What Do We Know About Shoulder Injury Related to Vaccine Administration? An Updated Systematic Review : Clinical Orthopaedics and Related Research®

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What Do We Know About Shoulder Injury Related to Vaccine Administration? An Updated Systematic Review

MacMahon, Aoife MD1; Nayar, Suresh K. MD1; Srikumaran, Uma MD, MBA, MPH1

Author Information
Clinical Orthopaedics and Related Research 480(7):p 1241-1250, July 2022. | DOI: 10.1097/CORR.0000000000002181
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Abstract

Introduction

Vaccinations are frequently administered into the deltoid muscle, which lies close to the subacromial bursa (sometimes referred to as the subdeltoid bursa in nonorthopaedic studies), tendons, and underlying humeral bone. Although local reactions, including pain of varying severity, swelling, erythema, inflammation, and induration, may occur after intramuscular vaccination through the deltoid, they are usually transient [7]. Bodor and Montavlo [5] were the first to posit that in two patients with shoulder pain and dysfunction, intramuscular deltoid vaccination may have been related to the vaccination itself. Later, in 2010, Atanasoff et al. [2] termed this correlation shoulder injury related to vaccine administration (SIRVA), which the authors defined as shoulder pain and limited ROM beginning within 48 hours of the administration of a vaccine intended for intramuscular administration in the upper arm and lasting more than 6 months, distinguishing the entity from the typical pain, soreness, and limited motion that most individuals experience transiently after vaccination [2, 7]. The term SIRVA will be used throughout this review article for the sake of simplicity—although it remains unproven and very controversial—because many studies on this topic have used this term. Although the suggestion that SIRVA is an immune-mediated inflammatory response to an antigen injected into or near the bursae or synovium has not been experimentally proven [7], one study found that inflammatory soft tissue damage and bone erosions in participants with SIRVA were associated with peripheral T- and B-cell activation and extracellular matrix-reactive autoantibodies [23].

The controversy over whether SIRVA is a distinct clinical entity has played out in the conflicting opinions of a number of leading national organizations. In 2011, the National Academy of Medicine’s committee on the adverse effects of vaccines stated that “the evidence convincingly supports a causal relationship between the injection of a vaccine and deltoid bursitis” [24]. Conversely, the American Academy of Orthopaedic Surgeons (AAOS) published a position statement in 2017, subsequently updated in 2020, stating that “vaccination administered to the shoulder is unlikely to cause or contribute to common shoulder pathologies such as rotator cuff tendinopathy and glenohumeral arthritis” [1], and concluded that there is no scientific evidence that vaccine administration can injure the shoulder. The AAOS statement astutely notes that the potential harms of promoting an uncertain disease entity of this kind may contribute to vaccine hesitancy. However, there also are risks to dismissing patients’ experiences. This can adversely affect clinical care and trust, both of which carry public health ramifications, particularly if potential harms—even rare ones—are not disclosed to patients. This may lead to vaccine hesitancy if the public believes risks were hidden by the medical community or pharmaceutical industry.

The AAOS concedes, “Position statements are developed as educational tools based on the opinions of the authors. They are not a product of systematic review” [1]. Since these statements, the National Academy of Medicine and AAOS have not had the benefit of recently published Level III studies with higher quality scores. Nevertheless, the AAOS acknowledged in its more recent statement that, “It is possible there may be a rare, vaccine-specific, severe pathology related to injection into the subacromial bursa and glenohumeral joint” and that “Surgeons can validate a patient’s experience of pain after vaccination without validating the concept that vaccine causes common chronic shoulder pathology” [1].

Studies related to SIRVA are limited and primarily consist of case reports and case series, but the number and quality have increased recently. Although this topic has been reviewed [7], three Level III studies [18, 20, 23] (currently the highest level of evidence available to date on the topic of SIRVA) have since been published. One of these is a population-based cohort study that substantially expands the size and scope of prior studies [20], as recommended by a commentary on the subject [44], and provides the most robust incidence report of SIRVA to date. With increasing rates of vaccination for coronavirus-19 (COVID-19), it is important to better understand the characteristics of this potential injury and strategies for prevention, and to dispel associated misconceptions.

In this systematic review, we therefore asked: What are the (1) clinical characteristics, (2) diagnoses, and (3) management approaches and outcomes reported in association with SIRVA?

