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Actinomycetoma caused by Gordonia westfalica: first reported case of human infection
Journal Pre-proof Actinomycetoma caused by Gordonia westfalica: first reported case of human infection Romain Gueneau, Denis Blanchet, Veronica Rodriguez-Nava, Emmanuelle Bergeron, Marie Soulier, Nassim Bestandji, Magalie Demar, Pierre Couppie, Romain Blaizot PII:
S2052-2975(20)30010-X
DOI:
https://doi.org/10.1016/j.nmni.2020.100658
Reference:
NMNI 100658
To appear in:
New Microbes and New Infections
Received Date: 27 October 2019 Revised Date:
8 January 2020
Accepted Date: 10 February 2020
Please cite this article as: Gueneau R, Blanchet D, Rodriguez-Nava V, Bergeron E, Soulier M, Bestandji N, Demar M, Couppie P, Blaizot R, Actinomycetoma caused by Gordonia westfalica: first reported case of human infection, New Microbes and New Infections, https://doi.org/10.1016/j.nmni.2020.100658. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.
Letter to the Editor
Actinomycetoma caused by Gordonia westfalica: first reported case of human infection
Key words: Mycetoma; Actinomyces; Spectrum analysis; Neglected Tropical Disease; Gordonia Word count: 499 Figures: 1
Romain Gueneau 1 Denis Blanchet 2 Veronica Rodriguez-Nava 3 Emmanuelle Bergeron 3 Marie Soulier 4 Nassim Bestandji 5 Magalie Demar 2,6 Pierre Couppie 1,6 Romain Blaizot 1,6 1: Dermatology Department, Hôpital Andrée Rosemon, Cayenne, French Guiana 2: Laboratory of Parasitology and Mycology, Hôpital Andrée Rosemon, Cayenne, French Guiana 3: UMR CNRS 5557, Center for Microbial Ecology, Observatoire Français des Nocardioses, Laboratoire de Mycologie Fondamentale et Appliquée aux Biotechnologies Industrielles, Faculté de Pharmacie, Université Claude Bernard Lyon I, Lyon, France. 4: Pathologistes associés, Martigues, France 5: Orthopaedics Department, Hôpital Andrée Rosemon, Cayenne, French Guiana 6: EA 3593 Ecosystèmes Amazoniens et Pathologies Tropicales, University of French Guiana, Cayenne, French Guiana Running title: Mycetoma caused by Gordonia westfalica
Corresponding author Dr Romain Blaizot Avenue des Flamboyants, Hôpital Andrée Rosemon 97300 CAYENNE, French Guiana Tel: +594 594 39 53 59 Fax: +594 594 39 52 83 [email protected]
1 2
Abstract Bacteria of the Gordonia genus are rarely involved in human infections. We report
3 4
here the case of a 30-year-old from Guinea Buissau with a mycetoma of the foot. 16S DNA
5
sequencing after a surgical biopsy identified Gordonia westfalica. This is the first report of
6
human infection caused by G. westfalica.
7 8
Text
9
Mycetoma is a neglected disease caused by bacterial (actinomycetoma) or fungal
10
(eumycetoma) microorganisms. Walking barefoot provides the usual route of entry for
11
causative pathogens 1. New microbiological techniques have recently improved the diagnosis
12
and led to the discovery of new agents 2, 3. The infection mostly affects males in arid tropical
13
areas with a short rainy season 1. West Africa and South-East Asia are endemic for
14
eumycetoma, with most cases caused by Madurella mycetomatis 1. In Latin America, most
15
cases have been reported in Mexico and Brazil, usually actinomycetoma induced by
16
Nocardia braziliensis or Actinomadura madurae 1,4. In French Guiana, only a few cases have
17
been reported 5, probably due to its wet equatorial climate 1. We report here a case of
18
imported mycetoma diagnosed in French Guiana, caused by the recently discovered
19
Gordonia westfalica.
20
A 30-year-old man with no medical history except a mild psoriasis consulted for a
21
cutaneous nodule of the left foot. The patient was born in Guinea Bissau and had recently
22
arrived in French Guiana. During his trip he stayed 6 months in Dakar, Senegal, then
23
travelled along the North East coast of Brazil for six months before arriving in Cayenne.
24
Clinical examination showed a 6-cm wide suppurative and nodular swelling of the first
25
interdigital space, with several discharging sinuses (Fig 1a). Given the suspicion of
26
mycetoma, the entire lesion was surgically removed. Per-operatory examination showed
27
yellow grains (Fig 1b). Histology showed a polymorphic, neutrophilic infiltrate and
28
inflammatory nodules structured around mycetoma granules (Fig 1c and 1d). Mycological
29
culture and direct examination were negative. Actinomycetes were visible on bacteriological
30
culture. Final identification was Gordonia westfalica assessed by a 611nt fragment of the 16S
31
rRNA gene6 and analysis with BLAST (http://www.blast.ncbi.nlm.nih.gov/Blast.cgi), (GenBank
32
accession number MN900722, 99.2% similarity with reference NR_025468). The patient
33
received four weeks of oral cotrimoxazole (800/160/d) and rifampicin (900mg/d). A
34
complete response was then observed, the antibiotic treatment was stopped. There was no
35
relapse at three months.
