Food poisoning and Salmonella infections in England and Wales, 1968

Food Poisoning and S a l m o n e l l a Infections in England and Wales, 1968 ENID VERNON B.SC.

Epidemiological Research L.qboratoo, of the Public Health Laboratory Service, Colindale Avenue, London, N, Itf.9. Food Poisoning of All Types FOOD poisoning and salmonellosis in England and Wales have been the subject of annual reports since 1949 (Cockburn and Vernon, 1969); the analyses are based on reports submitted by bacteriologists in public health and hospital laboratories to the Public Health Laboratory Service and by medical officers of health to the Department of Health and Social Security*. Incidents of food poisoning are classified into three categories: general outbreaks, involving more than one person from different households; family outbreaks, in which there are two or more cases or excreters in the same household; and sporadic cases which have no known relation to other cases. Each incident therefore represents, as far as can be ascertained, a separate focus of infection, although clustering of incidents due to the same organism in time or geographical location may suggest that they have an unidentified common source. It must be emphasised that many, perhaps the majority, of cases of food poisoning never come to the notice of the public health department or the bacteriologist. It is only when the symptoms are severe or the outbreak takes place in an institution or other well defined group that the reporting of cases is likely to be reasonably complete.

Frequency (Tables I and 1I) The records show a small reduction in the number of food poisoning cases from 11,095 in 1967 (Vernon, 1969) to 10,511 in 1968. The increase in the number of incidents to 5084, compared with 4256 in the pervious year, is largely accounted for by the greater number of sporadic cases of salmonellosis and of those due to unrecorded causes. Nearly three-quarters of the persons with food poisoning due to a known cause were infected with salmonellae. Compared with 1967 there was an increase in the number of cases of salmonellosis due to serotypes other than Salmonella typhimurium. The possible connection between this trend, which has been observed for some years, and salmonella isolations from farm stock and feeding stuffs is discussed under the causal agent Sabnonella. *The information about food and feeding stuffs in Tables VII and VHI was kindly provided by the Salmonella Reference Laboratory, Colindale and that about animals in Table IX by the Central Veterinary Laboratory, Weybridge, the Veterinary Laboratory, Lasswade and the Veterinary Investigation Service.

240

P U B L I C H E A L T H VOL. g4, NO. 5

The number of incidents of staphylococcal food poisoning increased from the unusually low figure of 29 in 1967 to 63, which is nearer the number recorded in the previous four years. However, the increase in incidents in 1968 was due to a greater number of sporadic cases, and the number of persons affected wa~ actually fewer than in the previous year. There was a reduction in both the number of incidents and the number of cases of food poisoning due to Clostridium welchii. Less than 2000 persons were known to have been affected, the lowest number recorded since 1962; however, it is salutary to recall that in 1963 the number of cases rose to a record 4721 (P.H.L.S., 1964). The improvement in 1968, therefore, gives no grounds for complacency. Two incidents of chemical poisoning were recorded and four incidents of shellfish poisoning; one of these was a large outbreak associated with the toxin of a dinoflagellate organism in mussels. ]n almost a quarter of cases the cause of the food poisoning remained undiscovered. In many of the outbreaks and sporadic cases no bacteriological examination was undertaken, often because the incident was investigated too late.

Deaths (Table I) In 1968, 51 deaths associated with isolation of food poisoning organisms were reported; in 44 cases gastro-enteritis or septicaemia due to a food poisoning organism probably contributed to the cause of death, but in seven cases the isolation of a food poisoning organism was regarded as incidental. All except two of the deaths were associated with salmonella infections; one of these two patients was infected with Staphylococcus aureus and the other with C1. welehii. Salm. typhimurium was isolated in 16 cases and 26 patients were infected with other salmonella serotypes, the most conunon being Salm. enteritidis and Salm. stanley, each of which was isolated in five cases, and Salm. dublin with four cases. Of the 42 patients with salmonella infections, 30 had symptoms of gastroenteritis. The Salmonella serotypes isolated were Salm. typhimurium 14, Sahn.

stanley 4, Sahn. enteritidis 3, Salm. panama 2, Sahn. agama 1, Salm. brandenburg 1, Salm. dublin 1, Sabn. montevideo 1, Sahn. senftenbeJN I, Salm. takoradi 1, and Sahn. virchow 1. Twenty-one of the 30 had some complicating condition (six pneumonia, two carcinoma, eight heart disease, one nephrosclerosis, one uraemia, one anaemia, one diabetes, and one with other unspecified conditions). These patients were all over sixty years of age except fbr a boy aged three with aplastic anaemia and a man aged 33 with myocardial infarction. Five of the nine cases with uncomplicated gastroenteritis were in patients over 60 and one was a b a b y ; three were in younger adults who were not reported to have had additional clinical conditions. Nine cases of Salmonella septicaemia were recorded; in at least six the

7846 16,600 27

All causes Incidents Cases Deaths 6428 13,700 35

2907 1047 98 97 2279

1960

5387 12,750 22

2503 1268 91 83 1442

1961

4521 9,696 23

1864 982 143 84 1448

1962

4372 9,975 19

1725 1368 107 85 1087

I964

4091 11,317 19

1721 1224 74 64 1008

1965

197 49

246

All agents Cause not discovered

TOTALS

100

28 42 7 (--) 22 1

546

412 134

201 190 15 . 6 . .