Materials and Methods

Search Methods

A search was conducted on October 4, 2021, using the PubMed and Medline databases and the Cochrane Database for Systematic Reviews without year restriction. The search terms and Boolean operators were “SIRVA” OR “shoulder injury related to vaccine administration” OR “shoulder” AND “vaccine” AND “injury.” Duplicate studies were excluded.

Study Selection and Data Extraction

All potential studies were independently reviewed by two authors (SKN and AM). Any differences in opinion were resolved via discussion with the third author (US), if necessary. The references of studies from the initial search were scanned for additional relevant studies.

Inclusion criteria were English-language comparative studies, case series, and case reports that involved shoulder pain occurring within 48 hours of vaccination. Studies that reported neurologic deficits after vaccination, including peripheral nerve injuries, were excluded because we do not believe this pattern is consistent with typically described SIRVA. Study quality was assessed for database case series and retrospective comparative studies using the Methodological Index for Non-randomized Studies tool [42]. Noncomparative studies were assessed in eight domains with a highest possible score of 16, and comparative studies were assessed in 12 domains with a highest possible score of 24 [42]. For noncomparative studies, quality was considered high for scores 12 and greater, moderate for scores greater than or equal to 4 and less than 12, and low for scores less than or equal to 4. Similarly, for comparative studies, quality was considered high for scores 16 and greater, moderate for scores greater than or equal to 8 and less than 16, and low for scores less than 8. General data from each article were extracted (authors, publication year, study period and location, and data source). Variables of interest included demographics (age, gender, and BMI); vaccine; injection site; onset of symptoms, signs, and symptoms; imaging modalities and findings; diagnosis; management; follow-up time; and clinical course and outcome in patients experiencing SIRVA. The occupation or specialty of the individual who reported the findings in each study, that is, the senior author, was also recorded (such as orthopaedic surgeon, general practitioner, or other specialty).

Search Results

The initial search yielded 35 unique studies. Three duplicate studies found in both PubMed/Medline and Cochrane were filtered. Three of these 35 studies were excluded after a review of the title and abstract and three were excluded after full-text review for nonrelevancy to the discussed topic. A review of the references of the remaining 29 studies resulted in 13 additional studies (Fig. 1). In total, 42 studies were included.

F1
Fig. 1:
This flow diagram shows the study selection for this systematic review.

Study Characteristics

There were three retrospective comparative studies (72 patients and 105 controls) (Table 1) [18, 20, 23], five database case series (2273 patients) (Table 1) [2, 19, 22, 31, 41], and 34 case reports (49 patients) (Supplementary Table 1; https://links.lww.com/CORR/A764). Among the five database case series (defined as database studies that describe patients who may have SIRVA without comparing them with controls, in contrast to comparative database studies) included in this review, the Vaccine Adverse Event Reporting System database yielded the highest number of patients with SIRVA (1220 patients from 2010 to 2017) (Table 1) [22]. All patients received the influenza vaccine in the database case series and retrospective comparative studies. Among database case series, reporters of study results included an employee of the Vaccine Injury Compensation Program [2], a pharmacologist [31], general preventive medicine physicians [22, 41], and an epidemiologist [19]. Among retrospective comparative studies, reporters included a public health physician [20], an orthopaedic surgeon [18], and an immunologist [23]. Among case reports, 14 were reported by orthopaedic surgeons [6, 10, 14-17, 21, 26, 33, 37, 38, 47, 49, 50]; four by radiologists [8, 29, 36, 51]; three by physical medicine and rehabilitation medicine physicians [5, 27, 35]; two each by occupational and preventive health physicians [4, 40], allergists [30, 45], and internists [13, 25]; and one each by a primary care and sports medicine physician [39], general practitioner [12], primary care physician [48], family medicine physician [3], emergency medicine physician [32], combined physiatrist and neurologist [46], and pharmacist [43] (Supplementary Table 2; https://links.lww.com/CORR/A765).

