Hepatic phaeohyphomycosis due to a novel dematiaceous fungus, Pleurostoma hongkongense sp. nov., and importance of antifungal susceptibility testing

Figures & data

Figure 1. Computed tomography image of the upper abdomen. A small fluid collection with gas pocket was found and rim enhancement was observed around the tubal drains.

Figure 2. Photomicrographs of the biopsied liver abscess wall tissue. (a) Abundant fungal hyphae, a small amount of necrotic tissue, brown bile pigments as well as a few acute inflammatory cells were observed (Periodic acid-Schiff staining, original magnification 200×). (b) The fungal hyphae were highly septate (Grocott methenamine-silver staining, original magnification 400×).

Figure 3. Growth of Pleurostoma hongkongense HKU44^T on various culture media after 7 days of incubation at 25°C. (a, d) Malt extract agar (MEA). (b, e) Sabouraud dextrose agar (SDA). (c, f) Potato dextrose agar (PDA). Brightness was adjusted individually for each panel.

Figure 4. Microscopic features of Pleurostoma hongkongense HKU44^T. Arrows indicate notable structures. (a–c) Scanning electron microscopy photographs of notable phialide and conidia features. Scale bars = 5 μm. (d–i) Bright-field microscopy of corresponding features using a slide culture preparation. Slides were prepared via wet mount and stained with lactophenol cotton blue (original magnification 1000×). Scale bars = 10 μm.

Figure 5. Phylogenetic tree showing the relationship of Pleurostoma hongkongense HKU44^T to its closely related species within the genus Pleurostoma. The tree was inferred from the concatenated sequence data of the internal transcribed spacer (ITS) region, partial β-tubulin gene, partial 18S nrDNA and partial 28S nrDNA by the maximum likelihood method with the substitution model T92 (Tamura 3-parameter model) + G (gamma-distributed rate variation) + I (estimated proportion of invariable sites). The scale bar indicates the estimated number of substitutions per base. Only nodes that were well supported by the maximum-likelihood method (≥70% bootstrap support) have their bootstrap support, calculated from 1,000 replicates, shown; and all these nodes were also well supported by the Bayesian inference method (posterior probabilities ≥0.99). The DDBJ/ENA/GenBank nucleotide accession numbers for Jattaea algeriensis STE-U 6201^T are EU367446 (ITS), EU367466 (β-tubulin), EU367462 (18S nrDNA) and EU367456 (28S nrDNA).

Table 1. Minimum inhibitory concentrations (MICs) or minimum effective concentrations (MECs) of different antifungal agents against Pleurostoma species.^a

Species	Strain	MICs/MECs (µg/mL)
		Triazoles						Echinocandins			Others
		FLC	ISA	ITC	POS	RAV	VRC	AFG	CAS	MFG	5FC	AMB
P. hongkongense	HKU44^T	>16	>16	>8	>8	>16	16	>16	16	>16	>16	0.5
P. repens	CBS 294.39^T	16	1	0.5	0.5	1	0.25	4	2	16	>16	0.25
P. richardsiae	ATCC 58041	>16	4	>8	1	4	2	>16	16	>16	>16	1
	ATCC 58116	>16	>16	>8	>8	>16	>16	>16	16	>16	>16	2
	CBS 270.33^T	>16	1	0.5	0.25	1	2	4	8	>16	>16	0.5
	CBS 271.66	>16	2	0.5	2	2	4	>16	16	>16	>16	1
	CBS 406.93	>16	>16	>8	>8	>16	>16	>16	16	>16	>16	2
	CBS 483.80	>16	>16	>8	>8	>16	>16	>16	>16	>16	>16	2
	CBS 506.90	>16	4	8	1	8	2	>16	4	>16	>16	2
	IFM 4926	>16	4	1	1	4	2	>16	16	>16	>16	1
	IFM 41579	>16	4	>8	8	4	4	2	8	>16	>16	1
	IFM 63001	>16	>16	>8	>8	>16	>16	>16	16	>16	>16	2
	IFM 63541	>16	>16	8	8	16	>16	4	8	2	>16	1
	UAMH 4377	>16	2	1	1	2	1	>16	16	>16	>16	1
	UAMH 5052	>16	>16	>8	>8	>16	>16	>16	8	>16	>16	1
	UAMH 5056	>16	2	1	1	4	4	>16	16	>16	>16	0.5
	UAMH 5058	>16	2	>8	>8	>16	1	4	4	>16	>16	1
	UAMH 8335	>16	>16	>8	>8	>16	8	>16	8	>16	>16	2
	UAMH 8654	>16	>16	>8	>8	>16	>16	>16	16	>16	>16	2
	UAMH 10082	>16	16	>8	>8	>16	16	>16	8	>16	>16	2
	UAMH 10452	>16	16	8	8	16	16	>16	8	>16	>16	1
	NCPF 2707	>16	8	>8	8	4	8	>16	2	>16	>16	1
	NCPF 2752	>16	4	2	1	4	4	>16	16	>16	>16	2
	NCPF 2765	>16	>16	>8	>8	>16	>16	>16	1	>16	>16	4
	NCPF 2961	>16	8	>8	8	4	2	>16	8	>16	>16	1
	NCPF 7565	>16	>16	>8	>8	>16	>16	>16	4	>16	>16	1
P. ochraceum	CBS 131321^T	4	0.5	0.25	0.25	0.5	0.5	4	0.5	4	>16	1
P. ootheca	CBS 115329	>16	16	>8	1	8	8	>16	8	>16	>16	1

