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The epidemiological situation of Salmonella enteritidis in Poland
International Journal of Food Microbiology., 21 (1994) 21-30 © 1994 Elsevier Science B.V. All rights reserved 0168-1605/94/$07.00
21
FOOD 00670
The epidemiological situation of Salmonella enteritidis in Poland Renata Gtognicka and Danuta Kunikowska Institute of Maritime and Tropical Medicine in Gdynia, National Salmonella Centre, Gdynia, Poland
The epidemiological situation connected with S. enteritidis in Poland, in the years 1961-1991. is described. During this period there were two increases in infections and food poisonings, which were of an epidemiological character. The first epidemic, in 1962-1976, affected primarily small children and spread by contact in a hospital environment. It caused serious diseases, or dangerous complications in already existing illnesses, with high mortality. A few foci of later food poisonings were caused by infected meat or meat by-products. The second epidemic, which began in 1980 or 1981 and still exists, has already affected about 500000 persons. It has often concerned cases of sporadic infections, mainly in the case of small children, but it has not been of a hospital epidemic character. It has been far more frequently associated with food poisoning outbreaks caused by contaminated ice-cream, cream cakes, eggs, mayonnaise and, less frequently, by meat and meat by-products. Attention is drawn to the large number of humans transmitting S. enteritidis infections in Poland. Key words: Salmonella enteritidis; Epidemic; Food poisoning; Children's hospital infection
Introduction
Increased infections and food poisonings caused by S. enteritidis bacteria have been noted throughout almost the whole world (Baggesen et al., 1992; Barrow, 1992; Fantasia et al., 1992; Van de Giessen et al., 1992; Mason and Ebel, 1992; Notermans et al., 1992; Sharp et al., 1992). Food poisoning and infections caused by Salmonella bacilli have constituted a problem for many years in Poland and, as from 1978, have occupied first place amongst bacterial infections in humans (Dera-Tomaszewska, 1984; Gtognicka, 1986, 1992). Bacteriological research has been conducted for diagnostic purposes since 1946. Population studies also have been carried out. Their purpose was to eliminate from work or exclude from employment in trades or professions connected with the production or distribution of food, carriers of typhoid fever, Correspondence address: R. Gtognicka, Institute of Maritime and Tropical Medicine in Gdynia, National Salmonella Centre, Gdynia, Poland, 9 b Powstania Styczniowego Street, 81-519 Gdynia, Poland. Tel. 22-30-11 (249); Fax, 058-22-33-54. SSDI 0 1 6 8 - 1 6 0 5 ( 9 3 ) E 0 0 8 6 - 7
paratyphoids and another salmonelloses. Together with long-term prophylactic immunizations against typhoid fever, these steps have contributed greatly to the extensive elimination of such infections as S. typhi, and S. paratyphi A, B and C in Poland. They did not, however affect the spread of other serotypes of Salmonella, amongst which S. enteritidis bacilli, together with S. typhimurium showed the greatest expansiveness. Already, in the years 1946-1956, S. enteritidis was isolated from 1743 persons, including 85% of sick people (Buczowski, 1961). Two epidemics of S. enteritidis with atypical and different courses noted in Poland in 1961 to 1991 are described in this paper.
Origin and methods of collecting material Examinations for enteric pathogens of different materials from humans were conducted at sanitary-epidemiological stations and in some hospital laboratories. The samples examined came from patients, convalescents, carriers, healthy persons, their environments, outbreaks of food poisoning, persons employed or applying for employment in various food-related institutions (it is forbidden to employ persons excreting enteric pathogens in these institutions). Moreover, several laboratories submitted products of animal origin, food and feed, for bacteriological examination. In cooperation with field laboratories, the National Salmonella Centre received cultures suspected of belonging to the Salmonella group, in order to diagnose them, or confirm diagnosis. Strains of S. typhi, S. paratyphi, B, S. typhimurium and S. enteritidis were also received for bacteriophage typing. Together with cultures, the field laboratories used, submitted forms containing information necessary, from the epidemiological point of view, about persons (carriers, covalescent, healthy) from whom the cultures had been isolated. Apart from the record-forms sent to the National Centre, the following sources were used for collecting epidemiological information: archives of field laboratories and some infectious diseases hospitals; Ministry of health reports concerning outbreaks of food poisoning. Data were also obtained from statistics recorded by the National Institute of Hygiene and those maintained by some veterinary institutions. With the introducing of martial law in 1981, it was forbidden to collecting of data concerning salmonellosis infections in 1980 and 1981. It means that information concerning such infections in Poland in the years 1982 and 1983, was incomplete.
Results and Discussion In Poland, S. enteritidis humans as from 1946, and number of persons from Salmonella were isolated
bacteria were isolated in the few cases of infection in about 160 were noted annually (Buczowski, 1961). The whom S. enteritidis and other serological types of in the particular years (excluding S. typhi and S.
