Listeria monocytogenes-associated spontaneous bacterial peritonitis in France: a nationwide observational study of 208 cases - 10/04/24

Doi : 10.1016/S1473-3099(24)00151-8

Florian Blanchard, MD ^a,^b,^c, Benoît Henry, MD PhD ^a,^d, Sofieya Vijayaratnam ^a, Etienne Canouï, MD ^b, Alexandra Moura, PhD ^a,^e, Pierre Thouvenot ^a, Hélène Bracq-Dieye ^a, Nathalie Tessaud-Rita ^a, Guillaume Valès ^a, Andrée Diakité ^a, Alexandre Leclercq, MSc ^a, Marc Lecuit, ProfMD PhD ^a,^e,^f,^g,^{*
Joint senior authors}, ⁎ , Caroline Charlier, ProfMD PhD ^a,^b,^e,^f,^{*
Joint senior authors}⁎
on behalf of the
Listeria monocytogenes-associated Spontaneous Peritonitis Study Group^{^†}
Members are listed in Supplementary Materials)

Mohamed Abdou, Ayman Abdulhai, Ayman Abdulhal, Samy Abel, Armand Abergel, Saïd Aberrane, Bruno Abraham, Maxime Adler, Christian Agard, Ilhem Agha-Mir, Claire Aguilar, Baptiste Agulles, Hamza Aldallal, Laurent Alric, Xavier Amiot, Pierre Andrau, Vladimir Andrieux, Séverine Ansart, Rodolphe Anty, Isabelle Archambeaud, Samir Arem, Laurence Armand, Lucie Aubailly, Juliette Audibert, Olivier Auguereau, Christelle Auvray, Karime Aziz, Marie-Nadège Bachelier, Karine Bacquaert-Dufour, Françoise Badet, Mohamed-Larbi Bahallah, Hélène Balanant, Régine Baraduc, Alexandre Bardis, Olivier Barraud, Jocelyn Barrier, Antoine Baudet, Thomas Baumert, Laurent Beaugerie, Cécile Bébéar, Hakim Becheur, Pascale Bemer, Caroline Benard, Marie-Pierre Benezet, Mohammed Benmahammed, Jaafar Bennouna, Zehaira Benseddik, Pierre-Yves Bensimon, Abdeslam Bental, Aliou Berete, Jean-Michel Bergier, Wacila Berkani, Franck Bernardi, Frederic Bert, Anne Bertrou, Pascal Beuret, Isabelle Beurton-Chataigner, Claude Beuscart, Christine Beusnel, Sibylle Bevilacqua, François Beze, Karine Bideau, Frédéric Bidegain, Laura Billon, Gilles Blaison, Michèle Blanc, Pierre Blanc, Sophie Blanchi, Gilles Blancho, Stephane Bland, Vincent Blondeau, Amale Boldron, Djemah Bon, Stéphane Bonacorsi, Lucas Bonzon, Anaïs Borderon, Elisabeth Botelho-Nevers, Jacques Bottlaender, Mathilde Bouc-Boucher, Olivier Bouchaud, David Bougon, Khaled Boukelikha, Thomas Bourlet, Samy Boussoukaya, Hamza Boutaleb, Nicole Bouziges, Philippe Bray, Caroline Bréchet, Laurent Bret, Nathalie Brieu, David Briffaut, Christine Brochet, Stanislas Brulez-Des-Varannes, Valéry Brunel, Maud Brung-Lefebvre, Christophe Bureau, Christophe Burucoa, Louis Buscail, Rodolphe Buzele, Catherine Cadot, Jean-Francois Cadranel, Anne Cady, Jocelyne Caillon, Sabine Camiade, Bernard Campillo, Franck Carbonnel, Etienne Carbonnelle, Émilie Cardot-Martin, Marie-Estelle Cariou, Michel Carles, Francois Caron, Lucrecia Carrara-Delarue, Paul Carrier, Céline Castang, Inès Castellano, Vincent Cattoir, Olivier Caubet, Xavier Causse, Amélie Chabrol, Emmanuel Chanard, Thomas Chatagnon, Olivier Chazouilleres, Halima Chedanni, Pauline Chevrel, Catherine Chirol, Catherine Chirouze, Renaud Chouquer, Christophe Clavière, Sylvain Codreuil, Philippe Colardelle, François Combarnous, Grégory Commeau, Anne Cornillet, Stephane Corvec, Yannick Costa, Philippe Couderc, Caroline Couffon, Cécile Courivaud, Henri Courtade, Etienne Cruchant, David Cuen, Jean-François Culard, Hong Ahn Cung, Sandrine Dahyot, Louis D’Altéroche, Manh Thông Dao, Fabien Darfeuil, Céline Darnaud, Sophie Daure, Ludivine De Grossouvre-Taillefer, Dominique Debriel, Jacques Debrueres, Thomas Decaens, Audrey Decambron, Dominique Decre-Grapinet, Nicolas Degand, Bruno Dehaye, Thierry Delacour, Jean-Marie Delarbe, Pierre Delobel, Éric