Comparison of Characteristics of Patients Infected by Campylobacter jejuni, Campylobacter coli, and Campylobacter fetus
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Emilie Bessède, Philippe Lehours, Leila Labadi, Sarah Bakiri and Francis Mégraud J. Clin. Microbiol. 2014, 52(1):328. DOI: 10.1128/JCM.03029-13. Published Ahead of Print 6 November 2013.
Comparison of Characteristics of Patients Infected by Campylobacter jejuni, Campylobacter coli, and Campylobacter fetus Emilie Bessède,a,b Philippe Lehours,a,b Leila Labadi,a Sarah Bakiri,a Francis Mégrauda,b ‹National Reference Center for Campylobacter & Helicobacter, Laboratoire de Bactériologie, Université de Bordeaux, Bordeaux, Francea; CHU de Bordeaux, Bordeaux, Franceb
T
hermotolerant Campylobacter spp. are recognized as the leading cause of bacterial enteric infections worldwide, while Campylobacter fetus often causes systemic infection. A subset of French clinical laboratories participates in the surveillance of Campylobacter infection, carried out by the National Reference Centre (NRC) for Campylobacters and Helicobacters under the leadership of the Institut de Veille Sanitaire (InVS), sending approximately a quarter of campylobacters isolated in France to the NRC. Our aim was to use this large database (⬎22,000 strains) to look for differences in the characteristics of the patients and the circumstances under which these Campylobacter species were isolated. (The results of this study were presented as posters at the European Congress of Clinical Microbiology and Infectious Diseases, London, United Kingdom, 2012, and at the Réunion Interdisciplinaire de Chimiothérapie Anti-infectieuse, Paris, France, November 2012.) Network of laboratories. The laboratories sending strains were not randomly selected but were contacted from the list of laboratories already sending isolated Salmonella species to the corresponding NRC. A survey performed in 2009 showed that equal proportions of all strains isolated came from the different regions, with a few exceptions (InVS-NRC, unpublished data). The methods used by these laboratories to isolate Campylobacter species were fairly uniform, including the use of Karmali medium or Campylosel (bioMérieux, Marcy l’Etoile, France) but no filtration techniques. Identification of campylobacters at the NRC. All of the Campylobacter isolates were identified by phenotypic methods at the genus level. From 2003 to 2009, identification to species level was performed both by standard phenotypic methods and a real-time PCR targeting the gyrA gene (accuracy, 99.9%) to differentiate Campylobacter jejuni and Campylobacter coli (1). In the case of negative results, primers specific for C. fetus were used. If no result was obtained, a PCR specific for Arcobacter species was carried out (2). These PCRs allowed the identification of approximately 99% of the isolates. For the remaining 1%, the 16S rRNA gene was sequenced. In 2010, these methods were replaced by matrix-assisted laser desorption ionization–time-of-flight (MALDI-TOF) mass spectrometry identification, which has an accuracy of 99.4% for C. jejuni and 100% for the other Campylobacter species (3). Susceptibility testing was performed by disk diffusion with the
same methods and cutoffs from the Comité de l’Antibiogramme de la Société Française de Microbiologie (CA-SFM) that have been used during all the years. Database analysis. The following information was collected: patient age, patient gender, month of isolation, region of France, whether the disease was part of an outbreak or a sporadic infection, whether the patient had traveled abroad, whether the patient was hospitalized or an outpatient, type of specimen, and quinolone and ampicillin resistance of the isolated strain. Univariate and multivariate analyses were performed on the characteristics of the different species using the program SPSS v. 11.5. A total of 22,244 isolates, obtained from both hospital and private laboratories, were studied between 2003 and 2010 (Table 1). No significant difference between the proportions of the different species was observed in different years. Comparison between C. jejuni and C. coli infection. Two regression models were performed, one without antibiotics (Table 2) and the other with antibiotics, and gave similar results; i.e., age, travel, and season, after adjustment for the other variables, remained significantly different for C. jejuni and C. coli. A higher risk of being infected by C. coli was found in older persons (34.6 years) compared to C. jejuni (27.5 years), a person who had traveled abroad in the preceding 2 weeks had a higher risk of being infected by C. coli, and in the summertime (May to September), a person had a higher risk of being infected by C. jejuni than C. coli. Comparison of C. jejuni/C. coli versus C. fetus. The same analyses were performed for the thermotolerant campylobacters C. jejuni and C. coli taken together versus C. fetus. In the multivariate analysis (Table 2), the difference in the mean age of infected patients, 28.6 years for C. jejuni/C. coli versus 68.4 years for C. fetus, was very significant. C. fetus infection led much more often to hospitalization than C. coli or C. jejuni infection. Furthermore, C. fetus was isolated more often from blood samples than C. coli or