.

100

1

49 46 4

Family out breaks No. ~

.

.

4292

3313 979

1398 1870 34 . 11 .

100

(--.)

42 56 1

Sporadic cases No. ~

3744 8,784 26

1407 1089 54 63 1131

1966

5084

3922 1162

1654 2142 63 1 60 2

100

42 55 2 (---) 2 (--)

AU incidents No. ~

*Includes 322 symptomless exereters of Salm. typhimurium and 742 symptomless excreters of other salmonellae + Excluding Salm. typhi and Sahn. paratyphi B (--) = less than 0.5 Vo

55 82 14 1 43 2

General outbreaks No. ~

Salm. typhbnurium Other salmonellae + Staphylococci Gonyaulax tamarensis toxin CL welchii Chemical

Presumed causal agents

4465 13,104 27

1820 1149 74 82 1340

1963

TABLE II Food poisoning of all types, 1968 General outbreaks, family outbreaks and sporadic cases according to causal agent

*Includes an outbreak of infection with Salm. typhimurium and Salm. derby

3198 1840 118 110 2580

1959

Salm. typhimurium Other salmonellae Staphylococci CI. welehii Other and unrecorded causes

Presumed causal agent

TABLE 1 Food poisoning of all types, 1959-68 Incidents according to year and causal agent

10,511

8197 2314

2460 3488 309 70 1840 30

No.

4256 11,095 27

100

30 43 4 1 22 (--)

5084 10,511 44

1654 2142 63 60 1065

1968

All cases*

1810" 1449' 29 80 889

1967

33

503

November

TOTALS

15

-

3

2

1

ft

87 68 18

October

December

68

4

‘z

20

6 2 3

2

2

4

September

2 3

37 80

r 1

1

2

discovered

Cause not

reports only)

i 2

July August

3

:

Clostridium welchii

::

r

toxid

Gonyaulax tamaremis

June

: 2

Staphylococci

18

34 It

Salmonellae

April May

---January E&:try

Month

Monthly frequency ofgetrertrl

TABLE III Food poisoning of all types, 1968 and family outbreaks (public health and hospital laboratory

71 572

25

loo

86 72

45

if

I9

22

2

All outbreaks

-

F O O D P O I S O N I N G A N D Sahnonella I N F E C T I O N S

243

organism was isolated by blood culture. Two cases were in infants aged 5 and 10 days who also had meningitis; Sahn. typhhnurium was isolated from cerebrospinal fluid of one child and Sahn. dublin from the meninges of the other. The salmonella serotypes infecting the adults with septicaemia were Sahn. bredeney 1, Sahn. choleraesuis I, Sahn. dublin 2, Sahn. enteritidis I, Sabn. oranienburg 1, and Sahn. stanley 1. Five adult patients had septicaemia without mention of gastroenteritis. One was a m a n aged 25 with sickle-cell anaemia and the other patients were aged between 59 and 76 years; one had leukaemia and one had staphylococcal empyema and cirrhosis of the liver. Salmonellae were isolated by blood culture from two elderly men who also had diarrhoea. In a case of staphylococcal pneumonia in a m a n aged 55, Salm. o,phhnurhan was isolated post-mortem from lung and faeces. In two cases there was no clear information on the role of the Sahnonella infection in the cause of death. One was a man aged 52 with a diagnosis o f suppurative portal thrombosis and acute appendicitis who was infected with Salm. takoradi and one was a woman aged 84 admitted to hospital with a bedsore; she was infected with Sahn. enteritidis. The patient with staphylococcal food poisoning was a m a n aged 60 who died with a coronary occlusion and Staph. aureus was found at autopsy; other members of his family were also ill. The remaining case was in a woman of 81 with myocardial degeneration who died in an outbreak of C1. welchii food poisoning in an oId people's home.

Seasonal variation (Table 1II) Laboratory reports of general and family outbreaks were analysed by month of occurrence; outbreaks reported only to the Department of Health were not included because the date of the outbreak was not routinely stated. Salmonella outbreaks were more frequent in the third and fourth than in the first two quarters of the year; 609/o took place during the four months August to November. No outbreaks due to staphylococci were reported in the first quarter of the year or during November and December. There was no seasonal variation in the frequency of outbreaks due to Cl. welchii.

