Food poisoning and salmonella infections in England and Wales, 1973–75

Pttbl. Hlth, Lond. (1977) 91,225--235

Food Poisoning and Salmonella Infections in England and Wales, 1973-75 An Analysis of Reports to the Public Health Laboratory Service Enid Vernon B.Sc.

Epidemio/ogica/ Research Laboratory*. Pub/ic Health Laboratory Service, Co/[nda/e Avenue, London NI/V9 5HT An anaJysis of cases of bacterial food poisoning and salmonella infections reported to the Public Health Laboratory Service during the three years 1973 to 1975 is presented. 21,428 of the 29,108 cases in which the causal organism was identified were due to salmonellas. Clostrldium welchii, Staphylococcus aureus, Bacillus cereus, V.ibrio parahaernolyticus and Escherichia coli were also incriminated in outbreaks. In 1973 and ~1974 the number of cases was slightly above the average for the previous 10 years; but in 1975 there ~as an increase of more than 50% above the average, mainly in salmonella infections. Salmonella infections contributed to the deaths of 131 persons, C. welchi~ to that ~oftwo and S. aureus to that of one. Many of the patients were already seriously ill and most were elderly, but there were eight deaths in children under one year of age. Six hundred and thirty-two general outbreaks were recorded. Of lhese, 296 were in hospitals, schools and other institutiol~sand 201 wereassociated with restaurants, hotels, receptions and parties. This distribution may in part be due to better reporting of institutional outbreaks. Of the 333 outbrea~ in which the type of food was Mentified, 39% were associated with meat, 31% with poultry and 30% with other foods. Annual I.neidence F o o d .poisoning ~incidents in which a bacterial cause has been identified are reported t o the Ep!demiologicaJ Research Laboratory by Peublic Health Laboratory Service and hospital laboratories throughout England and Wales. All salmonella infections except Salmonella typhf and S. paratyphi B, irrespective of whether or not they are known to have beer= foodborne, are inc/iuded. The last analysis o f ttaese returns concerned the years 1969-723 This report deals with the three years 1973-75. The annua;~ number of cases o f food poisoning b y cause is shown in Table I. The organisms reported were salmonellas, C. welc2'li~, S, aureus, ~. cereus (first recorded in these reports in 1971) and Bacillus sp., E. coti a',ad/I, parahaem61yticus (first recorded in the U.K. in i972). In each year salmonellas were/by far the most common causal organism. There ha,s been nao decline in the incidence .of" food poisoning f o r many y~,~s; indeed in 1975 there was a considerable increase, mainly in salmc~zella infectiorts. 'In this report, the term "family outbreak" relates to mer~bers o f the same household, "'general outbreak" to wider communities than a single household and "sporadic cases" t o those which have no known association with another case o f the same infection (Table 2). *Address now: Communicable Disease Surveilla.qeeCentre, Public Health Laboratory Service, Colindale Avenue, London NW9 51:/T.

226

E. Vernon Salmonella Infections

S a h n o n e l l a s a r e t h e m o s t c o m m o n c a u s e o f f o o d p o i s o n i n g i n E n g l a n d a n d W a l e s ( T a b l e I). I n 1 9 7 3 - 7 5 t h e r e w e r e 21,428 cases, 74~o o f t h e t o t a l n u m b e r o f c a s e s f r o m all r e c o g n i z e d b a c t e r i a l c a u s e s r e p o r t e d i n tk,ese y e a r s . A f u r t h e r 5146 s y m p t o m l e s s i n f e c t i o n s w i t h salmonellas were also recorded. T~'mLE |. Total cases according .to year and causal agent (1973-75) 1973 Causal agent Salmonella o'phimurium* Other salmonellas* Clostridium welehff Staphylococcus aurezts Bacillus cereus Bacillus spp. Escherichia coli Vibrio parahaemot)~icus Total

1974

No. 2367 4504 1311 168 66 . 141 17 8574

~

No.

27"6 52"5 15"3 2"0 0"8

2036 3627 2769 103 51 . ~ 5 859 l'i"

. 1"6 0"2 I00

.

1975 %/

No.