328
p. 328 –330
jcm.asm.org
Journal of Clinical Microbiology
Received 29 October 2013 Accepted 31 October 2013 Published ahead of print 6 November 2013 Editor: R. Patel Address correspondence to Francis Mégraud, [email protected]. Copyright © 2014, American Society for Microbiology. All Rights Reserved. doi:10.1128/JCM.03029-13
January 2014 Volume 52 Number 1
Downloaded from http://jcm.asm.org/ on March 31, 2014 by NATIONAL CHUNG HSING
A large database of Campylobacter isolates precisely identified at the species level was used to compare patients’ characteristics. In a multivariate analysis, Campylobacter coli was found more often in older patients and in patients having traveled abroad and less often in summertime than Campylobacter jejuni. Campylobacter fetus infection occurred in much older patients and in hospitalized patients with a systemic disease.
Campylobacter Epidemiology
TABLE 2 Regression model comparing Campylobacter infectionsa Comparison
Variable
OR
95% CI
P
Species or subspecies
No. (%) of isolates
C. jejuni vs. C. coli
Campylobacter jejuni Campylobacter coli Campylobacter fetus Campylobacter lari Campylobacter upsaliensis Campylobacter hyointestinalis Campylobacter jejuni subsp. doylei Campylobacter sputorum subsp. sputorum Campylobacter concisus Arcobacter butzleri Arcobacter cryaerophilus Arcobacter skirrowii Helicobacter pullorum Helicobacter canadensis Sutterella wadsworthensis Anaerobiospirillum succiniciproducens
17,625 (79.23) 3,393 (15.25) 875 (3.93) 95 (0.42) 27 (0.12) 9 3 1 1 172 (0.77) 13 1 15 12 1 1
Gender Age Travel Summertime
1.139 1.011 0.532 0.802
0.981–1.322 1.008–1.013 0.440–0.644 0.691–0.930
0.087 0.001 0.001 0.004
Thermotolerant Campylobacter vs. C. fetus
Gender Age Hospitalization Type of specimen Travel abroad Summertime
0.874 1.043 0.595 39.029 1.697 0.589
0.616–1.24 1.035–1.052 0.369–0.958 27.411–55.573 0.722–3.986 0.415–0.837
0.45 ⬍0.001 0.03 ⬍0.001 0.225 0.003
Total
22,244
C. jejuni. C. jejuni/coli were significantly more often isolated during summertime than C. fetus (P ⬍ 0.001). The main advantage of this study is the large number of cases for which precise species identification was carried out, i.e., more than 22,000 cases of infection by Campylobacter and related bacteria, while in many large studies on these bacteria, a differentiation was not made (4). In two Northern European studies where identification to species level was performed, the proportion of C. coli was lower than in our study (7% in England and Wales [5] and 8.5% in the Netherlands [6]) and was probably linked to differences in eating habits. Our study also shows that C. fetus, a bacterium leading to severe life-threatening infections (7), is the third most prevalent cause of Campylobacter infections (approximately 4% of the cases). The large number of C. jejuni and C. coli isolates allowed us to compare the characteristics of the corresponding infection, for which there are very limited data in the literature. There is a 7-year difference in the mean age of C. jejuni-infected patients (27.5 years) and C. coli-infected patients (34.6 years) (P ⫽ 0.001). A difference in age of borderline significance was also found in the study by Gillespie et al. (5), while the mean age was higher, 38.5 years for C. jejuni versus 42.9 years for C. coli. This difference appears to be real but cannot be explained. Travel abroad is a prominent risk factor for Campylobacter infection in some northern countries, like Norway, where it occurred in 65% of the cases (8), but less common in others, like Scotland (17%) (9), where it is in the same range as in France. In our study, we showed that C. coli is more frequently associated with a history of a travel abroad (P ⫽ 0.001) and is probably linked to eating habits in countries in the south (Morocco, West Indies, India, etc.). A similar association was found in a subgroup of patients of South Asian origin (5). C. jejuni infection, unlike C. coli infection, has a marked seasonality, and its occurrence almost doubles in the summertime. This can be explained by a higher contamination of food, especially poultry, with C. jejuni during the hotter period of the year (10). Furthermore, eating habits tend to be different in the summertime, with consumption of more
January 2014 Volume 52 Number 1
a
OR, odds ratio; CI, confidence interval.
