InSight+

A 72-year-old man developed septic arthritis in a prosthetic shoulder after intra-articular injection of radiographic contrast. This is the first published case in which molecular techniques matched oral commensal organisms cultured from joint aspirate with oral flora from the proceduralist, who was not wearing a mask.

Clinical record

A 72-year-old man presented in 2011 with acute-on-chronic right shoulder pain. Bilateral shoulder replacements had been performed 8 years earlier for osteoarthritis, with no surgical complications.

In the 6 months before presentation, the patient experienced increasing pain and decreased range of movement of the right shoulder. Four days before presentation, a computed tomography (CT) arthrogram of the right shoulder was performed to look for glenoid osteolysis and assess the linear integrity of the shoulder prosthesis. Eight millilitres of radiographic contrast with bupivacaine were injected into the joint space. The proceduralist used an aseptic technique and skin preparation with 0.5% alcoholic chlorhexidine, but did not wear a mask. Within 24 hours, the shoulder pain dramatically worsened and the range of movement became severely impaired.

The patient had a history of hypertension, severe obstructive sleep apnoea, and paroxysmal atrial fibrillation. He was taking indapamide, perindopril and warfarin, and used nocturnal continuous positive airway pressure. In 1993, he had been treated with radiotherapy for prostate cancer and was taking finasteride.

On presentation, the patient was febrile (38.4°C). Clinical examination showed a warm, swollen right shoulder and pain on passive movement of the joint. The C-reactive protein level was elevated at 229 mg/L (reference interval, < 5 mg/L).

Ultrasound-guided aspiration of the joint recovered a highly inflammatory fluid with a white cell count of 174.6 × 109/L, and 1 + gram-positive cocci were identified. Arthroscopic washout was performed, and the patient was given intravenous flucloxacillin 2 g every 6 hours and benzylpenicillin 1.8 g every 6 hours.

Culture yielded light growth on the primary plates of Streptococcus mitis group 1 and scant Haemophilus parainfluenzae. The antibiotic dose was changed to intravenous benzylpenicillin 2.4 g every 6 hours with synergistic gentamicin 240 mg daily for the first 2 weeks. After 4 weeks of intravenous therapy, the patient was switched to oral amoxicillin 1 g three times daily to complete a 3-month course of antibiotics.

Shortly after the patient presented, the proceduralist agreed to provide an oropharyngeal swab. Several organisms were cultured, including multiple viridans Streptococcus species. Pulsed-field gel electrophoresis (PFGE) was performed according to the method of Lefevre et al, with modifications.1 Using two different restriction enzymes (SmaI, ApaI), we found that the patient’s organism and a strain of S. mitis recovered from the proceduralist’s throat showed indistinguishable fragment patterns (Box). This strongly suggested droplet transmission of the proceduralist’s oral flora onto the needle or skin, with subsequent inoculation into the shoulder joint.

Six months after the acute presentation, joint failure, confirmed on arthrogram and by arthroscopy, necessitated full revision of the right shoulder prosthesis. The procedure was uncomplicated, and the patient remains well with no signs of recurrent infection.

Discussion

This is the first published instance of a molecular epidemiology technique showing probable transmission of oral flora from a proceduralist to the joint of a patient, resulting in iatrogenic septic arthritis.

Australian Medicare data for the period 2006–2009 show that an average of 516 562 claims were made annually for joint injections or aspirations.2 The estimated incidence of septic arthritis after intra-articular corticosteroid injection into a native joint is estimated to be between 1 per 3000 and 1 per 16 000 injections.3 Applying these incidence rates to Australian data, we would estimate that between 30 and 180 instances of iatrogenic septic arthritis per year are a result of joint injection or aspiration. It could be safely assumed that even fewer of these could be attributed to omission of a surgical mask. Given this apparently low burden of disease, should a surgical mask be a mandatory requirement of an aseptic technique for this procedure?

Infection control practices during the injection of sterile sites vary substantially across specialties and depend on the type of procedure and where it is performed (general practice, wards, operating theatres). Several studies confirm the anecdotal evidence that mask-wearing while injecting into sterile sites is not standard practice across a number of specialties, including rheumatology,4 obstetric anaesthesia5 and general practice.6 In some series, the rate is as low as 11%, and a debate exists in the surgical literature about whether surgical masks should be used at all in operating theatres.6

However, there is good microbiological evidence that oral bacterial flora, of which oral (viridans) streptococci predominate, can be deposited on an agar plate held at 30 cm from a speaking subject’s mouth for a period of 5 minutes.7 Thus, if a mask is omitted, procedures such as spinal anaesthesia, or any teaching procedure that can involve speaking to the patient or observers, may result in increased risk of contamination of the sterile field.

In the context of iatrogenic septic arthritis, viridans streptococci are infrequently identified as pathogens.8 They are regarded as low virulence organisms and are often dismissed as contaminants when recovered from joint aspirates. This may lead to an underestimation of their significance as pathogens in this context.

