Evolutive radiological findings in an exceptional case of Cryptococcal and Coccidioidal co-infection in an immunocompetent male. A case report.

doi:10.21203/rs.3.rs-4589261/v1

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Evolutive radiological findings in an exceptional case of Cryptococcal and Coccidioidal co-infection in an immunocompetent male. A case report.

https://doi.org/10.21203/rs.3.rs-4589261/v1

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Background: Bone infections such as chronic fungal erosive osteomyelitis are rare. uncommon forms of bone infection. The widespread yeast of the Cryptococcus species, the endemic dimorphic fungus Coccidioides, and the simultaneous infection by multiple pathogen species are even less common, especially in immunocompetent hosts. These infections frequently have no symptoms and the clinical signs remain undetected, allowing the infection to worsen over weeks or months. Mycotic arthritis is one of the rarest clinical symptoms; it is hard to distinguish from other types of arthritis, which slows down the diagnosis procedure.

Case presentation: In order to demonstrate the beginning and progression of radiological abnormalities in a case of aggressive fungal osteomyelitis, we provide the case of a 31-year-old male patient here. The man showed signs of extensive bone erosion and inflammatory involvement in his right knee and right hallux phalanx, although he had no prior history of immunodeficiency. The co-infection resulting from Cryptococcus Neoformans in his right knee and Coccidioides Immitis in his hallux were the reason for the injuries.

Conclusions: While an acute, benign, and self eradicating lung infection is the predominant presentation for most cases of cryptococcosis and coccidioidomycosis, a small percentage of patients experience a devastating extrapulmonary condition, which can include arthritis. The pathogenic mechanism of bone involvement are unknown, and it often remains untreated. Here, we discuss radiographic evidence of particular bone inflammation during the early phase and later phases of the disease, since management of this chronic condition remains a challenge. We propose that imaging may mimic osseous neoplasia in persistent fungal diseases, such as Coccidioidomycosis and Cryptococcosis.

Cryptococcosis

Coccidioidomycosis

Osteomyelitis

Synovitis

Joint effusion

Bone erosion

Fungal

Arthritis.

CRYPTOCOCCAL ARTHRITIS.Cryptococcus, which comprises almost 70 species and genera (Min et al. 2023; Fonseca et al. 2011; Chung et al. 2011; Desnos-Ollivier 2015; Deepa et al. 2014; Mayer et al. 2020), is an encapsulated yeast-like fungus prevalent in soil, spoiled milk, fruitsm and birds dropping (Bruno et al. 2002; Kabir et al. 2022). The two species of cryptococcal infection that currently affect humans are Cryptococcus neoformans and Cryptococcus gattii. The majority of cases of cryptococcal infection in immunocompromised individuals have been reported (Cho et al. 2021; Pasquier et al. 2022; Duràn et al. 2022). The majority of cases have initial respiratory tract involvement (Singh et al. 2008; Fisher et al. 2016; Rigby et al. 2012; Qu et al. 2012; Ye et al. 2012; Willenburg et al. 2009; Zhang et al. 2012; Ohkubo et al. 2023; Saguier Padilla et al. 2023; Yoshimine et al. 2021; Tonai et al. 2022), the primary point of entry, resulting in a temporary and subclinical lung illness. Cryptococcus can spread to other organs after inhalation, usually the brain and meninges (Mitaka et al. 2022; Elkhatib et al. 2021; Kurahara 2022). Cryptococcal arthritis is an uncommon condition (Bruno et al. 2002; Agrawal et al. 2000; Hsu et al. 2022) and ostemyelitis occurs in only 5-10% of patients with multi-organ cryptococcal infection. Very few reports of cryptococcal joint infection, which causes localized swelling, pain, and mobility disorders (Min et al. 2023). The diagnosis is, indeed, typically delayed (Agrawal et al. 2000). Particularly uncommon are radiological findings including soft tissue mass, peripheral abscesses, or bone destruction (Cho et al. 2021; Min et al. 2023).

