. 2024 Aug 7:45:101010.

doi: 10.1016/j.lanepe.2024.101010. eCollection 2024 Oct.

Epidemiology and prognostic factors of mucormycosis in France (2012-2022): a cross-sectional study nested in a prospective surveillance programme

Laura Gouzien^{1

2}, Didier Che³, Sophie Cassaing⁴, Olivier Lortholary^{1

5}, Valérie Letscher-Bru^{6

7}, Olivier Paccoud⁵, Thomas Obadia^{1

8}, Florent Morio⁹, Maxime Moniot¹⁰, Estelle Cateau¹¹, Marie Elisabeth Bougnoux^{12

13}, Taieb Chouaki¹⁴, Lilia Hasseine¹⁵, Guillaume Desoubeaux^{16

17}, Cecile Gautier¹, Caroline Mahinc-Martin¹⁸, Antoine Huguenin^{19

20}, Julie Bonhomme²¹, Karine Sitbon¹, Julien Durand³, Alexandre Alanio^{1

22}, Laurence Millon^{23

24}, Dea Garcia-Hermoso¹, Fanny Lanternier^{1

5}; French Mycoses Study Group

Affiliations

¹ Institut Pasteur, Paris Cité University, National Reference Center for Invasives Mycoses and Antifungals, Mycology Department, Paris, France.
² Intensive Care Unit, Centre Hospitalier de Versailles, Le Chesnay, France.
³ Sante Publique France, France.
⁴ Department of Parasitology and Mycology, CHU Toulouse, Restore Institute, Toulouse, France.
⁵ Paris Cité University, Necker-Enfants Malades University Hospital, Necker-Pasteur Center for Infectious Diseases and Tropical Medicine, Assistance Publique-Hôpitaux de Paris (AP-HP), France.
⁶ Parasitology and Medical Mycology Laboratory, Plateau Technique de Microbiologie, Strasbourg University Hospitals, Strasbourg, France.
⁷ Institute of Parasitology and Tropical Pathology, UR 3073 Pathogens-Host-Arthropods-Vectors Interactions, Strasbourg University, Strasbourg, France.
⁸ Institut Pasteur, Bioinformatics and Biostatistics Hub, Université Paris Cité, Paris 75015, France.
⁹ Nantes University, CHU Nantes, Cibles et Médicaments des Infections et de l'Immunité, UR1155, Nantes, France.
¹⁰ Parasitology-Mycology Department, Biology Center, Hôpital Gabriel Montpied, Clermont-Ferrand, France.
¹¹ Mycology Laboratory, CHU de Poitiers, UMR CNRS 7267, Poitiers, France.
¹² Parasitology-Mycology Laboratory, AP-HP, Hôpital Necker, Paris, France.
¹³ Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, Paris Cité INRAE University, Paris, France.
¹⁴ Mycology-Parasitology, CHU d'Amiens, Amiens, France.
¹⁵ Parasitology-Mycology Laboratory, Centre Hospitalier Universitaire de Nice, Nice, France.
¹⁶ Parasitology-Mycology-Tropical Medecine, Hôpital Bretonneau, Tours, France.
¹⁷ Centre d'Etude des Pathologies Respiratoires - Inserm UMR1100, Medecine Univeristy, Tours, France.
¹⁸ Mycology Parasitology Department, Centre Hospitalier Universitaire de Saint Etienne, Saint Etienne, France.
¹⁹ Reims Champagne Ardenne University, ESCAPE EA7510, Reims, France.
²⁰ Parasitology-Mycology Laboratory, Pôle de Biologie Pathologie, CHU de Reims, Reims, France.
²¹ Parasitology-Mycology Department, CHU Caen, ToxEMAC-ABTE, Université de Normandie Unicaen, France.
²² Parasitology-Mycology Laboratory, AP-HP, Hôpital Saint-Louis, Paris, France.
²³ Parasitology-Mycology Department, Besançon University Hospital, Besançon, France.
²⁴ Chrono-environnement UMR6249, CNRS, Franche-Comté University, Besançon F-25000, France.

PMID: 39220434
PMCID: PMC11363841
DOI: 10.1016/j.lanepe.2024.101010

Epidemiology and prognostic factors of mucormycosis in France (2012-2022): a cross-sectional study nested in a prospective surveillance programme

Laura Gouzien et al. Lancet Reg Health Eur. 2024.

. 2024 Aug 7:45:101010.

doi: 10.1016/j.lanepe.2024.101010. eCollection 2024 Oct.