%

23"7 42"2 32.2 1"2 0"6

2814 6080 2418 443 82 4 6 96 11,943

23"6 50"9 20"2 3.7 0"7 --0"1 0"8 100

~ 0"1 t00

Three years No. % 7217 14,211 6498 714 199 4 147 118 29,108

24"8 48"8 22"3 2"5 0.7 0.5 0"4 100 I',l

,

I,,

T

*In addition, the following numbers of symptomless excre{ers of salmonellas were reported: .1973 1974 1975 S. typhimurium 365 309 505 Other salmonellas 1263 956 1748 1"One case of mussel poisoning was also reported. TABLE2. Genera! outbreaks, I973-75 according to location and causal agent: family outbreaks and sporadic cases ,,

General outbreaks Hospitals Restaurants,* hotels, holiday camps Farms Receptions, parties Schools lnstitutionst Shops Canteens Holiday parties (U.K.) Local community Infected abroad Other or not specified All general outbreaks Family outbreaks Sporadic cases

157

44

45 47 35 21 28 23 1 5 16 t9 10 407 1278 15,084

16 . 5 20 18 -30 t -. 7 14'1 9 4

1

.

4 . 8 6 .

. 4 1 1 1 .

2 28 22 9

,

.

,,

,,

,

i

-.

1

-1 1

I

I .--

.

. 1 . . .

. . .

. . . 2

-1 -1

,

202 2

-.

,,

.

. .

-. . . . 1 46 5 5

I

.

45 . -.

.

.

r

~ 6 ~ 9

*Includes "take-away" restaurants. -['Includes old people's homes, hostels, halls of residence, nurseries and children's homes.

--3 ---

112 48 50 47 47 29 32 7 17 21 20 632 1314 15,112

Sahnonella i~!fections in E~Jglandand Wales, 1973-.7.5

22

Number and location of outbreak;8 Salmonella outbreaks occurred in hosl~itals, and als,o Originated in restaurants, farms. schools and shops; some patients were infected abroad (Table 2). One hundred and fiftyseven (39 ~o) of the 407 general outbreaks of salmoaelta ir.~fection were in hospitals, mainly in psychiatric, mental subnormality, maternity and children's hospitals and geriatric units. The source of infection was stated in 44 of the 157 hospital outbreaks; in 20 this was a foodstuffand in 24 the source was a patient infected before admission. In maternity hospitals some mothers infected their babies at birth and the infection spread to other infants. Eighty outbreaks (20 %) originated in restaurants, hotels, holiday camps and at functions supplied by caterers. Such outbreaks were often large. Farms were implicated in 47 (12 Yo) of ihe general salmonella outbreaks. In 30 o f the 47 farm outbreaks reported, the source was unpasteurized milk; this was usually drunk only by the farm workers and their families, but sometimes the .milk was more widely distributed. In one outbreak caused by S. agolm and S. anatum, in which a school and a training college had been supplied with unpasteurized milk, 2 more than 140 infections were found. In some farm outbreaks the int~ction was thought to have been acquired directly from farm animals. The 23 outbreaks associated with shops were mostly due to cooked meats bought in butchers and supermarkets. In 19 (5%) of the general outbreaks the patients became ill abroad or soon after their return and in 103 family episodes the infection was also contracted overseas. The countries most frequently mentioned were Spain, including the Balear~c Islands, where 46 outbreaks originated, and Tunisia with 20 outbreaks; 34 outbreaks were from European countries other than Spain but few were reported in travellers from Asia. Those affected in six o f t h e outbreaks had been on cruises or were members of ships" crews. A variety o f salmonella serotypes was isolated from these patients, the most c o m m o n being S. typhhnurium and S. enteritidis. Deaths Salmonellas were isolated from 145 patients who died during the years 1973-75. In 14 of these, the death was attributed to other causes and the infection was considered to be coincidental. One hundred of the remaining 131 Patient.s had gastroenteritis. In 35 patients this was the only clinical feature reported, but the 65 others had concurrent serious, often malignant, conditions. Thirty-one patients presented with other clinical features including meningitis, pneumonia and bacteraemia. Seventy-three (56 %) of the patients who died were ~ .ore than 60 years old a n d many were already seriously ill before they were infected. Eight patients were under one year o f age. Three of these infants had meningitis, two--both neonates--had sep~ieaemia, and the remaining three had gastroenteritis. There were four deaths in older children, all of whom had serious congenital disease or other illness. TwentySix different salmonella serotypes were identified in patients who died; those most frequently recorded were S . O'phiniurium (40 cases), S. enteritidis (18), S. heidelberg (15), S. agona (7) and S. virchow (7). Type of food 'The food responsible for the outbreak was established in 76 (19~o) of the 407 general outbreaks caused by salmonellas, but in only 31 (2%) of the 1278 family outbreaks. In many outbreaks the identity of the food was not confirmed by microbiological examination since the food remnants had been disposed of before the onset of symptoms, which are not usually apparent until 18-36 hours after the meal. The foods most commonly incriminated

~.