COCCIDIOIDAL ARTHRITIS.Coccidioidomycosis, otherwise known as Valley Fever or San Joaquin Valley Fever, is a fungal infection that can have high morbidity and potential mortality. It is caused by Coccidioides Immitis or Coccidioides Posadasii, which are dimorphic fungi endemic to the Southwestern United States, Mexico, and South America (Ramadan et al. 2022). Approximately 60% of infected individuals are asymptomatic, while it usually manifests itself as an acute respiratory infection (Bays et al. 2021; Johnson et al. 2021; Ashizawa et al. 2023), with symptoms similar to influenza or acute bronchitis (Alcauskas et al. 2022). Still, in some cases (1% of infections), after hematogenous or lymphogenous dissemination, a secondary extrapulmonary disease is possible, involving the skin, meninges, lymph nodes (Sri et al. 2023), peritoneum (Villafuerte et al. 2021), bones, and joints. Coccidioidomycosis is acquired by inhaling spores (arthroconidia) from desert soils, detached from branching septate hyphae (Ahmad et al. 2021; Nasrawi et al. 2020; Naeem et al. 2023). Typically, the inhaled spores mutate in the terminal bronchi into invasive multinucleate spherules, activating a granulomatous reaction and fibrosis that may cavitate or form nodular lesions (Castro-Lopez et al. 2017; Li et al. 2014; Blohm et al. 2023). Individuals with impaired cell-mediated immunity are more likely than healthy individuals to have a severe infection (Blair et al. 2019; Redemann et al. 2021; Naeem et al. 2021; Guo et al. 2022; de Lima-Neto et al. 2021; Bent et al. 2021). To date, very few reports have described extrapulmonary disseminated cases, manifesting as monoarticular joint involvement with destruction of bone and soft tissue (Viramontes et al. 2019; Giordani et al. 2023; Ong et al. 2012; Moni et al. 2023; Li et al. 2014). Coccidioidal arthritis has a multiplicity of radiological presentations, although it mainly either destroys the joint rapidly or remains a chronic synovitis. The latter case is a "core" that may determine further hematogenous dissemination (Bayer et al. 1979). The most frequent radiographic findings are joint effusion and multiple lucent, punched-out bone lesions (Li et al. 2014). MRI and CT scans, showing subchondral bone loss, extensive marrow oedema, and synovitis can be used to establish a diagnosis, but the findings remain often non-specific, mimicking a neoplasm or an atypical joint infection, as well as pigmental villonodular synovitis (Giordani et al. 2023). On chronicity, lesions with permeative or moth-eaten margins, or sclerotic borders may be identified (Li et al. 2014).

SOLITARY MASS-LIKE BONE LESIONS. Solitary osseous tumor-like lesions determining osteolysis, as well as marrow and soft tissue oedema, are uncommon conditions caused by different etiopathogenesis, which can be both neoplastic and non-neoplastic. They are routinely encountered by radiologists in various imaging modalities. Some benign, non-neoplastic lesions often mimic bone tumors.

a) Bone tumors. The 2020 World Health Organization Classification of Soft Tissue and Bone Tumors subdivided bone tumors as benign, intermediate (locally aggressive or rarely metastasizing), and malignant (Anderson et al. 2021). In general, a solitary bone lesion in an adult over the age of 40 has a higher likelihood of being malignant (Hoffman et al. 2022); in particular, the epiphyseal origin is primarily related to metastasis and pain is usually associated with lesional growth and a malignant transformation.

b) Benign non-neoplastic bone lesions. This group contains a broad range of normal variants, congenital abnormalities, post-traumatic/iatrogenic lesions, arthritic changes, and infectious/inflammatory processes (Broski et al. 2022).

The ability to differentiate between malignant and benign lesions based on images often depends on the experience of the radiologist (Vanel et al. 2012). A practitioner's first impression typically precedes four hypotheses: a) benign lesion, b) benign but likely of clinical significance, c) indeterminate, d) highly suspicious (Hoffman et al. 2022). A patient history is an essential element for the interpretation of imaging: the most useful information is symptomatology (the presence or absence of pain). Physical examination findings, as well as a prior history of malignancy, are also fundamental. Due to its greater sensitivity, MRI can detect changes in joints at an earlier stage thanradiographs. However, a biopsy is necessary, even when imaging indicates neoplastic bone lesions with a high degree of certainty.

