Erythema Induratum Caused by Mycobacterium chelonei in an Immunocompetent Patient

Shannon M. Campbell, DO, FAOCD; Richard R. Winkelmann, MS-III; Dawn L. Sammons, DO, FAOCD

Dr. Campbell is from Department of Specialty Medicine, Ohio University Heritage College of Osteopathic Medicine, Athens, Ohio; Mr. Winkelmann is from Ohio University Heritage College of Osteopathic Medicine, Athens, Ohio; Dr. Sammons is from Division of Dermatology, The Ohio State University, Columbus, Ohio.

Disclosure: The authors report no relevant conflicts of interest.

Abstract
Erythema induratum is a disease characterized by nodules on the flexural surface of the lower legs strongly associated with Mycobacterium tuberculosis infection. In the presented case, erythema induratum was found in a middle-aged woman caused by an atypical mycobacterium, Mycobacterium chelonei, identified via culture. Mycobacterium chelonei is best known for its pathogenicity in immunocompromised hosts and has been reported secondary to traumatic implantation. However, the patient described in this case did not have any comorbidities associated with erythema induratum, had a negative purified protein derivative skin test, and was immunocompetent. Disease resolution was achieved with clarithromycin and doxycycline therapy.
(J Clin Aesthet Dermatol. 2013;6(5):38–40.)

A 64-year-old immunocompetent female presented with a seven-month history of recurrent erythematous papules and nodules on the back of her right lower leg (Figure 1). Physical examination revealed three 5 to 6mm inflamed, subcutaneous, violaceous nodules with a fine overlying scale on the posterior aspect of the right lower leg. Lesions were surrounded by several hyperpigmented macules at sites of previous lesions. She reported that the nodules were tender, nonpruritic, and, at times, had a clear exudate. The patient denied any trauma to the area and initially attributed the eruption to mosquito bites. Prior to her visit at the authors’ clinic, the patient had not sought any treatment. She denied any personal or family history of skin cancers, and her medical history was unremarkable without prior exposure to tuberculosis or recent travel out of the country.

A 4mm punch biopsy of the lesion to the level of the dermis taken from the right posterior lower leg revealed suppurative inflammation and foci of necrosis (Figure 2). Acid-fast staining demonstrated acid fast, beaded bacilli consistent with mycobacterial infection (Figure 3). Complete blood count and complete metabolic panel were normal. Chest x-ray showed no evidence of active or latent pulmonary tuberculosis and purified protein derivative (PPD) testing was negative. The patient’s hepatitis panel was normal with no evidence of prior infection. Erythema induratum (EI), secondary to an atypical mycobacterium, was the favored diagnosis. Another 3mm punch biopsy of the lesion from the right posterior lower leg was performed for tissue culture. The culture identified Mycobacterium chelonei as the pathogenic organism and therapy was initiated with 500mg clarithromycin twice daily and 100mg doxycycline twice daily. After four months of therapy, the nodules resolved and the only visible lesions were the areas healing from each biopsy.

Review
EI was first described in 1855 by Bazin prior to the identification of tuberculids.[1,2] Although initially associated with pulmonary tuberculosis, there has been much debate over the role of Mycobacterium tuberculosis in the pathogenesis of EI. In the early 1900s, Whitfield[3,4] and Galloway[5] distinguished cases of EI unrelated to Mycobacterium tuberculosis infection as a separate clinical entity from those associated with tuberculosis. Four decades later in 1945, Montgomery[6] proposed the term nodular vasculitis to describe cases of EI lacking evidence of tuberculin origin. The relationship of EI with Mycobacterium tuberculosis has since been solidified by isolation of mycobacterial deoxyribonucleic acid (DNA) from EI biopsies via polymerase chain reaction (PCR), yet most clinicians use the term EI and nodular vasculitis interchangeably regardless of etiology.[7] Today, cases of EI are most prevalent in populations with a higher incidence of tuberculosis.[8]