~1 I ~ 1

II

11 t Jl

I II I / I t I I

I

ill

,~1-~

~1

I }-l

I I I 1 t I I I I

I

~.~'.~ ~

~t t-~

g~l

-+

~ ~'~ ~

t-~!

o

.

1 [ I / [-/

lllllllltllli

.

.

-I

!11111 t i II

~t I~1-

.

llJlll

I I o,

.

[ I t I I I

11111-1111111

-I--

~

All bacterial agents

Esci~rtchia coti

Vibrio parahaemolyticux

t?a.cilhts cereus

welchii

Clostriditm!

tll~rellS

Staphylococcus

Salmonellas

o

o

!

I I

I =

!

[o

!

o

I Frr~

1!

!

1

II

! O0

I',,J

Sahnonella h~fections in England and Wales, 1973-75

22

in the 107 definitive outbreaks were poultry 49 (46 % of the outbreaks), milk 30 (28 ,°/o),pork or ham 21 (20%) and other meat 6 (6 ~/~)(Table 3). In some outbreaks different forms of the same basic f~od were infected from a single source. For example, S. enteritidis was isolated from 70 persons who had eaten cream cakes from a bakery and also from the cakes, from poultry at the ,farm from which the bakery obtained eggs, and from bakery staff. TABLE 4. S o u r c e s * o f t h e 20 m o s t c o m m o n s a l m o n e l l a se,-(~types in m a n , 197327,5 ,,

Isolations f r o m man1"

°

r,

L,,,

,,,,,,,,

,,,,,

°

o

Serotype

1. 2. 3. 4. 5. 6. 7. 8. 9. 10. I I. 12. 13.

t4.

S. typhimuriurn ~. aguna S. enieritidis S. heidelberg S. anatum S. indiana S. newport S. b~fantis S. hadar ,9. bredeney S. virchow S. stanley S. panama S. saint-paul S. derby S. haifa $. livingstone S. kapemba S. braenderup S. brandenburg

15. 16. 17. 18. 19. 20. T o t a l o f 20 s e r o t y p e s O~ther s e r o t y p e s ¶ Total ,.

,,,,,

,,

,

,,

. ,

,,,,

,.

2602

32 14 10

1178 I009 931 908 698 512 494 471

4 4 4 3 3 2 2 2

21 -10 3 --_. 7 -~ 1

463

2

--

1 ~ 11 2 1 104 ~ 10 1 744 232 976

8396 3685

,,

,

374

I

--

364

1

--

293 273 215 210 203 180 23,459 3115 26,574

I l 1 1 1 I

88 12 100 ,

115 255 13 1~ 1 12

In 2 -2 1 1

h

3

165 25 14 3

1 ~ 2 ~ 7 2 54 90 144 ,

,

16 73 -2 24 11

,

3

~ -~ --

,

,,

. 2 5 54 25

.

. ~

--

.

.

7 288 25 313 ,,

,

1 37 3 40 ,,,

17 6 12 5

. ~ -~ --

,

20 5 ---

12

3 ----

.

-~ 6 -. . 1 . . 2 36 32 68

20 26 8 4 21 10

1

61 1 4 --

.

,,,

19 4 8 -| --

. 4 6 1 1 72 I 2 -228 356 584

4 ----

--

--

--

--

11

--

~ 3 ~ 1

1 ----

. ~ ~

--2

1 ~ ~ ~ -42 9 51

--1 -8 28 36

1

. . . . . . . . . . . . . . . . . . . . . . . . . .