Table 1. - Characteristics of database case series and retrospective comparative studies
Study Reporter Study period Location Data source Inclusion criteria Number of patients
Database case series
Atanasoff et al. [2] Employee of the United States Department of Health and Human Services National Vaccine Injury Compensation Program 2006 to 2010 United States Vaccine Injury Compensation Program administrative claims database Claimed injury: shoulder pain, arm pain, shoulder dysfunction, frozen shoulder, adhesive capsulitis, or shoulder bursitis 13
Martín Arias et al. [31] Pharmacologist 1982 to 2015 Spain Adverse Reaction Data of the Spanish Pharmacovigilance System database Adverse reaction coded in the Medical Dictionary for Regulatory Activities as HLGT-synovial and bursal disorders OR tendon, ligament, and cartilage disorders with suspected vaccine involvement 8
Shimabukuro [41] General preventive medicine physician 2010 to 2016 United States Vaccine Adverse Event Reporting System database Reports submitted to the Vaccine Adverse Event Reporting System of shoulder dysfunction after inactivated influenza vaccine, onset < 48 hours, symptoms lasting > 1 week 1006
Hibbs et al. [22] General preventive medicine physician 2010 to 2017 United States Vaccine Adverse Event Reporting System database Reports of atypical shoulder pain and dysfunction < 48 hours after vaccination continuing for > 7 days 1220
Hesse et al. [19] Epidemiologist 2010 to 2016 United States Vaccine Injury Compensation Program administrative claims database Petitions for the following alleged injuries: SIRVA, arm pain, shoulder pain, bursitis, rotator cuff tendonitis, and adhesive capsulitis 476
Retrospective cohort studies
Hesse et al. [20] Public health physician 2016 to 2017 United States Vaccine Safety Datalink ICD-10-CM diagnosis of shoulder bursitis 0-2 days postvaccination (risk interval) or 30-60 days postvaccination (control interval) Risk interval: 16
Control interval: 51
Gonzalez et al. [18] Orthopaedic surgeon 2009 to 2018 Austin, TX, USA Students and faculty receiving influenza vaccinations at a single-center university health service Shoulder problems diagnosed within 3 months before or 3 months after influenza vaccination by ICD-9 codes Pre-vaccination: 52
Post-vaccination: 40
Hirsiger et al. [23] Immunologist 2017 Basel, Switzerland A single work-related influenza immunization campaign Suspected SIRVA Cohort: 16
Controls: 14

Study Quality

The overall study quality was low because most of the included studies were case reports. However, each of the five noncomparative database case series [2, 19, 22, 31, 41] fulfilled five of the eight Methodological Index for Non-randomized Studies items (10/16 score), resulting in a moderate-quality rating (Table 2) [2, 19, 22, 31, 41]. The comparative studies by Hesse et al. [20] and Hirsiger et al [23] scored 20 of 24 and 18 of 24 respectively, indicating a high level of quality, while the study by Gonzalez et al. [18] scored 15 of 24, indicating a moderate level of quality.

Table 2. - MINORS scores for database case series and retrospective comparative studiesa
Study Clearly stated aim Inclusion of consecutive patients Prospective data collection Endpoints appropriate to study aim Unbiased assessment of study endpoint Follow-up period appropriate to study aim < 5% loss to follow-up Prospective study size calculation Adequate control group Contemporary groups Baseline equivalence of groups Adequate study analyses Score
Database case series
Atanasoff et al. [2] 2 2 0 2 0 2 2 0 10/16
Martín Arias et al. [31] 2 2 0 2 0 2 2 0 10/16
Shimabukuro [41] 2 2 0 2 0 2 2 0 10/16
Hibbs et al [22] 2 2 0 2 0 2 2 0 10/16
Hesse et al. [19] 2 2 0 2 0 2 2 0 10/16
Retrospective comparative studies
Hesse et al. [20] 2 2 0 2 0 2 2 2 2 2 2 2 20/24
Gonzalez et al. [18] 2 2 0 2 0 2 2 0 1 2 0 2 15/24
Hirsiger et al. [23] 2 2 2 2 0 2 2 0 1 2 1 2 18/24
aItems are scored 0 (not reported), 1 (reported but inadequate), or 2 (reported and adequate). The highest possible score (representing highest study quality) is 16 for non-comparative studies and 24 for comparative studies.

