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Decreasing Trend of Overlapping Multilocus Sequence Types between Human and Chicken Campylobacter jejuni Isolates over a Decade in Finland
Authors:C P A de Haan  R Kivist?  M Hakkinen  H Rautelin  M L H?nninen
Institution:Department of Food Hygiene and Environmental Health, University of Helsinki, Helsinki, Finland,1. Research Department, Finnish Food Safety Authority, Helsinki, Finland,2. Department of Bacteriology and Immunology, Haartman Institute, University of Helsinki and Helsinki University Central Hospital Laboratory, Helsinki, Finland,3. Department of Medical Sciences, University of Uppsala, Uppsala, Sweden4.
Abstract:We describe the long-term multilocus sequence typing (MLST) analysis of the population structure and dynamics of 454 Finnish human Campylobacter jejuni isolates, as well as 208 chicken isolates, collected during the mid-1990s to 2007. The sequence type clonal complexes (ST CC) ST-45 CC, ST-21 CC, and ST-677 CC were the most common ones found among all isolates, and they covered 73.9% of all isolates. The ST-283 CC also was found frequently among chicken isolates (8.2%). The predominant STs among all isolates were ST-45, ST-50, and ST-677. ST-137 and ST-230 were common among human isolates, and ST-267 was found more frequently among chicken isolates than human isolates. The ST-45 CC was significantly associated with chicken isolates (P < 0.01), whereas the ST-21 CC was associated with human isolates (P < 0.001). The ST-677 CC was not associated with any host (P = 0.5), and an opposite temporary trend of this complex was seen among chicken and human isolates, with an increase in the former and a decrease in the latter during the study period. Furthermore, the ST-22 and ST-48 CCs were significantly associated with human isolates (P < 0.01), but neither of the CCs was found in chicken isolates. The annual overlap between STs from human and chicken isolates decreased from 76% at the beginning of the study to 58% at the end. Our results suggest that the importance of chicken as a reservoir for strains associated with human infections has declined despite the consumption of domestic chicken meat increasing during the follow-up period by 83%.Campylobacter jejuni is the most common bacterial cause of gastroenteritis worldwide. In Finland, registered human Campylobacter infections have increased from 2,629 cases in 1996 to 4,107 cases in 2007 (http://www3.ktl.fi/stat/). Of the 4,107 cases in 2007, 45% were registered in the Helsinki-Uusimaa region, where the annual incidence was highest (122/100,000; the national average is 78/100,000) as well. Most of the cases were associated with traveling to other countries. In 2007, approximately 57% of the patients had traveled outside of Finland prior to their illness, 19% had not traveled abroad, and for 24% information was unavailable (http://www.ktl.fi/attachments/suomi/julkaisut/julkaisusarja_b/2008/2008b09.pdf).In Finland, most of the Campylobacter infections are sporadic and appear during the summer months (http://www.efsa.europa.eu/en/scdocs/doc/130r.pdf). Between 1996 and 2007, approximately 45 to 55% of all registered infections were reported between June and September (http://www3.ktl.fi/stat/). In contrast to sporadic Campylobacter infections, outbreaks of campylobacteriosis are uncommon, usually occurring in spring or autumn, and are associated with drinking contaminated water (36).Epidemiological studies performed in many countries indicate that handling or eating chicken meat is an important risk factor for the acquisition of campylobacteriosis (32, 46). A recent Finnish case-control study (39) identified swimming in lakes and rivers and drinking water from private wells as additional risk factors for acquiring the illness from domestic sources during the summer months. Contact with pets (19) and farm animals (21) and the consumption of raw milk (35) also have been identified as risk factors for Campylobacter infections.The annual consumption of chicken meat in Finland increased by 83% (from 53 million to 95 million kg) from 1997 to 2007 but remained stable, at around 83.5 million kg, between 2002 and 2006. However, from 2006 to 2007, the consumption of chicken meat increased by a further 8% (from 88 million to 95 million kg). Most of the chicken meat consumed in Finland comes from domestic production (https://portal.mtt.fi/portal/page/portal/mtt/mtt/julkaisut/suomenmaatalousjamaaseutuelinkeinot/jul108_SM2008.pdf). Finnish chicken flocks have been monitored for Campylobacter spp. according to the regulations of the European Union since 2004 (http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2003:325:0031:0040:EN:PDF). Seasonality similar to that observed in human infections can be found in the prevalence of Campylobacter-positive chicken slaughter batches, i.e., 7.7% of all chicken slaughter batches were Campylobacter positive from June to October in 2007; however, during the rest of the year no positive chicken flocks were detected (http://www.efsa.europa.eu/en/scdocs/doc/130r.pdf).To assess the relevance of a particular source and potential routes of transmission from animals to humans (6), the overlap between genotypes of Campylobacter isolates from patients and potential sources of infection has been studied using molecular typing techniques such as pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). Of the two typing methods, PFGE is more discriminatory and therefore is considered more suitable for short-term epidemiological investigations and for the determination of the source of infection in outbreak situations (24, 26, 28).In our previous studies, we have shown that during a seasonal peak, overlapping serotypes and PFGE genotypes exist between samples from patients suffering from campylobacteriosis and fecal samples from chicken (13, 17). Several other studies also have reported a 34 to 60% overlap between serotypes, genotypes, and/or sequence types (STs) of patient and poultry isolates using various typing techniques (20, 31, 37, 42).Due to the high diversity of types and the lack of standardized nomenclature, PFGE is not a useful technique in long-term epidemiological studies. Unlike PFGE, MLST has been successfully used in long-term epidemiological studies (27, 45) and in deciphering the population structure (2, 20, 28, 45) of Campylobacter on a global scale. MLST has high discriminatory power (23) and standardized nomenclature for STs and clonal complexes (CCs) (3, 26).The aim of our study was to analyze by MLST the overlap and dynamics of C. jejuni types among isolates collected from domestically acquired sporadic human infections from the Helsinki-Uusimaa region from 1996 to 2006 and isolates collected from domestic chicken production from 1999 to 2007.
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