* F i g u r e s f o r i s o l a t i o n s f r o m s o u r c e s o t h e r t h a n m a n a r e f o r 1973 a n d 1974 o n l y . i q n c l u d i n g s y m p t o m l e s s exereters. , C h i c k e n 9 3 3 ; d u c k 23; t u r k e y 19; g o o s e 1. § I m p o r t e d p r a w n s 14; i m p o r t e d s h r i m p s 5; i m p o r t e d t u r t l e m e a t 8; m u s s e l s 5 ; c o c k l e s 2; c l a m s I ; i m p o r t e d h a l i b u t 1. ¶209 d i f f e r e n t s e r o t y p e s .

Turkey is an increasingly c o m m o n source o f food poisoning, not only at Christmas but at weddings and receptions at other times of the year. Catering facilities for such functions are often overstretched and consequently the turkeys may be cooked 2-3 days before they are due to be eaten. Large frozen banqueting birds, which weigh up to 35 lb and need two days defrosting, are especially likely to be insufficiently thawed and inadequately cooked. They may then b e kept at ambient temperature for long periods after cooking and final reheating is often at temperatures too low to destroy bacteria. For example, about 600 persons had turkey for dinner at a club function and 209 were known to have become ill afterwards with So typhimurium infection. The turkeys were large and undercooked and one batch was left

•

E. Vernon

230

overnight in the coolir~g ovens. The)" were then refrigerated, subsequently carved and reheated for only half an hour. s In another outbreak, S. agona was isolated from 127 persons of 465 who attended a dinner dance at which reheated turkey was served. ~ Several general and family outbreaks associated with turkey were due to S. enteritidis. In one of these, turkeys were prepared in a hospital kitchen and 'more than 100 infections were recorded including patients, nurses, catering staff and delegates to a conference. Crosscontamination of a rice salad contributed to the spread o f infection. S. enteritidis is in fact a common infection of poulvry and v~as isolated from poultry, egg products and animal feedingstuffs during 1973-74 (Table 4). A series o f outbreaks of S. indimza infection shortly after Christmas, 1974, was also attributed to turkey. Two hundred and fourteen cases and excreters were reported in three weeks, many of them from dinner parties held at an hotel in the Midlmads; infected hotel guests and members o f the hotel staff had also eaten turkey. The source of these outbreaks was frozen turkeys from a poultry packing station where S. indiana infection was endemic,b Other salmonella serotypes involved in turkey-borne outbreaks were S. heidelberg, S. hadar and ,7. saint-paul. In the summer of 1975 there were numerous outbreaks of S. agona and S. anatum infection, mainly in the Midlands; six were associated with wedding receptions provided by a firm of caterers. Boiled ham from one factory was implicated in these outbreaks and in others within the area o f distribution o f the factory's products. Bacteriological investigations at .this factory confirmed that contamination o f the ham had occurred; moreover, there was evidence of insufficient cooking and poor hygiene,e

Sabnonella serotypes During this period a total of 26,574 human infections was reported and 229 different serotypes were identified (Table 4). The most common types were S. tkThimurium, S. agona and S. enteriditis. The other 226 serotypes each accounted for less than 5 ~ o f the infections. The relative proportions of the different serotypes in 1973-75 were broadly similar to those observed in the preceding four years, a ~third of the isolations being o f S. typhimurium and I5 o f the 20 most common serotypes being among the commorf types in 1969-72. As in the previous four years there was a number of outbreaks in which more than one salmonella serotype wa~.,:,~ :o1~,ed. These outbreaks have been classified in Table 4 under the serotype most fre~,"'~ "ed from the patients. As shown~L "~ f the serotypes common in man were also found in meat, poultry andaa~, ., S. typhimurium was found in all the sources listed in~the table, including m. ~and pasta. S. agona was isolated from meal, milk an~t poultry, but not from egg~, j~,~ta o r seafood. S. infantis was commonly foundqn poultry, pork products and feedingstuffs. In a survey of pork sausages from manufacturers, S. infantis, S. agona and S. derby were found to be the serotypes most frequently.isolated.7 S. enteriditis was mainly a contaminant o f eggs and poultry and was also found in animal feedingstuffs. Contaminated feedingstuffs are believed to play a large part in the aetiology of salmonellosis in pigs and poultry s a n d limitation of infectioa in food animals and poultry, both at the farm and the abattoir, is an important element in any attempt to control salmonellosis in nlan.