barbecued, undercooked poultry and possibly cross contamination of salads. In contrast to other reports, a large number of C. fetus isolates were identified in this study. The main reason is that campylobacters from all specimens were included, not only those from feces. Indeed, almost 80% were isolated from systemic infections, but 21.7% were still isolated from feces (n ⫽ 190), in contrast to the unique C. fetus isolate among 3,764 campylobacters found in stools in England and Wales (5). A possible explanation lies in the recommendations made in France to incubate stool cultures at 37°C and not at 42 or 43°C like in most countries, to compensate for the lack of thermotolerance of C. fetus. The differences observed in the characteristics of C. fetus infection versus C. jejuni/C. coli infections are the well-known difference in the mean age of approximately 40 years, in line with the type of patients affected, who are often immunocompromised with an underlying disease and very often hospitalized. There are, however, limits to this study, since detailed information on the eating habits and other risk factors were not collected, nor do we have information on the severity and outcome of infection. We must also acknowledge that the infections observed most likely represent severe infections, since almost one-third of the patients were hospitalized. Furthermore, the strains received depend on the methods of isolation used by the clinical laboratories all over the country. However, because a filtration method is seldom used and anaerobic incubation not performed, we lack strains of species such as Campylobacter concisus, which appear to be common in surveys targeting this organism. Despite these limitations, the present study gives the opportunity to obtain interesting information of public health value for these pathogens of major importance, the cost of which has been estimated at 1.7 billion dollars in the United States (11). ACKNOWLEDGMENTS We thank the Institut National de Veille Sanitaire and especially Anne Gallay and Lisa King, who contributed to our Campylobacter surveillance network during all these years.
REFERENCES 1. Ménard A, Dachet F, Prouzet-Mauleon V, Oleastro M, Mégraud F. 2005. Development of a real-time fluorescence resonance energy transfer PCR to identify the main pathogenic Campylobacter spp. Clin. Microbiol. Infect. 11:281–287. http://dx.doi.org/10.1111/j.1469-0691.2005.01072.x. 2. Abdelbaqi K, Ménard A, Prouzet-Mauleon V, Bringaud F, Lehours P, Mégraud F. 2007. Nucleotide sequence of the gyrA gene of Arcobacter
jcm.asm.org 329
Downloaded from http://jcm.asm.org/ on March 31, 2014 by NATIONAL CHUNG HSING
TABLE 1 Number of Campylobacter and related bacterial isolates identified at the French National Reference Center, 2003 to 2010
Bessède et al.
3.
4.
6.