Location of general outbreaks (Table IV) The place where the infection occurred or the suspected food was bought or eaten was recorded in 212 of the 246 general outbreaks. As in previous years, hospitals were most frequently mentioned; 64 of the 66 hospital outbreaks were due to salmonellae and in outbreaks of this type case to case spread frequently plays some part. Thirty-six outbreaks arose in restaurants, hotels, clubs or holiday camps; in 12 of these the causal organism was not discovered. Of the 72 outbreaks after meals in industrial canteens, schools and other institutions 32 were due to CI. welchii; in many of them there was evidence of precooking of meat dishes and p o o r conditions of storage of the cooked meat;

244

PUBLIC HEALTH VOL. 84 NO. 5

t h e r e is a l w a y s a p o t e n t i a l h a z a r d w h e n large q u a n t i t i e s o f m e a t are c o o k e d and not consumed immediately. T e n o u t b r e a k s o f h u m a n s a l m o n e l l o s i s were a s s o c i a t e d with f a r m s a n d o n e with a c h i c k e n h a t c h e r y ; t w o o f the o u t b r e a k s i n v o l v e d m e m b e r s o f the public, b u t in t h e o t h e r s o n l y the f a r m w o r k e r s a n d t h e i r families were affected. I n n i n e o f t h e o u t b r e a k s the i n f e c t i n g Sahnonella s e r o t y p e was also i s o l a t e d f r o m c o w s or calves o n t h e f a r m a n d in t h e o u t b r e a k at a h a t c h e r y chicks, staff a n d their c o n t a c t s w e r e infected w i t h t h e s a m e serotype. T h r e e family o u t b r e a k s o f s a l m o n e l l o s i s a m o n g f a r m w o r k e r s w e r e also r e p o r t e d . In f o u r g e n e r a l o u t b r e a k s a n d 20 f a m i l y o u t b r e a k s the p a t i e n t s were i n f e c t e d a b r o a d ; all except o n e were d u e to s a l m o n e l l a e , 11 to Sabn. typhinntrhml a n d 12 to o t h e r Sahnonella serotypes. I n 16 of the i n c i d e n t s t h e p a t i e n t s visited S p a i n or t h e Balearic o r C a n a r y Islands.

TABLE IV

Food poisoning of all types, 1968 Location of general outbreaks (excluding family outbreaks) Presumed causal agents CI. Salmon- Staphy- Gon. ellae lococci tamaren- welchff Chemical

sis toxb~

Hospitals Restaurants, clubs hotels, holiday camps Canteens Institutions Schools Shops Butchers Chicken barbecue Fish Other Farms Dinners, dances, receptions Infected abroad Other & not stated ALL PLACES

64

-

-

14 11 3

4 3 -

-

3 5 2 I1

2 . 1 .

2 3 19

1 . 3

137

14

.

2

-

-

66 36 26 25 21

6

-

12

18

1

7

6 8

-

5 J0

.

.

.

. 1 .

. .

.

. . -

.

.

.

-

.

5 ) 5 [ 15 2 3 J 11

-

-

3

1

43

.

1

.

-

.

Not All disAgents covered

1

5 1 8

8 4 34

2

49

246

.

Vehicles o f bfection (Table V) T h e vehicle o f i n f e c t i o n w a s e s t a b l i s h e d w i t h r e a s o n a b l e c e r t a i n t y in 82 (33 %) o f ' g e n e r a l o u t b r e a k s a n d 13 ( 2 % ) o f family o u t b r e a k s . A p a r t i c u l a r f o o d w a s i n c r i m i n a t e d in 88°//o o f g e n e r a l o u t b r e a k s d u e to Cl. welchii a n d in 7 1 % o f those d u e to s t a p h y l o c o c c i , b u t in o n l y 16 % o f g e n e r a l o u t b r e a k s o f s a l m o n e l l o sis. Tile p r o p o r t i o n o f f a m i l y o u t b r e a k s i n w h i c h a p a r t i c u l a r f o o d c o u l d be identified as t h e likely vehicle w a s l o w e r . I n 80 o f t h e 95 general a n d f a m i l y

FOOD

POISONING

Sahmmclla

AND

INFECTIONS

245

outbreaks attributed to a particular food, meat and poultry was the vehicle of infection. TABLE

V

Food poisonhtg o f all O'pes, 1 9 6 8 Vehicles o f infection and causal agents hi general and family outbreaks .

Vehicle of infection

.

.

.

.

,.

.

Sabn. tp)'~himurium

Other salmonellae

3

21

12

-

-

-

1 -

. 1

Meat and poultry* Fish Canned Shell Milk Unpasteurized Beverages Sweet Eggs Sauce

2 . I -

Vegetables Potato

.

ALL FOODS

6

. .

. -

.

t

:

39

.

.

.

.

.

1

. . .

.

.

1

. 15

.

.

.

I

5

80

-

3

1 I 4 ~-

2

-

. .

.

.

.

. 39

All Agents

-

.

.

.

Not discovered

.

-

.

.

. 23

.

sis toxin

2 .

.

Presumed causal agents StaphyGon. Ci. lococci tamaren-welchii C h e m i c a l

2

4 2 I I 1

1

1

9

95

*See Table VI for details

Meat and poultry (Table VI) In more than half the outbreaks due to meat or poultry the meat concerned had been precooked and served cold or reheated. Usually it had been cooked one or more days before consumption and had either not been refrigerated at all after cooking or had been left for some hours at ambient temperature before refrigeration. Roast meat which had apparently been freshly cooked was incriminated in only six outbreaks. Eight outbreaks of salmonella infection were associated with barbecued chicken and altogether over 400 persons were ill. These are discussed later. Canned meat was suspected as the vehicle of infection in four small outbreaks of staphylococcal food poisoning. Three of the outbreaks took place after patients had eaten corned beef from 6-1b cans opened at shops and a car6. In two outbreaks the can was said to have been freshly opened and Staph. aureus was isolated from the meat. In the third the can had been placed in a refrigerator for 7 hours after ~ was opened and a heavy growth of Staph. aureus was obtained fror~ the remainder of the meat in the can. It seems possible that in each episode staphylococci had grown and produced enterotoxin in the can before it was opened. In the fourth outbreak a family became ill after eating imported canned tongue and a heavy growth o f Staph. aureus was obtained from the empty can.

