Abstract
Background
There are few data on the epidemiology of infections caused by Streptococcus bovis (Sb). Some studies suggest that both residence in rural areas and contact with livestock could be potential risk factors.
Methods
We performed a retrospective study for the period 2005–2016 of all cases of bacteremia caused by Sb in Galicia (a region in the northwest of Spain). The association between the incidence rate of Sb bacteremia and the number of cattle by province and district was analyzed.
Results
677 cases were included with a median age of 76 years, 69.3% males. The most frequent infections were endocarditis (234 cases, 34.5%), primary bacteremia (213 cases, 31.5%) and biliary infection (119 cases, 17.5%). In 252 patients, colon neoplasms were detected (37.2%). S. gallolyticus subsp. gallolyticus was the predominant species (52.3%). Mortality was 15.5% (105 cases). The annual incidence rate was 20.2 cases/106 inhabitants and was correlated with the density of cattle (p < 0.001), but not with rurality. When comparing the two provinces with a strong predominance of rural population, but with important differences in the number of cattle, such as Orense and Lugo, with 6% and 47.7% of Galician cattle, respectively, the rates were very different: 15.8 and 43.6 cases/106, respectively, with an RR of 2.7 (95% CI, 2.08–3.71). Some districts of the province of Lugo had rates higher than 100 cases/106 inhabitants.
Conclusions
Our study shows a significant correlation between the rates of Sb bacteremia and cattle density, suggesting a possible transmission of Sb from cows to people.
Similar content being viewed by others
References
Corredoira J, Rabuñal R, Alonso MP. Streptococcus bovis: 100 years of an intriguing pathogen. Clin Microbiol Newslett. 2017;39:1–9.
Dekker JP, Lau AF. An update on the Streptococcus bovis group: classification, identification, and disease associations. J Clin Microbiol. 2016;54:1694–9.
Ruoff K, Miller SI, Garner CV, Ferraro MJ, Calderwood SB. Bacteremia with Streptococcus bovis and Streptococcus salivarius: clinical correlates of more accurate identification of isolates. J Clin Microbiol. 1989;27:305–8.
Boleij A, van Gelder MM, Swinkels DW, Tjalsma H. Clinical importance of Streptococcus gallolyticus infection among colorectal cancer patients: systematic review and meta-analysis. Clin Infect Dis. 2011;53:870–8.
Lee RA, Woo PC, To AP, Lau SK, Wong SS, Yuen KY. Geographical difference of disease association in Streptococcus bovis bacteraemia. J Med Microbiol. 2003;52:903–8.
Jean S, Teng LJ, Hsueh PR, Ho SW, Luh KT. Bacteremic Streptococcus bovis infections at a university hospital, 1992–2001. J Formos Med Assoc. 2004;103:118–23.
Sheng WH, Chuang YC, Teng LJ, Hsueh PR. Bacteraemia due to Streptococcus gallolyticus subspecies pasteurianus is associated with digestive tract malignancies and resistance to macrolides and clindamycin. J Infect. 2014;69:145–53.
Matesanz M, Rubal D, Iñiguez I, Rabuñal R, García-Garrote F, Coira A, et al. Is Streptococcus bovis a urinary pathogen? Eur J Clin Microbiol Infect Dis. 2015;34:719–25.
Gómez-Garcés JL, Gil Y, Burillo A, Wilhelmi I, Palomo M. Diseases associated with bloodstream infections caused by the new species included in the old Streptococcus bovis group. Enferm Infecc Microbiol Clin. 2012;30:175–9.
Corredoira J, Grau I, Garcia-Rodriguez JF, García-País MJ, Rabuñal R, Ardanuy C, et al. Colorectal neoplasm in cases of Clostridium septicum and Streptococcus gallolyticus subsp. gallolyticus bacteraemia. Eur J Intern Med. 2017;41:68–73.
Kumar R, Herold JL, Schady D, Davis J, Kopetz S, Martinez-Moczygemba M, et al. Streptococcus gallolyticus subsp. gallolyticus promotes colorectal tumor development. PLoS Pathog. 2017;13:e1006440.