^a AFG, anidulafungin; AMB, amphotericin B; CAS, caspofungin, FLC, fluconazole; ISA, isavuconazole; ITC, itraconazole; MFG, micafungin; POS, posaconazole; RAV, ravuconazole; VRC, voriconazole; 5FC, flucytosine.

Table 2. Microscopic features of different Pleurostoma species during asexual life cycles.

Species	Hyphae	Phialides	Conidia
P. hongkongense	2–6 μm wide, septate, verruculose, and hyaline	3–30 μm long, phialide variety similar to P. ochraceum	Microconidia 2–8 μm long, spherical, ellipsoidal or oblong; macroconidia most commonly allantoid and reniform
P. repens	2–4 μm wide, septate, smooth and initially hyaline, pale brown when matured	6–30 μm long, inconspicuous, slightly flared collarrettes on elongated phialides, conidiophores often branched	3–6 μm long, cylindrical to allantoid only
P. richardsiae	2–4 μm wide, septate and smooth when young, heavily septated, thick-walled and brown when matured	10–35 μm long, flask shaped with distinct saucer-shaped flared collarette at apex	2–6 μm long, commonly spherical or ellipsoidal
P. ochraceum	1.2–3.2 μm wide, branched, septate, smooth and verruculose	6–20 μm long, three types of phialides described: type 1 adelophialides, type 2 elongate-ampulliform, and larger, longer type 3 cyclindrical/ampulliform phialides	1.5–6 μm long, melanised sub-spherical or ellipsoidal
P. ootheca	1.8–3.3 μm wide, septate and hyaline	6–19 μm long, inconspiciously flared collarettes, short phialides	3–6 μm long, most commonly oblong, straight, or allantoid; shorter and ellipsoid conidia also present

The asexual morph of P. candollei is not known [2]. Data for P. hongkongense were obtained in this study, data for the other Pleurostoma species were cited from the literature [18, 26, 55].

Table 3. Infections caused by Pleurostoma species.

