The first child with mixed invasive pulmonary Mucor and Aspergillus infection: a case report and literature review

doi:10.21203/rs.3.rs-3339074/v1

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Case Report

The first child with mixed invasive pulmonary Mucor and Aspergillus infection: a case report and literature review

https://doi.org/10.21203/rs.3.rs-3339074/v1

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Cases of mixed infections of Mucor and Aspergillus in the lungs of children have not been reported. Here, we successfully treated and reported the first case of pulmonary coinfection with invasive fungal species in a diabetic girl. The patient was initially treated with a voriconazole-based regimen, but the infection only worsened. Subsequently, bronchoalveolar lavage fluid culture and mNGS were performed, leading to the clear diagnosis of simultaneous pulmonary infection by Aspergillus fumigatus and Rhizopus microsporum. Susceptibility testing revealed the resistance of the fungal strains to voriconazole. Therefore, we employed a combination of AmB liposomes and isaconazole to eradicate fungal infection effectively. This case demonstrates the significance of early and definitive identification of fungal pathogens, determination of effective antifungal medications, and timely administration of properly planned therapeutic regimens. Additionally, we conducted a comprehensive review of 10 cases of pulmonary Mucor and Aspergillus mixed infection, summarizing their characteristics and identifying commonalities.

Mucor

Aspergillus

Pulmonary

Coinfection

Child

Invasive pulmonary mucormycosis (IPM) is a rare but potentially life-threatening opportunistic fungal disease with a severe mortality rate of 40% to 80% ^[¹^]. The clinical manifestations of pulmonary zygomycosis cannot be easily distinguished from those of pulmonary aspergillosis. Patients may present with a fever and cough. Hemoptysis, pleuritic chest pain and pleural effusion can present as well but are less common ^[²^].

Invasive pulmonary aspergillosis (IPA) is another opportunistic infection that commonly affects immunocompromised patients and significantly escalates their morbidity and mortality ^[³^]. The symptoms of IPA include fever, cough, chest/pleuritic pain, shortness of breath, and/or hemoptysis. In some cases, patients with profound immunosuppression or neutropenia may present with few or no symptoms. This is due to the lack of an inflammatory response, and IPA may only become suspected after signs of angioinvasion (chest pain or hemoptysis) are noted ^[⁴^].

Coinfections or consecutive infections of Mucor and Aspergillosis are extremely rare and mainly observed in immunocompromised patients ^[⁵^]. Here, we report a combination pulmonary infection with Mucor and Aspergillus in a diabetic girl. In this scenario, the onset occurs in March 2023 during the late stages of widespread COVID-19 infection. As is well documented, patients with COVID-19 are at a greater risk of developing fungal infections due to its effect on the immune system and because treatments for COVID-19 can weaken the body's defenses against fungi ^[⁶^]. According to Iulia Bogdan's study ^[⁷^], there is a growing trend of drug resistance among these fungal infections. An increasing number of reports have emerged from azole-resistant strains of Aspergillus species ^[⁸^,⁹^].

An 11-year-old girl with a severe fever presented to "A Hospital" 20 days ago due to an unexplained cough. She was eventually diagnosed with diabetes mellitus. Despite undergoing 4 days of treatment, the patient's symptoms remained unresolved, prompting her to seek additional medical attention at the "B Hospital. The antibiotic treatments ware peramivir, meropenem, linezolid and azithromycin. On the 11th day of illness, bronchoscopy and alveolar wash were performed to investigate the cause further, and metagenomic next-generation sequencing (mNGS) revealed Aspergillus and Rhizopus. As a result, the antibiotics voriconazole and cefoperazone-sulbactam were added. After nine days of treatment, her condition did not improve. She was, therefore, presented to our hospital.