23 TABLE I Salmonellosis in humans in Poland (1961-1991) Year
1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991
Number of persons
s. enteritidis
Other Salmonella serotypes
Total
256 1036 2199 4539 7570 6958 7214 4885 4840 4006 4109 4513 2184 2277 2156 1027 842 1795 9053 11808 27656 41757 54 893 59825 83 748 70599 66 276 72124
4 725 3414 3 520 2192 2 946 3 629 5240 6162 12174 9 699 7 713 10434 10766 14041 13017 7869 10 801 17434 17469 17261 20143 23 288 14 692 14 826 11412 8 065 5 855 4767
4981 4450 5 7t9 6731 10516 10587 12454 11047 17014 13 705 11822 14947 12950 16318 15173 8 896 11643 19229 26522 29069 47 799 65 045 69585 74 651 95160 78 664 72131 76891
paratyphi A, B a n d C bacilli) can be s e e n in T a b l e I. T h e p e r c e n t a g e s of S. enteritidis a n d two p r e d o m i n a n t Salmonella serotypes, isolated from h u m a n s , are shown in T a b l e II. A b o u t 40 o t h e r serotypes were identificated. T h e i n c r e a s i n g p e r c e n t a g e of S. enteritidis i n f e c t i o n s since 1962 r e a c h e d 93.8% in 1991. Significant d e c r e a s e of S. typhimurium, S. agona a n d o t h e r Salmonella serotypes infections in h u m a n s was also observed. T h e first e p i d e m i c of S. enteritidis o c c u r r e d in P o l a n d d u r i n g the p e r i o d from 1962 to 1976, a n d the i n f e c t i o n affected 59513 persons. T h e course of the e p i d e m i c s is p r e s e n t e d in the Fig. 1. A r a p i d increase in the n u m b e r of cases was o b s e r v e d in the initial years: in 1962, 4-fold; in 1964, 18-fold; a n d in 1965, a b o u t 30-fold, as c o m p a r e d with 1961. T h e r e was a g r a d u a l drop in the n u m b e r of cases n o t e d over a p e r i o d of 9 years ( T a b l e I). I n f e c t i o n with S. enteritidis s p r e a d m a i n l y in c h i l d r e n ' s hospitals (age 0 - 1 4 years) a n d was n o t e d over almost the whole of P o l a n d . T h e sources of infection
24
BOO0
--
7000
--
6000
--
5000
--
4000
--
3000
--
-
-
S, enteritidls
/ /
E
/ /' //
2000
/
--
1000
// /
--
/
Yx
/
/
'
0
'
i
!
Ynlof!
Fig. 1. S. enteritidis in h u m a n s
in P o l a n d
(1961-1978).
were most frequently sick children brought to hospitals as patients. The strains of S. enter#idis excreted by them constituted the source of contact infections which were spread through the medium of personnel, diapers, bed linen, equipment, insects, droplet infection. The percentage of children infected in hospitals was between 12 and 90% (Magdzik and Anusz, 1973). Epidemics within hospitals spread rapidly. The majority of infections caused by S. enteritidis were observed among the newborn (especially premature babies) and infants, less frequently infants of up to one year, often weak, with accompanying diseases and underweight. The course of the disease was more serious and mortality, higher in the younger children. The mortality (caused by S. enteritidis) among the newborns was 25%, among the infants 6-8% (Anusz, 1970). In older children and adults, a short-lasting gastroenteritis or asymptomatic form was usually observed. Throughout the whole epidemic, the percentage of those sick was very high and fluctuated between 85 and 92% (Fig. 3). Food poisoning foci were rarely observed, the food products infected being mainly meat and meat products (Pietkiewicz and Buczowski, 1969). Lalko (1977), however, noted a focus of food poisoning caused by S. enteritidis-contaminated ice-cream. From the clinical point of view, most cases were in the form of diarrhoea, rarely in the septic form, occasionally with neurological symptoms or with the majority of symptoms in the respiratory tract, urinary system, or local inflamation. S. enteritidis strains were most frequently isolated from the faeces of sick children, less frequently from urine, blood, or from the nose or nasal-pharyngeal cavity. Strains were also cultivated from pus and organs taken during autopsies.
25 The consequence of infection and illness was a carrier state which is maintained for several or many months (Buczowski, 1970). The strains of S. enteritidis were resistant to the majority of antibiotics used by Anusz (1970). Of over 2000 strains typed by Lalko (1977) with her own group of bacteriophages, those most frequent were phage types 8, 5 and 7. In the opinion of Magdzik and Anusz (1973), that epidemic was probably independent of infections existing in the animal world. Studies conducted by Buczowski et al. (1970), which included farm animals (cattle, calves, pigs, chickens and ducks), their surroundings and feed, as well as plants manufacturing food products (slaughter-houses and butchers), indicated the presence of single strains of S. enteritidis in pigs, and in post-slaughter material from calves and ducks. No S. enteritidis bacilli were found in eggs. A considerable decrease in infections caused by S. enteritidis bacteria was noted in 1977. An increase in Salmonella infections was noted in 1978, when there were two serious epidemics of S. enteritidis: one caused by milk (822 cases) and the second by ice-cream (492 cases) (Anusz, 1980). An increase in salmonellosis was noted in pigs, cattle and, particularly, poultry in 1971-1978 (Anusz, 1980). A second S. enteritidis epidemic probably commenced in Poland in 1980 or 1981. Its course and comparison with the previous epidemic are illustrated in Tables I and II and in Fig. 2. The smallest number of infections with these bacteria in humans (842 cases) was noted in 1977. An ll-fold increase was observed in 1982, 33-fold in 1984, 65-fold in 1986 and almost 100-fold in 1988, as against the number of S. enteritidis cases in humans in 1977. Infections in 1989, 1990 and 1991 were 80-times greater than this number of cases (Table I). The increasing percentages of S. enteritidis infections since 1977 reached 93.8% in 1991 (Table II), with significant decrease of other Salmonella serotype infections in men. The existing S. enteritidis epidemic mainly involved, up until 1986, sporadic infections, primarily in small children. Increasing numbers of loci of food poisoning appeared, however, these having predominated among infections as from 1987. The percentage of sick persons dropped to 60% (Fig. 3); S. enteritidis was isolated from healthy persons more frequently than in the previous epidemic. Infections with S. enteritidis in hospitals continue to be frequent, but their course is not so dramatic as described previously. From 1987 to 1991, the greater number of sick persons were from foodborne outbreaks, with a predominance of adults. About 45% of persons with sporadic infections and food poisoning were hospitalized. Official data in Poland give a very low mortality as the result of salmonellosis in humans. During the years 1975-1991 salmonellosis percentages an increase from 37.5 to 91.3% among all bacterial foodborne diseases in Poland was observed (Table III). The main cause of food poisonings by S. enteritidis became eggs and egg products. Smaller epidemics, from several to several dozen persons infected, were caused by cakes, creams and mayonnaise. Ice-cream and cream cakes were the , cause of many epidemics, often affecting several hundred persons. The incubation time of S. enteritidis in such foodborne infections, fluctuated from one hour to 12