246

PUBLIC

HEALTIt

V O I . . 84 N O . 5

In all except two of the len outbreaks associated with meat pies, the pies were tnadc at home or in the kitchen o f a cantecn; the meat used had been precooked and reheated. Seven of these outbreaks were due to CI. welchii. TABLE

VI

Food poisoning o f all t)Tes, t 9 6 8 General atul family outbreaks associated with meat and poultry

Vehicle of infection

Salmoneilae

Cold meat Processed meat* Flare, boiled bacon Tongue Fresh meatt Beef Chicken Turkey Pork Mutton Reheated meat Beef Chicken Turkey Mutton Stew, including mince Meat pies Manufactured Cornish pasty Made at home or canteen Steak~ Shepherds~ Steak pudding Origin not stated Spit-roasted chicken Roast meat, not known to have been reheated or served cold Beef Chicken Turkey Pork Mutton Ox Heart Canncd meat Corned beef Tongue Brawn Gravy Dripping Various meat products ALL

M~AT D I s H r ~ s

*Semi-preserved meat tUncurcd meat ~ : S t e a k p i e s c o n s i s t o f m e a t in a d i s h with potato in place of pastry.

Presumed Staphylococci

causal

agents

CI. welchii

Not discovered

All agents

2 -

1 1

-

"~ 2 4 -

3 1 -

5 1 1 "

--

3 3 3

--

3

1

4 4

-

3 1

1

E

""

6

--

5

-

1 2

1 -

-

7

1

1 8

1

-

-

-

1

8

-

4 2 I

1 -

5 2 I

l

-

-

l

-

-

-

-

1 1 1 1 1 l

1 3

3 1 t -

-

24

12

39

with

pastry

on

t

top;

shepherds"

26

/ I I J

8

6

I -

5

3 t 4 If I ! 1 3

80

pies are similar

but

F O O D P O I S O N I N G A N D Sahmm,'tla I N F E C T I O N S

247

In one large family outbreak infection was probably introduced into tile kitchen via knacker meat which was cut with a knife also used for human food. Thirteen persons became ill after eating cold roast turkey and five were found to be infected with Sahn. typhhnurhml phage type U71. The family bought meat for their dogs from a knacker's yard and Sahn. typhhnurhtm of the same phage type was isolated from drains at the knacker's yard and from pet meat at a shop supplied from this source. Regulations introduced in 1969, which require the sterilization of knacker and other meat designated as unfit for human consumption, should prove a safeguard for domestic pets and their owners (Statutory Instrument, 1969; Lancet, 1969).

Shel~sh and other.fish Five outbreaks were associated with fish, four with shellfish and one with canned salmon. An outbreak of mussel poisoning was reported in the north east of England in May and June 1968 (McCotlum et al., 1968). The first case was a woman admitted to hospital with vomiting, numbness of the lips and extremities, muscular weakness and incoordination. She became ill half-anhour after eating mussels which she had cooked herself. During the next three days 70 similar cases were diagnosed and I8 were admitted to hospital; all recovered. The outbreak was attributed to the neurotoxin of the dinoflagellate microorganism Gonyaulax tamarensis which had accumulated in the mussels as a result of an unusual profusion of the organism in seawater off the northwest coast of England. Bivalve molluscs, which feed by filtering, may concentrate the toxin and thus become a health hazard (Clark, 1968). Two outbreaks were reported after restaurant meals at which oysters were served. The seven members of a party who had eaten oysters became ill 4 to 50 hours after the meal; but five guests who did not take the oysters were not ill. The symptoms, which included nausea, vomiting, diarrhoea and malaise, lasted for three to seven days. The oysters were received by rail from an oyster farm in Cornwall and were believed to have been cleansed before despatch. The second outbreak was due to oysters reported to be from the East coast; nine persons had symptoms 2 to 70 hours after a luncheon party. None of the usual pathogens were isolated from the six oysters examined. Similar outbrcaks of unknown aetiology associated with oysters were reported by Gunn & Rowlands (1969), Barrow & Miller (1969) and Preston (1968). In the fourth outbrcak two persons became ill after eating cockles and mussels at a seaside resort. A staphylococcal outbreak was due to salmon which had been left at room temperature for three weeks after the can was op.ened; Staph. aureus of the same phage type was isolated from the one patient examined and from the salmon.