9

Closteidium welehii C. welchii was the second .most common cause of.food poisoning, accounting for 6498.cases in 1973-75, between 15~o and 3 2 ~ o f the annual totals from all bacterial causes, There were I50 outbreaks, mostly associated with hospitals, schools, institutions and, canteens; only nine were confined to one household. Outbreaks due to C. welchii tend to b~ larger than

Sabnoneila it(ections in England attd Wales, 1973-75

231

those due to other organisms; 50 persons on average per outbreak were affected and there were three outbreaks in each of which no less than 300 persons were ill. One of these was in a mental hospital where 379 patients had diarrhoea and one died after eating minced ham which had been cooled slowly in a warm kitchenY ° The food responsible was confirmed by bacteriological examination in 121 of the 150 general and family outbreaks; all but four were caused by infected meat or poultry. A typical outbreak occurred when 126 of 230 persons had diarrhoea and abdominal pain 12-t4 hours after eating turkey at a staffcanteen Christmas dinner. On this occasion frozen turkeys each weighing about 20 lb had been thawed, and after being stuffed were roasted for only four hours. They were then left for 24 hours unrefrigerated in a warm kitchen before beingcarved.The meatwas held fora furtherday at r o o m temperature, reheated to 200°F and then it finally remained on a hotplate for another hour before consumption. Heat-resistant Co welchii were isolated from all patients tested and from the remains of the turkeys. The causative serotype of (7. welchii has been established in more than half of the outbreaks investigated in 1973-75; the most c o m m o n types were 3, 4 and 8. n Two patients with (7. welchii food poisoning died; both were already seriously ill. Staphylococcus aureus There were 714 cases of staphylococcal food poisoning in this period, between 1% and 4Yo of the annual totals o f cases. Of the 50 outbreaks, 28 were general outbreaks--12 associated with restaurants or receptions and six in schools--and 22 were confined to a single family. A food was incriminated in 48 of the 50 outbreaks; in 4 4 ~ the food was meat, in 33~o poultry,--in 15 ~o sweets and cakes and in 8 Yo seafood. Typically, cooked food had been allowed to stand at a warm temperature after contamination by a food-handler, with consequent multiplication of tile organisms and production ofenterotoxin. In one outbreak, 47 of 95 passengers on a river trip in June developed vomiting and diarrhoea 3-6 hours after a meal which included chicken pieces ~hat had been kept warm after cooldng. Similar strains of staphylococci were isolated from a patient, from the chicken and from a dressing on the finger o f one of the food=handlers; all the strains produced enterotoxin A. In another outbreak, 30 of 7g guests at a wedding vomited 1-__2-hoursafter a reception at which chicken was served; the cooked chicken had been kept overnight in an unrefrigerated van.- A count of I-4× 10 x° S. aureus per g was obtained from the chicken, which had: been prepared by a nasal carrier of staphylococci of a similar phage type. There were two large outbreaks in schools. In one 129 of 348 pupils vomited 3 hours after eating custard; similar enterotoxin-producing strains of S. aureus were isolated from a patient, the custard and two food-handlers. In the second, chicken had been sliced by hand and then left at r o o m temperature: the patients, the chicken and the nose of a food-handler yielded similar strains of S. aureus producing enterotoxin A. Tests for enterotoxin A - E were ran_de in many o f the outbreaks investigated; most were associated with enterotoxin A. 1~- Most Of the strains o f S. aureus which were phage-typed belonged to group HI. Only one death was recorded; an octogenarian developed vomiting and prostration after eating ham. S. aureus of the same phage type was isolated from the patient's lung and intestine and the ham. Baeiltus cereus and B. subtilis One hundred and ninety-nine cases o f food poisoning were caused by B. cereus. This is less than 1 ~o o f the total number of cases from all causes, but the number of reported outb r ~ k s due to this organism is increasing. Most patients had acute nausea and vomiting