Case	Sex^a/Age (year)	Ethnicity	Underlying medical conditions	Clinical syndrome	Isolation source	Fungal species	Antifungal treatment	Outcome	Reference
1	M/80	American	Congestive heart failure	Subcutaneous cystic mass on proximal interphalangeal joint of left fifth finger	Cyst fluid	P. richardsiae	Surgical excision	Remission	[12]
2	F/50	German	Not mentioned	Dacryocystitis	Lacrimal sac stone	P. richardsiae	Surgical excision	Remission	[36]
3	M/79	African American	None	Chronic bursitis on right elbow	Cystic mass	P. richardsiae	Surgical excision	Remission	[31]
4	M/65	American Puerto Rican	Diabetes mellitus	Right foot sole lesion	Purulent fluid from lesion	P. richardsiae	Surgical excision and drainage	Remission	[13]
5	M/43	American Jamaican	Diabetes mellitus, adrenocortical carcinoma, multiple hepatic metastases	Ulcerative lesion on right leg	Lesion discharge	P. richardsiae	Not mentioned	Deceased	[13]
6	M/52	American	None	Subcutaneous lesion on left index finger	Subcutaneous mass	P. richardsiae	Surgical excision	Remission	[7]
7	F/70	American	Myeloproliferative disease	Osteomyelitis of right foot	Bone	P. richardsiae	Debridement of infected bone, amphotericin B for 1 week followed by flucytosine for 2.5 weeks	Deceased due to subsequent disseminated Nocardia infection	[32]
8	M/54	American	Tendinitis, received methylprednisolone injection	Subcutaneous mass on right dorsal index finger	Not mentioned	P. richardsiae	Surgical excision	Not mentioned	[14]
9	M/30	Malaysian Indian	Left femur fracture with skeletal traction and intramedullary nailing	Cutaneous lesions over left lower tibia & ankle	Lesion biopsy	P. richardsiae	Oral griseofulvin and topical naftifine for three weeks, surgical excision five months after recurrence	Persisted for two more months and then lost to follow-up	[15]
10	M/47	French Senegalese	Hepatitis B virus carrier, recurrent duodenal ulcer	Cutaneous nodule at right patella	Cystic mass biopsy	P. richardsiae	Surgical excision	Remission	[16, 20]
11	M/30	Japanese	Non-Hodgkin’s lymphoma, steroid-induced diabetes mellitus, osteoporosis	Subcutaneous abscess on right dorsal foot	Pus	P. richardsiae	Oral flucytosine, topical amphotericin B & surgical excision	Deceased due to disseminated intravascular coagulation	[17]
12	F/60	American	Hypertension, diabetes mellitus, atherosclerotic heart disease, obesity	Subcutaneous cystic nodule on left medial foot	Cyst aspirate	P. richardsiae	Surgical excision	Remission	[18]
13	M/64	Australian	Polymyalgia rheumatica, on prednisone & azathioprine therapy	Cutaneous nodules on right knee, right thigh and elbows	Skin biopsy	P. richardsiae & Exophiala jeanselmei	Oral flucytosine for 10 days, then ketoconazole for 1 week, then itraconazole for 3 months	Remission	[19]
14	M/39	French	Renal transplant	Knee bursitis	Not mentioned	P. richardsiae	Surgical drainage and antifungal therapy, then surgical excision after recurrence	Not mentioned	[20]
15	F/15	Indian	None	Cutaneous lesion near waistline	Skin scrapings & biopsy	P. richardsiae	Topical clotrimazole for 15 days	Remission	[8]
16	F/50	Indian	None	Cutaneous lesion near waistline	Skin scrapings & biopsy	P. richardsiae	Topical clotrimazole for 15 days	Remission	[8]
17	M/52	British	Diabetes mellitus, porcine mitral valve replacement	Endocarditis & fungaemia	Blood, aortic & porcine mitral valves	P. richardsiae	Aortic and mitral valves replacement, amphotericin B for nearly 6 weeks	Deceased	[39]
18	M/54	British Afro-Caribbean	Renal transplant, hypertension, steroid-induced diabetes mellitus	Cutaneous lesions on right ring finger & left knee	Pus	P. richardsiae	Surgical excision	Remission	[21]
19	M/28	French	HIV, hepatitis C, intravenous drug use, tuberculosis, orthopaedic reconstructive surgery of right foot	Osteomyelitis	Bone aspirates of left elbow & left foot	P. richardsiae	Amphotericin B and flucytosine followed by itraconazole	Not mentioned	[33]
20	M/41	American	Surgical left ankle bone chip removal	Left ankle osteomyelitis	Surgical debridement specimens	P. repens	Surgical debridement, amphotericin B, oral ketoconazole for several months	Remission	[34]