330
jcm.asm.org
7. Pacanowski J, Lalande V, Lacombe K, Boudraa C, Lesprit P, Legrand P, Trystram D, Kassis N, Arlet G, Mainardi JL, Doucet-Populaire F, Girard PM, Meynard JL. 2008. CAMPYL Study Group. Campylobacter bacteremia: clinical features and factors associated with fatal outcome. Clin. Infect. Dis. 47:790 –796. 8. Guzman-Herrador B, Vold L, Nygard K. 2012. Surveillance of travelassociated gastrointestinal infections in Norway, 2009 –2010: are they all actually imported? Euro Surveill. 17:20294. http://dx.doi.org/10.1086 /591530. 9. Strachan NJ, Rotariu O, Smith-Palmer A, Cowden J, Sheppard SK, O’Brien SJ, Maiden MC, Macrae M, Bessell PR, Matthews L, Reid SW, Innocent GT, Ogden ID, Forbes KJ. 2013. Identifying the seasonal origins of human campylobacteriosis. Epidemiol. Infect. 141:1267–1275. http://dx.doi.org/10.1017/S0950268812002063. 10. Lawes JR, Vidal A, Clifton-Hadley DA, Sayers R, Rodgers J, Snow L, Evans SJ, Powell LF. 2012. Investigation of prevalence and risk factors for Campylobacter in broiler flocks at slaughter: results from a UK survey. Epidemiol. Infect. 140:1725–1737. http://dx.doi.org/10.1017 /S0950268812000982. 11. Hoffmann S, Batz MB, Morris JG, Jr. 2012. Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J. Food Prot. 75:1292–1302. http://dx.doi.org/10.4315/0362 -028X.JFP-11-417.
Journal of Clinical Microbiology
Downloaded from http://jcm.asm.org/ on March 31, 2014 by NATIONAL CHUNG HSING
5.
species and characterization of human ciprofloxacin-resistant clinical isolates. FEMS Immunol. Med. Microbiol. 49:337–345. http://dx.doi.org/10 .1111/j.1574-695X.2006.00208.x. Bessède E, Solecki O, Sifré E, Labadi L, Mégraud F. 2011. Identification of Campylobacter species and related organisms by matrix assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry. Clin. Microbiol. Infect. 17:1735–1739. http://dx.doi.org/10.1111/j.1469 -0691.2011.03468.x. Gillespie IA, O’Brien SJ, Penman C, Tompkins D, Cowden J, Humphrey TJ. 2008. Demographic determinants for Campylobacter infection in England and Wales: implications for future epidemiological studies. Epidemiol. Infect. 136:1717–1725. http://dx.doi.org/10.1017 /S0950268808000319. Gillespie IA, O’Brien SJ, Frost JA, Adak GK, Horby P, Swan AV, Painter MJ. 2002. Campylobacter Sentinel Surveillance Scheme Collaborators. A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses. Emerg. Infect. Dis. 8:937–942. http://dx.doi.org/10.3201/eid0809.010187. Doorduyn Y, Van Den Brandhof WE, Van Duynhoven YT, Breukink BJ, Wagenaar JA, Van Pelt W. 2010. Risk factors for indigenous Campylobacter jejuni and Campylobacter coli infections in The Netherlands: a case-control study. Epidemiol. Infect. 138:1391–1404. http://dx.doi.org /10.1017/S095026881000052X.
Updated information and services can be found at: http://jcm.asm.org/content/52/1/328 These include: REFERENCES
CONTENT ALERTS
This article cites 11 articles, 1 of which can be accessed free at: http://jcm.asm.org/content/52/1/328#ref-list-1 Receive: RSS Feeds, eTOCs, free email alerts (when new articles cite this article), more»
Information about commercial reprint orders: http://journals.asm.org/site/misc/reprints.xhtml To subscribe to to another ASM Journal go to: http://journals.asm.org/site/subscriptions/
Downloaded from http://jcm.asm.org/ on March 31, 2014 by NATIONAL CHUNG HSING
Emilie Bessède, Philippe Lehours, Leila Labadi, Sarah Bakiri and Francis Mégraud J. Clin. Microbiol. 2014, 52(1):328. DOI: 10.1128/JCM.03029-13. Published Ahead of Print 6 November 2013.