Beck M, Frodl R, Funke G. Comprehensive study of strains previously designated Streptococcus bovis consecutively isolated from human blood cultures and emended description of Streptococcus gallolyticus and Streptococcus infantarius subsp. coli. J Clin Microbiol. 2008;46:2966–72.
Giannitsioti E, Chirouze C, Bouvet A, Béguinot I, Delahaye F, Mainardi JL, et al. Characteristics and regional variations of group D streptococcal endocarditis in France. Clin Microbiol Infect. 2007;13:770–6.
Corredoira J, Alonso MP, Pita J, Alonso-Mesonero D. Association between rural residency, group D streptococcal endocarditis and colon cancer? Clin Microbiol Infect. 2008;14:190.
Coffey S, Nadarasa K, Pan A, van der Linden A, Chu J, Schultz M. The increasing incidence of Streptococcus bovis endocarditis and bacteraemia: a case series from 1997 to 2010. Int J Cardiol. 2012;161:111–3.
Hoen B, Chirouze C, Cabell CH, Selton-Suty C, Duchêne F, Olaison L, et al. Emergence of endocarditis due to group D streptococci: findings derived from the merged database of the International Collaboration on Endocarditis. Eur J Clin Microbiol Infect Dis. 2005;24:12–6.
Corredoira J, Grau I, Garcia-Rodriguez JF, Alonso-Garcia P, Garcia-Pais MJ, Rabuñal R, et al. The clinical epidemiology and malignancies associated with Streptococcus bovis biotypes in 506 cases of bloodstream infections. J Infect. 2015;71:317–25.
Muñoz P, Kestler M, De Alarcon A, Miro JM, Bermejo J, Rodríguez-Abella H, et al. Current epidemiology and outcome of infective endocarditis: a multicenter, prospective, cohort study. Medicine (Baltim). 2015;94:e1816.
Corredoira J, García-Pais MJ, Rabuñal R, Alonso MP. Streptococcus bovis endocarditis: epidemiological differences depending on geographical source. Am Heart J. 2016;177:e1–2.
Dumke J, Hinse D, Vollmer T, Schulz J, Knabbe C, Dreier J. Potential transmission pathways of Streptococcus gallolyticus subsp. gallolyticus. PLoS One. 2015;10:e0126507.
Jans C, Meile L, Lacroix C, Stevens MJ. Genomics, evolution, and molecular epidemiology of the Streptococcus bovis/Streptococcus equinus complex (SBSEC). Infect Genet Evol. 2015;33:419–36.
Lun ZR, Wang QP, Chen XG, Li AX, Zhu XQ. Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis. 2007;7:201–9.
Bordes-Benítez A, Sánchez-Oñoro M, Suárez-Bordón P, García-Rojas AJ, Saéz-Nieto JA, González-García A, et al. Outbreak of Streptococcus equi subsp. zooepidemicus infections on the island of Gran Canaria associated with the consumption of inadequately pasteurized cheese. Eur J Clin Microbiol Infect Dis. 2006;25:242–6.
Devriese LA, Laurier L, De Herdt P, Haesebrouck F. Enterococcal and streptococcal species isolated from faeces of calves, young cattle and dairy cows. J Appl Bacteriol. 1992;72:29–31.
Gonzalez-Quintela A, Fernández-Conde S, Alves MªT, et al. Temporal and spatial patterns in the rate of alcohol withdrawal syndrome in a defined community. Alcohol. 2011;45:105–11.
Ministerio de Medio Ambiente y Medio Rural y Marino. Secretaría general técnica. Subdireccion general de estadística. http://www.mapama.gob.es/es/estadistica/temas/estadisticas-agrarias. Accessed 10 Feb 2018.
Instituto Galego de Estatística. http://www.ige.eu/igebdt/igeapi/datos/5230/0:2010,1:0,2:0,9915:12:15:27:32:36 Accessed 1 Dec 2017.