Delpierre, René Delrez, Didier Delvert, Sylvie Demartino, Marie-Clémence Deniel, Bernard Denis, Guy Derumeaux, Marine Desroches, Rodrigue Dessein, Simon Devillez, Didier Deweerdt, Sylvain Diamantis, Emmanuel Diaz, Raffenot Didier, Vincent Dimartino, Ludivine Dion, Mohand Djemai, Christophe Doche, Maud Donascimento, Ian Dorval, Carol Douala, Florence Doucet-Populaire, Valérie Drouillat, Vincent Dubée, Anne-France Dudermel, Betty Dumont, Clarisse Dupin, Mathieu Dupont, Philippe Dupont, Marion Dupuy, Jean-Pierre Dupuychaffray, Francois Durand, Pascale Dusser, Valérie Duval, Nicolas Duveau, Abdelghani El-Azouzi, Hynd El-Gharras, Antoine Elsendoorn, Loïc Emile, Olivier Epaulard, Nicolas Etchepare, Jean-Pierre Etienne, Mathieu Eveillard, Annie Evers, Joelle Fach, Claudia Faizoun, Marie-Sarah Fangous, Jean Pierre Farmachidi, Armelle Fatome, Bernard Faulques, Karine Faure, Charlotte Felix, Marc Ferec, Janine Ferey, Serge Ferracci, Jean-Marc Feryn, Pierre Fesler, Hélène Fiette, Emilie Flevin, Pauline Floch, Eric Fort, Nicolas Fortineau, Jacques Fourcade, François Fraissinet, Patricia Franck, Thiebaut Françoise, Serge Fratte, Jean-Marc Galempoix, Yves Garcera, Anne Garcia, Pierre Garcon, Charlotte Garret, Clement Gayet, Pierre Gazeau, Florence Gerber, Raclot Gilles, Jean-Michel Gillot, Eric Goarant, Sylvain Godreuil, Julien Goret, Julie Gorret, Cecile Goujard, Thiphaine Goulenok, Jérôme Gournay, Marie Gousseff, Alain Goux, Emmanuelle Graf, Jean-Didier Grange, Alain Gravet, Alix Greder-Belan, Olivier Gronier, Marine Grosset, Sabra Guellouz, Dalida Guenenna, Mohammed Guerbaa, Meggie Guerin, Dominique Guerrot, Benoit Guery, Jean Gugenheim, Bertrand Guidet, Raphael Guiheneuf, Christelle Guillet-Caruba, Yves Guimard, Jérome Guinard, Laure Guindre, Albert Hagege, Hervé Hagege, Paul-Arthur Haineaux, Rémy Hamon, Firas Hassan, Mélanie Hassine, Ludovic Helie, Anne Herber-Mayne, Pascale Hervio, Geneviève Héry-Arnaud, Hikombo Hitoto, Théophile Hubsch, Nicolas Hunaut, Monika Hurtova, Stéphanie Husson-Wetzel, Pascal Hutin, Théo Izopet, Jean-Louis Jacob, Christine Jacomet, Marie-Christine Jaffar-Bandjee, Fréderic Janvier, Benoît Jaulhac, Stephane Jaureguiberry, Nicolas Javaud, Katty Jeannot, Noureddine Joundy, Moez Kacem, Rouis Karama, David Karsenti, Marie Kempf, Sarah Khatibi, Florence Kikolski, Christine Kittirath, Stephane Koch, Tchamba Kouatchet-Achille, Yves Krummel, Karine La Combe, Damien Labarriere, Jean-Eric Laberenne, Hervé Lacroix, Laure Ladrat, Stéphanie Lagarde, Jean-Paul Lagasse, Ahmed-Saïd Laggoune, Benedicte Lambare, Nathalie Landgraf, Luce Landraud, Jean-Francois Laude, François Laurent, Jean-Philippe Lavigne, Vincent Lavoue, Rozenn Le Berre, Vallérie Le Goff, Hervé Lebars, Hervé Lebars, Armandine Lebrun, Anne-Lise Lecapitaine, Sylvie Lechat, Alain Lecoustumier, Gérard Ledreau, Benjamin Lefevre, Véronique Leflon, Agnès Lefort, Florence Legall, Isabelle Legoff, Eric Legrand, Simon Lehello, Catherine Le-Henaff-Bourhis, Olivier Leleu, Lucie Lelievre, Adrien Lemaignen, Xavier Lemaire, Charles Le-Maout, Chantal Lemblé, Yolande Lemeille, Olivier Lemenand, Violaine Lemeunier, Yannick Lemeur, Sylvia Lemierre, Sophie Leotard, Lucie Lepileur, Claire Letellier-Demonchy, Hervé Levecq, Marc Levy, Nicolas Limal, Christophe Locher, Benjamin Lopez, Marie-Charlotte Loron, Joelle Loulergue, Isabelle Loury-Larivière, Véronique Loustaud-Ratti, Véronique Loustaud-Ratti, Valèrie Macchi, Moise Machado, Serge Madaule, Jean-Luc Mainardi, Silvija Males, Philippe Malherbe, Benjamin Maneglier, Maryline Marceau, Kévin