S P E C I A L C l i n i c a l

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F E A T U R E S e m i n a r

Coccidiomycosis Thyroiditis in an Immunocompromised Host Post-Transplant: Case Report and Literature Review Elizabeth A. McAninch, Chengyu Xu, Violet S. Lagari, and Brian W. Kim Division of Endocrinology, Diabetes, and Metabolism, University of Miami, Miami, Florida 33136

Context: Acute infectious thyroiditis, particularly fungal thyroiditis, is rare and typically presents in immunocompromised individuals. Here we report the first case of coccidiomycosis thyroiditis occurring in an organ recipient as a consequence of likely allograft contamination and discuss the management strategies for thyroid masses in the setting of disseminated infection. Evidence Acquisition and Synthesis: In this clinical case seminar, we summarize the previously published cases of coccidiomycosis thyroiditis based on a MEDLINE search of all peer-reviewed publications (original articles and reviews) on this topic. We identified six other cases, five of which also occurred in immunocompromised hosts, although none occurred in organ recipients. Conclusion: A case of coccidiomycosis thyroiditis occurring in a post-liver transplant immunocompromised host is reported. Analysis of donor serum revealed the liver allograft as the likely infectious source, resulting in hematological spread to the thyroid. Although our patient’s thyroid gland was lacking gross structural abnormalities at presentation, new-onset thyroid masses developed after relative immune restoration and initiation of antifungal therapies. The differential diagnosis of new-onset thyroid masses in immunocompromised hosts is discussed, with a focus on immune reconstitution inflammatory syndrome. The role of thyroidectomy in the management of fungal thyroiditis is also discussed. (J Clin Endocrinol Metab 99: 1537–1542, 2014)

cute infectious thyroiditis is an uncommon diagnosis and may arise from direct extension through a piriform sinus fistula, congenital malformation, or neighboring tissue infection, or by lymphatic or hematological spread (1). The thyroid has several anatomic attributes that may protect it from infection, including its rich blood supply, abundant lymphatic drainage, high iodine content, and encapsulation (2). Acute infectious thyroiditis should be suspected in patients with systemic signs of infection in association with thyroid tenderness, mass, or abscess. Bacterial etiologies are more common than fungal, with fungal thyroiditis only accounting for about 12% of cases in the literature of the 20th century (3). Rare causes of infectious thyroiditis include mycobacteria, parasites, and treponemes (1, 2, 4). Viral infection has been associated with acute thyroiditis, although few cases dem-

onstrate direct evidence of viral components (5). Fungal thyroiditis is typically associated with disseminated infection in immunocompromised individuals, with Aspergillus species representing the most common fungal pathogens (6). Here we present a case of fungal thyroiditis due to Coccidioides immitis and describe its evolution in an immunocompromised host with disseminated infection while highlighting a number of challenging management questions.

ISSN Print 0021-972X ISSN Online 1945-7197 Printed in U.S.A. Copyright © 2014 by the Endocrine Society Received December 11, 2013. Accepted February 11, 2014. First Published Online February 25, 2014

Abbreviations: CT, computed tomography; FNA, fine-needle aspiration; IRIS, immune reconstitution inflammatory syndrome.

A

doi: 10.1210/jc.2013-4373

Clinical Presentation A 42-year-old Nicaraguan woman with autoimmune hepatitis status post liver transplant 4 months before admission presented with a 3-week history of fevers, chills, severe anterior neck pain radiating to her jaw bilaterally,