Results

Clinical Characteristics

Among case series and retrospective comparative studies, the mean age of patients with SIRVA ranged from 21 years (range 20-26 years) [18] to 56 years (range 38-83 years) [31], and the proportion of women ranged from five of eight [31] to 11 of 13 [2]. Among patients in the case reports, the median age was 51 years (range 15-90 years), and 73% (36 of 49) were women. In database case series and retrospective comparative studies, the mean BMI ranged from 21.3 kg/m2 (range 20-22.3 kg/m2) [23] to 28.1 kg/m2 (range 17.0-51.7 kg/m2) [19]. BMI was reported for 24% of patients (12 of 49) in case reports, with a median of 23.5 kg/m2 (range 21-37.2 kg/m2) [4, 15, 29, 36, 49].

Among database case series, the injection site was described by patients as “too high” by 17.7% (217 of 1770) [22] to 79.7% (177 of 222) [41]. Among comparative studies, the proportion of patients describing the injection site as “too high” ranged from one of 16 patients [20] to five of 16 patients [23]. Among case reports, the injection site was described as “too high” on the arm, shoulder, or deltoid muscle by 20% (10 of 49) [4, 5, 12, 21, 35, 40, 46] and from 1 cm to 3 cm or one to three fingerbreadths distal to the acromion in 20% (10 of 49) [3, 4, 6, 8, 10, 13, 29, 33, 38].

Among database case series and comparative studies, symptom onset was reported to have occurred within 24 hours in three of eight to 15 of 16 patients [23]. In case reports, symptom onset was reported to have occurred immediately in 29% of patients (14 of 49) [4, 12, 21, 25, 35, 36, 38-40, 45, 51], within 24 hours in 39% (19 of 49) [3, 4, 6, 8, 13, 15-17, 27, 29, 30, 32, 37, 43, 47-49], and after 24 hours in 18% (seven of 39) [4, 5, 10, 14, 33, 37, 46]. The most common signs and symptoms of SIRVA were shoulder pain and decreased shoulder ROM. Among case reports, all patients had shoulder pain, and 39% (19 of 49) had decreased shoulder ROM.

Only one study calculated the incidence of SIRVA [20]. The authors of that study compared the incidence of subdeltoid bursitis occurring within 2 days of an inactivated influenza vaccination compared with subdeltoid bursitis occurring within 30 to 60 days afterwards. They found an incidence ratio of 3.24 (95% confidence interval 1.85 to 5.68), occurring in 16 of 2,943,493 patients (0.0005%), and that the attributable risk was 7.78 (95% CI 2.19 to 13.38) additional cases of bursitis per 1 million persons vaccinated [20].

Diagnoses Associated with the Condition

Common diagnoses included shoulder bursitis, adhesive capsulitis, and rotator cuff tears. Among patients with reported diagnoses in case series, proportions of shoulder bursitis ranged from one of 11 [22] to three of eight [31], adhesive capsulitis from 5% (26 of 476) [19] to two of eight [31], and rotator cuff tears from 14% (66 of 476) [19] to two of eight [31]. Hesse et al. [20] assessed diagnoses of bursitis only. Among 16 patients reported by Hirsiger et al. [23], four had subdeltoid bursitis. Sixty-three percent (31 of 49) of patients in case reports had a diagnosis, including adhesive capsulitis in 32% (10 of 31) and bursitis in 32% (10 of 31).

Management and Outcomes

The management of SIRVA commonly included physical therapy, NSAIDs, steroid injections, and surgery. Among case series and comparative studies that described the management and outcomes of SIRVA, between six of 16 [23] and 80% (381 of 476) [19] of patients received physical or occupational therapy, 47% (254 of 546) [22] to six of 16 [23] received NSAIDs or non-narcotic analgesics, one of six [20] to eight of 13 [2] received steroid injections, and 3% (16 of 546) [22] to four of six [20] received surgery. Among the 49 patients in case reports, 65% (32 patients) received physical therapy, 49% (24 of 49) received NSAIDs or non-narcotic analgesics, 43% (21 of 49) received steroid injections, and 20% (10 of 49) received surgery. Database case series and comparative studies that reported surgery for SIRVA did not describe the type of surgery performed [2, 19, 20, 22, 41, 49]. The most common procedures performed for bursitis and adhesive capsulitis were irrigation and debridement, synovectomy, and bursectomy [13, 16-18, 21, 32, 47, 49]. Symptoms were reported to have resolved in 4.1% (50 of 1220) [22] to four of 13 [2] of patients in case series and in 59% of the patients in case reports (29 of 49).