In Table 1 we report a review of commonly encountered knee-bone tumors and lesions that can mimic bone tumors (Kwee et al. 2016, Stern et al. 2020, Crawford et al. 2013, Abe et al. 2020, Rodriguez-Merchan 2012, Matcuk et al. 2016, Jain et al. 2022, Ahlawat et al. 2020, Junaid et al. 2021, Kager et al. 2022).

A 31-year-old male had clinical features typical of pneumonia and subsequent arthritis, presented with a painful lump in his right knee. The patient, who had no previous medical history, went to his general practitioner (October 2018) due to a persistent cough and fever (40°C), lasting for one week. The patient had been touring California and Arizona, including camping in the wilderness, 20 days before his illness. The patient had no history of primary immunodeficiency or autoimmune diseases. He had neither chronic comorbidities nor conditions or diseases that could lead to an immunodeficiency disorder.He did not report the use of any drugs or harmful habits, such as excessive usage of alcohol or smoking. The patient was treated with broad-spectrum empirical antibiotic therapy (amoxicillin and clavulanic acid), leading to the clinical resolution of pneumonia after a few days. However, six weeks later (January 2019), he had a new fever, lasting three days (38°C). In August 2019, the patient returned to his general practitioner due to intense swelling and persistent pain in the right knee joint (new symptoms), limited mobility, and a local high skin temperature. The patient did not have any recurrent fever, chest tightness, chest pain, abdominal pain, diarrhea, or lack of appetite.

An anteroposterior radiograph of the knee did not show any appreciable findings in the bone, whereas CT and MRI visualized i) an ovular tumor-like lesion in the lateral condyle of the tibia with inflammatory involvement of the surrounding soft tissues (peripheral abscesses), ii) joint degeneration, and iii) the anterior tibial cavity, including cortical bone (Figure 1). Magnetic resonance imaging STIR-T2 sequence shows a focal subarticular lytic hyperintense pseudotumor mass through the proximal tibia with marked perilesional bone marrow and soft tissue oedema.

The diagnosis of solitary bone lesions includes clinical and radiological signs, and the combination of well analyzed signs leads to an efficient diagnostic probability. Osseous tumor-like lesions determining osteolysis and marrow and soft tissue oedema are uncommon conditions ascribable to different etiopathogenesis, ranging from neoplastic to non-neoplastic entities (Schmitt 2017; Norman et al. 1986; Stacy et al. 2011; Cottias et al. 1997; Sanghvi et al. 2009; Junaid, Bilal et al. 2021). The appearance of bone infection and bone tumors is often similar on imaging (Moser et al. 2012; Chung et al. 2012; Junaid S, Gnanananthan V et al. 2021).

By focusing our analysis on imaging, Hoffman's diagnostic approach to solitary bone lesions (Hoffman et al. 2022) is very instructive. Hoffman proposed a dual algorithm, first based upon CT imaging and then MRI, with the purpose of distinguishing between indolent and aggressive lesions.

Lesional density itself on CT scans does not discriminate with accuracy between benign and malignant, but other findings from our patient are worth considering (Table 2):

1. Margins. Ill-defined margins, without sclerotic borders (Vanel et al. 2009), as in this case, correspond most likely to aggressive lesions.

2. Matrix. Bone is a mineralized organic matrix containing osteocytes, osteoblasts, and osteoclasts. The local alterations in mineralization could be due to altered remodeling (tumors) or to the action of enzymes (osteomyelitis; Hofstee et al. 2020). In our case, a poorly organized matrix, intermixed with lytic areas, indicates aggressive behavior.

3. Size. Lesions shorter than 6 cm are statistically more likely to be non malignant.

4. Cortical involvement. The cortical integrity has been violated, suggesting the presence of an aggressive lesion and/or an infection.

5. Periosteal reaction. CT scans show some segments characterized by a thin, calcified periosteal reaction at the periphery. This is irregular and interrupted, which could indicate the aggressive nature of the lesion.

Lastly, the CT scan gives us an important detail. In the center of the lesion, it is possible to recognize an irregular region having a texture similar to the bone, suggesting the presence of a "sequestrum", which is an irregular bone fragment with a surrounding clear zone. If confirmed, the presence of a sequestrum would be very suggestive of infection (Moser et al. 2012).