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and lower poles. The patient tolerated FNA poorly due to pain, such that the scant serosanguinous aspirate was only sufficient for analysis by culture, but not cytology. Empiric voriconazole was initiated with resolution of fever, pain, and odynophagia within 48 hours. Repeat CT showed improvement in the lung nodules. All cultures were negative except for the thyroid specimen, which was positive for C. immitis by DNA probe. Biopsy of the liver lesion showed changes consistent with mild acute cellular rejection, possible early, concurrent chronic hepatitis Figure 1. Thyroid ultrasound upon presentation with fever, chills, and severe anterior neck pain. with plasma cell infiltration, and a The thyroid gland is enlarged and slightly heterogeneous but does not reveal a well-defined nodule or abscess. single focus of severely dilated and congested sinusoids possibly repreand odynophagia. Home medications included tacrolisenting peliosis hepatis—a vascular abnormality of the mus, trimethoprim/sulfamethoxazole, lamivudine for doliver. Staining of the liver sample was negative for fungal nor hepatitis B positivity, and ganciclovir for donor cytoelements. The donor had lived in an endemic region, and megalovirus positivity; methylprednisolone taper was retrospective analysis of the donor’s serum was consistent completed just before admission. Liver transplant was perwith prior coccidiomycosis infection because qualitative formed in the United States. The patient had no prior hisimmunodiffusion was positive for IgM antibodies. The tory of thyroid disease. Symptoms persisted despite 1 week donor’s other organ recipients were without infectious of empiric broad-spectrum antibiotics; endocrinology was signs or symptoms. consulted for consideration of thyroiditis. Given the positive C. immitis DNA probe result, antiPhysical examination revealed a normotensive female fungal therapy was changed to oral fluconazole without in moderate distress with fever, rigors, tachycardia, and hepatotoxicity, and tacrolimus dose was decreased to tachypnea. There was no exophthalmos. The thyroid was exquisitely tender to palpation, diffusely enlarged, smooth, achieve about half of the prior serum target while staying and mobile without distinct nodules. Perithyroidal soft within the therapeutic range to provide a degree of imtissue was boggy and tender. There was left cervical mune restoration. One month later, the patient remained clinically well but developed two extremely firm, nonlymphadenopathy. Labs on admission showed leukopenia, normal liver tender, hypoechoic left thyroid masses measuring 1.1 ⫻ enzymes and coagulation parameters; TSH, 1.68 ␮IU/mL 1.2 ⫻ 1.0 cm in the left upper pole and 2.9 ⫻ 1.8 ⫻ 2.0 cm (normal range, 0.27– 4.2 ␮IU/mL); free T4, 0.93 ng/dL in the left mid pole (Figure 2). At this time the patient was (normal range, 0.93–1.7 ng/dL); T3, 77.4 ng/dL (normal afebrile and had no thyroid tenderness and no other sysrange, 80 –200 ng/dL); and antithyroid peroxidase anti- temic signs of infection. In considering the differential dibodies, 3 IU/mL (range, ⬍20 IU/mL). HIV and QuantiF- agnosis for these new-onset thyroid lesions, the possibility ERON TB tests were negative. On ultrasound, the thyroid of immune reconstitution inflammatory syndrome (IRIS) was enlarged and heterogeneous without focal lesions, was weighed vs progressive fungal infection with abscess and had diffusely increased vascularity (Figure 1). Non- formation. Given the vast improvement of her overall clincontrast computed tomography (CT) showed normal-ap- ical status and the typical IRIS characteristics of these pearing thyroid but revealed bilateral innumerable lung masses (lesions arising at the site of a prior opportunistic infection in an individual with restoration of immunity), it nodules and an ill-defined hepatic hypodensity. An extensive infection workup including bronchoal- was felt that IRIS was the likely diagnosis. In hopes of veolar lavage, liver biopsy, and bilateral thyroid fine-nee- differentiating between these entities, FNA was attemptdle aspiration (FNA) was performed; because no lesions ed; although the procedure was not painful, the lesions were identified on ultrasound and she had diffuse thyroid were nearly impenetrable, “like concrete.” Cytology was tenderness, targets for FNA were chosen in bilateral upper insufficient, and culture was negative. Given the overall

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doi: 10.1210/jc.2013-4373

Figure 2. Thyroid ultrasound at 1-month follow-up shows interval development of thyroid masses after initiation of antifungal therapies and decrease in tacrolimus dose. Two solid, hypoechoic masses in the left lobe are demonstrated.