Milk Four outbreaks were associated with unpasteurized milk; two were due to

248

PUISLIC H E A L T H VOL. 84 NO. 5

Sahn. o,phimurium and two to Sahn. &~blin. In the autumn of 1968 there was an outbreak of gastroenteritis in a village in the south west of England; the only common factor was the consumption of untreated farm-bottled milk from the same producer-retailer and Sahn. typhimurhml phage type 1 was isolated from 59 cases and excreters, from an unopened bottle of the milk, from a sample taken from the bulk tank and from an individual milk sample from one cow. Fourteen farm workers and members of their families were infected. One cow, which was not in milk at the time of the outbreak, died with Sahn. typhimurium infection of the gut, but the rest of the herd were clinically healthy. The second outbreak was associated with farm-bottled raw milk from a herd in which two cows werc excreting Sabn. typhimurhtm phage type 11 in the faeces. The farmer and his family had been ill and 18 cases of salmonettosis were confirmed among his customers. In one of the outbreaks due to Sahn. dublin the employees of an estate and members of their families became ill after drinking raw milk; the milk had been left at ambient temperature for up to 24 hours on an exceptionally hot day. Sahn. dublin was isolated from 10 o f the patients and from the milk of a sick cow. The other Sah,. dublin outbreak was also in farm workers; the organism was recovered from five patients, two cows and a milk filter from the farm. Beverages Two chemical outbreaks were associated with beverages; one was due to copper sulphate in tea brewed with water from a corroded geyser and the other to cadmium in a soft drink. Both outbreaks are discussed later under chemical food poisoning.

Sweet In an outbreak ill April 63 persons became ill I to 4 hours after eating dairy cream trifles from a local bakery. The base of the trifles wasjellied spongecake, jam and custard, which was prepared the previous day, kept in a cbldroom overnight and topped with fresh cream the next day, when the trifles were covered with cellophane and distributed to retailers. Staph. aureus was isolated in large numbers from the base and the cream of partially eaten trifles and also from those recalled from the retailers; strains o f Staph. attretts from nasal carriers at the bakery belonged to different phage types. Eggs An outbreak of Satin. typhinutrhml infection was reported in a family who ate mousse prepared with uncooked egg albumen. The eggs were from their own hens and Sahn. typhhnuriun: of the same phage typc was isolated from the droppings of the birds. No incident associated with commercially produced bulk egg products was recorded. In one outbreak Bernaise and Hollandaise sauces were the suspected vehicles and Staph. attreus of the same phage type

F O O D POISON I N G A N D Salmolmlla I N F E C T I O N S

249

was isolated fi'om both; these sauces are usually made with raw egg, but it is possible that they were contaminated after preparation at the same restaurant.

Vegetabh.,s In an outbreak of food poisoning at a summer camp 14 persons became ill one to two hours after eating fried potatoes which had been boiled one or two days earlier and stored at kitchen temperature; campers who did not eat the fried potatoes were not ill. The remainder of the potatoes yielded a heavy mixed growth of organisms and Staph. aureus was isolated from the cook, but it was not clear which organism was responsible for the outbreak. Other Foods In some of the other outbreaks a specific food was mentioned as the suspected vehicle, but the bacteriological and epidemiological evidence incriminating these foods was inconclusive.

Causal Agent Sahnonella (Tables VII, VIII and IX) In 1968, 30% of cases due to a known food poisoning organism were infected with Sahn. typhimurium and 43 % with other Salmonella serotypes. The numbers of incidents due to each serotype are set out in Table VII, which also gives the rank order of the ten serotypes causing the greatest number of incidents in 1968. The most frequently reported serotypes were: Sahn. O,phimurium 1654 incidents, Sahn. pananla 379, Sahn. enteritidis 271, Sahn. virckow 253, Salm. stanley 169 and Sab~l. dublin 100. Other serotypes 3vere each responsible for less than 100 incidents. Only serotypes causing human infection during the year were included in the table; isolations o f the same serotypes of salmonellae from food and feedingstuffs are also given. Among the larger outbreaks of salmonellosis in 1968 were those associated with barbecued (spit-roasted) chicken. A large outbreak due to Sahn. virchow associated with eating barbecued chicken in the north of England was mentioned in the 1967 report (Vernon, 1969); another outbreak of Sahn. virchow infection involving some 160 persons in the /Vlerseyside area was investigated in 1968 (Semple et al., 1968). The source of the outbreak was deep-frozen chickens; carcasses at the packing station and chicks at the hatchery and rearing farms were found to be infected with Salm. virchow (Pennington et aL, 1968). An outbreak due to Sahn. montevideo occurred among customers of a barbecue in a south-western town; frozen chickens were spit-roasted and reheated when required; tools and working surfaces were contaminated with Sahn. montevideo and isolation of the organism from spits indicated that salmonellae at the centre of the chicken had survived spit-roasting (Hill, 1969). Sahn. panama was isolated from 32 of 130 persons who ate chicken at a hospital social club barbecue (Payne, 1969a),

aberdeen abony adelaide agama agbeni anatum arechava&,ta ayinde

bareilly blockley bonariensis bonn bradford braenderttp brandenburg bredeney

cairo california canada chester choleraesuis coeln

Salm. Salm. Salm. Salm. Salm. Salm. Salm. (! O) S a l m .

Saint. Salm. Salm. Salm. Sabn. Salm.

Salm. typhimurium

T y p e o f Salmonella (excluding S a l m . typhi and Salm. p a r a t y p h i B )

Sahn. Salm. SaOn. Sahn. Salm. Saint. Salm. Sahn.