Comparison of Characteristics of Patients Infected by Campylobacter jejuni, Campylobacter coli, and Campylobacter fetus Emilie Bessède,a,b Philippe Lehours,a,b Leila Labadi,a Sarah Bakiri,a Francis Mégrauda,b ‹National Reference Center for Campylobacter & Helicobacter, Laboratoire de Bactériologie, Université de Bordeaux, Bordeaux, Francea; CHU de Bordeaux, Bordeaux, Franceb
T
hermotolerant Campylobacter spp. are recognized as the leading cause of bacterial enteric infections worldwide, while Campylobacter fetus often causes systemic infection. A subset of French clinical laboratories participates in the surveillance of Campylobacter infection, carried out by the National Reference Centre (NRC) for Campylobacters and Helicobacters under the leadership of the Institut de Veille Sanitaire (InVS), sending approximately a quarter of campylobacters isolated in France to the NRC. Our aim was to use this large database (⬎22,000 strains) to look for differences in the characteristics of the patients and the circumstances under which these Campylobacter species were isolated. (The results of this study were presented as posters at the European Congress of Clinical Microbiology and Infectious Diseases, London, United Kingdom, 2012, and at the Réunion Interdisciplinaire de Chimiothérapie Anti-infectieuse, Paris, France, November 2012.) Network of laboratories. The laboratories sending strains were not randomly selected but were contacted from the list of laboratories already sending isolated Salmonella species to the corresponding NRC. A survey performed in 2009 showed that equal proportions of all strains isolated came from the different regions, with a few exceptions (InVS-NRC, unpublished data). The methods used by these laboratories to isolate Campylobacter species were fairly uniform, including the use of Karmali medium or Campylosel (bioMérieux, Marcy l’Etoile, France) but no filtration techniques. Identification of campylobacters at the NRC. All of the Campylobacter isolates were identified by phenotypic methods at the genus level. From 2003 to 2009, identification to species level was performed both by standard phenotypic methods and a real-time PCR targeting the gyrA gene (accuracy, 99.9%) to differentiate Campylobacter jejuni and Campylobacter coli (1). In the case of negative results, primers specific for C. fetus were used. If no result was obtained, a PCR specific for Arcobacter species was carried out (2). These PCRs allowed the identification of approximately 99% of the isolates. For the remaining 1%, the 16S rRNA gene was sequenced. In 2010, these methods were replaced by matrix-assisted laser desorption ionization–time-of-flight (MALDI-TOF) mass spectrometry identification, which has an accuracy of 99.4% for C. jejuni and 100% for the other Campylobacter species (3). Susceptibility testing was performed by disk diffusion with the
same methods and cutoffs from the Comité de l’Antibiogramme de la Société Française de Microbiologie (CA-SFM) that have been used during all the years. Database analysis. The following information was collected: patient age, patient gender, month of isolation, region of France, whether the disease was part of an outbreak or a sporadic infection, whether the patient had traveled abroad, whether the patient was hospitalized or an outpatient, type of specimen, and quinolone and ampicillin resistance of the isolated strain. Univariate and multivariate analyses were performed on the characteristics of the different species using the program SPSS v. 11.5. A total of 22,244 isolates, obtained from both hospital and private laboratories, were studied between 2003 and 2010 (Table 1). No significant difference between the proportions of the different species was observed in different years. Comparison between C. jejuni and C. coli infection. Two regression models were performed, one without antibiotics (Table 2) and the other with antibiotics, and gave similar results; i.e., age, travel, and season, after adjustment for the other variables, remained significantly different for C. jejuni and C. coli. A higher risk of being infected by C. coli was found in older persons (34.6 years) compared to C. jejuni (27.5 years), a person who had traveled abroad in the preceding 2 weeks had a higher risk of being infected by C. coli, and in the summertime (May to September), a person had a higher risk of being infected by C. jejuni than C. coli. Comparison of C. jejuni/C. coli versus C. fetus. The same analyses were performed for the thermotolerant campylobacters C. jejuni and C. coli taken together versus C. fetus. In the multivariate analysis (Table 2), the difference in the mean age of infected patients, 28.6 years for C. jejuni/C. coli versus 68.4 years for C. fetus, was very significant. C. fetus infection led much more often to hospitalization than C. coli or C. jejuni infection. Furthermore, C. fetus was isolated more often from blood samples than C. coli or
328
p. 328 –330
jcm.asm.org
Journal of Clinical Microbiology
Received 29 October 2013 Accepted 31 October 2013 Published ahead of print 6 November 2013 Editor: R. Patel Address correspondence to Francis Mégraud, [email protected]. Copyright © 2014, American Society for Microbiology. All Rights Reserved. doi:10.1128/JCM.03029-13
January 2014 Volume 52 Number 1
Downloaded from http://jcm.asm.org/ on March 31, 2014 by NATIONAL CHUNG HSING
A large database of Campylobacter isolates precisely identified at the species level was used to compare patients’ characteristics. In a multivariate analysis, Campylobacter coli was found more often in older patients and in patients having traveled abroad and less often in summertime than Campylobacter jejuni. Campylobacter fetus infection occurred in much older patients and in hospitalized patients with a systemic disease.