improved clinical picture, surgical biopsy or thyroidectomy was deferred. Serial imaging of the thyroid about 2 months later revealed evolution of these masses into heterogeneous structures, some with anechoic centers and irregular borders (Figure 3); there were now four lesions measuring 2.6 ⫻ 1.8 ⫻ 2.5 cm in the superior left pole, 3.6 ⫻ 1.7 ⫻ 1.9 cm in the middle left pole, 3.2 ⫻ 1.7 ⫻ 1.8 cm in the inferior left pole, and 2.0 ⫻ 0.9 ⫻ 1.5 cm in the isthmus. In addition to the dramatic changes in her thyroid morphology, there was a parallel deterioration in her overall clinical status because she developed a diffuse eruption of sc skin nodules that were culture positive for C. immitis, she developed possible mastoid osteomyelitis, and her lung lesions progressed in both size and number. Primary hypothyroidism also developed, TSH was 5.46 ␮IU/mL, free T4 was 0.92 ng/dL, and levothyroxine replacement was initiated. Liver function remained stable without progression of the liver hypodensity. Parenteral amphotericin B was added to her regimen of oral fluconazole, but despite these efforts, the existing thyroid masses enlarged further, and one mass began spon-

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taneously draining through a cutaneous fistula. Presumably as a consequence of antifungal therapies, there was deterioration in renal function as well as development of electrolyte abnormalities requiring titration of magnesium and potassium supplements. Given their dramatic progression and the patient’s accompanying overall clinical deterioration, the etiology of the thyroid masses was thought to be less consistent with IRIS and more likely evidence of worsening coccidiomycosis thyroidal infection. Although the disease was disseminated, involving lung, skin, and bone as well as the thyroid, the decision was made to recommend thyroidectomy. Surgery was performed 6 months after initial presentation; the operation was complex because the left thyroid lobe was virtually indistinguishable from surrounding inflammatory tissue in the paratracheal and paraesophageal areas. Gross examination of the masses revealed that they were mostly solid rather than fluidfilled. In the area of the cutaneous fistula, a cuff of strap muscle was removed to obtain an infection-free margin. Recurrent laryngeal nerves and parathyroid glands were preserved. Pathology revealed necrotizing granulomatous thyroiditis extending into the adjacent subcutis and skin; staining was consistent with extensive Coccidioides infiltration. The patient tolerated the surgery well with appropriate wound healing and intact bilateral vocal cord function. Her antifungal regimen was changed to voriconazole on postoperative day 3. In the 2 months after surgery, the sc skin nodules resolved, her renal function improved on the updated antifungal regimen and liver function remained normal, and lung lesions on CT appeared stable, although they did not resolve. Her clinical status is being closely monitored for signs or symptoms of continued infection. Antifungal therapy will be continued indefinitely.

Discussion Here we present a case of a 42-year-old liver transplant recipient who developed disseminated coccidiomycosis

Figure 3. Despite dual antifungal therapies, the masses evolved into four abscess-like structures with irregular borders and cystic components as viewed in the transverse (A and B) and longitudinal (C) axes.

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Table 1.

A Case of Coccidiomycosis Thyroiditis

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Reported Cases of Coccidioides Thyroid Infection

First Author, Year (Ref.)

Age, y/Sex

Previous Thyroid Disease?

Factors Affecting Immune Status

Current Case

42/F

No

Tacrolimus status post-liver transplant

Jinno, 2012 (10)

44/M

No

HIV/AIDS

Smilack, 1998 (12), case 1

72/F

Yes, Hashimoto

Prednisone for pulmonary sarcoidosis

Smilack, 1998 (12), case 2

78/M

No

None

Loeb, 1979 (11), patient 1

46/M

No

Prednisone for polyarteritis nodosa

Loeb, 1979 (11), patient 2

31/F

No

History of sarcoidosis

Berry, 1968 (13)

26/F

No

Glucocorticoids for systemic lupus erythematosus

Features of Thyroid Involvement

Thyroid Hormone Status

Disseminated Infection? Treatment

Thyroid tenderness, diffuse enlargement. US–no definite nodule/abscess at presentation; later developed large abscesses with cutaneous fistula. Thyroid pain and swelling. CT–large, loculated thyroid abscesses. Thyroid nodule with spontaneously draining sinus tracts. US– diffuse heterogeneity, hypoechoic nodule. CT– thyroid abscess. Left thyroid nodule. RAI uptake and scan-– 67% at 24 h, no uptake left nodule. Diffuse thyroid tenderness. US–no cyst. RAI uptake and scan-– 4% at 24 h, diffuse patchy uptake. Thyroid tenderness. RAI uptake and scan-–2.6% at 24 h, patchy uptake in left lobe, no uptake in right lobe. US– cystic right thyroid mass. Nontender thyroid nodule.