(1)

TABLE VII

1 4 2 4 7 1

11 8 1 1 1 14 56 59

-

-

1654

. .

. . .

. . . . 4 .

. . . . . 1 . .

5

Incidents in h u m a n beings¢

l 6 3 2 1 39 1 I

Homeproduced and imported egg a n d egg products

.

.

. .

-

2 .

.

.

. . .

. . .

. .

.

.

. . -

14

.

37 . .

.

.

.

Poultry'~

. . . . 3 .

. . .

1

. .

.

.

.

. .

-

.

.

.

1

.

6

.

.

.

.

. . .

. .

.

-

.

Imported meat a n d offal for human consumption

.

. .

.

.

.

.

.

. . .

2

.

.

.

-

.

1 . .

.

2

.

.

.

Meat and offal for human consumption (not specified as imported)

.

.

.

.

.

.

. . . .

. .

.

.

-

3

-

.

2

.

.

.

2

.

I

.

.

Sausages and made-up meat

.

.

.

. . .

. .

.

.

1

1

. .

2

-

.

.

.

-

.

.

.

.

.

. . .

. .

.

.

.

3

.

1

.

.

.

3

.

.

.

.

.

1

I00

-

. . .

. .

.

.

5

1

7

.

-

1

2

3

Imported Knacker K a n g a r o o h o r s e m e a t meat and meat intended pet meat for f r o m U.K. animals

T y p e s o f sahnonellae isolated fi'om o u t b r e a k s a n d sporadic cases h~ man, 1968 Tire f r e q u e n c y o f isolation o f these types f r o m eggs, meat, unpasteurized milk*, shellfisht a n d fertilizers attd fi, eding stuff's

6

2

4

10

13

4

36

I

25

bone, blood, fish and feather meal

Meat,

1

5 4

Salm. kottbtts

2 l

1

3

1

2 87 41 3

1

1 2 4 35

1 1

7 6 l

271 1

1

3

1

2 1

! 1

1

Sabn. kinshasa

1

m

!

3

3

2

2

4

14

100 5

m

1

1

21

2

1

Salm. ibadan (8) Salm. indiana Salm. infantis Salm. isangi Salm. jedburgh Salm. johannesburg Sa#n. kaapstad Salm. kapemba Salm. kentucky Sabn. kiambu

Salm. give Salm. gombe Sabn. guinea Sat,n. ha~fa Salm. hamburg Sahn. hartford Sahn. havana Salm. heidelberg Sabn, hvittbtgfoss

Salm. fischerkietz

Salm. derby Salm. drypool (6) Sabn. dublin Sahn. duisburg Salm. durban Salm. durham Salm. eastbourne Salm. edinburg Salm. edmonton Salm. eimsbuettel Salm. emek (3) Salm. enterRidis Sahn. eppendorf

Sabn. eoleypark Salm. colorado Salm. eubana

~ -

2

2

1

|

E

I

I

21

I

8

I

1

3 !

I

4

7

, 4

5

17

I

1

1

5

13

1

SaIm. e#derstepoort

1

41 2 2

(9) Salm. oranienburg Salm. orion (2) Salm, panama Salm. poona Sahn. potsdam

Salm. reading Salm. richmond Salm. riggil

61 1 379 5

3

43

2 1

4

8

1 88

1

3 1 4

I0

1 1 15

Incidents in human beingso

Salm. napoli Salm. newbrunswick Salm, newington Salm. newport

Sahn. labadi Salm. lexington Salm. livhzgstone Sahn. london Salm. manhattan Sabn. meleagridis Salm. menston Salm. miami Salm. mikawasima (7) Salm. montevideo Sabno muenchen Salm. muenster

Type of Salmonella excluding Salm. typhi and Salm. paratyphi B)

Table VII Continued

m

3

m

Homeproduced and imported egg and egg products

m

1

3

3

2

N

1

1

D

I

m

M

m

1

Imported Meat and meat and offal for offal for human Poultry~ human consurhpcontion (not sumption specified as imported)

m

m

1

1

m

D

1

1

I

M

!

m

I

6

6

N

i

2

m

3

1

N

1 1

m

m

Imported Knacker Sfiusages and Kangaroo horsemeat meat and intended pet meat made-up meat meat for from U.K. animals

7 1 1

2

6

53

9

2

m

6 1 4

10 1

13 75 !

meal

Meat, bone, blood, fish and feather

4,12:d;--

TOTALS

Mixed infectionsx

Salm,

Salm. zega

Salm. wil Salm. worthington

Salm. wien Salm. westerstede

Salm. virchow

38 2

1

2

3796

2

1 1

253

1

Saint. vinchrady

26

Salm. thompson

i 3

2 1 7

Salm. taksony Salm. telelkebir Salm. tennessee

Salm. uganda S a l m . vefle

32

Salm. takoradi

-

-

-

49

.

m

-

16

-

m

m

m

-

-

.

-

-

113

11

w

34

-

n

.

-

-

-

-

-

35

.

-

-

7

.

