Explosive increase of Salmonella Java in poultry in the Netherlands : Consequences for public health

sante pour exploiter les progrès en microbiologie moléculaire, et qu’elle reste associée à ce domaine en pleine expansion. Ceci implique d’investir au niveau national dans des programmes de formation à l’épidémiologie de terrain, et de maintenir en Europe le Programme européen de formation à l’épidémiologique d’intervention (European Programme for Intervention Epidemiology Training, EPIET) (12). Sans la possibilité d’évaluer rapidement les clusters moléculaires au niveau épidémiologique, les opportunités de prévention seront perdues.


S
almonella enterica Paratyphi B variation Java, or simply Java, began to increase alarmingly among chickens and in chicken products in the Netherlands in 2000.This serovar causes gastro-enteritis in humans through the consumption of contaminated food, but it can also be invasive, producing typhus-like clinical symptoms, and lead to outbreaks (1-4).In this article, we try to assess the potential threat to public health associated with the increase of Java among poultry in the Netherlands.

Trends in S. Java in The Netherlands and abroad
Results from the monitoring of chicken products by the KvW show that positive Java samples increased drastically, even though the total percentage of salmonella-positive samples more than
In 1998 and 2000, information via Enter-net (the European surveillance network for human infections involving salmonella and Verocytotoxin-producing E. coli) revealed a similar low level of salmonellosis due to Java in humans in other European countries.At meetings of the European NRLs in 1999 and 2000, NRL-Berlin and NRL-The Netherlands reported the same development of Java in poultry since 1995, and the explosive increase in 2000 (figure).The NRLs from other European countries considered that this was uniquely a German and Dutch problem.In December 2002, however, Scotland sent out a request for information via Enter-net regarding what seems to be an emerging problem in humans: the infection with multiresistant Java (see article pp35-40).

Antimicrobial resistance
The poultry sector in the Netherlands first encountered problems with Java in five chicken farms in 1996.Currently 50-100 farms are battling this infection.Java clones persist despite perfectly adequate quality control scores (8), whereas S. Enteritidis, Hadar, Infantis, Virchow etc, can be successfully eliminated with the standard cleaning and disinfection procedures.Still, Java was no more resistant to disinfectants than other serotypes found in the farms at the same time.
Java isolates found in poultry in the Netherlands are generally m u l t i r e s i s t a n t , i n contrast to the other serotypes (table 2).According to the resistance pattern, the human clones isolated from the 1980s until the mid-1990s most closely resemble the genetically diverse and antibiotic-sensitive strains prevalent in 1960-90s (9-11).The poultry isolates until 1 9 9 5 m o s t l i k e l y belong to a group deriving from a few clones multiresistant to chloramphenicol, sulphonamide, tetracycline, trimethoprim and often also kanamycin, neomycin and nalidixic acid (9).The isolates from 1996 onwards most likely derive from a recent clone, which had practically replaced all the others in poultry, and is resistant to trimethoprim in combination, to sulphonamide, streptomycin, nalidixic acid and ampicillin (9).This clone was also found in Germany by molecular typing for two isolates from poultry sent to the NRL-Berlin and, in December

Poulet / Chicken Homme / Human
Tous les sérotypes à l'exclusion de Java / S. Java S. Java All serotypes excluding Java 1984-1995 1996-2001 1984-1995 1996-2001 1984-1995 1996 ➤ A worrying development is the rapid increase in resistance of the Java clone against quinolones.Between 1996 and 2000, only 3% was flumequine-resistant, 19% in 2001 and 39% in 2002 (tables 2 and 3).Table 3 shows the shift occurring in the past four years towards higher MIC values for flumequine and ciprofloxacin.No evidence yet exists for clinical resistance to ciprofloxacin, but reduced sensitivity has been demonstrated.
According to German searchers, the development of resistance could be related to the high selection pressure due to vaccination and the intensive use of antibiotics in poultry farming, for example, to control the previous S. Enteritidis crisis (9).In 2000-01, 13% of flocks were treated with a quinolone, mainly flumequine.This resistance has developed much faster in Java than in other serotypes (table 2).The easy spreading of this resistant clones in chickens, and the persistence in the environment once a farm is infected are the likely reasons for the accelerated development of resistance.Besides, the high percentages of resistance (table 2) could be explained by therapeutic treatments of cotrimoxazole.The use of nitrofurans (furazolidone in table 2) has, however, been forbidden for more than 10 years.It seems that clonality of the strains is the determining factor for the (chromosomally determined) high level of resistance to furazolidone.