26 TABLE II
The percentages of S. enteritidis and other predominant Salmonella serotypes in humans in Poland Year
1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991
Salmonella serotypes (%) S. enter#idis
S. typhimurium
4.5 23.2 38.5 67.5 72.0 65.9 57.8 44.3 28.4 29.2 34.8 30.2 16.8 13.9 14.2 11.7 6.9 9.7 35.5 40.7 57.9 64.4 79.0 76.2 88.1 89.9 91.9 93.8
38.7 50.9 25.9 19.3 17.2 15.1 16.5 22.5 25.9 20.2 28.5 22.6 30.6 32.7 29.5 40.2 49.9 45.2 39.2 36.4 23.9 18.1 13.2 12.9 7.5 6.8 5.0 2.8
Total number S. agona 0.2 0.8 11.0 13.8 12.5 9. l 14.4 19.6 24.4 21.6 14.9 12.9 11.2 4.3 3.2 1.2 0.8 0.2 0.2
Other serotypes
of persons (100%)
56.8 25.9 35.6 13.2 10.8 19.0 25.7 33.2 45.7 50.4 35.9 36.2 38.8 40.9 47.2 33.7 23.6 20.7 3.7 8.0 5.3 6.3 3.5 7.7 3.2 2.5 2.9 3.2
4981 4450 5 719 6 731 10516 10587 12 454 11047 17014 13 705 11822 14 947 12950 16318 15 173 8 896 11643 19 229 26 522 29069 47 799 65 045 69585 74651 95 160 78 664 72131 76891
days; the average was 12-24 h. The S. enteritidis bacteria were isolated from over 80% of patients in the foci, as well as from cakes, creams, ice-cream and egg mass used in the production of such goods. Large foci of food poisoning were usually accompanied by secondary contact infection, mainly in small children. The cause of the food poisoning was rarely meat or meat by-products. This was due to the introduction of food restrictions and rationing from 1981-1989. Eggs were not rationed. Egg-products examined by Maciak and Kubifiski (1990) shoved a high degree of Salmonella contamination: 15% of 20 egg-pulp samples were contaminated with S. enteritidis and S. gallinarurn; 24.61% of 65 egg-powder samples were contaminated and only S. enteritidis was isolated. The main symptoms of disease described were acute gastroenterocolitis with high temperature. Cases of septic infection, inflammation of the respiratory tract, urocystitis, pyelitis, or atypical forms of influenza appeared rarely (Prokopowicz,
1986).
27
90000
-[,
80000
" I
70000
$, entlritidil
/ \~
~
I --"-0'-- Other Salmonella ~
//
- -
i
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i
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/ 5oo00
, "
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/ 30000 T 20000 -10000
m
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m
m
~
m
m
~
m
~
m
m
~
m
m
m ~
m
m
m
m
m
Yllll
Fig. 2. S. enteritidb in humans in Poland (1961-1991).
100.00
-fi [
90.00 ~
~°°°~',i ~
ii 3o.o0-
o.o0 ,-
'~' ~ healthy
~!
~
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.
.
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,
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vea~
Fig. 3. Percentage of healthy and sick persons positive for S. enteritidis.
,
i
28 TABLE III Foodborne diseases caused by" Sa&tonella and other bacteria in the years 1975-1991 (percentages) Year
Salmonellosis
Other bacteria ~
1975 1976 1977 1978 1979 1980 198l 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991
37.5 25.0 34.4 62.3 46.5 66.4 64.2 58.2 60.5 72.8 75.5 77.0 83.5 86.3 89.2 87.4 91.3
62.5 75.0 65.6 37.7 53.5 33.6 35.8 41.8 39.5 27.2 24.5 23.0 16.5 13.7 10.8 12.6 8.7
a
Shigella, Staphylococcus, Clostridium botulinum
and not identified.
Strains of S. enteritidis were most frequently isolated from the faeces of both sick and healthy humans, but rarely from other material (urine, blood, pus). The cultivated strains indicated considerable resistance to the antibiotics used (Chloramphenicol, Erythromycin, Neomycin, Gentamycin, Colistin, Oxytetracycline, Ampicilin). The bacteriophage typing of about 2100 strains in the years 1980-1990 by Glognicka et al. (1990), after Lalko's schema (1977), illustrated that the majority of them belonged to phage types 7, 1 and 6. The most frequently described bacteriophage type in S. enteritid& infections and food poisonings worldwide, is type PT4 (Barrow, 1992). Comparison of lytic activity of this phage and the phages from Lalko's schema is under investigation. The results of official studies on animals have confirmed the presence of Salmonella in all species. As shown by Wojtofi (1989), these studies embraced almost solely sick or dead individuals, as well as meat from slaughter-houses and butchers. Checks at chosen veterinary field laboratories confirm a modest degree of infection by S. enteritidis in calves, pigs and cattle, and a tremendous degree in the case of poultry and eggs on poultry farms. Bacteriological tests of feed and raw materials used for its production, were carried out. The presence of many serotypes of Salmonella, but not S. enteritidis bacilli, was noted. Summing up the results presented, it can be noted that the S. enteritidis infections occurring in Poland over the 30 years in question, caused dangerous epidemics. Although the first was smaller as regards number, it caused serious diseases and the death of many children. The second epidemic, on the other hand, has been milder in course, but has affected 10-times more people and is currently
29 still in existence, a l t h o u g h cases of S. enteritidis food p o i s o n i n g have fallen slightly. Results of b a c t e r i o p h a g e typing indicate that a r e l a t i o n s h i p exists b e t w e e n the two epidemics: that S. enteritidis type 7 strains occur in both. T h e r e is no d o u b t that the p o o r state of h e a l t h of the Polish p o p u l a t i o n i n f l u e n c e s such n u m b e r of cases of salmonellosis. T h e p r e d o m i n a n t p r o d u c t s involved in food p o i s o n i n g were eggs, b u t o n e c a n n o t omit the role of m e a t a n d m e a t by-products, which were fairly f r e q u e n t l y the cause of the disease. A n i m p o r t a n t role, however, in the t r a n s m i s s i o n of infections, is played by h u m a n s .