Euthyroid at presentation, progressed to hypothyroidism

Yes

Voriconazole, fluconazole, ampho B, thyroidectomy

Hypothyroidism

Yes

Incision and drainage, ampho B, fluconazole

Transient hyperthyroidism

Yes

Ampho B, fluconazole

Hyperthyroidism ⫹ thyroid-stimulating Ig

No

Subtotal thyroidectomy, fluconazole

Euthyroid

Yes

Ampho B, total thyroidectomy, iv and intrathecal miconazole

Transient hyperthyroidism

Yes

Ampho B, incision, and drainage

Not reported

Yes

Abscess excision, ampho B

Abbreviations: F, female; M, male; ampho B, amphotericin B; US, ultrasound; RAI, radioactive iodine.

with a focus of thyroid involvement in the setting of posttransplant immunosuppression. Presumably, the initial source of infection was liver allograft contamination. The presenting infectious signs and symptoms were localized to the thyroid, although the patient likely had disseminated disease at presentation because lung lesions were found on initial CT. Fungal thyroiditis has been previously described in immunosuppressed solid-organ transplant recipients (7–9), but all of these cases were due to Aspergillus species. To our knowledge there are six previously reported cases of coccidiomycosis involvement of the thyroid, five of which also occurred in immunocompromised hosts either due to HIV/AIDS (10), as a secondary consequence of sarcoidosis (11), or as a complication of immunosuppressive therapy (11–13) (Table 1). This case is unique in that coccidiomycosis occurred in a post-transplant organ recipient, likely as a result of donor-to-host transmission. Our patient had no prior history of thyroid disease, which is typical for fungal thyroiditis in contrast to bacterial thyroiditis (6). Although coccidiomycosis thyroiditis has been associated with gross structural abnormalities of the thyroid, eg, abscess formation, structural changes

might be absent in immunocompromised hosts due to the lack of the appropriate inflammatory response. This may explain why the thyroid ultrasound at presentation showed only nonspecific findings. Acute infectious thyroiditis must be considered in immunocompromised individuals with signs or symptoms localized to the thyroid even in the absence of gross structural thyroid abnormalities, and clinicians should have a low threshold to perform diagnostic FNA. Of note, targeting of the infectious focus for FNA might have been improved utilizing radioiodine or technetium-99 scanning because involved areas typically appear as “cold” regions (2), but in our case, due to her clinical deterioration, the team proceeded without delay to obtain tissue diagnosis. Aside from infectious thyroiditis, other entities in the differential diagnosis of thyroid pain include subacute painful thyroiditis, primary or metastatic neoplasm, amyloidosis, amiodarone-induced thyrotoxicosis, intrathyroidal hemorrhage, thyroid infarction, Graves’ disease, radiation thyroiditis, and rarely Hashimoto’s thyroiditis (2, 14, 15). Although thyrotoxicosis and hypothyroidism have been described in other cases of fungal thyroiditis, our patient presented with normal thyroid function tests,