Marcel, Alain Marmonier, Benoît Martha, Xavier Martin, Guillaume Martin-Blondel, Camille Martinez, Fabrice Marty, Patrick Marty, Olivier Matray, Arnaud Maurin, Sandie Mazerand, Nadia Mazouz, Muriel Medevielle, Alain Mercat, Laurent Méreghetti, Noureddine Merzoug, Ilham Meziane, Anthony Michaud, Marc Michel, Pierre Michel, Sophie Mignard, Anne-Marie Milesi-Lecat, Mathieu Mion, Nabil Mnasri, Abdo Mohareb, Samir Mohib, Henri Moindrot, Eric Monlun, Audrey Montewis, Thierry Morin, Driffa Moussata, Sandrine Muller, Valérie Muzellec, Stéphane Nancey, Ahmad Nassereddine, Sebastien Naude, Didier Neau, Negru Calin Ovidiu, Thuy Ngo, Marthe-Andree Ngwhotue, Patrick Nivet, Patrice Nordmann, Jean-Baptiste Nousbaum, Bernadette Nouvel, Stephane Obled, Eric Oswald, Marie-Pierre Otto, Georges-Philippe Pageaux, Gregory Papin, Fabrice Parant, Arnaud Patenotte, Thierry Paupard, Arnaud Pauwels, Jean Michel Pawlotsky, Hervé Pelloux, Gabriel Perlemuter, Jean-Marie Peron, Martine Pestel-Caron, Natasha Peter, Sophie Petillon, Richard Petit, Helene Petitprez, Francois Pettinelli, Jean Marc Phelip, Jean-Baptiste Philit, Valérie Phoutthasang, Gilles Pialoux, Caroline Piau-Couapel, Benoit Pichard, Maxime Pichon, Magali Picon-Coste, Marie Picque, Henri Pierson, Jean Francois Piques, Béatrice Piton, Orianne Planade, Claire Plassart, Patrick Plésiat, Marie-Cécile Ploy, Patrice Poubeau, Philippe Pouderoux, Pascal Pouedras, Annabelle Pourbaix, Thierry Poynard, Florence Preau, Dumitrita Pricope, Gwenaëlle Queffelec, Lucille Queneherve, Thomas Quentin, Didier Raffenot, Daniella Rakotoniaina, Celine Ramanantsoa, Solofoniaina Ramarijaona, Lila Rami-Arab, Olivia Raulin, Jean Michel Rebibou, David Renault, Philippe Rey, Agnès Riche, Jean Philippe Rigaud, Antoine Rivière, Brigitte Rivière, Jérôme Robert, Pascal Roblot, Helene Roger, Christophe Rolland, Emilie Rondinaud, Isabelle Rosa-Hezode, Martine Roubille, Olivier Rouquette, Juliette Roux, Raymond Ruimy, Sonia Sachot-Ollivier, Laurent Sailler, Sarah Salamant, Silvia Sarbu-Pop, Jacques Sartre, François Schmitt, Myriam Scribe-Outtas, David Sefrioui, Rachid Sehouane, Hacène Sekhri, Lawrence Serfaty, Odile Sevin, Cédric Shawali, Souad Siladi, Christine Silvain, Mireille Simon, Batiste Simonet, Leila Sinayoko, Estelle Sirach, Mustafa Smati, Aurélie Smets, Dhaoui Soltani, André Sommabere, Karine Soulier-Guerin, Jean Paul Soulillou, Alain Soupison, Laurent Souply, Claude-James Soussy, Claire Stampfli, Bernard Strullu, Diana Suatean, Nacer Tadjerouni, Jean-Philippe Talarmin, Jacques Tankovic, Abdullah Tarroun, Juliette Tchuenbou, Jean-Louis Teboul, Husni Tedlaouti, Charlotte Tellini, Dominique Thabut, Philippe Thannberger, Henri Thiebault, Françoise Thiebaut, Joséphine Thomazeau, Guillaume Tielman, Jean-Francois Timsit, Patrick Tognon, David Tougeron, Fatouma Toure, Albert Tran, Jean-Luc Tranvouez, Christophe Trésallet, Lise Trubert, Laurent Tsakiris, Eterne Twizeyimana, Anne Vachee, Hélène Valade, Isabelle Valat, Anne Vandendriessche, Nathalie Vandermee, Marc Vanheste, Emmanuelle Varon, Marc Vasse, Philippe Vasseur, Elisabeth Vaucel, Anne Vauthier, Delphine Verdavaine-Loidreau, Charlotte Verdet, Renaud Verdon, Michel Vergnaud, Nicolas Véziris, Guillaume Vignaud, Jérôme Viguier, Marc Villemain, Laurent Villeneuve, Alexandre Vimont-Vicary, Thomas Vincent, Jean-Baptiste Vuillemenot, Violaine Walewski, Elodie Warmoes, Hélène Watry, Jean-Christophe Weber, Marie Thérèse Witz, Paul-Louis Woerther, Yazdan Yazdanpanah, Oana Zamfir, Jonathan Zarka, Patrick Zavadil, Nabil Zeboudj, Franck Zerbib