232

E. Vernon

t-5 hours after a meal which included rice: this was followed by diarrhoea in about a quarter of the cases. Incubation periods o f 11 hours have, however, been recorded3 ~ Only a few persons were reported in each episode, most o f which were associated with r[ce dishes from Chinese restaurants and "take-away" shops. Usually the rice had been boiled in bulk, stored at room temperature, and then briefly reheated, often by frying. One family ate pasteurized cream which had been Purchased on the day of consumption and kept refrigerated. The cream tasted normal, although it had the "bitty-cream'" consistency typical o f spoilage by B . cereus, which was found in the cream. Bacillus subtilis may have been the cause of one outbreak; pasties which had been reheated before consumption were found to be heavily contaminated with this organism. Vibrio parahaemolytieus tL parahaemolyticus is a nmrine bacterium recognized as a cause of food poisoning throughout the world, especially in Japan3 4 It first appeared in these reports in 1972. In 1975, 96 cases of food poisoning were reported, a substantial increase from the total Of 22 during the preceding two years, 1973-74. There were six outbreaks during 1973-75, four associated with prawns, scampi or crab and two aboard aircraft. At least 19 o f 91 persons who attended a dinner dance had vomiting, diarrhoea and abdominal pain 8-30 hours later. The meal included prawn cocktail made with Malaysian cooked and peeled prawns. Kanagawa-positive strains o f V. parahaemotyticus were isolated from six o f 10 patients and from the prawns, In a second outbreak at least 24 persons became ill 12 hours after eating imported frozen prawns at a restaurant, A third episode also involved prawns consumed at a restaurant. At least 12 holidaymakers had acute gas~oenteritis 16-18 hours after eating dressed crab from the same fishmonger at a seaside resort. The crab was of British origin. Specimens from six patients yielded Kanagawa-positive strains of IC para!'ae:::o!ytict~.s3 s In two outbreaks, and also in some sporadic cases, the patients became ill after flights from the Far East. More than 50 persons on a jumbo jet had diarrhoea, vomiting and abdominal pain 5-10 hours after eating shrimps taken on board in the ,Far East; /I. parahaemolyticus was isolated from .two patients examined in London. In the second outbreak on board an aircraft Malaysian prawns were implicated. Escherlchia coli No foodborne outbreaks due to E. coli have been reported in England and Wales since 1967, but there were three in the period under review, each of which arose in different circumstances. In the l/irgest, 141 o f 500 guests at a dance developed diarrhoea a n d a b d o m inal pain, sometimes with vomiting, 2-22 hours after supper. E. coil 0 127 was isolated from the 15 patients tested, from the catering staff and from ham and egg pie Which had been sliced in the morning, refrigerated during tile day and left at r o o m temperature for 5 hours. 1~ Cornish pasties were implicated in the second outbreak which occurred in a technical college. Four students were known to have had diarrhoea 36-48 hours after eating pasties displayed in a warmed cabinet. E. coli 0 86 was the only pathogen isolated from the one student examined; there were no cases among students who had not eaten pastiesY The third outbreak concerned two infants who lived: in different villages, but whose fathers worked o n the same farm. The infants, fed o n raw milk from the farm, had loose stools and failed to thrive. On investigation, cattle at the farm were found to have mastiffs and a sample of the milk yielded E. coli 0 26 of a similar antibiotic sensitivity pattern to strains isolated from the infants3 a

Sahnonetla infections hi England aim tVales, t973-75

23 ?