Discussion

The concept of SIRVA is controversial and relatively new. The public health risks of promoting a poorly understood disease entity must be balanced with the risks associated with denying its existence. Much of the existing data are limited to low-quality case series, although newer higher-level studies are beginning to quantify the rarity of the condition (if it exists), better describe its common presentations, and speculate about possible molecular mechanisms [20, 23]. In this systematic review, we sought to update the reader with the best-available evidence and to reconcile conflicting viewpoints by bringing more-recent research to bear on an important topic. Given this new level of evidence as well as the substantial increase in new vaccinations related to the COVID-19 pandemic and their potential link to SIRVA [10], it is important for clinicians to understand strategies for preventing, diagnosing, and managing this poorly understood condition.

Limitations

Case reports and most case series are of low quality, and as such are limited in their ability to draw any firm conclusions (Table 2). Many of the study designs suffered from the same kinds of bias and methodologic shortcomings, some of which might make it seem more likely that vaccines were responsible for the symptoms reported by patients. Recall bias, secondary gain (some of these studies came from compensation databases, which may affect the reporting; it is possible that patients in those databases made statements suggesting greater symptom severity and denying or underreporting the benefits of treatments they received), the post hoc ergo propter hoc fallacy (the fact that a symptom occurs after an injection does not mean the injection caused the symptom), and inconsistency of diagnostic approaches, among others, can contribute to an overestimation of the presence of this condition. In addition, some of the diagnoses captured by these studies cannot plausibly be attributed to an injection, no matter how inaccurately placed; for example, the chronic conditions of arthritis and rotator cuff tendon tears cannot reasonably be directly attributed to a vaccine injection in the shoulder.

Although no study has been sufficiently robust to confirm causation, two newer Level III studies with higher-quality scores that used appropriate controls have suggested the rare association of inflammation of structures of the shoulder with vaccination [20, 23]. One recent study that collected some data prospectively, including blood serum samples, provided some evidence of the vaccine’s association with objective biologic markers [23]. We believe that the consistency of the reports worldwide, many from noncompensation databases, in conjunction with these new comparative studies, make a more-convincing case that SIRVA is likely a distinct pathologic entity, at least in some patients, although this has not been experimentally proven.

It is likely that some of the associated diagnoses noted in the case reports and case series are simply incidental findings on imaging studies or noted in the clinical record as part of the differential diagnosis. Moreover, many studies had limited follow-up periods, and much is left to learn about the duration of symptoms and their appropriate treatments. Finally, because there was wide variability in the diagnostic criteria for SIRVA and vaccinations in the evaluated studies, we were unable to pool data and perform a statistical analysis.

Discussion of Key Findings

SIRVA-related diagnoses are most appropriately defined as inflammation of the structures beneath the deltoid, including the bursae, tendon, and joint capsule or synovium. SIRVA should not be confused with the transient muscle soreness typical of vaccinations that commonly resolves within a few days or weeks. The likelihood of SIRVA is most consistent when a patient presents with early-onset shoulder pain (within 24-48 hours), often unrelenting or progressive in nature over an extended duration of weeks to months. By definition, other chronic conditions, such as arthritis and rotator cuff tears, cannot be caused by vaccines.

A recent study combining in vivo and in vitro investigation began to shed some light on the possible immune-mediated inflammatory mechanism initially postulated by Atanasoff eta al. [2]. Hirsiger et al. [23] studied 16 individuals with suspected SIRVA and compared them with controls from a single vaccination campaign from a clinical and experimental perspective. They noted that 12 of 16 patients (all young and previously healthy) had imaging findings consistent with tissue inflammation, including six patients with bone erosions not consistent with the erosions seen in arthrosis. This finding of bone erosions has been noted in other studies, some of which predate the concept of SIRVA [4, 16, 27, 29, 33, 38, 43] and perhaps represented incidental findings from imaging studies of patients suspected to have SIRVA. Hirsiger et al. [23], however, demonstrated that all patients with erosions had T-cell responses in blood serum samples targeting heparan sulfate proteoglycan and that T cells could activate osteoclasts via the RANK/RANK-L pathway. They additionally found via in vitro studies that a component of the vaccine, alpha-tocopheryl succinate, could also stimulate osteoclasts and result in bone toxicity. Although the work by Hirsiger et al. [23] suggests there may be a molecular mechanism for SIRVA and a potential blood marker for SIRVA as a disease entity, additional confirmatory trials are needed for definitive conclusions.