21	M/36	American	Metallic intraocular foreign body	Right eye endophthalmitis	Vitreous samples	P. richardsiae	Pars plana vitrectomy and ketoconazole, followed by a repeat vitrectomy with intraocular lens removal, intravitreal amphotericin B and miconazole	Recurred after 12 months post-second vitrectomy	[37]
22	M/77	American	None	Septic infrapatellar bursitis & contiguous cellulitis	Bursal & superficial pustule aspirates, skin punch biopsy	P. richardsiae	Intravenous amphotericin B for 2 weeks, followed by oral itraconazole for 3 months	Remission	[22]
23	M/45	New Zealander	Renal transplant, transplant-related diabetes mellitus	Subcutaneous left foot abscess	Lesion aspirates, tissues	P. richardsiae	Surgical excision and liposomal amphotericin B for 1 week, repeat debridement & liposomal amphotericin B for 2 weeks followed by itraconazole for 6 weeks after recurrence	Remission	[23]
24	M/59	Japanese	Liver cirrhosis, hepatocellular carcinoma, hepatitis C	Eumycetoma on left foot	Lesion biopsy	P. richardsiae	Surgical excision	Remission	[24]
25	M/43	Korean	None	Right shin chromoblastomycosis	Skin tissue biopsy	P. richardsiae	Oral itraconazole 3 months, then combined with terbinafine for 3 months	Remission	[25]
26	M/60	Sudanese	None	Yellow-grain eumycetoma on right foot	Grains	P. ochraceum	Surgical debulking	Lost to follow-up	[26]
27	M/54	Canadian	None	Subcutaneous nodule on right patella & prepatellar bursitis	Prepatellar fluid aspirate	P. richardsiae	Therapy declined by patient	Lost to follow-up	[9]
28	M/59	Martinican	Renal transplant	Left ankle abscess	Cutaneous tissue	P. ootheca	Itraconazole for 1.5 months, then posaconazole for 2 months	Remission	[27]
29	M/43	American	Alcoholic cardiomyopathy, porcine mitral valve replacement, intravenous drug abuse, on systemic corticosteroid therapy	Endogenous endophthalmitis of right eye associated with osteomyelitis and endocarditis	Vitreous biopsy	P. richardsiae	Intravitreal amphotericin B during initial diagnostic vitrectomy, topical natamycin & intravenous amphotericin B, intravenous voriconazole added later, followed by repeat vitrectomy and intravitreal amphotericin B	Deceased due to massive intracranial haemorrhage	[35]
30	F/75	Dutch Chinese	Diabetes mellitus, chronic kidney disease, rheumatoid arthritis	Left arm infection	Pus and wound	P. richardsiae	Voriconazole for 6 months, repeated surgical eradication, discontinuation of immunosuppression	Deceased due to subsequent progressive multifocal leukoencephalopathy due to Human polyomavirus 2 reactivation	[28]
31	M/78	Japanese	Diabetes mellitus, prostate & bladder cancers, myelodysplastic syndrome	Subcutaneous cyst on right crus	Pus	P. richardsiae	Local heat therapy with disposable chemical pocket warmers for 2 months, then combined with intracutaneous amphotericin B for 3 months	Deceased due to cancers	[29]
32	F/35	Indian	None	Perilacrimal organised lesion with transient nasolacrimal duct obstruction	Perilacrimal mass	P. richardsiae	Surgical excision	Remission	[10]
33	M/72	Turkish	Papillary urothelial carcinoma	Urinary tract infection	Urine	P. richardsiae	Amphotericin B for 4 days followed by itraconazole for 14 days	Remission	[38]
34	M/78	Spaniard	None	Subcutaneous cyst nodule on right dorsal hand	Cyst biopsy	P. richardsiae	Therapy declined by patient	Not mentioned	[30]
35	M/57	Thai	Hepatitis B virus-related cirrhosis, liver transplant	Fungaemia associated with hepatic artery and portal vein thrombosis	Blood and liver blood clot	P. richardsiae	Second liver transplant, amphotericin B for 4 weeks	Remission	[40]
36	M/74	Singaporean Chinese	Renal transplant, bronchiectasis	Subcutaneous thigh nodules	Skin biopsy and pus	P. richardsiae	Surgical excisions, itraconazole for 10 months	Remission	[11]
37	M/65	Hong Kong Chinese	Hepatitis B virus-related liver failure, liver transplant	Progressive liver failure	Subhepatic abscess pus and drain fluids	P. hongkongense	Second liver transplant, amphotericin B and voriconazole	Remission	Present case

^a F, female; M, male.

Note: The fungal strains (UTMB 184 = CBS 423.75 [60] and SM 3531 = ATCC 58115 = BB 903 = CBS 110366 [56, 57]) isolated from two reported cases of Pleurostoma repens were subsequently reidentified as Phaeoacremonium krajdenii by molecular studies [58].

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