On admission, her vitals were as follows: body temperature, 36.5℃; heart rate, 102 beats/min; respiratory rate, 38 breaths/min; and blood pressure, 131/78 mm Hg. Routine blood tests yielded the following results: white blood cell count, 15.36×10⁹/L; neutrophil count, 14.75×10⁹/L; and C-reactive protein (CRP) level, 276.75 mg/L; renal function tests showed that the serum creatinine level was 26 µmmol/L (normal range: 27–66 µmmol/L) and urea nitrogen level was 2.00 mmol/L (normal range: 2.50–6.50 mmol/L). As the patient had been diagnosed with both fungal infection and diabetes mellitus at a previous hospital, the treatment plan involved the use of insulin, voriconazole, imipenem and linezolid.

On day 2, the patient had an unstable body temperature, and the procalcitonin level was 0.36 ng/ml. The results of the G test, Candida mannan and serum galactomannan level were negative, and Candida-IgG antibodies and Aspergillus-IgG antibodies were positive. Chest computed tomography (CT) showed air crescent signs, halo signs and consolidation signs in the right lower lobe; B-ultrasound examination of the right lower lung on the dorsal side revealed a range of 7.3×6.8×7.1 cm of solid lung tissue echo and air bronchial signs (Fig. 1. A-C), which diagnosed lobar consolidation of the right lung and a minor amount of bilateral pleural effusion by the radiologist.

After 3 days of treatment, the patient's condition did not improve. She began vomiting yellow sputum and gastric contents, but the sputum culture results were negative. Therefore, we changed voriconazole to isaconazole. On day 4, she was transferred from the pediatric intensive care unit (PICU) to the respiratory intervention unit, and her inflammatory markers returned to normal. As a result, isaconazole was discontinued on day 5. However, on day 6, CT showed that the lobar consolidation of the right lung was larger than before, and pleural effusion appeared on the left side. Additionally, ultrasound revealed a minor amount of ascites and pelvic effusion. The patient developed paroxysmal pain in the left upper quadrant. To address this, we added liposomal amphotericin B (AmB, 150 mg/day). After 5 days of treatment (11th day), the patient's condition improved; therefore, we reduced the dose of methylprednisolone.

However, on the 12th day, her body temperature improved to 37°C, although she still experienced abdominal pain and vomited light yellow‒green fluid. To relieve her symptoms, midazolam, isaconazole, and promethazine were administered. A CT scan showed virus infection, bilateral pleural effusion, and fluid accumulation in the pelvis. Bronchoscopy revealed erosion of the tracheal opening and middle and lower lobes of the right lung, destroyed bronchial structure in the distal lobe, narrow lumen, and the presence of a large amount of yellow and white pus moss (Fig. 1.E). During the operation, budesonide (0.5 mg) and epinephrine (1 mL) were given, and vancomycin was added to treat infections.

On the 14th day, she developed hypokalemia, possibly due to the use of insulin and AmB. Consequently, potassium supplementation was initiated. A CT scan revealed typical halo signs, pulmonary necrosis, right pleurisy, and bilateral pleural effusion. On day 23, surgical removal of the middle and lower lobes of the right lung was performed. The dissected lesions displayed yellow and black caseous necrotic material, indicating their hardness (Fig. 1F). A gross specimen of the postoperative right middle and lower lobes of the lung revealed the presence of fungal clusters (blue arrow) and several small abscesses (red arrow) (Fig. 1G). After the operation on day 24, mechanical ventilation and closed thoracic drainage were conducted. Two days later, the patient was successfully weaned from the ventilator and transferred to the respiratory intervention unit. Simultaneously, tracheal tubes were cultured. A CT scan on day 27 displayed right pleural effusion after right middle and lower lobectomy. Tracheal tube cultures on day 30 isolated carbapenem-resistant Acinetobacter baumannii, leading to the administration of cefoperazone/sulbactam and tigecycline and discontinuation of vancomycin. The CT scan on day 35 showed improvement in her condition (Fig. 1. H, I). On day 37, the results of the tissue culture indicated the presence of Aspergillus fumigatus and Rhizopus microsporum (Fig. 1J-M). Furthermore, A. fumigatus was found to be resistant to voriconazole, resulting in the discontinuation of its usage. After 12 days of continuous treatment, the girl was discharged from our hospital. Upon discharge, she was prescribed faropenem, isaconazole, and nifedipine. The girl underwent CT scans at 2 and 6 weeks postdischarge (Fig N-R), which showed progressive improvement. Regular follow-up by the parents is recommended.