However, viridans streptococci have been implicated in other settings as nosocomial pathogens, most spectacularly with bacterial meningitis after spinal anaesthesia or myelography. A review of 179 cases of iatrogenic meningitis provides corroborative evidence that low virulence organisms can be dispersed from the oropharynx to sterile sites and cause infection.9 The evidence indicates that the risk of meningitis is far higher when there is inoculation into a sterile site (eg, spinal anaesthesia) than simple needle puncture of the site (eg, lumbar puncture). Similarly, the risk of iatrogenic septic arthritis is likely to be greater with inoculation than aspiration alone. That a low virulence organism can cause such morbidity, and occasionally death from meningitis, likely relates to the breach of usual host immune defences by direct inoculation into the site of infection. On rare occasions molecular confirmation of the source, using either PFGE or polymerase chain reaction, has been documented after recovery of identical organisms from the oropharynx of the proceduralist.10

It is always challenging to prove relatedness of bacterial strains, as typing techniques are often dependent on the specific bacterial species. PFGE has been shown to be a reliable technique for differentiating strains of S. mitis in other studies.11,12 In our case, the use of two different restriction endonucleases with identical results adds robustness to the data. While molecular methods can only ever prove two bacterial strains are different, there are established criteria for relatedness.13 The combination of our two pulsed-field gels satisfies the Tenover criteria for indistinguishable strains.

For most procedures, it is highly improbable that oral flora from the patient are the source of contamination, simply because of the physical configuration of the patient’s mouth relative to the sterile field. In addition, the microbiological similarity between iatrogenic septic arthritis and post-lumbar puncture meningitis (where contamination by the patient’s oral flora cannot reasonably be asserted) is compelling. Other sources of contamination from patients, such as skin flora or groin organisms, are unlikely given the preponderance of viridans streptococci and the striking absence of gram-negative bacilli and Staphylococcus species. We did not feel it necessary to take a mouth swab from the patient in this case.

Although no reports to date have been able to link a proceduralist’s oral flora to the causative pathogen in nosocomial septic arthritis, we consider the transmission of an oral Streptococcus species to a sterile joint space as analogous to the demonstration of identical organisms in iatrogenic meningitis.

Some authors have suggested that the efficacy of surgical masks is unproven, and that viridans streptococci may be introduced in ways other than direct contamination from the oropharynx.14 In particular, it has been suggested that transmission could be explained by more general deficiencies in aseptic technique, including contamination of the equipment during set-up or improper skin sterilisation. However, the compelling evidence that oral commensal bacteria can be aerosolised, and molecular confirmation of the source in several cases, including our own, would suggest that a surgical mask serves a role in aseptic technique.

Based on this case, we would recommend that clinicians seek a history of recent joint intervention in circumstances in which viridans streptococci are isolated from joint culture, particularly when the organism grows from the direct inoculum as well as the enrichment medium. We consider a surgical mask to be a low-cost, simple addition to the aseptic technique that may assist in prevention of nosocomial septic arthritis.

Pulsed-field gel electrophoresis dendrogram: Streptococcus mitis isolates from the patient’s joint fluid (Lane 1), and the proceduralist’s oropharynx (Lane 2 and Lane 3), showing an indistinguishable restriction fragment pattern. The lanes below are other oral Streptococcus isolates from the proceduralist along with control organisms

Distinguishing medical conditions from artists’ stylistic embellishments can contribute to our historical understanding of diseases like arthritis

When visiting art galleries, one often sees abnormal anatomical features depicted in paintings and sculptures. In the recent Brisbane exhibition of works from the Prado museum in Spain, viewers could find instances of medical conditions in the works of several artists — for example, dwarfism (Velasquez) and club-foot (Ribera), as well as mandibular abnormalities in Hapsburg family members (Titian).1 Here, we report that we have observed what we argue to be pathological changes, albeit subtle ones, depicted in the hands of two portrait subjects in the Art Gallery of New South Wales.

Portrait 1: Cosimo I de’ Medici in armour

Cosimo I de’ Medici (1519–1574), Duke of Florence from 1537 and Grand Duke of Tuscany from 1569, was painted in about 1545 by his court artist Agnolo Bronzino (1503–1572), a master of the late Renaissance mannerist style.2,3 This painting is an official portrait, of which many copies were made by Bronzino’s workshop. Cosimo, young and determined, in armour, like a warrior, is shown with his right hand situated prominently in the foreground, resting on his helmet.

Agnolo Bronzino (1503–1572). Cosimo I de’ Medici in armour, c. 1545. Oil on poplar, 86.0 × 67.0 cm. Art Gallery of New South Wales. Art Gallery of NSW Foundation Purchase 1996. Photo © Art Gallery of NSW. (Reproduced by permission of the Art Gallery of NSW.)

The fingers of the right hand in this portrait present certain deformities that are also seen in the left hand of three other portraits of the duke, one by Bronzino and two by his older contemporary Jacopo Pontormo (1494–1557).4 The metacarpophalangeal (MP) joints are depressed and dorsiflexed, the proximal interphalangeal (PIP) joints of the four fingers are swollen and flexed, and the distal interphalangeal joints appear to be somewhat extended. This is not a natural position for the fingers, and it would be very painful for someone with normal hands to hold the finger joints in this position voluntarily for any length of time (as would be required when sitting for a portrait).