The clinical picture of EI is characterized by tender, violaceous nodules and plaques most commonly affecting the posterior lower legs of adolescent or perimenopausal women.[2,7] Lesions have a tendency to ulcerate and drain. Spontaneous resolution of lesions is common within a few months leaving areas of postinflammatory hyper-pigmentation and atrophic scarring.[8] EI runs a chronic, recurrent course in which lesions return every 3 to 4 months over the span of many years.8 Histopathological examination of EI demonstrates a predominant lobular panniculitis with granulomatous inflammation. A neutrophilic vasculitis is usually present and affects contiguous small and medium-sized vessels.[7,9,10] Necrosis of fat lobule adipocytes may also be present and occasionally form palisading granulomas.[8–10]

Despite the current support for the tuberculous origin of EI, many authors believe other etiopathogenic factors should be considered. Previous cases have reported an association of EI with infectious disorders caused by Nocardia, Pseudomonas, Fusarium, Hepatitis C, and Hepatitis B.[7] Several cases have also been linked to autoimmune disease and propylthiouracil therapy.[11] A recent study examined the possibility that atypical mycobacteria may cause EI, but failed to isolate atypical species from lesions via PCR.[12] Interestingly, the same study looked for DNA from 11 different atypical mycobacterial species, but did not test for the presence of Mycobacterium chelonei.

Mycobacterium chelonei is a rapidly growing atypical mycobacterium belonging to the Runyon group IV classification.[13] Although originally isolated from the sea turtle, Chelona corticata, Mycobacterium chelonei is found ubiquitously in the environment in soil, water, and dust particles.[14] Cultures between 25 and 40°C form nonpigmented colonies with either a rough or smooth surface.[15] Clinically, Mycobacterium chelonei is rare, but can cause disseminated disease in patients immunosuppressed by organ transplantation,[16] collagen vascular disease,[17] malignancy, or corticosteroid therapy.[18] Localized infection may occur due to implantation into the skin following surgery, injections, or trauma.[15] Following inoculation, it is likely Mycobacterium chelonei remains localized in these patients because their immune system is strong enough to mount a cell-mediated immune response against the bacterium. Treatment of Mycobacterium chelonei infection is challenging. In the few cases of Mycobacterium chelonei infection found in the literature, antimicrobial therapy was complicated due to the highly resistant nature of Mycobacterium chelonei to standard antibiotics.[13] Clarithromycin has been found to be effective against 100 percent of isolates in vitro,[15] but monotherapy is ill advised due to the rapid development of resistance via a point mutation in the gene coding for the 23S rRNA molecule.[13] To avoid the development of resistance in the patient in this case, the authors elected to supplement 500mg clarithromycin therapy twice daily with 100mg doxycycline twice daily, shown to treat 25 percent of Mycobacterium chelonei isolates.[14] Other antibiotics effective against Mycobacterium chelonei are tobramycin, amikacin, imipenem, and ciprofloxacin.[19]

Conclusion
The authors present a case of EI secondary to Mycobacterium chelonei in an immunocompetent woman. Mycobacterium chelonei is best known for its pathogenicity in immunocompromised hosts and has been reported secondary to traumatic implantation. However, the authors’ patient did not have any comorbidities associated with EI, had a negative purified protein derivative (PPD) skin test, and was immunocompetent. Although the patient denied any history of trauma to the lower extremity, this is likely the route of transmission. There is one case report of an 84-year-old immuno-competent patient diagnosed with a disseminated Mycobacterium chelonei infection.[14] The patient may have been at risk due to her advanced age, and her immune system may have been compromised as a result. The case described here suggests that Mycobacterium chelonei should be considered as an etiological agent of EI in immunocompetent hosts. When faced with a diagnosis of EI, clinicians should include atypical mycobacteria among possible etiological organisms, even in those with competent immune systems. Due to the ability of mycobacteria to rapidly develop resistance to antibiotic therapy, timely identification and treatment of atypical mycobacteria is necessary to prevent spread of resistant strains. Therefore, in addition to performing a biopsy for histological evaluation, tissue cultures should also be performed and tested for antimicrobial resistance. The authors’ case demonstrates the need for clinicians to include atypical mycobacteria among possible etiological organisms for EI, even in those with competent immune systems.

