The Preferred Treatment of Sternoclavicular Joint Infections: A Systematic Review

The treatment of sternoclavicular joint infection is a topic of controversy. This systematic review aims to evaluate the preferred treatment of sternoclavicular joint infections. A literature search using PubMed/MEDLINE®/Embase databases was conducted to identify publications on the surgical management of sternoclavicular joint infections. Case reports and studies without surgical management were excluded. The outcomes of interest included patient demographics, comorbidities, infectious etiologies, radiographic features, surgical management, and complications. Sixteen articles met the inclusion criteria. The mean age of the subjects was 53.4 years; there was a predominance of males (65%), and a minority of the subjects were obese (15%). The most common infectious etiology was methicillin-susceptible Staphylococcus aureus (MSSA) (48%). CT scan was reported in 46% of cases. The most common treatment was surgical resection of the joints (85%), followed by muscle flap closure of the wounds (54.2%). The complication rate ranged from 0-40%. Specifically, recurrence of infection was low with resection of the joint, followed by muscle flap closure. Given the heterogeneity of the methodology and inconsistency in the outcomes, a meta-analysis could not be performed. Overall, the current literature favors the resection of the sternoclavicular joint as the gold standard treatment. Closure of the wound using muscle flap seems to adequately treat this problem without any major untoward events.


Introduction And Background
Sternoclavicular joint infection is a rare disease. The true incidence rate of the condition is unknown, and it has an estimated prevalence of less than 1% [1,2]. The management of sternoclavicular joint infection, for the most part, remains controversial. The management ranges from nonoperative methods with intravenous antibiotics to invasive surgical interventions. Also, there is a wide variation in the surgical treatment options (i.e., ranging from incision and drainage, debridement and curettage, to radical resection of the sternal clavicular joint) [3,4]. Furthermore, following resection of the sternoclavicular joint, there are many different reconstructive options, ranging from primary closure to different types of muscle flaps [1,5,6]. Given the rare nature of the disease, studies have been limited to individual case series.
The aim of this systematic review was to identify the quality of the available literature regarding surgical management of this disease and to examine the patient demographics, comorbidities, symptoms, radiographic features, surgical treatment options, and outcomes associated with it.

Literature Search
A literature search using PubMed/MEDLINE®/Embase databases was conducted to identify publications regarding surgical management of sternoclavicular joint infections. The literature search was performed using appropriate keywords in English: "surgery," "treatment," "surgical intervention," "sternoclavicular joint infection," and "sternoclavicular joint septic arthritis."

Study Selection
We performed this systematic literature review according to the Preferred Reporting Items for Systematic reviews and Meta-analyses (PRISMA) statement guidelines [7]. Studies were selected for inclusion based on the following criteria: (1) the study reported surgical management of sternoclavicular joint infection; and (2) the studies were original studies. Studies were excluded if they: (1) did not involve surgical management of sternoclavicular joint infections; (2) were single case reports; (3) were written in a foreign language; and (4) were not available as full-length texts [8,9].

Data Extraction
Abstracts found using the aforementioned search terms were screened for eligibility by two independent reviewers. If consensus could not be reached, a third reviewer was asked to adjudicate. Full transcripts of the selected studies were then critically assessed for patient characteristics and clinical endpoints. Data extracted included study year, sample size, study design, patient characteristics, demographics, comorbidities, clinical data, radiographic data, microbiology, surgical management, and the complications associated with surgical management.

Outcome Measures
Outcomes measures of interest were overall complications, recurrence of osteomyelitis, mortality, hospital length of stay, and follow-up duration.

Assessment of the Level of Evidence
We used the Jovell and Navarro-Rubio classification to characterize the quality, quantity, and consistency of the studies, as shown in Table 1 [10]. We used this taxonomy to determine the quality of the level of evidence in order to assess the strength of the recommendation.

Level
Strength of evidence

Assessment of Methodological Quality
Two independent reviewers assessed the methodological quality of each study using the Coleman methodology score system, as shown in Table 2 [11].
Components of the Coleman score (maximum score)

Assessment of Meta-Analysis
Given the small number of available studies with small individual sample sizes, we did not think performing a meta-analysis was feasible. This was further reinforced by the wide heterogeneity of surgical treatments, unclear description of surgical procedures, and inconsistency in reporting complications.

Flowsheet Illustrating the Study Selection Process
Our electronic database search identified a total of 113 articles without duplicates. We removed two records as the publications were not peer-reviewed, and 111 titles and abstracts were screened. Of these articles, 95 full-text articles were excluded after assessing for eligibility, and 16 met the inclusion criteria for a systematic review, as shown in Figure 2.

Study Characteristics
We included a total of 16 studies pertaining to the surgical management of sternoclavicular joint infections ( Tables 3, 4). The sum aggregate of sample size was 264 patients, with a range of 5-50. All of these studies were retrospective. Only one study, by Ali et al., was statistically powered given its largest sample size among all and would qualify for level VI evidence [1]. The rest were all descriptive studies and would qualify for level VIII evidence. We did not include individual case reports. The Coleman methodology scores ranged from 5-42. The diagnosis was certain in all studies. The description of surgical procedures was not clear enough in 13 of the 16 studies to distinguish between incision and drainage, debridement and curettage, and formal resection of the joint. The description of postoperative rehabilitation was also not clearly stated in any of the studies.   5 until they appear healthy, is indicated. Small wounds can be allowed to heal by secondary intention. Larger wounds may require the involvement of the plastic surgeon to advance an ipsilateral pectoralis major muscle flap

Patient Characteristics
We calculated cumulative means and percentages based on the available data, as shown in Table 5. The total number of patients reported in these studies was 264. The mean age of the patients was 53.4 years; they were predominantly male (65%), and a minority was obese (BMI >30, 15%). The most common symptoms were pain, swelling, and fever (57%, 46%, and 19%, respectively). The most common comorbidities were diabetes mellitus, intravenous drug use, hypertension, and renal insufficiency (33%, 15%, 11%, and 6%, respectively). The most common diagnostic imaging was a CT scan with 46% reported. The most common organism on final wound cultures was methicillin-susceptible staphylococcus aureus (MSSA) (48%).