Most patients reported to have SIRVA are women, although this may be attributed to a higher proportion of women receiving the influenza vaccination [28]. The average BMIs ranged from normal weight to overweight, and the range of BMIs included patients who were underweight to patients with morbid obesity, suggesting no clear association of BMI with SIRVA. Although only one study was able to assess incidence, Hesse et al. [20] suggested in a comparative analysis that SIRVA is exceedingly rare, determining that the additional risk of bursitis over the baseline bursitis risk is an additional 7.78 patients with the condition for every 1 million vaccinated patients. These incidence calculations, in turn, can explain another Level III study that was unable to show a difference in the incidence of bursitis after vaccination, because it was grossly underpowered to detect such a rare condition [18]. Another limitation of the study by Gonzalez et al. [18] was that it did not distinguish between shoulder problems diagnosed in the immunized versus the nonimmunized shoulder.

SIRVA, if it exists, generally responds in a way that is consistent with typical shoulder bursitis: it frequently resolves with nonsurgical treatment. Providers should use this fact to reassure their patients. Although we do not completely understand the entity, nor how molecularly or mechanistically it might (or might not) be related to symptoms, we are confident that it is very rare and treatable in most patients who may have it. We also believe that easy-to-implement measures can help prevent shoulder injuries that might be attributed to intramuscular injections. Our focus can therefore remain on aggressively treating any symptoms of bursitis; some have suggested an early cortisone injection may be effective [30].

It is likely that the injection technique plays a role in SIRVA, if the elicitation of inflammation theory is correct, and if the condition exists. Many patients in the included studies described injections as too high on the shoulder, although this is subject to reporting bias. A 1-inch needle can feasibly penetrate the bursa and even reach the bone in some patients, leading to a local inflammatory and immune response [5, 11, 23].

The Centers for Disease Control Advisory Committee on Immunization Practices has issued guidelines on recommended needle lengths for injection into the deltoid muscle for men and women, stratified by weight [9]. Based on the position of the axillary nerve and subdeltoid and subacromial bursa, Cook [11] stated that vaccine injections should be administered greater than 7.4 cm below the mid-acromion in adults, midway between the acromion and the deltoid tuberosity. To identify this site, the patient’s hand should be placed on the ipsilateral hip with the arm abducted to 60°, which relaxes the deltoid muscle and improves recognition of the deltoid tuberosity, including in patients with obesity. The vaccinator then places his or her index finger on the acromion and the thumb on the deltoid tuberosity, and administers the injection midway between those anatomic landmarks. As orthopaedic surgeons, we can advocate for the appropriate education of our patients and healthcare practitioners on the safest injection techniques.

Our research community can continue to investigate the potential disease mechanism experimentally, although Level II or Level I studies are not likely to be performed because of ethical and practical concerns. Some work has suggested that alternate sites for injection, such as the mid-lateral aspect of the thigh, warrant further consideration to avoid structures such as the bursa or synovium altogether [9, 34]. This must be balanced against alternative sites that provide an equivalent immune response for disease protection.

Conclusion

Findings from our review suggest a rare association of some inflammatory conditions of the shoulder (such as bursitis) and vaccinations. Although other conditions were noted to be SIRVA [3, 16, 19, 22, 27, 29, 33, 38, 41, 43], they more likely represent incidental findings from imaging of chronic conditions than pathologic findings related to vaccination. It will be important for more studies to search for a causal link; the current evidence on this remains sparse and preliminary [23]. Fortunately, surgeons can reassure the small number of patients who may present with persistent shoulder pain after vaccinations that their symptoms are likely to abate with nonsurgical approaches. One preliminary study suggests [30], and we agree, that early subacromial corticosteroid injection may be worth considering. Only a small percentage of patients with SIRVA symptoms undergo surgical treatment. Following vaccine administration guidelines in selecting the correct needle length and identifying a safe injection site may help to further minimize the risk of SIRVA [9, 34], if it exists.

Acknowledgments

None.

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