Campylobacter Epidemiology
TABLE 2 Regression model comparing Campylobacter infectionsa Comparison
Variable
OR
95% CI
P
Species or subspecies
No. (%) of isolates
C. jejuni vs. C. coli
Campylobacter jejuni Campylobacter coli Campylobacter fetus Campylobacter lari Campylobacter upsaliensis Campylobacter hyointestinalis Campylobacter jejuni subsp. doylei Campylobacter sputorum subsp. sputorum Campylobacter concisus Arcobacter butzleri Arcobacter cryaerophilus Arcobacter skirrowii Helicobacter pullorum Helicobacter canadensis Sutterella wadsworthensis Anaerobiospirillum succiniciproducens
17,625 (79.23) 3,393 (15.25) 875 (3.93) 95 (0.42) 27 (0.12) 9 3 1 1 172 (0.77) 13 1 15 12 1 1
Gender Age Travel Summertime
1.139 1.011 0.532 0.802
0.981–1.322 1.008–1.013 0.440–0.644 0.691–0.930
0.087 0.001 0.001 0.004
Thermotolerant Campylobacter vs. C. fetus
Gender Age Hospitalization Type of specimen Travel abroad Summertime
0.874 1.043 0.595 39.029 1.697 0.589
0.616–1.24 1.035–1.052 0.369–0.958 27.411–55.573 0.722–3.986 0.415–0.837
0.45 ⬍0.001 0.03 ⬍0.001 0.225 0.003
Total
22,244
C. jejuni. C. jejuni/coli were significantly more often isolated during summertime than C. fetus (P ⬍ 0.001). The main advantage of this study is the large number of cases for which precise species identification was carried out, i.e., more than 22,000 cases of infection by Campylobacter and related bacteria, while in many large studies on these bacteria, a differentiation was not made (4). In two Northern European studies where identification to species level was performed, the proportion of C. coli was lower than in our study (7% in England and Wales [5] and 8.5% in the Netherlands [6]) and was probably linked to differences in eating habits. Our study also shows that C. fetus, a bacterium leading to severe life-threatening infections (7), is the third most prevalent cause of Campylobacter infections (approximately 4% of the cases). The large number of C. jejuni and C. coli isolates allowed us to compare the characteristics of the corresponding infection, for which there are very limited data in the literature. There is a 7-year difference in the mean age of C. jejuni-infected patients (27.5 years) and C. coli-infected patients (34.6 years) (P ⫽ 0.001). A difference in age of borderline significance was also found in the study by Gillespie et al. (5), while the mean age was higher, 38.5 years for C. jejuni versus 42.9 years for C. coli. This difference appears to be real but cannot be explained. Travel abroad is a prominent risk factor for Campylobacter infection in some northern countries, like Norway, where it occurred in 65% of the cases (8), but less common in others, like Scotland (17%) (9), where it is in the same range as in France. In our study, we showed that C. coli is more frequently associated with a history of a travel abroad (P ⫽ 0.001) and is probably linked to eating habits in countries in the south (Morocco, West Indies, India, etc.). A similar association was found in a subgroup of patients of South Asian origin (5). C. jejuni infection, unlike C. coli infection, has a marked seasonality, and its occurrence almost doubles in the summertime. This can be explained by a higher contamination of food, especially poultry, with C. jejuni during the hotter period of the year (10). Furthermore, eating habits tend to be different in the summertime, with consumption of more
January 2014 Volume 52 Number 1
a
OR, odds ratio; CI, confidence interval.