References Anusz, Z. (1970) Wra~,liwog6na antybiotyki, sulfatiazol i nitrofurantoin~ szczep6w Salmonella wyosobnionych od zwierzat na terenie Polski w latach 1967-1968. Przeg. Epidemiol. 24, 305-312. Anusz, Z. (1980) Salmonelozy u ludzi i zwierz~t w Polsce w latach 1971-1978. Meal. Wet. 36, 265-267. Anusz, Z. (1989) Aspekty epidemiologiczne drobnoustroj6w Salmonella. Materiaty Sesji Naukowej "Problemy Drobnoustroj6w Salmonella w Srodowisku ludzi i Zwierz~t". Mi~dzyzdroje, Polska, 21-22. Sept. Ref. III pp. 1-9. Baggesen, D.L., Brown, D.J., Gaarslev, K., Olsen, J.E. and Bisgaard, M. (1992) Characterization of Danish isolates of Salmonella enterica serovar Enteritidis by phage typing and plasmid profiling comparison of strains obtained from man and broilers. International Symposium on Salmonella and Salmonellosis in Ploufragan, France, 15-17, Sept. Proceedings Posters, pp. 147-148. Barrow, P.A. (1992) Salmonellosis in Poultry. International Symposium on Salmonella and SalmonelIosis in Ploufragan, France, 15-17. Sept. Reports and Communications, pp. 141-163. Buczowski, Z. (1961) Salmonelloses of man diagnosed in the years 1946-1956 in Poland. Bull. Inst. Mar. Med. 12, 51-71. Buczowski, Z. and Pietkiewicz, K. (1969) Salmonelozy ludzi rozpoznane w Polsce w ostatnim dwudziestoleciu. Materiaty Konferencji Naukowej "Salmonelozy", Gdafisk-Gdynia, Polska, 19-20 Sept., pp. 7-15. Buczowski, Z., Strzelecki, E., Pietkiewicz, K. and Cader-Strzelecka, B. (1970) Bakterie Salmonella u niekt6rych gatunk6w zwierz~t w Polsce. Przeg. Epidemiol. 24, 293-304. Dera-Tomaszewska, B. (1984) Serological types of Salmonella bacilli isolated from men in Poland between 1967 and 1978. Bull. Instr. Mar. Trop. Med. Gdynia 35, 56-72. Fantasia, M., Filetici, E. and Anastasio, M.P. (1992) Phage types, resistance types and plasmid profiles of Salmonella enteritidis isolates, Italy, 1986-1991. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Proceedings Posters, pp. 153-156. Van de Giessen, A.W., Frankena, K., Van Leeuwen, W.H. and Notermans, S.H.W. (1992) An approach for monitoring Salmonella serotypes in farm animals. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Reports and Communications, pp. 375-385. Gtognicka, R. (1986) Salmonellosis in Poland. 2nd World Congress Foodborne Infections and Intoxications. Berlin, Germany, 26-30 May, Proceedings Vol. II, pp. 1223-1224. Gtognicka, R. (1992) Salmonella surveillance in Poland. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Proceedings Posters, pp. 157-158. Gtognicka, R., Kunikowska, D., Dziadziuszko, H. and Tokarska-Klunejko, E. (1990) Distribution of Salmonella enteritidis phage types in Poland in 1981-1990. Bull. Inst. Mar. Trop. Med. Gdynia 41, 145-148. Lalko, J. (1977) Salmonella enteritidis bacteriophage typing. Bull. Instr. Mar. Trop. Med. Gdynia 28, 187-194. Maciak, T. and Kubifiski, T. (1990) Paleczki Salmonella w produktach spo£'ywczych pochodzenia zwierz~cego w gwietle badafi ZHW w Warszawie. Med. Wet. 46, 305-307.
30 Magdzik, W. and Anusz, Z. (1973) Salmonelozy odzwierz~ce (Salmonellosis). In: J. Kostrzwski (Ed.). Choroby zaka2ne w Polsce i ich zwalczanie w latach 1961-1970. P.Z.W.L., Warszawa, pp. 152-169. Mason, J. and Ebel, E. (1992) Report of the current status of the United States Department of Agriculture Salmonella enteritidis Control Program. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Reports and Communications, pp. 312-325. Notermans, S.H.W., Van de Giessen, A.W. and Oosterom, J. (1992) Aspects of intervention measures to reduce human infections with Salmonella. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Reports and Communications, pp. 235-244. Pietkiewicz, K., Buczowski, Z. (1969) Salmonellosis in man in Poland 1957-1966. Publ. Hlth. Rep. 84, 712-720. Prokopowicz, D. (1989) Obraz kliniczny i leczenie salmoneloz cztowieka. Materialy Sesji Naukowej. Problemy Drobnoustroj6w Salmonella w Srodowisku Ludzi i Zwierz~t. Mi~dzyzdroje, Polska, 21-22 Sept. Ref. VII. pp. 1-15. Sharp, J.C.M., Reilly, W.J., Munro, D.S. and Girwood, R.W.A. Salmonellosis in Scotland: an integrated inter-disciplinary approach. International Symposium on Salmonella and Salmonellosis. Ploufragna, France, 15-17 Sept. Reports and Communications, pp. 333-340. Wojtofi, B. (1989) Przyczyny i uwarunkowania wyst~powania Salmonel w £'ywnogci zwierz~cego pochodzenia. Materiaty Sesji Naukowej, Problemy Drobnoustroj6w Salmonella w Srodowisku Ludzi i Zwierz~t. Mi~dzyzdroje, Polska, 21-22 Sept. Ref. IV. pp. 1-10.