Transmission to humans
It is unclear why Java (up to now) seems innocuous to humans.However, recent PFGE-typing results show that the multiresistant poultry clone definitely crosses over to humans, which is consistent with the changed resistance pattern of Java among humans (table 2).Eleven out of 22 isolates preserved from the period 1998-2002 had a PFGE pattern identical to that of the Java poultry clone, and two unrelated isolates were associated to foreign travel.

Conclusions and recommendations
Until the end of 2002, the spreading of a resistant clone was considered as a local problem.However, in December 2002, a request for information from Scotland about an emerging Java problem in humans, revealed the clone involved could be traced back to isolates from poultry imported from Germany and Holland (see article pp35-40).This may cause a serious public health threat, especially given that fluoroquinolones are the first antibiotics of choice to treat a serious salmonellosis, and puts the problem into an international perspective.

Transmission à l'homme
Les raisons pour lesquelles Java semble (jusqu'à présent) inoffensif chez l'homme restent inconnues.Cependant, les récents résultats de typage en PFGE montrent clairement qu'un clone de volaille multirésistant se transmet à l'homme, ce qui concorde avec les modifications des profils de résistance de Java chez l'homme (tableau 2).Onze des 22 isolats prélevés en 1998-2002 avaient un profil PFGE identique au clone de Java de volaille, et deux isolats non apparentés ont été associés à des voyages à l'étranger.Aux Pays-Bas, les services de santé publique et les services vétérinaires, les instituts de recherches (RIVM, ID-Lelystad, le service de santé animale, et le KvW), ainsi que l'industrie avicole ont lancé des initiatives coordonnées pour traiter ce problème émergent.■ In the Netherlands, public health and veterinary services, research institutes (RIVM, ID Lelystad, the Animal Health Service and KvW), and the poultry industry have initiated coordinated initiatives to address this emerging issue.■ Introduction P oultry and poultry products, including meat and eggs, have long been recognised as an important source of food-borne infections caused by Salmonella enterica (1,2).The global increase in human infections with serovar Enteritidis observed in the late 1980's and early 1990's (3) was almost entirely attributable to the presence of this organism within the poultry production industry worldwide.However, the implementation of national monitoring programmes, together with control measures including vaccination, has resulted in recent years in a reduction in cases of human salmonellosis associated with the consumption of poultry and egg products in the UK (4).

Conclusions et recommandations
The Scottish Salmonella Reference Laboratory (SSRL) receives all strains of S. enterica isolated from cases of human infection from hospital laboratories.Regional veterinary laboratories, public analysts and water authorities submit isolates of animal, food and environmental origin.All isolates are fully serotyped, phage typed (where applicable), and tested for resistance to 15 antimi-➤

Figure
FigureRésultats positifs pour S. Java en proportion de tous les isolats de Salmonella dans les produits à base de poulet (KvW) et en nombre absolu d'isolats reçus par le LNR-Berlin / Positive results for S. Java as a proportion of all Salmonella isolates from chicken products and as absolute number of isolates received by the NRL-Berlin.

Progression de la résistance de Salmonella Paratyphi B var. Java isolée de divers produits de volaille. Resistance development of Salmonella Paratyphi B var. Java isolated from poultry materials
Les souches ont été isolées de divers produits dérivés du poulet (fécès, viande, peau du cou, caeca, etc.) d'après la distribution de la fréquence des valeurs de la CMI des isolats pour la ciprofloxacine et la fluméquine, analysés pour 1999-2000, 2001 et 2002 (jusqu'en novembre).Une résistance clinique pertinente apparaît dans les zones grisées, le taux de résistance est noté dans la dernière colonne.The strains were isolated from various materials derived from chicken (faeces, meat, neck skin, caeca, etc.), based on the frequency distribution of MIC values of isolates for ciprofloxacin and flumequine, tested in the periods 1999-2000, 2001 and 2002 (up through November).Clinical relevant resistance starts to be noted in the shaded areas, the resistance percentage is given in the last column.