36
Gordonia spp. are members of the actinomycete family, and are widely spread in the
37
environment, especially in soils 7. Gordonia are mostly involved in respiratory tract infections
38
in patients with immunosuppressive disease, but clinical manifestations also include
39
catheter-associated bacteraemia, arthritis, endocarditis, central nervous system and soft
40
tissue infections 7. Only two cases of mycetoma caused by Gordonia terrae have been
41
reported so far
42
estimated due to the difficult isolation using conventional microbiological techniques. Our
43
case is the third report of mycetoma caused by a Gordonia bacteria, and the first one caused
44
by Gordonia westfalica. This bacteria was first described in Germany in 2008, as a rubber-
45
degrading actinomycete isolated in foul water inside an old automobile tyre10. Since then, it
46
has never been reported as an animal or human pathogen.
8,9
. The importance of Gordonia bacteria in mycetoma is probably under-
47
This case is remarkable as the patient was diagnosed in a non-endemic area, though
48
he was probably contaminated in Africa. This example underlines the utility of sequencing to
49
improve the identification of pathogens in neglected tropical dermatoses.
50
51 52
References
53 54 55
1.
Zijlstra EE, van de Sande WWJ, Welsh O, Mahgoub ES, Goodfellow M, Fahal AH. Mycetoma: a unique neglected tropical disease. Lancet Infect Dis. 2016 Jan;16(1):100– 12.
56 57
2.
Ahmed AA, van de Sande W, Fahal AH. Mycetoma laboratory diagnosis: Review article. PLoS Negl Trop Dis. 2017 Aug;11(8):e0005638.
58 59 60 61
3.
Nenoff P, van de Sande WWJ, Fahal AH, Reinel D, Schöfer H. Eumycetoma and actinomycetoma--an update on causative agents, epidemiology, pathogenesis, diagnostics and therapy. J Eur Acad Dermatol Venereol JEADV. 2015 Oct;29(10):1873– 83.
62 63
4.
Castro LGM, Piquero-Casals J. Clinical and mycologic findings and therapeutic outcome of 27 mycetoma patients from São Paulo, Brazil. Int J Dermatol. 2008 Feb;47(2):160–3.
64 65 66 67
5.
Iriart X, Binois R, Fior A, Blanchet D, Berry A, Cassaing S, et al. Eumycetoma caused by Diaporthe phaseolorum (Phomopsis phaseoli): a case report and a mini-review of Diaporthe/Phomopsis spp invasive infections in humans. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2011 Oct;17(10):1492–4.
68 69 70
6.
Rodríguez-Nava V, Couble A, Devulder G, Flandrois JP, Boiron P, Laurent F. Use of PCRrestriction enzyme pattern analysis and sequencing database for hsp65 gene-based identification of Nocardia species. J Clin Microbiol. 2006 Feb;44(2):536-46.
71 72
7.
Andalibi F, Fatahi-Bafghi M. Gordonia: isolation and identification in clinical samples and role in biotechnology. Folia Microbiol (Praha). 2017 May;62(3):245–52.
73 74
8.
Zampella JG, Kwatra SG, Kazi N, Aguh C. Madura foot caused by Gordonia terrae misdiagnosed as Nocardia. Australas J Dermatol. 2017 Aug;58(3):e129–31.
75 76
9.
Bakker XR, Spauwen PHM, Dolmans WMV. Mycetoma of the hand caused by Gordona terrae: a case report. J Hand Surg Edinb Scotl. 2004 Apr;29(2):188–90.
77 78 79
10. Linos A, Berekaa MM, Steinbüchel A, Kim KK, Sproer C, Kroppenstedt RM. Gordonia westfalica sp. nov., a novel rubber-degrading actinomycete. Int J Syst Evol Microbiol. 2002 Jul;52(Pt 4):1133–9.