Discussion Each of the repor.ts on which .the above analysis is based concerns an episode in which, the causal organism ~ s _i0entified by laboratory examination: the findings thus provide a valid account of the bacteria] causes of food poisoning during i973-75. However, the report does not include food poisoning in which a bacterial cause was not identified. In many episodes of food poisoning ehher no specimens are sent for !aboratory examination or, where they are sent, an aetioiogical agent is sometimes not found. In this period, I l such outbreaks, comprising more than 250 cases, were recorded. It is possible that they could have had a viral aetiology, but this was not established~ The incidence o~ food poisoning in England and Wales is without doubt far greater than the number of cases included in this report. The incidence of food poisoning shows no tendency to decrease. Indeed in ]975 there was a pronounced increase and the number of cases of bacterial food poisoning and satmoneilosis was the highest so far recorded by the P.H,L.S., 11,943 cases, c o m p a r e d with an annual average of 7630 for the preceding 10 years. The greatest increase occurred in salmonella infections; 8894 cases were reported, more than 60% above the a0n_ua] average for the I0 years to 1974. The h u m o r of cases due to C. welchii was 2769 in 1974 and 2418 in 1975, the highest annual totals since 1965. ~ Reports o f food poisoning due to V. parahaemotyticus a n d B. cereus, -both reported in England and Wales only in recent years, have also increased. The occurrence of outbreaks due to these organisms in part reflects current social patterns. Thus, two outbreaks due to I/. parahaemolyticus investigated in England originated in the Far East and air passengers were ill on arrival at'Heathrow. The outbreaks were associated w~th shrimps and prawns consumed o n board the aircraf~ The consumption of s e a f o o d ~ t h e usual vehicle of infection of this o r g a n i s m ~ m a y be gaining in popularity; many crustaceans, such as prawns and shrimps, are imported. The increase in B. cereus outbreaks, mainly associated with the consumption of rice, probably reflects the current popularity o f Chinese restaurants and the convenience of ::take-away" Chinese food. Spores of B. cereus can survive boiling and germinate at ambient temperatures; ~° the organisms multiply in rice held for Iong periods between cooking and consumption. The results of serotyping, ~t, "*-"enterotoxin studies 23 and feeding tests in monkeys~4indicate that there are two types of illness, the emetic type often associated with rice and a diarrhoea! illness with a longer incubation period. Most o f the instances were of the former type. The continuing problem of the main forms of food poisoning, caused by salmonellas, C. welchii and S. aureus, may in part reflect a gradual increase in large scale catering. Social changes also affected the trend of salmonella infections in recent years. O f especial importance is the increased consumption of poultry, now estimated at over 18 lb a year for each person. ~ The consumption of turkeys, as well as chickens, has increased. Salmonellas, introduced b y contaminated feeding-stuffs, may become endemic in poultry flocks and large numbers of infected birds are reaching the kitchen and, not infrequently, the table, The use of whole large turkeys up to 35 lb in weight (well over the safe weight o f 3 kg), too brief defrosting, inadequatecooking, slowcooling, prolonged storage at ambient temperatures and holding rewarmed meat o n a hotplate, are all important causes of food poisoning. Many of the outbreaks could have been avoided if the food had been adequatelycooked and promptly stored in a refrigerator. Failure to apply these simple rules, particularly in hot weather, may in part account for the increase in food poisoning during the hot summer of 1975. Inadequate cooking, slow cooling and unrefrigerated storage are at the root of most of the c~utbreaks due to C. welchii, many o f which are in hospitals, schools and other institutions where meat is cooked in bulk.

234

E. Vernon

Unrefr~gerated storage, not inadequate cooking, is the most important cause o f staphylococcal food poisoning. It has been estimated that 15-20 ~o o f the population carry enterotoxigenic staphylococci ~ and contamination of cooked food by food-handlers, with subsequeut multiplication of organisms while the food is held at room temperature, is a common pattern in ~taphylococcal food poisoning. Food-borne outbreaks of Escheridda coli were recorded in the U.K. for the first time since 1967 ~ although ombreaks o f gastroenteritis due to this cause have been reported abroad. -*s E n t e r o p a t h o ~ n i c strains o f E. coil are now recognized as a cause of gastroenteritis in adults. 29 Acknowledgements Thanks are due to the laboratories making lhe returns. Acknowledgement is also due to the Directors and staff of the Food Hygiene Laboratory'and the Salmonella Reference Laboratory for advice and ta Mrs S. A. Le Baigue and Mrs S. F. Dobin for assistance in the preparation of this report. References I. Vernon, Enid & Tillett, Hilary E. (1974). Food poisoning and salmonella infections in England and Wales, 1969-1972..Public Health, London 88, 225-35. 2. Public ~Health Laboratory Service (1974¢). Salmonellosis from raw milk. British Atedical Jo~rnat.i~; ~53. 3. Public Headth Laboratory Service (1974b). Hazards of turkey. I. British Medical Journal ii, 128. 4, Public Hea~th Laboratory Service (1974c). Outbreak o f Salmonella agona food poisoning. British l~ledical Journal iii. 477. 5. Public Health Laboratory Service (1975a). Salmonella indiana from turkey. British Medical Journal ii.i, 107. 6. Public Healeh Laboratory Service (1975b). Widespread salmonellosis from contaminated meats. British ~Vfe~eal Journal iv, 529. 7. Roberts, D., .Boag, K., Hall, M. L. M. & Shipp, C. R. (1975). The iso!ation 0f salmonellas from British pork ~sausagesand sausage meat. Journal of Itygiene, Cambridge 75, 173-84. 8. Public Healt~a Laboratory Service Working Group; $kovgaard, bliels & Nielsen, B. Brest 0972). S~lmonellas in pigs and animal feeding stuffs:in England ~nd Waiesand in Denmark. Journal of ~'ygiene, Cambridge 70, 127-40. 9. McCoy, J. H. (1975). Trends in salmondta food poisoning in England and Wales 1941=72. Journal o f Hygiene, Cambridge 74, 271-82. 10. Stringer, M. ~F. (1977). Personal communication. 11. Thomas, ~VI.E. M., Noah, N. D,, Male, G. E., Stringer, M. F., Ker~dall, M., Gilbert, R. J., Jones, P. I~, & Phillips, K. D. (1977). A hospital outbreak o f Closiridium perfringens food poisoning. Lancet i, 1046=8 12. Wieneke, .~atonnette A. (1974). Enterotoxin production by strains of Staphylococcus aureus isolated from foods and human beings. JournalofHygiette, Cambridge 73, 255-62. 13. Gilbert, R.;J. & Taylor, A. J. (1976). Bacitluscereus food poisoning. In Microbiology in Agriculture, Fisheries and Food (Skinner, F. A, & Carr, J.G., Eds), pp. 197-213, Society for Applied Bacteriology Symposium Series No. 4. London: Academic Press. 14. Barrow, ~G..I. (1974). Microbiological andother hazards from Seafoods with special re['~rence to Vibrio plarahaemolyticus. Postgradudse Medical Journal ~0, 612-19. 15. Hooper, ~ . L., 8arrow, G.~L & McNab, D. J. N. (I974). VibrioFarahaemolytieusfoodpoisoning in Bfi-rain. Lancet i, 1'100-2. 16. Department of Healt'h & Social Security (1974). Food poisoning. Annual Report o f the Chief Medical Officer i973, p. 39: London: H.M.S.O.