21
FOOD 00670
The epidemiological situation of Salmonella enteritidis in Poland Renata Gtognicka and Danuta Kunikowska Institute of Maritime and Tropical Medicine in Gdynia, National Salmonella Centre, Gdynia, Poland
The epidemiological situation connected with S. enteritidis in Poland, in the years 1961-1991. is described. During this period there were two increases in infections and food poisonings, which were of an epidemiological character. The first epidemic, in 1962-1976, affected primarily small children and spread by contact in a hospital environment. It caused serious diseases, or dangerous complications in already existing illnesses, with high mortality. A few foci of later food poisonings were caused by infected meat or meat by-products. The second epidemic, which began in 1980 or 1981 and still exists, has already affected about 500000 persons. It has often concerned cases of sporadic infections, mainly in the case of small children, but it has not been of a hospital epidemic character. It has been far more frequently associated with food poisoning outbreaks caused by contaminated ice-cream, cream cakes, eggs, mayonnaise and, less frequently, by meat and meat by-products. Attention is drawn to the large number of humans transmitting S. enteritidis infections in Poland. Key words: Salmonella enteritidis; Epidemic; Food poisoning; Children's hospital infection
Introduction
Increased infections and food poisonings caused by S. enteritidis bacteria have been noted throughout almost the whole world (Baggesen et al., 1992; Barrow, 1992; Fantasia et al., 1992; Van de Giessen et al., 1992; Mason and Ebel, 1992; Notermans et al., 1992; Sharp et al., 1992). Food poisoning and infections caused by Salmonella bacilli have constituted a problem for many years in Poland and, as from 1978, have occupied first place amongst bacterial infections in humans (Dera-Tomaszewska, 1984; Gtognicka, 1986, 1992). Bacteriological research has been conducted for diagnostic purposes since 1946. Population studies also have been carried out. Their purpose was to eliminate from work or exclude from employment in trades or professions connected with the production or distribution of food, carriers of typhoid fever, Correspondence address: R. Gtognicka, Institute of Maritime and Tropical Medicine in Gdynia, National Salmonella Centre, Gdynia, Poland, 9 b Powstania Styczniowego Street, 81-519 Gdynia, Poland. Tel. 22-30-11 (249); Fax, 058-22-33-54. SSDI 0 1 6 8 - 1 6 0 5 ( 9 3 ) E 0 0 8 6 - 7
paratyphoids and another salmonelloses. Together with long-term prophylactic immunizations against typhoid fever, these steps have contributed greatly to the extensive elimination of such infections as S. typhi, and S. paratyphi A, B and C in Poland. They did not, however affect the spread of other serotypes of Salmonella, amongst which S. enteritidis bacilli, together with S. typhimurium showed the greatest expansiveness. Already, in the years 1946-1956, S. enteritidis was isolated from 1743 persons, including 85% of sick people (Buczowski, 1961). Two epidemics of S. enteritidis with atypical and different courses noted in Poland in 1961 to 1991 are described in this paper.
Origin and methods of collecting material Examinations for enteric pathogens of different materials from humans were conducted at sanitary-epidemiological stations and in some hospital laboratories. The samples examined came from patients, convalescents, carriers, healthy persons, their environments, outbreaks of food poisoning, persons employed or applying for employment in various food-related institutions (it is forbidden to employ persons excreting enteric pathogens in these institutions). Moreover, several laboratories submitted products of animal origin, food and feed, for bacteriological examination. In cooperation with field laboratories, the National Salmonella Centre received cultures suspected of belonging to the Salmonella group, in order to diagnose them, or confirm diagnosis. Strains of S. typhi, S. paratyphi, B, S. typhimurium and S. enteritidis were also received for bacteriophage typing. Together with cultures, the field laboratories used, submitted forms containing information necessary, from the epidemiological point of view, about persons (carriers, covalescent, healthy) from whom the cultures had been isolated. Apart from the record-forms sent to the National Centre, the following sources were used for collecting epidemiological information: archives of field laboratories and some infectious diseases hospitals; Ministry of health reports concerning outbreaks of food poisoning. Data were also obtained from statistics recorded by the National Institute of Hygiene and those maintained by some veterinary institutions. With the introducing of martial law in 1981, it was forbidden to collecting of data concerning salmonellosis infections in 1980 and 1981. It means that information concerning such infections in Poland in the years 1982 and 1983, was incomplete.
Results and Discussion In Poland, S. enteritidis humans as from 1946, and number of persons from Salmonella were isolated
bacteria were isolated in the few cases of infection in about 160 were noted annually (Buczowski, 1961). The whom S. enteritidis and other serological types of in the particular years (excluding S. typhi and S.