Coinfections or consecutive infections of Mucor and Aspergillosis are fairly rare, especially in children. This report describes the first case of coinfection by Aspergillus fumigatus and Rhizopus microsporum in a diabetic girl. Aspergillus species are widely distributed and saprophytic fungi that commonly cause pulmonary infection when their conidia or mycelial fragments are inhaled from the environment ^[10]. Aspergillus colonizes the cavity lesions, especially in the healed tubercular cavities of the lungs ^[11]. Within the cavity, the fungus forms a freely moving fungal ball consisting of fungal hyphae (commonly Aspergillus spp., occasionally of Mucor spp. or a combination of both), inflammatory cells, and fibrin material ^[12]. Mucormycosis or zygomycosis is a rare opportunistic fungal infection caused by Mucorales^[13]. Fungal toxins erode the walls of the cavity walls and spread through local destruction, leading to extensive hemoptysis, which can be predominant and frequently the sole symptom of the disease ^[14]. In our patient, she initially presented with a fever and cough, and no classical symptoms were found in the lungs. It was not until the results of BAL mNGS suggested Aspergillus and Rhizopus infection that she was diagnosed with Aspergillus and Rhizopus infections.

Histology examination of lung tissue has been the gold standard for diagnosis, but it is difficult to perform due to compromised respiratory function and elevated risk of bleeding; therefore, BAL still plays an essential role in the diagnostic process ^[15]. Research by Naohisa Urabe showed that when compared with tests on BAL, serum GM and G tests had lower sensitivity and diagnostic odds ratios for chronic pulmonary aspergillosis diagnosis ^[16]. In addition, detection of fungal GM antigenemia is a method to diagnose Eurotium infection ^[17]. The results for GM antigenemia are negative in Mucor, suggesting that caution should be taken not to exclude Mucor infection when testing for GM is negative ^[18]. In this patient, we found Rhizopus and Aspergillus in the histological examination of lung tissue. However, the results for G and GM were negative.

Research has shown that the risk factors for IPM include diabetes mellitus (DM) and metabolic acidosis, iron overload and deferoxamine therapy, immunosuppression, skin or soft tissue breakdown, broad-spectrum azole use and other risk factors ^[2]. In addition, research has shown that viral pneumonia increases patients’ susceptibility to bacterial and fungal superinfections ^[19]. Among the risk factors mentioned above, our patient had only diabetes, did not even have metabolic acidosis, and had a history of COVID-19 infection two months ago.

During our course of treatment, voriconazole was used to combat the infection, but it did not work successfully, probably due to Mucor's resistance to voriconazole. Isoniazid was then used in combination with AmB, and the patient's symptoms improved. Research has shown that AmB has antibacterial activity against both Mucor and Aspergillus^[20–22]. Compared with voriconazole, isavuconazole was the better choice against Aspergillus^[23]. The results of drug sensitivity indicated that the isolated Aspergillus fumigatus was resistant to voriconazole, which is caused most commonly by mutations in the target site for triazoles (CYP51A) ^[4]. Posaconazole is extremely active in vitro against Aspergillus spp. but has mostly been studied for invasive fungal infection (IFI) prophylaxis among high-risk patients ^[24] and as salvage therapy among patients with refractory fungal infections ^[25]. Therefore, posaconazole was not used in our treatment. In the course of our treatment. During the course of our treatment, the patient developed hypokalemia due to liposomal AmB and insulin use, but her kidney function was not impaired, and we subsequently performed this treatment. Although Chenguang Yang's research showed that liposomal AmB showed a lower degree of hemolysis, reduced nephrotoxicity, increased maximum tolerated dose and lower toxicity in vivo compared with free AmB ^[26], we still need to pay attention to the kidney condition when using liposomal AmB.