I

8

-

w

5

n

16

m

M

m

*Unpasteurized milk: Salm. dublin 4, Salm. typhimurium 4. "['Shellfish: S a l m . e n t e r i t i d i s 1, S a l m . p a n a m a l , S a l m . t y p h b n u r i u m 1, S a i m . v i r c h o w 1. N o isolations were recorded from coconut or gelatine. oEach incident is represented by one strain only; the ten most frequent types are shown in rank order. x P o u l t r y : chicken 49, turkey 12, d u c k 51, n o t specified 1. xSalm, anatum with Sabn. senftenberg; Salm. montevideo with Salm. panama.

(4)

1

169

8

1

5 1

Salm. stanleyville

<5) Salm. stanley

Salm. sofia

Sa!m. sladtm

Salm. singapore Salm. sinstorf

2

Salm. senegal Salm. senftenberg

33

4

17

Salm. schwarzengrund

1

Salm. ruiru Salm. saintpaul

1

Salm. rubislaw

15

u

3

1

,

,,.

, ,, . . . . . . .

•

128

m

......

47

534

I0

w

m

3

2

J

m

21

1

2

2

I 1

113

N

,,

m

4

N

1

3

1

2 5

25;~

P U B U C H E A L T H VOL. 84 NO. 5

In three hospital outbreak.s of salmonellosis c?icken was suspected as the vehicle of infection. Some of the episodes in hospitals were concurrent with irff'ection due to the same serotype in the local community and may have originated with the admission o f a symptomiess excreter. An outbreak of Salm. rirchow infection in a maternity hospital look place after the admission of an excreter who infected her new-born baby; 15 babies had diarrhoea and one, with congenital malformations, died (Ro:we et aL, 1969). In an outbreak of Sahn. oranienburg irffection ~he first recog-nised case was in a hospital midwife; ~he organism was later isolated from 89 cases and excreters, mainly among the staff, and the hospital was closed. The first isolates of an unnamed monophasic Sahnonella serotype 4,12:d :were ~made in the summer o f 1968 and by the end of the year 68 human cases and exc,re.ters had been reported. There were outbreaks in two hospitals and a nursing home, and three family outbreaks. The vehicle of infection could not be established with confidence in any of these incidents, although minced chicken was suspected in one outbreak in a children's hospital. Sahn. 4,I2:d:- has been isolated from meat products, poultry, sheep, pigs, abattoir swabs and feedingstuffs. One hundred and thirteen strains of salmonellae were isolated from cooked and uncooked chicken, duck and turkey (Table VII); 34 strains of Sahib. virckow were obtained from chicken and Salm. typh#nurium was isolated from 32 ducks. Fifteen different salmonella serotypes were isolated from egg and egg products; 24 strains (I0 serotypes) were obtained from imported egg noodles and pasta. Salmonellae were also isolated from imported liquid, flake and spray-dried albumen, not yet required to be pasteurized under legislation, and raw liquid whole egg. Imported meat and offal for human consumption was most frequently infected with Sabn. dublin, Salm. se~enberg and SahT~. typkOnurium. Surveillance of imported boneless and carcase meat has given rates of up tO 24 ~ of samples contaminated with salmonellae (Hobbs & Gilbert, 1970). Imported and home-produced pet meat and knacker meat yielded 175 strains of salmonellae belonging to types also associated with human infection; much of this material was horsemeat or horse offal from South America. A variety of protein meals and complete feeding-stuffs were examined; these included meat, bone, fish and feather meals, dried bone and bone dust, dried blood, concentrates and complete foods. Much of the meal was intended for animal feeding-staffs, but some may have been used as fertiliser. Altogether, 95 different serotypes were isolated, but only 54 of these were types also associated with human infection. Studies of salmonellae in meat meals have given isolation rates between 1 6 ~ and 92% of samples positive (Taylor and McCoy, 1969). In Table VIII a comparison is made between the total number of serotypes obtained from non-human sources and the number of serotypes also causing illness in man. In food for human consumption between 8 3 ~ and 100~ of

FOOD P O I S O N I N G A N D Salmonella I N F E C T I O N S

255

serotypes isolated were also found in man; in animal feeding-stuffs a lower proportion of serotypes were common to man, presumably because some salmonellae found in feeding-stuffs failed to become endemic in livestock. The number of isolations of salmonellae from non-human sources depends greatly on the number and type of samples taken, but the figures show that foods for both human and animal consumption are frequently contaminated with organisms causing illness in man. Bacteriological surveys of abattoirs over a period of time have established a relationship between salmonella serotypes isolated from human infections and the serotypes present in local abattoirs (Payne, 1969b). The number of salmonella isolations from animals made in veterina~, laboratories is shown in Table IX; most were assumed to be from outbreaks of illness among farm stock. As far as possible the figures have been compiled on the same basis as those for human infections, that is, each incident is represented by one strain of the relevant serotype. Host+specific serotypes, such as Sahn. pullorum, Sahn. gallinarum and Sahn. abortusovis, have been omitted. Sahn. typhimurh+m was isolated from all the f a r m animals and poultry listed; it was the commonest serotype isolated from fowl, duck and turkey. Sahn+ dublin accounted for about four-fifths of the incidents in cattle and was also found in pigs and sheep; it was the sixth commonest serotype in man. Many of the common serotypes in man were also isolated from poultry; these incIuded Sa~m. virchow, Sahn. enteritidis, Sahn. stanley and Sahn. #1diana. It should be emphasised that these isolations were associated with sick animals; the frequency of symptomless carriage of salmonellae which may infect meat and poult~' for human consumption at the abattoir or packing station is rarely known, and requires further investigation.