MRI imaging, following Hoffman's diagnostic criteria, confirmed this first evaluation: generally, aggressive lesions have a T1 iso-hypointense and T2 hyperintense signal and extension to the soft tissue (Table 3). The perilesional oedema could be described in our case as large and irregularly outlined, with juxtaosseus oedema also evident, as typically in osteomyelitis (Vanel et al. 2009).

In conclusion, Hoffman's approach suggests the presence of highly aggressive osteomyelitis, and a recommendation for further evaluation (biopsy) would be reasonable.

An alternative diagnostic approach has been developed by the Society of Skeletal Radiology, a collaborative multi-institutional work to provide a bone reporting and data system (Bone-RADS) for solitary bone lesions identified on CT and MRI, integrated by clinical conditions (Chang et al. 2022; Connie et al. 2022). Following this algorithm, the knee solitary lesion above can be described as a Bone-RADS-4 (Table 4, fromChang et al. 2022, modified) and needs to undergo biopsy and/or oncologic evaluation. Adams' radiological approach for intra-articular mass, where the lesion can be classified as "Type 1" (Table 5, fromAdams et al. 2007), also leads to a biopsy requirement.

For diagnostic purposes, a CT guided biopsy (December 2019) demonstrated the presence of giant-cell granulomatous chronic osteitis with spores from Cryptococcus.

Five and a half years after the patient's California and Arizona tour (February 2024), his knee symptomatology was attenuated (after voriconazole for six months). However, the CT and MRI of the knee showed an enlargement of the osteolysis (Figure 2) featuring extensive synovial thickening, as well as an enhancement compatible with synovitis, in addition to an evolutive inflammatory involvement of the patella and femur (Figure 3).

In June 2023, the patient returned to his general practitioner, complaining about pain and swelling in his right foot big toe. Physical examination demonstrated joint effusion and palpable soft tissue mass in the interphalangeal joint. Laboratory studies were significant for erythrocyte sedimentation rate (37 mm/h), C-reactive protein (16.7 mg/dL), and IgG1 quantification (15.8 g/l). In particular, an increment in the ratio CD4/CD8 was found (2.3), due to the reduction of the CD8+ T-lymphocytes (20% T-lymphocytes CD3+CD8+, flow cytometry). Further investigation, including CT and MR imaging of the affected joint, showed erosive changes of the first phalanx of the right hallux, with radiological findings very similar to the previous knee-joint arthritis (Figure 4).

The patient underwent an excisional biopsy in August 2023, which showed necrotizing giant-cell granulomatosis and evidence for spherical PAS+/Grocott+ corpuscles, resembling Coccidioides Immitis. Filamentous fungi were isolated in fungal culture in September.

Although the vast majority of cryptococcosis and coccidioidomycosis occur as an acute, benign, self-limited respiratory infection, an unlucky minority of people are faced with a debilitating disseminated extrapulmonary disease, including arthritis. The pathological mechanism of bone involvement is an enigma to many, and it often goes undiagnosed. As management of this chronic disease remains problematic, here we describe radiological findings of specific bone inflammation during the early phase and late evolution, as well as similarities with other most common conditions, to provide new insights for precocious recognition. We suggest that chronic fungal infections, like Cryptococcosis and Coccidioidomycosis, can mimic osseous neoplasm by imaging.

ADC: Apparent diffusion coefficient

STIR: Short Tau Inversion Recovery

PAS: Periodic acid–Schiff stain

MRI: magnetic resonance imaging

Ethics approval and consent to participate. Consent to participate was obtained according to national and European regulations (Italian D.Lgs. 196/2003 and European Declaration 679/2016).

Consent for publication: This case report involves a human participant investigated in our Department for ordinary radiological follow-up. We confirm that the patient expressed his consent to share these images and this information with the scientific and medical communities. Their anonymity has not been compromised.

Availability of data and material: All the data are available for further investigations.

Competing interests: The authors declare that they have no competing interests.

Funding: N/A

Authors' contributions: All authors contributed to the study conception and design. Material preparation was performed by Dr. PLM, Dr. AA, Dr. RC, Dr. AN, Dr. CR, Dr. AR, Dr. AT and Dr. GV. The first draft of the manuscript was written by Dr. PLM and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Acknowledgements: N/A

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Evolutive radiological findings in an exceptional case of Cryptococcal and Coccidioidal co-infection in an immunocompetent male. A case report.

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