Vergara-López S, de Alarcón A, Mateos-Gómez A, Georgieva RI, González-Nieto JA, Guerrero Sánchez F, et al. [Descriptive analysis of diseases associated with Streptococcus bovis bacteremia]. Med Clin (Barc). 2011;137:527–32.
Hoen B, Alla F, Selton-Suty C, Béguinot I, Bouvet A, Briançon S, et al. Changing profile of infective endocarditis: results of a 1-year survey in France. JAMA. 2002;288:75–81.
Corredoira J, García-Garrote F, Rabuñal R, López-Roses L, García-País MJ, Castro E, et al. Association between bacteremia due to Streptococcus gallolyticus subsp. gallolyticus (Streptococcus bovis I) and colorectal neoplasia: a case control study. Clin Infect Dis. 2012;55:491–6.
Romero B, Morosini MI, Loza E, Rodríguez-Baños M, Navas E, Cantón R, Campo RD. Reidentification of Streptococcus bovis isolates causing bacteremia according to the new taxonomy criteria: still an issue? J Clin Microbiol. 2011;49:3228–33.
Dumke J, Vollmer T, Akkermann O, Knabbe C, Dreier J. Case-control study: Determination of potential risk factors for the colonization of healthy volunteers with Streptococcus gallolyticus subsp. gallolyticus. PLoS One. 2017;12:e0176515.
Actualitix. World Atlas. Statistics by country. https://es.actualitix.com. Accessed 10 Feb 2018.
Xunta de Galicia. Programa galego de prevención e control da tuberculose. Dirección Xeral de Saude Pública. Santiago de Compostela. 2017. http://www.sergas.es/saude-publica. Accessed 10 Feb 2018.
Marmolin ES, Hartmeyer GN, Christensen JJ, Nielsen XC, Dargis R, Skov MN, et al. Bacteremia with the bovis group streptococci: species identification and association with infective endocarditis and with gastrointestinal disease. Diagn Microbiol Infect Dis. 2016;85:239–42.
Papadimitriou K, Anastasiou R, Mavrogonatou E, Blom J, Papandreou NC, Hamodrakas SJ, et al. Comparative genomics of the dairy isolate Streptococcus macedonicus ACA-DC 198 against related members of the Streptococcus bovis/Streptococcus equinus complex. BMC Genom. 2014;15:272.
Lin IH, Liu TT, Teng YT, Wu HL, Liu YM, Wu KM, Chang CH, Hsu MT. Sequencing and comparative genome analysis of two pathogenic Streptococcus gallolyticus subspecies: genome plasticity, adaptation and virulence. PLoS One. 2011;6:e20519.
Rusniok C, Couvé E, Da Cunha V, El Gana R, Zidane N, Bouchier C, et al. Genome sequence of Streptococcus gallolyticus: insights into its adaptation to the bovine rumen and its ability to cause endocarditis. J Bacteriol. 2010;193:2266–76.
Jans C, Follador R, Hochstrasser M, Lacroix C, Meile L, Stevens MJ. Comparative genome analysis of Streptococcus infantarius subsp. infantarius CJ18, an African fermented camel milk isolate with adaptations to dairy environment. BMC Genom. 2013;14:200.
Schulz J, Dumke J, Hinse D, Dreier J, Habig C, Kemper N. Organic Turkey flocks: a reservoir of Streptococcus gallolyticus subspecies gallolyticus. PLoS One. 2015;10:e0144412.
Tsakalidou E, Zoidou E, Pot B, Wassill L, Ludwig W, Devriese LA, et al. Identification of streptococci from Greek Kasseri cheese and description of Streptococcus macedonicus sp. nov. Int J Syst Bacteriol. 1998;48:519–27.
Jans C, Kaindi DW, Bock D, Njage PM, Kouamé-Sina SM, Bonfoh B, et al. Prevalence and comparison of Streptococcus infantarius subsp. infantarius and Streptococcus gallolyticus subsp. macedonicus in raw and fermented dairy products from East and West Africa. Int J Food Microbiol. 2013;167:186–95.