Authors

Affiliations

¹ Institut Pasteur, Paris Cité University, National Reference Center for Invasives Mycoses and Antifungals, Mycology Department, Paris, France.
² Intensive Care Unit, Centre Hospitalier de Versailles, Le Chesnay, France.
³ Sante Publique France, France.
⁴ Department of Parasitology and Mycology, CHU Toulouse, Restore Institute, Toulouse, France.
⁵ Paris Cité University, Necker-Enfants Malades University Hospital, Necker-Pasteur Center for Infectious Diseases and Tropical Medicine, Assistance Publique-Hôpitaux de Paris (AP-HP), France.
⁶ Parasitology and Medical Mycology Laboratory, Plateau Technique de Microbiologie, Strasbourg University Hospitals, Strasbourg, France.
⁷ Institute of Parasitology and Tropical Pathology, UR 3073 Pathogens-Host-Arthropods-Vectors Interactions, Strasbourg University, Strasbourg, France.
⁸ Institut Pasteur, Bioinformatics and Biostatistics Hub, Université Paris Cité, Paris 75015, France.
⁹ Nantes University, CHU Nantes, Cibles et Médicaments des Infections et de l'Immunité, UR1155, Nantes, France.
¹⁰ Parasitology-Mycology Department, Biology Center, Hôpital Gabriel Montpied, Clermont-Ferrand, France.
¹¹ Mycology Laboratory, CHU de Poitiers, UMR CNRS 7267, Poitiers, France.
¹² Parasitology-Mycology Laboratory, AP-HP, Hôpital Necker, Paris, France.
¹³ Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, Paris Cité INRAE University, Paris, France.
¹⁴ Mycology-Parasitology, CHU d'Amiens, Amiens, France.
¹⁵ Parasitology-Mycology Laboratory, Centre Hospitalier Universitaire de Nice, Nice, France.
¹⁶ Parasitology-Mycology-Tropical Medecine, Hôpital Bretonneau, Tours, France.
¹⁷ Centre d'Etude des Pathologies Respiratoires - Inserm UMR1100, Medecine Univeristy, Tours, France.
¹⁸ Mycology Parasitology Department, Centre Hospitalier Universitaire de Saint Etienne, Saint Etienne, France.
¹⁹ Reims Champagne Ardenne University, ESCAPE EA7510, Reims, France.
²⁰ Parasitology-Mycology Laboratory, Pôle de Biologie Pathologie, CHU de Reims, Reims, France.
²¹ Parasitology-Mycology Department, CHU Caen, ToxEMAC-ABTE, Université de Normandie Unicaen, France.
²² Parasitology-Mycology Laboratory, AP-HP, Hôpital Saint-Louis, Paris, France.
²³ Parasitology-Mycology Department, Besançon University Hospital, Besançon, France.
²⁴ Chrono-environnement UMR6249, CNRS, Franche-Comté University, Besançon F-25000, France.

PMID: 39220434
PMCID: PMC11363841
DOI: 10.1016/j.lanepe.2024.101010

Abstract

Background: Mucormycosis is a deadly invasive fungal infection recently included in the WHO priority pathogen list. Here we sought to describe epidemiological trends of mucormycosis in France, and to evaluate factors associated with mortality.

Methods: From 2012 to 2022, we implemented a nationwide prospective surveillance programme for mucormycosis in France, focusing on epidemiology, species, seasonal variations. Factors associated with 3-month mortality were studied by univariable and multivariable logistic regression.

Findings: Among 550 cases of mucormycosis, the main underlying conditions were haematological malignancy (HM, 65.1%, 358/550), trauma (8%, 44/550), diabetes (7.5%, 41/550) and solid-organ transplants (6.5%, 36/550). Site of infection was pulmonary in 52.4% (288/550), rhinocerebral in 14.5% (80/550), and cutaneo-articular in 17.1% (94/550). Main species identified were Rhizopus arrhizus (21%, 67/316), Rhizopus microsporus (13.6%, 43/316), Lichtheimia corymbifera and Mucor circinelloides (13.3%, 42/316 each), Rhizomucor pusillus (12%, 38/316), and Lichtheimia ramosa (10.8%, 34/316). We found associations between underlying condition, site of infection, and infecting species, including a previously undescribed triad of trauma, cutaneo-articular localisations, and L. ramosa/M. circinelloides. Diagnostic contribution of Polymerase Chain Reaction (PCR) increased from 16% (4/25) in 2012 to 91% (61/67) in 2022, with more than 50% of diagnoses relying solely on PCR in 2022. We also found seasonal variations with relatively more cases in autumn. Ninety-day mortality was 55.8% (276/495). Independent prognostic factors were age, diagnosis in Intensive Care Unit (ICU), and HM while diagnosis after 2015 (i.e. large implementation of PCR) and surgery were associated with reduced mortality.

Interpretation: This study reveals major mucormycosis epidemiological changes in France, with a large predominance of HM patients, and a parallel between PCR multicentre implementation and improved prognosis. We also evidence new associations between species, localisations and risk factors, as well as seasonal variations.

Funding: Recurrent financial support from Santé Publique France and Institut Pasteur.

Keywords: Epidemiology; Fungal infection; Mucorales; Mucormycosis; Mucormycosis serum PCR; Zygomycosis.

PubMed Disclaimer

Conflict of interest statement

SC reports travel grants for congresses for Gilead and Pfizer. GD reports being a speaker for Gilead. LM reports personal travel grants for Gilead and Pfizer. FL reports being a speaker for MSD and F2G board. AA reports educational lecture and travel grant from Gilead. Other authors declare no competing interests.

Figures

**Fig. 1**
**Mucormycosis cases distribution (n = 550).** Legend: Type: cases type, defined as Proven, Probable, or Putative (putative: cases diagnosed with at least one PCR-positive serum or broncho-alveolar lavage (BAL) sample (excluding proven or probable cases)). PCR +: cases with at least one PCR-positive sample; PCR −: cases without any PCR-positive sample.

**Fig. 2**
**Interplays between species, localization and main underlying disease. a** Proportion of species involved according to main underlying disease; b Proportion of species involved according to localization; c Proportion of main underlying disease according to localization; d Proportion of localization according to main underlying disease e. Proportion of main underlying disease according to species; f Proportion of localization according to species.

**Fig. 3**
**Seasonality of mucormycosis diagnosis. a**—Number of cases per month; b—species plotted by month c—localization plotted by month.

**Fig. 4**
**90 Day survival. a**–according before and after 2015, b–according to main underlying disease.

See this image and copyright information in PMC

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Epidemiology and prognostic factors of mucormycosis in France (2012-2022): a cross-sectional study nested in a prospective surveillance programme

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Epidemiology and prognostic factors of mucormycosis in France (2012-2022): a cross-sectional study nested in a prospective surveillance programme

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Abstract

Conflict of interest statement

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