We searched PubMed for all cases of coinfections between Mucor and Aspergillus in the English literature and included only cases with pulmonary or pulmonary-plus disease. We identified 10 cases (excluding our patient) in 9 published articles. As detailed in Table 1, 4 patients were females and 6 were males, with a female-to-male ratio of 4:6. The mean age was 51.4 (range 27–70). All patients had infections of the right lung, and 3 of the infections also involved the left lung, which may be related to the special anatomical structure of the right lung. Four patients had diabetes mellitus (DM), 2 patients had organ transplantation, 1 patient had HIV, 1 had acute myeloid leukemia, 1 had serious high fall injury, and 2 patients had no known underlying condition. The mean time from onset to diagnosis in these 11 patients was 26.8 days (the time of diagnosis was uncertain in 1 patient). The average stay was 43 days (3 patients died, and the time of discharge from the hospital was unclear for 3 patients). We outline the radiographic manifestations of all patients, with only 3 patients showing the typical crescent sign and reverse halo sign. The distribution of the disease was as follows: 3 patients had bilateral disease, 2 had upper lobe disease, 3 had lower lobe disease, and 5 had unilateral multilobular disease. The diagnosis was established using histology alone in most patients (6 patients), microbiology alone in 1 patient, and both histology and microbiology in 2 patients. Of the 10 patients, only 1 patient with acute myeloid leukemia developed infection while undergoing prophylactic antifungal therapy. Most patients (7 patients) underwent medical therapy alone, 3 patients underwent combined medical and surgical therapies, and none underwent surgical therapy alone. Six patients received voriconazole therapy as part of their medical regimen, and the duration of the therapy ranged from 1 week up to 4 months. Four patients received oral posaconazole therapy, and the therapy duration ranged from 4 weeks to 2 months. Seven patients received liposome AmB therapy, and the duration of the therapy ranged from 1 week up to 1 year. The primary reason for discontinuation was the development or fear of acute kidney injury. Surgical treatments were performed if the antifungal therapies were believed to be inadequate in controlling the disease, and they mainly comprised local debridement with wedge resection or lobectomy.