Lazarovitch T, Shango M, Levine M, Brusovansky R, Akins R, Hayakawa K, et al. The relationship between the new taxonomy of Streptococcus bovis and its clonality to colon cancer, endocarditis, and biliary disease. Infection. 2013;41:329–37.
Dumke J, Hinse D, Vollmer T, Knabbe C, Dreier J. Development and application of a multilocus sequence typing scheme for Streptococcus gallolyticus subsp. gallolyticus. J Clin Microbiol. 2014;52:2472–8.
Acknowledgements
List of Collaborators:
GESBOGA—Study Group of Streptococcus bovis bacteremia in Galicia: List of participating centers and researches: Hospital da Costa (Burela, Lugo): Serrano M (Microbiology), Jove MJ (Internal Medicine); Hospital Comarcal de Monforte de Lemos (Lugo): Alonso P (Microbiology), Justo E, Piñeiro JC (Internal Medicine); Hospital Universitario Lucus Augusti (Lugo): Alonso MP, García-Garrote F, Coira MA (Microbiology), Blanco A (Methodology and Clinical Research Unit. Ramón Domínguez Foundation), Gómez-Méndez R (Internal Medicine), García-Pais MJ, Rabuñal R, López-Álvarez MJ, J Corredoira, Eva Romay (Infectious Diseases Unit); Hospital Virxe da Xunqueira (Cee, A Coruña): Abel V (Internal Medicine); Complexo Hospitalario Universitario A Coruña (A Coruña): Miguez E (Infectious Diseases Unit), Cerezales A, Vieito D (Internal Medicine), Rodriguez-Mayo M, Gude MJ (Microbiology); Complexo Hospitalario Universitario de Ferrol (Ferrol, A Coruña): García-Rodríguez JF (Infectious Diseases Unit), Agulla JA (Microbiology); Complexo Hospitalario Universitario de Santiago (Santiago de Compostela, A Coruña): Mateo LM, González-Quintela A (Internal Medicine), Hernández M, Manso T, Aguilera A, Pérez del Molino ML (Microbiology), Hospital da Barbanza (Ribeira, A Coruña): Martínez-Braña L (Internal Medicine); Complexo Hospitalario Universitario de Ourense (Ourense): Fernández-Rodríguez R (Infectious Diseases Unit), Paz MI (Microbiology); Hospital de Valdeorras (O Barco de Valdeorras, Ourense), González-Dominguez M (Microbiology), Morales F (Internal Medicine); Hospital de Verín (Verín, Ourense): Soto I (Internal Medicine); Complexo Hospitalario Universitario de Vigo (Vigo, Pontevedra): Vasallo FJ (Microbiology), Pérez-Gonzalez A, Pérez-Alvarez R (Internal Medicine); Hospital POVISA (Vigo, Pontevedra): de la Fuente J, Sanjurjo A, Lamas JL, Álvarez-Ferreiro J (Internal Medicine), Rodríguez-Conde MI (Microbiology), Hospital do Salnes (Vilagarcia de Arousa, Pontevedra), Pazos A (Internal Medicine); Complexo Hospitalario Universitario de Pontevedra (Pontevedra), Pulian MV, Guzmán DM, García-Campello M (Microbiology), Diz J (Internal Medicine).
Funding
No grant support was available for this investigation.
Author information
Authors and Affiliations
Consortia
Corresponding author
Ethics declarations
Ethical statement
The Institutional Review Boards approved this study, and they specifically waived the need for consent because the study analyzed the data retrospectively and the source of data was anonymized.
Conflict of interest
All authors declare no conflicts of interest with this investigation.
Additional information
The list of participating centers and researches in GESBOGA—Study Group of Streptococcus bovis bacteremia in Galicia—has been provided in Acknowledgements.
Rights and permissions
About this article
Cite this article
Corredoira, J., Miguez, E., Mateo, L.M. et al. Correlation between Streptococcus bovis bacteremia and density of cows in Galicia, northwest of Spain. Infection 47, 399–407 (2019). https://doi.org/10.1007/s15010-018-1254-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s15010-018-1254-x