References
1.    Bazin E. Lecons Theoriques et Cliniques sur la Scrofula. 2nd Edition. Paris: Dalahaye; 1861.
2.    Sharon V, Goodarzi H, Chambers CJ, et al. Erythema induratum of Bazin. Dermatol Online J. 2010;16(4):1.
3.    Whitfield A. On the nature of the disease known as erythema induratum scrofulosorum. Am J Med Sci. 1901;122:828–834.
4.    Whitfield A. A further contribution to our knowledge of erythema induratum. Br J Dermatol. 1905;15:241–247.
5.    Galloway J. Case of erythema induratum giving no evidence of tuberculosis. Br J Dermatol. 1913;25:217–225.
6.    Montgomery H, O’Leary PA, Barker NW. Nodular vascular diseases of the legs: erythema induratum and allied conditions. JAMA. 1945;128:335–345.
7.    Gilchrist H, Patterson JW. Erythema nodosum and erythema induratum (nodular vasculitis): diagnosis and management. Dermatol Ther. 2010;23:320–327.
8.    Mascaró JM Jr, Baselga E. Erythema induratum of bazin. Dermatol Clin. 2008;26:439–445.
9.    Segura S, Pujol RM, Trindade F, Requena L. Vasculitis in erythema induratum of Bazin: a histopathologic study of 101 biopsy specimens from 86 patients. J Am Acad Dermatol. 2008;59:839–851.
10.    Schneider JW, Jordan HF. The histopathologic spectrum of erythema induratum of Bazin. Am J Dermatopathol. 1997;19:323–333.
11.    Wolf D, Ben-Yehuda A, Okon E, et al. Nodular vasculitis associated with propylthiouracil therapy. Cutis. 1992;49: 253–255.
12.    Bayer-Garner IB, Cox MD, Scott MA, Smoller BR. Mycobacteria other than Mycobaterium tuberculosis are not present in erythema induratum/nodular vasculitis: a case series and literature review of the clinical and histologic findings. J Cutan Pathol. 2005;32:220–226.
13.    Vemulapalli RK, Cantey JR, Steed LL, et al. Emergence of resistance to clarithromycin during treatment of disseminated cutaneous Mycobacterium chelonae infection: case report and literature review. J Infect. 2001;43:163–168.
14.    Halpern J, Biswas A, Cadwgan A, Tan BB. Disseminated cutaneous Mycobaterium chelonei infection in an immunocompetant host. Clin Exp Dermatol. 2010;35: 269–271.
15.    Terry S, Timothy NH, Zurlo JJ, Manders EK. Mycobacterium chelonae: nonhealing leg ulcers treated successfully with an oral antibiotic. J Am Board Fam Pract. 2001;14:457–461.
16.    Tebas P, Sultan F, Wallace R Jr, Fraser V. Rapid development of resistance to clarithromycin following monotherapy for disseminated Mycobacterium chelonae infection in a heart transplant patient. Clin Infect Dis. 1995;20:443–444.
17.    Forslund T, Rummukainen M, Kousa M, et al. Disseminated cutaneous infection due to Mycobacterium chelonae in a patient with rheumatoid arthritis, amyloidosis, and renal failure. Nephrol Dial Transplant. 1995;10:1234–1236.
18.    Wallace R Jr, Brown BA, Onyi GO. Skin, soft tissue, and bone infections due to Mycobacterium chelonae: importance of prior corticosteroid therapy, frequency of disseminated infections, and resistance to oral antimicrobials other than clarithromycin. J Infect Dis. 1992;166:405–412.
19.    Iseman MD. Group IV. Rapid growing mycobacteria. In: Yu VI, Merigan TC Jr, Barriere SL, eds. Antimicrobial Therapy and Vaccines. Baltimore: Williams and Wilkins. 1999:494–497.