Table 1

Reported cases of coinfections between *Mucor* and *Aspergillus* from pulmonary disease
No	Age	Sex	Comorbidity	Ventilation	Immune suppressant	Complication	Antibiotics	Antifungal	CT of Lung	Right or left	Lobe	Laboratory evidence	G	GM	Biopsy	Diagnosis	Antifungal drugs (days)	Course	Outcome
1^[27]	67	M	ARDS	Y	high-dose steroid(5 weeks)	kidney and cerebral ischemia	clindamycin, ganciclovir, levofloxacin	N	massive infarct pneumonia on both sides	right and left	upper/middle/lower lobes	negative	/	/	Mucor and Aspergillus	42	N	42	dead
2^[18]	44	M	renal transplantation	N	tacrolimus, methylprednisolone tablets	acute renal failure	moxifloxacin, valganciclovir	Y	ground-glass opacification, solid mass opacity with empty opacities, scattering patchy shadows	right and left	upper lobe	BAL and sequencing showed Mucor and Aspergillus	+	-	/	19	voriconazole 1st-15th, intravenous liposomal AmB posaconazole 15th-60th	60	survival
3^[28]	34	F	HIV	N	CHOP chemotherapy	meningitis	ampicillin cotrimoxazole	N	ground-glass attenuation, focal consolidations, typical cavitation,	right lung	upper/lower lobes	negative	/	/	Mucor and Aspergillus	21	liposome AmB 22th-42th;posaconazole 43th-103th	/	survival
4^[29]	27	F	diabetes mellitus	Y	/	/	levofloxacin cefaperazone-sulbactum,	N	consolidation, cavitation	right lung	upper lobe	broad right-angled branching aseptate hyphae in BAL	/	/	/	12	voriconazole 12th-18th	18	dead
5^[30]	52	M	diabetes cardiac transplant	N	prednisone, tacrolimus,	/	valganciclovir, trimethoprim- sulfamethoxazole	N	nodular	right and left	lower lobe	Aspergillus fumigatus and septate hyphae	/	+	Mucor and Aspergillus	60	caspofungin 60th-88th;voriconazole 60th-165th	88	dead
6^[31]	58	F	acute myeloid leukemia	N	cytarabine, etoposide daunorubicin	grade 4 diarrhea electrolyte imbalance	Posaconazole	Y	pleural effusion, consolidation, cavitation, pulmonary abscess	right lung	middle/lower lobes	negative	/	/	Mucor and Aspergillus	45	posaconazole 3rd-15th day;voriconazole 18th-60th day༛liposome AmB 18th-391th day	111	survival
7^[32]	54	F	2 diabetes mellitus	N	/	/	Levofloxacin cefminox	N	multiple nodules, air crescent signs, bilateral pleural effusion,	right lung	upper/middle/lower lobes	negative	/	+	Mucor and Aspergillus	29	voriconazole 23-30th, AmB 30-44th, liposome AmB 45-55th, posaconazole 50th-end	78	survival
8^[33]	43	M	high fall injury	Y	/	hydrothorax	amoxicillin and clavulanate potassium	N	scattering patchy shadows	right lung	lower lobe	Mucor and Aspergillus from BAL	/	-	/	8	liposome AmB 8th-15th, voriconazole 13th-27th	33	survival
9^[5]	70	M	hemoptysis fever	N	/	/	/	N	air crescent signs, right middle lobe fibrosis and traction bronchiectasis	right lung	upper lobe	/	/	/	Mucor and Aspergillus	21	liposome AmB 21 days	/	survival
10^[5]	65	M	cough hemoptysis expectoration	N	/	/	/	N	reverse halo sign, cavitating consolidation	right lung	upper and middle lobes	/	/	/	Mucor and Aspergillus	/	intravenous liposomal AmB	/	survival

Our patient described here had DM, and despite the absence of metabolic acidosis, her lungs were in extremely serious condition, eventually requiring surgical removal of the right lung. This highlights the importance of considering mixed infection of Mucor and Aspergillus in patients at risk, even with mild immunosuppression and subacute presentation.

In summary, we have reported the first case of mixed Aspergillus and Mucor infection in a child's lungs. Precise microbiological and pathological diagnosis, imaging support, timely surgical intervention, the benefits of interdisciplinary collaboration, and the effective utilization of mNGS technology are crucial for successfully treating childhood lung infections involving both Aspergillus and Mucor. With additional advances, mNGS technology holds great potential for enhanced clinical applications, specifically in the precise design of treatment strategies for coinfections of Aspergillus and Mucor.

Acknowledgment

This study was supported by the clinical promotion and research of precision diagnosis and treatment of infectious diseases in children carried out by the multidisciplinary collaboration from the Shandong Provincial Clinical Research Center for Children's Health and Disease (RC006) and the Science and Technology plan of Jinan Municipal Health Commission (2022-1-45 and 2022-2-149).

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request

Ethics statement

This study was reviewed and approved by the Ethical Review Committee of Children's Hospital Affiliated to Shandong University (approval no. SDFE-IRB/P-2022017). All procedures followed were in strict compliance with the Ethical Review of Biomedical Research Involving Human Subjects (2016), the Declaration of Helsinki, and the International Ethical Guidelines for Biomedical Research Involving Human Subjects.

Written informed consent was obtained from the minor(s)’ legal guardian/next of kin for the publication without any potentially identifiable images or data included in this article.

Conflict of Interest Disclosures

The authors declare no competing interests.

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No competing interests reported.

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The first child with mixed invasive pulmonary Mucor and Aspergillus infection: a case report and literature review

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