^a Listeria National Reference Center and WHO Collaborating Center, Institut Pasteur, Paris, France

^b Antibiotic stewardship team, Department of Infectious Diseases and Tropical Medicine, Cochin Port-Royal University Hospital, APHP, Paris, France

^c Department of Anesthesiology and Critical Care Sorbonne University, GRC 29, AP-HP, DMU DREAM, Pitié-Salpêtrière Hospital, Paris, France

^d Division of Infectious Diseases and Tropical Medicine, Bicêtre University Hospital, APHP, Le Kremlin-Bicêtre, France

^e Biology of Infection Unit, Institut Pasteur, Université Paris Cité, Inserm U1117, Paris, France

^f Université Paris Cité, Paris, France

^g Department of Infectious Diseases and Tropical Medicine, Necker-Enfants Malades University Hospital, APHP, Institut Imagine, Paris, France

^* Correspondence to: Prof Caroline Charlier, Biology of Infection Unit, Institut Pasteur, Université Paris Cité, Inserm U1117 75015 Paris, France Biology of Infection Unit Institut Pasteur Université Paris Cité Inserm U1117 75015 Paris France ^** Prof Marc Lecuit, Biology of Infection Unit, Institut Pasteur, Université Paris Cité, Inserm U1117 75015 Paris, France Biology of Infection Unit Institut Pasteur Université Paris Cité Inserm U1117 75015 Paris France

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Summary

Background

Listeriosis is a foodborne infection caused by Listeria monocytogenes. Three main forms of listeriosis are well characterised, but little is known about L monocytogenes-associated spontaneous bacterial peritonitis. We used data from the French national surveillance of listeriosis to perform a nationwide retrospective study.

Methods

All patients with L monocytogenes isolated by culture from a peritoneal fluid sample in France between April 1, 1993, and Dec 31, 2022, were included. Individuals for whom bacterial peritonitis was not confirmed and those who also had another type of invasive listeriosis were excluded. A standardised checklist was used to collect demographic, clinical, and biological data as well as antibiotic treatment and follow-up data. The primary outcome was to determine the characteristics of L monocytogenes-associated spontaneous bacterial peritonitis. We did descriptive analyses and assessed risk factors for 1-month mortality using an exploratory multivariable Cox model analysis.

Findings

Among the 8768 L monocytogenes cases reported, 208 (2%) were patients with L monocytogenes-associated spontaneous bacterial peritonitis. Mean age was 65 years (SD 13), 50 (24%) of 208 patients were female, and 158 (76%) were male (no data on race or ethnicity were available). 200 (98%) of 205 patients with L monocytogenes-associated spontaneous bacterial peritonitis with available data had immunosuppressive comorbidities, including cirrhosis (148 [74%] of 201 with available data), ongoing alcoholism (58 [62%] of 94), and ongoing neoplasia (60 [31%] of 195). Causes of ascites included cirrhosis (146 [70%] of 208), ongoing neoplasia (26 [13%]), end-stage heart failure (13 [6%]), and peritoneal dialysis (11 [5%]). Among those with available data, presentation was pauci-symptomatic and non-specific; only 67 (50%) of 135 patients presented with fever, 49 (37%) of 132 with abdominal pain, and 27 (21%) of 129 with diarrhoea. 61 (29%) of 208 patients were dead at 1 month, 92 (44%) were dead at 3 months, and 109 (52%) were dead at 6 months after diagnosis. Ongoing neoplasia (hazard ratio 2·42 [95% CI 1·05–5·56]; p=0·039), septic shock (8·03 [2·66–24·02]; p=0·0021), and high blood leukocyte count (1·05 [1·00–1·09]; p=0·045) were independently associated with 1-month mortality.

Interpretation

Despite the non-specific and mild presentation of L monocytogenes-associated spontaneous bacterial peritonitis, the outcome is poor and similar to that of neurolisteriosis, and so identification of L monocytogenes in ascitic fluid samples requires urgent parenteral amoxicillin-based treatment to avoid a fatal outcome.