23 TABLE I Salmonellosis in humans in Poland (1961-1991) Year
1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991
Number of persons
s. enteritidis
Other Salmonella serotypes
Total
256 1036 2199 4539 7570 6958 7214 4885 4840 4006 4109 4513 2184 2277 2156 1027 842 1795 9053 11808 27656 41757 54 893 59825 83 748 70599 66 276 72124
4 725 3414 3 520 2192 2 946 3 629 5240 6162 12174 9 699 7 713 10434 10766 14041 13017 7869 10 801 17434 17469 17261 20143 23 288 14 692 14 826 11412 8 065 5 855 4767
4981 4450 5 7t9 6731 10516 10587 12454 11047 17014 13 705 11822 14947 12950 16318 15173 8 896 11643 19229 26522 29069 47 799 65 045 69585 74 651 95160 78 664 72131 76891
paratyphi A, B a n d C bacilli) can be s e e n in T a b l e I. T h e p e r c e n t a g e s of S. enteritidis a n d two p r e d o m i n a n t Salmonella serotypes, isolated from h u m a n s , are shown in T a b l e II. A b o u t 40 o t h e r serotypes were identificated. T h e i n c r e a s i n g p e r c e n t a g e of S. enteritidis i n f e c t i o n s since 1962 r e a c h e d 93.8% in 1991. Significant d e c r e a s e of S. typhimurium, S. agona a n d o t h e r Salmonella serotypes infections in h u m a n s was also observed. T h e first e p i d e m i c of S. enteritidis o c c u r r e d in P o l a n d d u r i n g the p e r i o d from 1962 to 1976, a n d the i n f e c t i o n affected 59513 persons. T h e course of the e p i d e m i c s is p r e s e n t e d in the Fig. 1. A r a p i d increase in the n u m b e r of cases was o b s e r v e d in the initial years: in 1962, 4-fold; in 1964, 18-fold; a n d in 1965, a b o u t 30-fold, as c o m p a r e d with 1961. T h e r e was a g r a d u a l drop in the n u m b e r of cases n o t e d over a p e r i o d of 9 years ( T a b l e I). I n f e c t i o n with S. enteritidis s p r e a d m a i n l y in c h i l d r e n ' s hospitals (age 0 - 1 4 years) a n d was n o t e d over almost the whole of P o l a n d . T h e sources of infection
24
BOO0
--
7000
--
6000
--
5000
--
4000
--
3000
--
-
-
S, enteritidls
/ /
E
/ /' //
2000
/
--
1000
// /
--
/
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/
/
'
0
'
i
!
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Fig. 1. S. enteritidis in h u m a n s
in P o l a n d
(1961-1978).
were most frequently sick children brought to hospitals as patients. The strains of S. enter#idis excreted by them constituted the source of contact infections which were spread through the medium of personnel, diapers, bed linen, equipment, insects, droplet infection. The percentage of children infected in hospitals was between 12 and 90% (Magdzik and Anusz, 1973). Epidemics within hospitals spread rapidly. The majority of infections caused by S. enteritidis were observed among the newborn (especially premature babies) and infants, less frequently infants of up to one year, often weak, with accompanying diseases and underweight. The course of the disease was more serious and mortality, higher in the younger children. The mortality (caused by S. enteritidis) among the newborns was 25%, among the infants 6-8% (Anusz, 1970). In older children and adults, a short-lasting gastroenteritis or asymptomatic form was usually observed. Throughout the whole epidemic, the percentage of those sick was very high and fluctuated between 85 and 92% (Fig. 3). Food poisoning foci were rarely observed, the food products infected being mainly meat and meat products (Pietkiewicz and Buczowski, 1969). Lalko (1977), however, noted a focus of food poisoning caused by S. enteritidis-contaminated ice-cream. From the clinical point of view, most cases were in the form of diarrhoea, rarely in the septic form, occasionally with neurological symptoms or with the majority of symptoms in the respiratory tract, urinary system, or local inflamation. S. enteritidis strains were most frequently isolated from the faeces of sick children, less frequently from urine, blood, or from the nose or nasal-pharyngeal cavity. Strains were also cultivated from pus and organs taken during autopsies.
25 The consequence of infection and illness was a carrier state which is maintained for several or many months (Buczowski, 1970). The strains of S. enteritidis were resistant to the majority of antibiotics used by Anusz (1970). Of over 2000 strains typed by Lalko (1977) with her own group of bacteriophages, those most frequent were phage types 8, 5 and 7. In the opinion of Magdzik and Anusz (1973), that epidemic was probably independent of infections existing in the animal world. Studies conducted by Buczowski et al. (1970), which included farm animals (cattle, calves, pigs, chickens and ducks), their surroundings and feed, as well as plants manufacturing food products (slaughter-houses and butchers), indicated the presence of single strains of S. enteritidis in pigs, and in post-slaughter material from calves and ducks. No S. enteritidis bacilli were found in eggs. A considerable decrease in infections caused by S. enteritidis bacteria was noted in 1977. An increase in Salmonella infections was noted in 1978, when there were two serious epidemics of S. enteritidis: one caused by milk (822 cases) and the second by ice-cream (492 cases) (Anusz, 1980). An increase in salmonellosis was noted in pigs, cattle and, particularly, poultry in 1971-1978 (Anusz, 1980). A second S. enteritidis epidemic probably commenced in Poland in 1980 or 1981. Its course and comparison with the previous epidemic are illustrated in Tables I and II and in Fig. 2. The smallest number of infections with these bacteria in humans (842 cases) was noted in 1977. An ll-fold increase was observed in 1982, 33-fold in 1984, 65-fold in 1986 and almost 100-fold in 1988, as against the number of S. enteritidis cases in humans in 1977. Infections in 1989, 1990 and 1991 were 80-times greater than this number of cases (Table I). The increasing percentages of S. enteritidis infections since 1977 reached 93.8% in 1991 (Table II), with significant decrease of other Salmonella serotype infections in men. The existing S. enteritidis epidemic mainly involved, up until 1986, sporadic infections, primarily in small children. Increasing numbers of loci of food poisoning appeared, however, these having predominated among infections as from 1987. The percentage of sick persons dropped to 60% (Fig. 3); S. enteritidis was isolated from healthy persons more frequently than in the previous epidemic. Infections with S. enteritidis in hospitals continue to be frequent, but their course is not so dramatic as described previously. From 1987 to 1991, the greater number of sick persons were from foodborne outbreaks, with a predominance of adults. About 45% of persons with sporadic infections and food poisoning were hospitalized. Official data in Poland give a very low mortality as the result of salmonellosis in humans. During the years 1975-1991 salmonellosis percentages an increase from 37.5 to 91.3% among all bacterial foodborne diseases in Poland was observed (Table III). The main cause of food poisonings by S. enteritidis became eggs and egg products. Smaller epidemics, from several to several dozen persons infected, were caused by cakes, creams and mayonnaise. Ice-cream and cream cakes were the , cause of many epidemics, often affecting several hundred persons. The incubation time of S. enteritidis in such foodborne infections, fluctuated from one hour to 12