80 81
Figure legends
82
Figure 1: cutaneous mass with discharging sinuses (a) and per-operatory findings with
83
macroscopic yellow grains (b). H&E stain, X5, inflammatory nodules structured around grains
84
(c); X20, neutrophilic infiltrate surrounding bacteria (d)
85 86 87 88
Author contributions:
89
Denis Blanchet, Veronica Rodriguez-Nava, Emmanuelle Bergeron, Magalie Demar, Marie
90
Soulier, Pierre Couppie, Nassim Bestandji : acquisition of data
91
Romain Gueneau, Romain Blaizot : conception and design, drafting
92
All authors : final approval
S2052-2975(20)30010-X
DOI:
https://doi.org/10.1016/j.nmni.2020.100658
Reference:
NMNI 100658
To appear in:
New Microbes and New Infections
Received Date: 27 October 2019 Revised Date:
8 January 2020
Accepted Date: 10 February 2020
Please cite this article as: Gueneau R, Blanchet D, Rodriguez-Nava V, Bergeron E, Soulier M, Bestandji N, Demar M, Couppie P, Blaizot R, Actinomycetoma caused by Gordonia westfalica: first reported case of human infection, New Microbes and New Infections, https://doi.org/10.1016/j.nmni.2020.100658. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.
Letter to the Editor
Actinomycetoma caused by Gordonia westfalica: first reported case of human infection
Key words: Mycetoma; Actinomyces; Spectrum analysis; Neglected Tropical Disease; Gordonia Word count: 499 Figures: 1
Romain Gueneau 1 Denis Blanchet 2 Veronica Rodriguez-Nava 3 Emmanuelle Bergeron 3 Marie Soulier 4 Nassim Bestandji 5 Magalie Demar 2,6 Pierre Couppie 1,6 Romain Blaizot 1,6 1: Dermatology Department, Hôpital Andrée Rosemon, Cayenne, French Guiana 2: Laboratory of Parasitology and Mycology, Hôpital Andrée Rosemon, Cayenne, French Guiana 3: UMR CNRS 5557, Center for Microbial Ecology, Observatoire Français des Nocardioses, Laboratoire de Mycologie Fondamentale et Appliquée aux Biotechnologies Industrielles, Faculté de Pharmacie, Université Claude Bernard Lyon I, Lyon, France. 4: Pathologistes associés, Martigues, France 5: Orthopaedics Department, Hôpital Andrée Rosemon, Cayenne, French Guiana 6: EA 3593 Ecosystèmes Amazoniens et Pathologies Tropicales, University of French Guiana, Cayenne, French Guiana Running title: Mycetoma caused by Gordonia westfalica
Corresponding author Dr Romain Blaizot Avenue des Flamboyants, Hôpital Andrée Rosemon 97300 CAYENNE, French Guiana Tel: +594 594 39 53 59 Fax: +594 594 39 52 83 [email protected]
1 2
Abstract Bacteria of the Gordonia genus are rarely involved in human infections. We report
3 4
here the case of a 30-year-old from Guinea Buissau with a mycetoma of the foot. 16S DNA
5
sequencing after a surgical biopsy identified Gordonia westfalica. This is the first report of
6
human infection caused by G. westfalica.
7 8
Text
9
Mycetoma is a neglected disease caused by bacterial (actinomycetoma) or fungal
10
(eumycetoma) microorganisms. Walking barefoot provides the usual route of entry for
11
causative pathogens 1. New microbiological techniques have recently improved the diagnosis
12
and led to the discovery of new agents 2, 3. The infection mostly affects males in arid tropical
13
areas with a short rainy season 1. West Africa and South-East Asia are endemic for
14
eumycetoma, with most cases caused by Madurella mycetomatis 1. In Latin America, most
15
cases have been reported in Mexico and Brazil, usually actinomycetoma induced by
16
Nocardia braziliensis or Actinomadura madurae 1,4. In French Guiana, only a few cases have
17
been reported 5, probably due to its wet equatorial climate 1. We report here a case of
18
imported mycetoma diagnosed in French Guiana, caused by the recently discovered
19
Gordonia westfalica.
20
A 30-year-old man with no medical history except a mild psoriasis consulted for a
21
cutaneous nodule of the left foot. The patient was born in Guinea Bissau and had recently
22
arrived in French Guiana. During his trip he stayed 6 months in Dakar, Senegal, then
23
travelled along the North East coast of Brazil for six months before arriving in Cayenne.
24
Clinical examination showed a 6-cm wide suppurative and nodular swelling of the first
25
interdigital space, with several discharging sinuses (Fig 1a). Given the suspicion of
26
mycetoma, the entire lesion was surgically removed. Per-operatory examination showed
27
yellow grains (Fig 1b). Histology showed a polymorphic, neutrophilic infiltrate and
28
inflammatory nodules structured around mycetoma granules (Fig 1c and 1d). Mycological
29
culture and direct examination were negative. Actinomycetes were visible on bacteriological
30
culture. Final identification was Gordonia westfalica assessed by a 611nt fragment of the 16S
31
rRNA gene6 and analysis with BLAST (http://www.blast.ncbi.nlm.nih.gov/Blast.cgi), (GenBank
32
accession number MN900722, 99.2% similarity with reference NR_025468). The patient
33
received four weeks of oral cotrimoxazole (800/160/d) and rifampicin (900mg/d). A
34
complete response was then observed, the antibiotic treatment was stopped. There was no
35
relapse at three months.