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doi: 10.1210/jc.2013-4373

only developing hypothyroidism later in the course, as the infection progressed and the masses evolved. Differentiating IRIS from worsening thyroid gland infection proved to be a challenge in this case. IRIS is a complex clinical syndrome that can have two distinct forms: one is an immune restoration disease triggered by pathogen-specific antigens that results in immunopathology; the other is the development of autoimmune diseases or sarcoidosis (16). The immune restoration form of IRIS may be triggered by pathogen-specific antigens arising from known or subclinical opportunistic infections; alternatively, HIV itself may provoke an IRIS response during antiretroviral therapy (17). Mechanistically, an exuberant, disordered inflammatory response leads to a clinical presentation involving lymphadenopathy, organomegaly, and/or other systemic signs such as fever (18). Although this dysfunctional immunopathological response may be misinterpreted as representing worsening infection, in fact it may lead to the eradication of the underlying infection without additional antimicrobial therapy. The mechanism of the noninfectious form of IRIS is less well understood, but patients may present with either autoimmune diseases, such as Graves’ disease and Hashimoto’s disease, or with sarcoidosis. At the time that the thyroid masses developed, the immunosuppressive regimen had been reduced, and our patient had classic characteristics of IRIS, including: 1) new appearance of a mass consistent with an inflammatory process; 2) onset after initiation of appropriate antifungal therapy that was not explained by another newly acquired infection; and 3) negative culture results (19, 20). When manifesting in the thyroid, IRIS has been associated with the development of either Graves’ disease (21) or Hashimoto’s thyroiditis (22), and it has also been associated with abscess development in one case in which a patient with HIV developed tuberculous thyroiditis after initiation of antiretroviral therapy (23). Thus, it was reasonable to consider this the leading diagnosis early in the clinical course. In retrospect, a core needle biopsy could have been pursued after the failed FNA. A cutting needle, although more traumatic than a fine needle, might have been able to penetrate the “concrete” mass lesions enough to provide a core sample demonstrating the presence of fungus. Although the optimal management of IRIS has not been defined, agents including corticosteroids and nonsteroidal anti-inflammatories have been implemented, but experts generally reserve these therapies for individuals with central nervous system manifestations, a lifethreatening condition due to the IRIS itself, or severe organ dysfunction (19, 20), none of which were present. One of the most challenging clinical questions in this case was whether thyroidectomy should have been pur-

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sued earlier, or at all. Ultimately, the diagnosis of IRIS was rejected because of the evidence of worsening disseminated infection and because of the development of the spontaneously draining cutaneous fistula. Given the abscess-like ultrasonographic appearances of the masses, the efficacy of antifungal therapies to adequately penetrate the tissue was questioned. It was further hypothesized that the infected thyroid was acting as a possible source of systemic fungal seeding. Thus, thyroidectomy was pursued. This course of action was in line with the previous case reports of coccidiomycosis involving the thyroid, in most of which various surgical interventions were employed (Table 1). Thyroidectomy earlier in her course might have decreased disease progression. On the other hand, removing one nidus of infection could prove futile if the other foci cannot be eradicated with medical therapy. That our patient improved dramatically after surgery indirectly supports the decision to pursue thyroidectomy in this case, although we cannot rule out that the change in antifungal therapy back to voriconazole explains some of the clinical improvement. The initial switch away from voriconazole was logical because voriconazole is not approved by the Food and Drug Administration for treatment of coccidiomycosis and is not recommended in the current treatment guidelines (24). There are, however, case reports of improved clinical outcome with voriconazole in refractory disseminated coccidiomycosis (25–27). Mortality is high in fungal thyroiditis (6), and it remains to be seen whether our patient can clear her disseminated coccidiomycosis infection. Lifelong antifungal therapy is anticipated.

Conclusion Although less common than bacterial thyroiditis, fungal thyroiditis should be considered in immunocompromised individuals. This represents the first reported case of coccidiomycosis thyroiditis likely obtained from a contaminated allograft in a post-liver transplant patient. IRIS involving the thyroid has been previously associated with tuberculous mass formation and autoimmune thyroid disease. Thus, IRIS should be in the differential diagnosis of infectious thyroiditis in patients experiencing immune reconstitution. Diagnostic tests to differentiate these entities may include ultrasound, radioiodine scan, FNA, and core needle biopsy as necessary. In our case, evidence of progressive disseminated infection made the diagnosis of IRIS less likely, and the final surgical pathology confirmed that the coccidiomycosis infection of the thyroid had not been eradicated by antifungal therapy.

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Thyroidectomy should be considered in the management of fungal thyroiditis if clinical and imaging evidence suggests that the thyroidal infection is progressing despite optimal medical therapy.

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10. 11. 12.

Acknowledgments Address all correspondence and requests for reprints to: Brian W. Kim, MD, University of Miami Miller School of Medicine, 1580 NW 10th Avenue, Suite 619, Miami, FL 33136. E-mail: [email protected]. This work was funded by the Department of Endocrinology, Diabetes and Metabolism at the University of Miami Miller School of Medicine. Disclosure Summary: The authors have nothing to disclose.

13.

14. 15. 16. 17.

18.

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Coccidiomycosis thyroiditis in an immunocompromised host post-transplant: case report and literature review.

Acute infectious thyroiditis, particularly fungal thyroiditis, is rare and typically presents in immunocompromised individuals. Here we report the fir...
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