26 TABLE II
The percentages of S. enteritidis and other predominant Salmonella serotypes in humans in Poland Year
1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991
Salmonella serotypes (%) S. enter#idis
S. typhimurium
4.5 23.2 38.5 67.5 72.0 65.9 57.8 44.3 28.4 29.2 34.8 30.2 16.8 13.9 14.2 11.7 6.9 9.7 35.5 40.7 57.9 64.4 79.0 76.2 88.1 89.9 91.9 93.8
38.7 50.9 25.9 19.3 17.2 15.1 16.5 22.5 25.9 20.2 28.5 22.6 30.6 32.7 29.5 40.2 49.9 45.2 39.2 36.4 23.9 18.1 13.2 12.9 7.5 6.8 5.0 2.8
Total number S. agona 0.2 0.8 11.0 13.8 12.5 9. l 14.4 19.6 24.4 21.6 14.9 12.9 11.2 4.3 3.2 1.2 0.8 0.2 0.2
Other serotypes
of persons (100%)
56.8 25.9 35.6 13.2 10.8 19.0 25.7 33.2 45.7 50.4 35.9 36.2 38.8 40.9 47.2 33.7 23.6 20.7 3.7 8.0 5.3 6.3 3.5 7.7 3.2 2.5 2.9 3.2
4981 4450 5 719 6 731 10516 10587 12 454 11047 17014 13 705 11822 14 947 12950 16318 15 173 8 896 11643 19 229 26 522 29069 47 799 65 045 69585 74651 95 160 78 664 72131 76891
days; the average was 12-24 h. The S. enteritidis bacteria were isolated from over 80% of patients in the foci, as well as from cakes, creams, ice-cream and egg mass used in the production of such goods. Large foci of food poisoning were usually accompanied by secondary contact infection, mainly in small children. The cause of the food poisoning was rarely meat or meat by-products. This was due to the introduction of food restrictions and rationing from 1981-1989. Eggs were not rationed. Egg-products examined by Maciak and Kubifiski (1990) shoved a high degree of Salmonella contamination: 15% of 20 egg-pulp samples were contaminated with S. enteritidis and S. gallinarurn; 24.61% of 65 egg-powder samples were contaminated and only S. enteritidis was isolated. The main symptoms of disease described were acute gastroenterocolitis with high temperature. Cases of septic infection, inflammation of the respiratory tract, urocystitis, pyelitis, or atypical forms of influenza appeared rarely (Prokopowicz,
1986).
27
90000
-[,
80000
" I
70000
$, entlritidil
/ \~
~
I --"-0'-- Other Salmonella ~
//
- -
i
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i
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/ 5oo00
, "
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/ 30000 T 20000 -10000
m
~
m
m
m
m
~
m
m
~
m
~
m
m
~
m
m
m ~
m
m
m
m
m
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Fig. 2. S. enteritidb in humans in Poland (1961-1991).
100.00
-fi [
90.00 ~
~°°°~',i ~
ii 3o.o0-
o.o0 ,-
'~' ~ healthy
~!
~
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.
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.
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,
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,
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vea~
Fig. 3. Percentage of healthy and sick persons positive for S. enteritidis.
,
i
28 TABLE III Foodborne diseases caused by" Sa&tonella and other bacteria in the years 1975-1991 (percentages) Year
Salmonellosis
Other bacteria ~
1975 1976 1977 1978 1979 1980 198l 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991
37.5 25.0 34.4 62.3 46.5 66.4 64.2 58.2 60.5 72.8 75.5 77.0 83.5 86.3 89.2 87.4 91.3
62.5 75.0 65.6 37.7 53.5 33.6 35.8 41.8 39.5 27.2 24.5 23.0 16.5 13.7 10.8 12.6 8.7
a
Shigella, Staphylococcus, Clostridium botulinum
and not identified.
Strains of S. enteritidis were most frequently isolated from the faeces of both sick and healthy humans, but rarely from other material (urine, blood, pus). The cultivated strains indicated considerable resistance to the antibiotics used (Chloramphenicol, Erythromycin, Neomycin, Gentamycin, Colistin, Oxytetracycline, Ampicilin). The bacteriophage typing of about 2100 strains in the years 1980-1990 by Glognicka et al. (1990), after Lalko's schema (1977), illustrated that the majority of them belonged to phage types 7, 1 and 6. The most frequently described bacteriophage type in S. enteritid& infections and food poisonings worldwide, is type PT4 (Barrow, 1992). Comparison of lytic activity of this phage and the phages from Lalko's schema is under investigation. The results of official studies on animals have confirmed the presence of Salmonella in all species. As shown by Wojtofi (1989), these studies embraced almost solely sick or dead individuals, as well as meat from slaughter-houses and butchers. Checks at chosen veterinary field laboratories confirm a modest degree of infection by S. enteritidis in calves, pigs and cattle, and a tremendous degree in the case of poultry and eggs on poultry farms. Bacteriological tests of feed and raw materials used for its production, were carried out. The presence of many serotypes of Salmonella, but not S. enteritidis bacilli, was noted. Summing up the results presented, it can be noted that the S. enteritidis infections occurring in Poland over the 30 years in question, caused dangerous epidemics. Although the first was smaller as regards number, it caused serious diseases and the death of many children. The second epidemic, on the other hand, has been milder in course, but has affected 10-times more people and is currently
29 still in existence, a l t h o u g h cases of S. enteritidis food p o i s o n i n g have fallen slightly. Results of b a c t e r i o p h a g e typing indicate that a r e l a t i o n s h i p exists b e t w e e n the two epidemics: that S. enteritidis type 7 strains occur in both. T h e r e is no d o u b t that the p o o r state of h e a l t h of the Polish p o p u l a t i o n i n f l u e n c e s such n u m b e r of cases of salmonellosis. T h e p r e d o m i n a n t p r o d u c t s involved in food p o i s o n i n g were eggs, b u t o n e c a n n o t omit the role of m e a t a n d m e a t by-products, which were fairly f r e q u e n t l y the cause of the disease. A n i m p o r t a n t role, however, in the t r a n s m i s s i o n of infections, is played by h u m a n s .