36
Gordonia spp. are members of the actinomycete family, and are widely spread in the
37
environment, especially in soils 7. Gordonia are mostly involved in respiratory tract infections
38
in patients with immunosuppressive disease, but clinical manifestations also include
39
catheter-associated bacteraemia, arthritis, endocarditis, central nervous system and soft
40
tissue infections 7. Only two cases of mycetoma caused by Gordonia terrae have been
41
reported so far
42
estimated due to the difficult isolation using conventional microbiological techniques. Our
43
case is the third report of mycetoma caused by a Gordonia bacteria, and the first one caused
44
by Gordonia westfalica. This bacteria was first described in Germany in 2008, as a rubber-
45
degrading actinomycete isolated in foul water inside an old automobile tyre10. Since then, it
46
has never been reported as an animal or human pathogen.
8,9
. The importance of Gordonia bacteria in mycetoma is probably under-
47
This case is remarkable as the patient was diagnosed in a non-endemic area, though
48
he was probably contaminated in Africa. This example underlines the utility of sequencing to
49
improve the identification of pathogens in neglected tropical dermatoses.
50
51 52
References
53 54 55
1.
Zijlstra EE, van de Sande WWJ, Welsh O, Mahgoub ES, Goodfellow M, Fahal AH. Mycetoma: a unique neglected tropical disease. Lancet Infect Dis. 2016 Jan;16(1):100– 12.
56 57
2.
Ahmed AA, van de Sande W, Fahal AH. Mycetoma laboratory diagnosis: Review article. PLoS Negl Trop Dis. 2017 Aug;11(8):e0005638.
58 59 60 61
3.
Nenoff P, van de Sande WWJ, Fahal AH, Reinel D, Schöfer H. Eumycetoma and actinomycetoma--an update on causative agents, epidemiology, pathogenesis, diagnostics and therapy. J Eur Acad Dermatol Venereol JEADV. 2015 Oct;29(10):1873– 83.
62 63
4.
Castro LGM, Piquero-Casals J. Clinical and mycologic findings and therapeutic outcome of 27 mycetoma patients from São Paulo, Brazil. Int J Dermatol. 2008 Feb;47(2):160–3.
64 65 66 67
5.
Iriart X, Binois R, Fior A, Blanchet D, Berry A, Cassaing S, et al. Eumycetoma caused by Diaporthe phaseolorum (Phomopsis phaseoli): a case report and a mini-review of Diaporthe/Phomopsis spp invasive infections in humans. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2011 Oct;17(10):1492–4.
68 69 70
6.
Rodríguez-Nava V, Couble A, Devulder G, Flandrois JP, Boiron P, Laurent F. Use of PCRrestriction enzyme pattern analysis and sequencing database for hsp65 gene-based identification of Nocardia species. J Clin Microbiol. 2006 Feb;44(2):536-46.
71 72
7.
Andalibi F, Fatahi-Bafghi M. Gordonia: isolation and identification in clinical samples and role in biotechnology. Folia Microbiol (Praha). 2017 May;62(3):245–52.
73 74
8.
Zampella JG, Kwatra SG, Kazi N, Aguh C. Madura foot caused by Gordonia terrae misdiagnosed as Nocardia. Australas J Dermatol. 2017 Aug;58(3):e129–31.
75 76
9.
Bakker XR, Spauwen PHM, Dolmans WMV. Mycetoma of the hand caused by Gordona terrae: a case report. J Hand Surg Edinb Scotl. 2004 Apr;29(2):188–90.
77 78 79
10. Linos A, Berekaa MM, Steinbüchel A, Kim KK, Sproer C, Kroppenstedt RM. Gordonia westfalica sp. nov., a novel rubber-degrading actinomycete. Int J Syst Evol Microbiol. 2002 Jul;52(Pt 4):1133–9.
80 81
Figure legends
82
Figure 1: cutaneous mass with discharging sinuses (a) and per-operatory findings with
83
macroscopic yellow grains (b). H&E stain, X5, inflammatory nodules structured around grains
84
(c); X20, neutrophilic infiltrate surrounding bacteria (d)
85 86 87 88
Author contributions:
89
Denis Blanchet, Veronica Rodriguez-Nava, Emmanuelle Bergeron, Magalie Demar, Marie
90
Soulier, Pierre Couppie, Nassim Bestandji : acquisition of data
91
Romain Gueneau, Romain Blaizot : conception and design, drafting
92
All authors : final approval