This particular representation of the joints of the fingers is not found in Bronzino’s or Pontormo’s portraits of other individuals, so we conclude that it is not a stylistic preference on any of these artists’ part but the representation of a condition existing in the subject.

By contrast, although one can also see that the two middle fingers of Cosimo’s hand in Bronzino’s portrait are pressed together as they would be in syndactyly, this feature is so commonly found in the paintings of the period — both by Bronzino (for example, in his 1543 portrait of Cosimo’s wife Eleonora of Toledo [1522–1562], National Gallery in Prague, http://www.wga.hu/html/b/bronzino/1/eleonorb.html) and by many other artists — that we must regard it as a matter of artistic style rather than pathological abnormality.5

Throughout the three centuries of the Medici family’s predominance in Florence (from the mid 15th to the mid 18th centuries), many of its members suffered joint ailments. The evidence suggests a complex hereditary condition that affected both the senior line of the family and also the cadet line from which Cosimo was descended.4,6,7

Cosimo was reported to have suffered from disabling joint problems throughout his middle and later years, and further information was gained about these problems when his pathology was recently investigated in the exhumed skeleton. X-rays showed no evidence of gout, which was the premodern explanation of Medici joint pathologies, but they identified a number of arthritic and other pathological changes in the spine and leg bones. The hand had a localised erosion of the joint only at the PIP joint level, which indicates a specific pathology and not accidental damage due to the ravages of time.4 This erosion corresponds to the swollen PIP joints in Cosimo’s portrait.

Portrait 2: Portrait of an officer

Portrait of an officer, by the French rococo artist Nicolas de Largillière (1656–1746), probably completed by 1715, shows a young man of around 20 years of age dressed in military attire. The figure wears an elegant lace cravat and cuffs, a high powdered wig and an armoured breastplate. The work was initially considered to be a portrait of John Churchill, 1st Duke of Marlborough (1650–1722); however, this suggestion has not been confirmed and the identity of the figure remains unknown.8

On visual inspection, two anatomical anomalies are obvious — red cheeks and swollen knuckles. We can draw no conclusion concerning the red cheeks, which are common in Largillière’s portraits of both men and women. They may indicate an ongoing pathological condition such as lupus or a temporary one such as fever. Equally, they may have been caused by an overheated room in which the subject posed for his portrait or by the use of cosmetics (which was fashionable among upper class men and women at the time). Or they may be the result of the artist’s stylistic embellishment of the sitter’s complexion.

More significant, however, are the swollen knuckles — namely, the MP joints in both hands — not subluxated, but inflamed and reddish. Largillière is considered by art historians to have had a “genius for depicting hands”,9
so the accuracy of his representation on this point is highly probable. His other works show men’s hands both with normal joints and with swellings in other joints apart from the MP joints,8 from which we conclude that the swollen MP joints in Portrait of an officer are not a regular stylistic feature of Largillière’s male portraits but a naturalistic representation.

Any diagnosis proposed on the basis of the limited information available would have to be highly tentative. However, if one treats the redness of the officer’s face as a non-pathological feature, as we have argued, then a possible diagnosis in the context of swollen but undeformed fingers could be rheumatic fever or juvenile rheumatoid arthritis.

Discussion

We argue that these two portraits in the Art Gallery of NSW, from different epochs of European art, reliably depict certain rheumatic diseases in young men.

When investigating apparent pathological conditions
in old master paintings, one must always be conscious
of the fact that artists’ representations are not clinical photographs. The artist may exaggerate or tone down different aspects of the sitter’s anatomical features, or even depict wholly imaginary features that the person does not have.10,11 As we have done here, it is always necessary
to look for evidence that will assist the investigator in distinguishing between features that are likely to be naturalistic representations of what the artist saw, and those that are likely to be stylistic embellishments added for aesthetic effect.

This requires investigation of such factors as the medical history of the period concerned, the characteristic features of the artist’s style, the biography of the sitter (if his or her identity is known) and the history of the artwork itself (especially the circumstances and purpose of its origin).

Deciphering the content of artworks is a specialised discipline, which art historians have cultivated since the 16th century. However, we believe this decoding system would not be complete without taking account of the medical conditions that were at times represented, intentionally or inadvertently, in the people shown in paintings or statues.

When relevant information is available and caution is exercised in the research, the results of this analysis can add much to our historical understanding of the occurrence and appearance of diseases in earlier times.

Nicolas de Largillière (1656–1746). Portrait of an officer, c. 1714–1715. Oil on canvas, 65.7 x 54.2 cm. Art Gallery of New South Wales. Gift of James Fairfax AO 1995. Photo © Art Gallery of NSW. (Reproduced by permission of the Art Gallery of NSW.)

Preference: Rheumatology

The doctor and the mask: iatrogenic septic arthritis caused by Streptoccocus mitis

Medicine on the walls of the art gallery