barbecued, undercooked poultry and possibly cross contamination of salads. In contrast to other reports, a large number of C. fetus isolates were identified in this study. The main reason is that campylobacters from all specimens were included, not only those from feces. Indeed, almost 80% were isolated from systemic infections, but 21.7% were still isolated from feces (n ⫽ 190), in contrast to the unique C. fetus isolate among 3,764 campylobacters found in stools in England and Wales (5). A possible explanation lies in the recommendations made in France to incubate stool cultures at 37°C and not at 42 or 43°C like in most countries, to compensate for the lack of thermotolerance of C. fetus. The differences observed in the characteristics of C. fetus infection versus C. jejuni/C. coli infections are the well-known difference in the mean age of approximately 40 years, in line with the type of patients affected, who are often immunocompromised with an underlying disease and very often hospitalized. There are, however, limits to this study, since detailed information on the eating habits and other risk factors were not collected, nor do we have information on the severity and outcome of infection. We must also acknowledge that the infections observed most likely represent severe infections, since almost one-third of the patients were hospitalized. Furthermore, the strains received depend on the methods of isolation used by the clinical laboratories all over the country. However, because a filtration method is seldom used and anaerobic incubation not performed, we lack strains of species such as Campylobacter concisus, which appear to be common in surveys targeting this organism. Despite these limitations, the present study gives the opportunity to obtain interesting information of public health value for these pathogens of major importance, the cost of which has been estimated at 1.7 billion dollars in the United States (11). ACKNOWLEDGMENTS We thank the Institut National de Veille Sanitaire and especially Anne Gallay and Lisa King, who contributed to our Campylobacter surveillance network during all these years.
REFERENCES 1. Ménard A, Dachet F, Prouzet-Mauleon V, Oleastro M, Mégraud F. 2005. Development of a real-time fluorescence resonance energy transfer PCR to identify the main pathogenic Campylobacter spp. Clin. Microbiol. Infect. 11:281–287. http://dx.doi.org/10.1111/j.1469-0691.2005.01072.x. 2. Abdelbaqi K, Ménard A, Prouzet-Mauleon V, Bringaud F, Lehours P, Mégraud F. 2007. Nucleotide sequence of the gyrA gene of Arcobacter
jcm.asm.org 329
Downloaded from http://jcm.asm.org/ on March 31, 2014 by NATIONAL CHUNG HSING
TABLE 1 Number of Campylobacter and related bacterial isolates identified at the French National Reference Center, 2003 to 2010
Bessède et al.
3.
4.
6.
330
jcm.asm.org
7. Pacanowski J, Lalande V, Lacombe K, Boudraa C, Lesprit P, Legrand P, Trystram D, Kassis N, Arlet G, Mainardi JL, Doucet-Populaire F, Girard PM, Meynard JL. 2008. CAMPYL Study Group. Campylobacter bacteremia: clinical features and factors associated with fatal outcome. Clin. Infect. Dis. 47:790 –796. 8. Guzman-Herrador B, Vold L, Nygard K. 2012. Surveillance of travelassociated gastrointestinal infections in Norway, 2009 –2010: are they all actually imported? Euro Surveill. 17:20294. http://dx.doi.org/10.1086 /591530. 9. Strachan NJ, Rotariu O, Smith-Palmer A, Cowden J, Sheppard SK, O’Brien SJ, Maiden MC, Macrae M, Bessell PR, Matthews L, Reid SW, Innocent GT, Ogden ID, Forbes KJ. 2013. Identifying the seasonal origins of human campylobacteriosis. Epidemiol. Infect. 141:1267–1275. http://dx.doi.org/10.1017/S0950268812002063. 10. Lawes JR, Vidal A, Clifton-Hadley DA, Sayers R, Rodgers J, Snow L, Evans SJ, Powell LF. 2012. Investigation of prevalence and risk factors for Campylobacter in broiler flocks at slaughter: results from a UK survey. Epidemiol. Infect. 140:1725–1737. http://dx.doi.org/10.1017 /S0950268812000982. 11. Hoffmann S, Batz MB, Morris JG, Jr. 2012. Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J. Food Prot. 75:1292–1302. http://dx.doi.org/10.4315/0362 -028X.JFP-11-417.
Journal of Clinical Microbiology
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