in low-volume community-based hospitals99. Aggressive measures, including use of laminar air-flow operating rooms, body exhaust suits, and judicious perioperative antibiotic prophylaxis, have reduced the risk of infection to 0.3% in primary total hip arthroplasty and 0.5% in primary total knee arthroplasty122. The question is whether we can further reduce infection rates. In this direction, the application of clean-room technology in the operating-room environment might be the most efficient prevention strategy. Additionally, biomedical engineering companies, through the manufacture of implants less vulnerable to bacterial attachment, could assist in reducing the rate of postoperative infections.
With a focus on the three specific health-care strategies of prevention, early diagnosis, and effective treatment, the wise use of antimicrobials and the prevention of transmission could establish lower rates of infection for all hospitals. Regarding prevention, innovations such as hand-hygiene protocols that are clear, simple, compatible with organizational structure, and unequivocal in their effectiveness are more easily adopted. An innovation with a visible, measurable benefit that also improves task performance is also more likely to be universally adopted123. Proposed solutions to the problem of inadequate levels of hand hygiene are staff training, sufficient and conveniently located supplies, efficient mechanisms for continuous supervision and follow-up, and rewarding of good practices. Because of concerns about the emergence of resistance to antiseptics, antimicrobial soaps are generally not recommended for regular hand-washing124. In the same direction, it has been shown that the use of examination gloves can be hazardous for both the patient and the health-care worker unless certain precautions are taken. Latex gloves are easily punctured and can provide an ambient medium (moisture and warmth) for bacteria to breed rapidly. Therefore, washing hands and applying antimicrobial substances to them before donning gloves and washing hands immediately after removing the gloves is recommended125.
Computer hardware in the health-care environment creates a potential reservoir for bacteria and might be a factor in the dissemination of microbes. One control measure would be to relocate the computer or isolate it with a water-impermeable barrier126. In an attempt to reduce surgical morbidity, the Surgical Infection Prevention Project and the Surgical Care Improvement Project have outlined evidence-based recommendations, bundling several strategies into a comprehensive approach127. They include the initial administration of perioperative antibiotics within one hour before the surgical incision and the preoperative use of hair clippers or no hair removal, as opposed to shaving of hair. The weight of evidence suggests that chlorhexidine-alcohol should replace povidone-iodine as the standard for preoperative surgical scrubs128. Moreover, intranasal mupirocin and chlorhexidine baths for carriers of Staphylococcus aureus who have been identified preoperatively by means of a real-time polymerase chain reaction assay could be administered primarily to all patients receiving an implant and all immunosuppressed surgical candidates129.
Antimicrobial management programs130 are important and should be based on a complete understanding of the relationship between antimicrobial use and resistance. Essential to a successful antimicrobial stewardship program is the presence of at least one physician trained in infectious diseases who designs, implements, and administers the program. Pharmacists whose primary role is in processing medication orders and dispensing drugs in the hospital may note when restricted antimicrobials are ordered and notify the prescriber that authorization is required; only selected antimicrobial agents should be freely dispensed by the pharmacy130. This could also easily prevent the trend of change in practice habits associated with medicolegal risks, as it has been reported that physicians believe that the use of antibiotics might avert a lawsuit or provide a better defense in the event of a lawsuit116. The hospital clinical microbiology department should provide summary data on antimicrobial resistance rates, which will allow the antimicrobial stewardship team to determine the current burden of antimicrobial resistance in the hospital, facilitating the decision-making. Hospital epidemiologists have the expertise in surveillance and study design to lend to efforts to investigate the effect of various antimicrobial stewardship measures. The refinement of advanced molecular approaches is needed to aid in the rapid and effective diagnosis and epidemiologic analysis of nosocomial infections130. Quality control of practices and establishment of centers specialized in the treatment of infectious diseases should be promoted by each health-care system. The teams dedicated to treating infections can allocate the resources to make the treatment not only clinically optimal but also optimally efficient from a cost-of-care point of view.
In the current socioeconomic environment, health-care-associated infections continue to be an important patient safety problem and the financial and social costs have become staggering. Hospitals are under pressure to decrease costs associated with preventable hospital-acquired infections, most specifically those affecting the musculoskeletal system. However, how best to achieve this goal is not clear and further research is required with regard to the comparative effectiveness of specific interventions. Cost is a parameter that needs to be considered when clinical practices are assessed. Understanding the true societal costs relating to musculoskeletal infections occurring both in and out of the hospital will be important. Infection prevention, early diagnosis, and immediate intervention for an effective management have become a focus of attention for patients, payers, and regulatory organizations now demanding accountability and reductions in the rates of periprosthetic infections. Rigorous economic evaluation and formal cost-effectiveness analysis comparing various infection control and prevention strategies are required, and this research should be conducted from multiple perspectives.
Infection prevention is not only of interest to patients and surgeons but is also a major focus of payers and health policy makers and regulators. Therefore, it is necessary for all orthopaedic surgeons to become familiar with the known evidence-based best practices such as prophylactic antibiotic use, surgical site skin-preparation techniques, and hand-hygiene rules and also to constantly adhere to all preoperative, intraoperative, and postoperative interventions that could effectively prevent infection. However, policy makers in the United States are well aware of the costs of surgical infections, and they are going to make it very difficult for physicians and institutions that have, in the view of these policy makers, unacceptable outcomes. Consequently, it is necessary that orthopaedic surgeons and the allied infection specialist physicians do not adopt a defensive posture but rather engage local and national health policy makers to adopt and institute a realistic and evidence-based system that will provide comprehensive care to all patients with musculoskeletal infections and not deprive high-risk patients of appropriate care.
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