Preferred Treatment
There was considerable variation in surgical treatment in the available studies. However, resection of the entire sternoclavicular joint was the most commonly performed procedure (85% of the time) compared to debridement (9.7%) and incision and drainage (5.2%). Within the surgical management articles, there was a minority of patients who were treated with intravenous antibiotics alone (4.5%). We ranked studies according to their Coleman methodology scores, as shown in Figure 3. Apart from one study, most others appeared to recommend surgical resection of the entire sternoclavicular joint over antibiotic therapy alone [4].

Outcomes
Overall complications had a wide range of reporting, and five studies did not specify 30-day complications versus long-term complications. Additionally, two studies did not specifically clarify whether the mortality was related to sternoclavicular joint infection, related conditions, or remote unrelated causes. Overall, complication rates varied from 0% ( [13].

Literature Quality and Risk of Bias
The majority of the reports did not provide high-quality evidence. The relatively small sample sizes and inconsistency in reporting of outcome measures rendered the studies not feasible for a meta-analysis.

Discussion
Infections of the sternoclavicular joint are rare, representing 0.5% of all joint infections seen, and the true incidence is unknown [1]. This is a separate clinical entity from sternomanubrial joint infections and/or post-sternotomy osteomyelitis following cardiac surgery procedures [2,3]. Many risk factors have previously been described, including intravenous drug use, diabetes mellitus, obesity, and renal failure [1,[3][4][5][6]. In our review, we found that the clinical presentation varies greatly, often leading to a delay in diagnosis and resulting in a progression of the infection into deeper structures. If not identified early, patients will inevitably require surgical intervention in order to effectively treat and eradicate the infection. In this systematic review, we aimed to identify the demographics, initial presentation, and diagnostic workup of this condition, as well as compare different treatment modalities and the complications associated with them. After screening all articles related to sternoclavicular joint infections, we extensively reviewed 16 peer-reviewed full-text original studies that met the inclusion criteria.
Initial patient presentations varied, considering the etiology of the infection, and morbidities. In general, however, the majority of patients presented with pain, swelling, or fever, though this was not a universal finding. Although a clinical diagnosis never seems to be an issue, results from bacterial cultures vary, and oftentimes there is no organism found in the final culture results. The most common organism that cultures did yield was MSSA, followed by methicillin-resistant Staphylococcus aureus (MRSA), Streptococcus species, and Pseudomonas aeruginosa. Consistent with the standard of care for osteomyelitis in other sites of the body, all the studies in this review reported the initial treatment plan including a total of four to six weeks of intravenous antibiotics regardless of the isolation of an organism on the final wound cultures [1,5,6].
Based on this review, it appears that the gold standard for the treatment of sternoclavicular joint infection should be surgical resection of the entire joint. This has been most widely adopted with the most favorable outcomes. Resection of the joint in addition to intravenous antibiotics eliminates the disease process effectively and expeditiously, as favored by the stronger studies in on this topic [1,3,[12][13][14][15][16]18,19,22]. There was only one study where minimal debridement was compared with intravenous antibiotics alone and no resection of the joint at all. However, the study concluded that resection should be performed if there are neck and chest wall abscess [4].
The closure of the wound after resection of the sternoclavicular joint infection seems to favor using myocutaneous flaps, as evidenced by the stronger studies [1,5,6,22]. The use of myocutaneous flap can help obliterate the dead space resulting from resection of the sternoclavicular joint. By virtue of vascularized tissue, it can help clear the infection, which presumably translates into the promotion of healing and recovery. There was only one powered study that compared myocutaneous flap coverage to that of wound vacuum therapy. This paper demonstrated that myocutaneous flap closure was statistically superior to vacuum therapy alone [1].
Limitations to this review include our inability to include articles in foreign languages. Additionally, we point out our difficulty in performing a standard meta-analysis. Meta-analysis requires a quantitative integration of evidence from a number of related studies. For a rare disease such as sternoclavicular joint infections, the literature is limited to small series, and the data is often inconclusive. Hence, pooling the data adds strength to the study to help identify the best surgical management and complications associated with it. Unfortunately, the heterogeneity of the methodologies and inconsistency of outcome reporting we found in the literature precluded a formal standard meta-analysis.
This study does, however, provide a comprehensive review of the surgical management of this rare disease and provides a holistic picture of the current state of the literature, examines the quality of evidence, and leads towards a weighted conclusion Additional citation pertaining to tables 1 and 2 (see correction notice): [23].

Conclusions
The current literature favors resection of the entire sternoclavicular joint as the gold standard treatment in sternocleidomastoid joint infections. Furthermore, the authors conclude from this review that closure of the wound using muscle flap has been associated with the most favorable of outcomes, with the least amount of recurrent osteomyelitis and a reasonable flap-related complication rate.

Conflicts of interest:
In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.