Sabnonella h~fections b~ L)rgland and Wales, 1973-.75

235

17. Public Health Laboratory Service (1976). E. coil gastroenteritis from food. British Medical Journal i, 911. 18. Public Health Laborator~r Service Working Party (1976). Survey on colony counts and prcdominant organisms in samples of boiled and fried rice from Chinese and Indian restaurants and "Take-away" shops. Environmental Health 84, 141-3. 19. Vernon, Enid (1966). Food poisoning in England and Wales, 1965. Monthly Bulletin o f the Ministry o f Health 25, 194-207. 20. Gilbert, R. J., Stringer, M. F. & Peace, T. C. (I 974). The survival and grownth of Bacillus cereus in boiled and fried rice in relation to outbreaks of food poisoning. Journal of ttygiene, Cambridge 73, 433--44. 21. TayMr, A. J. & Gilbert, R. J. (1975). Bacillus cereus food poisoning: a provisional serotyping scheme. Journal o f Medical Microbiology 8, 543-50. 22. Gilbert, R. J. & Parry, J. M. (1977). Serotypes o f Bacillus cereus from outbreaks of food poisoning and from routine foods. Journal of Hygiene, Cambridge 78, 69-74. 23. Turnbull, P. C. B. (1976). Studies on the production of enterotoxins by thzcillus cereus. Journal o f Clinical Pathology 2,9, 941-8. 24. Melling, J., Capel, B. J., Turnbull, P. C. B. & Gilbert R. J. (1976). Identification o f a novel enterotoxigenic activity from Bacillus cereus. Journal of Clinicai Pathology 29, 938-40. 25. Ministry of Agriculture, Fisheries and Food (1976). Household food consumption and expenditure: Nationa',~Food Survey. 26. Gilbert, R. J. ~(1974). Staphylococcal food poisoning and botulism. Postgraduate Medical Journal 50, 603-11. 27. Vernon, Enid (1969). Food poisoning and salmonella infections in Eng!and and Wales, 1967. Public Health, London 83, 205-23. 28. Marier, R., Wells, J. G., Swanson, W., R. C., Callahan, w. & Mehlman, I . J. (1973). An outbreak o f enteropathogenic EschericMa coli foodb0me disease traced to imported ~French cheese. Lmtcet ii, 1376-8. 29. Lancet (1975). E. coil enteritis. Lancet ii, 1131-2.