References Anusz, Z. (1970) Wra~,liwog6na antybiotyki, sulfatiazol i nitrofurantoin~ szczep6w Salmonella wyosobnionych od zwierzat na terenie Polski w latach 1967-1968. Przeg. Epidemiol. 24, 305-312. Anusz, Z. (1980) Salmonelozy u ludzi i zwierz~t w Polsce w latach 1971-1978. Meal. Wet. 36, 265-267. Anusz, Z. (1989) Aspekty epidemiologiczne drobnoustroj6w Salmonella. Materiaty Sesji Naukowej "Problemy Drobnoustroj6w Salmonella w Srodowisku ludzi i Zwierz~t". Mi~dzyzdroje, Polska, 21-22. Sept. Ref. III pp. 1-9. Baggesen, D.L., Brown, D.J., Gaarslev, K., Olsen, J.E. and Bisgaard, M. (1992) Characterization of Danish isolates of Salmonella enterica serovar Enteritidis by phage typing and plasmid profiling comparison of strains obtained from man and broilers. International Symposium on Salmonella and Salmonellosis in Ploufragan, France, 15-17, Sept. Proceedings Posters, pp. 147-148. Barrow, P.A. (1992) Salmonellosis in Poultry. International Symposium on Salmonella and SalmonelIosis in Ploufragan, France, 15-17. Sept. Reports and Communications, pp. 141-163. Buczowski, Z. (1961) Salmonelloses of man diagnosed in the years 1946-1956 in Poland. Bull. Inst. Mar. Med. 12, 51-71. Buczowski, Z. and Pietkiewicz, K. (1969) Salmonelozy ludzi rozpoznane w Polsce w ostatnim dwudziestoleciu. Materiaty Konferencji Naukowej "Salmonelozy", Gdafisk-Gdynia, Polska, 19-20 Sept., pp. 7-15. Buczowski, Z., Strzelecki, E., Pietkiewicz, K. and Cader-Strzelecka, B. (1970) Bakterie Salmonella u niekt6rych gatunk6w zwierz~t w Polsce. Przeg. Epidemiol. 24, 293-304. Dera-Tomaszewska, B. (1984) Serological types of Salmonella bacilli isolated from men in Poland between 1967 and 1978. Bull. Instr. Mar. Trop. Med. Gdynia 35, 56-72. Fantasia, M., Filetici, E. and Anastasio, M.P. (1992) Phage types, resistance types and plasmid profiles of Salmonella enteritidis isolates, Italy, 1986-1991. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Proceedings Posters, pp. 153-156. Van de Giessen, A.W., Frankena, K., Van Leeuwen, W.H. and Notermans, S.H.W. (1992) An approach for monitoring Salmonella serotypes in farm animals. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Reports and Communications, pp. 375-385. Gtognicka, R. (1986) Salmonellosis in Poland. 2nd World Congress Foodborne Infections and Intoxications. Berlin, Germany, 26-30 May, Proceedings Vol. II, pp. 1223-1224. Gtognicka, R. (1992) Salmonella surveillance in Poland. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Proceedings Posters, pp. 157-158. Gtognicka, R., Kunikowska, D., Dziadziuszko, H. and Tokarska-Klunejko, E. (1990) Distribution of Salmonella enteritidis phage types in Poland in 1981-1990. Bull. Inst. Mar. Trop. Med. Gdynia 41, 145-148. Lalko, J. (1977) Salmonella enteritidis bacteriophage typing. Bull. Instr. Mar. Trop. Med. Gdynia 28, 187-194. Maciak, T. and Kubifiski, T. (1990) Paleczki Salmonella w produktach spo£'ywczych pochodzenia zwierz~cego w gwietle badafi ZHW w Warszawie. Med. Wet. 46, 305-307.
30 Magdzik, W. and Anusz, Z. (1973) Salmonelozy odzwierz~ce (Salmonellosis). In: J. Kostrzwski (Ed.). Choroby zaka2ne w Polsce i ich zwalczanie w latach 1961-1970. P.Z.W.L., Warszawa, pp. 152-169. Mason, J. and Ebel, E. (1992) Report of the current status of the United States Department of Agriculture Salmonella enteritidis Control Program. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Reports and Communications, pp. 312-325. Notermans, S.H.W., Van de Giessen, A.W. and Oosterom, J. (1992) Aspects of intervention measures to reduce human infections with Salmonella. International Symposium on Salmonella and Salmonellosis, Ploufragan, France, 15-17 Sept. Reports and Communications, pp. 235-244. Pietkiewicz, K., Buczowski, Z. (1969) Salmonellosis in man in Poland 1957-1966. Publ. Hlth. Rep. 84, 712-720. Prokopowicz, D. (1989) Obraz kliniczny i leczenie salmoneloz cztowieka. Materialy Sesji Naukowej. Problemy Drobnoustroj6w Salmonella w Srodowisku Ludzi i Zwierz~t. Mi~dzyzdroje, Polska, 21-22 Sept. Ref. VII. pp. 1-15. Sharp, J.C.M., Reilly, W.J., Munro, D.S. and Girwood, R.W.A. Salmonellosis in Scotland: an integrated inter-disciplinary approach. International Symposium on Salmonella and Salmonellosis. Ploufragna, France, 15-17 Sept. Reports and Communications, pp. 333-340. Wojtofi, B. (1989) Przyczyny i uwarunkowania wyst~powania Salmonel w £'ywnogci zwierz~cego pochodzenia. Materiaty Sesji Naukowej, Problemy Drobnoustroj6w Salmonella w Srodowisku Ludzi i Zwierz~t. Mi~dzyzdroje, Polska, 21-22 Sept. Ref. IV. pp. 1-10.