Typhoid and paratyphoid fever Information on isolations of Salm. t)Thi and Sahn. paratyphi made in public health and hospital laboratories is not included in the above table.s Reports were received o f 169 persons infected with Sahn. typhi; 120 had symptoms, 31 were known to be carriers and 18 others were symptomless at the time o f examination. Sixty-two patients (52 ~ ) were known to have been infected a b r o a d ; 32 in Europe, 19 in Asia, 9 in Africa, 1 in the West Indies and in one case the country was not stated. Three patients are known to have died; a child aged four in contact with a carrier from Jamaica, a man aged 25 who was probably infected in India and a man aged 59 whose source of infection was not stated. No major outbreaks of typhoid lever occurred. There were 13 incidents in which two or more cases or excreters were reported in the same family, four outbreaks in which friends or neighbours of the family were also infected and two infections in each of two institutions, a mental hospital and a home for the chronic sick. There were five patients with and two without symptoms infected with

256

PUBLIC HEALTH VOL. 84 NO. 5

Salmo. paratyphi A; all but one had been infected abroad. Ninety-seven isolations of Sabn. paratyphi B were recorded; 78 of the patients had symptoms at the time of examination and nine were known carriers; 3 1 ~ of the clinical cases were infected abroad; 14 patients acquired their infection in Europe and seven in Africa. Six patients and two symptomless excreters of the same phage type became infected at an English seaside resort in June, 1968; four patients were members of two families who stayed on a caravan site, one patient stayed in a fiat, two were day visitors and one a local child: investigations of food shops and retailers of icecream and shellfish failed to trace the source of the outbreak. There were eight family outbreaks; in one a mother and her two children were infected and Sahn. paratyphi B of the same phage type was isolated from their pet terrapin. No deaths from paratyphoid fever were recorded. Staphylococci In 1968, 63 incidents of staphylococcal food poisoning were recorded compared with 29 in 1967. However, the increase was mainly in sporadic cases and the number of persons affected was fewer than in 1967. Only seven outbreaks comprised ten or more cases of illness; in the largest, 63 persons became ill after eating trifles from a bakery. Fifty patients required hospital treatment after a wedding reception (Fernandes, 1968); the same phage type of Staph. aureus was isolated from the vomit or faeces of 12 patients, from samples of cold chicken and jelly served at the reception and from the fingers of the caterer. In a similar outbreak at a medical conference, 15 persons were admitted to hospital after a lunch of cold chicken and ham; strains of Staph. aureus from patients and from the chicken and ham belonged to the same phage type but that from the chef, who had a nasal discharge, had a different phage-typing TABLE VIII Salmonella isolations from food and feeding stuffs, 1968 Proportion of strains belonging to serotypes associated with disease in man Food and feeding stuffs

Home produced and imported egg and egg products Poultry (~:hicken, duck, turkey) ImporteA meat and offal for human consumption Meat a n d offal for h u m a n consumption (not specified as imported) Sausages and made-up meat Kangaroo meat Imported horsemeat intended for animals Knacker meat and pet meat from O.K. Meat, bone, blood, fish and feather meals *Excluding Salm. typhi and Salm. paratyphi B tSee Table VII

Total no. of serotypes*

No. of seroWpes also found in rnan~ No. ~o

18 11 9

15 II 9

83 100 100

5 7 15 20 I7 95

5 7 10 14 14 54

100 100 67 70 82 57

FOOD POISONING AND Salmonella INFECTIONS

257

TABLE IX

Salmonella* isolations from animals and poultry, 1968 (From the Central Veterinary Laboratory Weybridge; the Veterinary Laboratory, Lasswade, and the Veterinary Investigation Services) (Includes some figures from Scotland) Type of Salmonella*

Salm. agama Salm. amsterdam Salm. anatum Salm. blockley Salm. california Salm. chester Salm. choleraesuis Satin. derby Salm. dublin Salm. enteritidis Salm. farmsen Sa[m. give Salm. hato Salm. heidelberg Salm. indiana Salm. infantis Salm. kiambu Salm. kinshasa Satin. lomita Salm. menston Salm. muenster Salmo .newhaw Salm. othmarschen Salm, poona Salm. reading Salm. saintpaul Salm. schwarzengrund Salm. senftenberg Salm. stanley Salm. thompson Salm. virchow Salm. 4, 12:d:Satin. typhimurium TOTAL

Cattle

Pigs

Sheep Chicken

.

.

.

.

1

.

.

.

.

!

-

1

-

.

.

I

-

l

.

.

.

.

.

.

.

.

.

.

.

.

.

.

-

.

4

-

l

.

.

.

1

5

-

-

4

-

1

2

2

-

2

-

2

-

2

16

.

.

j

.

.

. I

l

-

.

.

.

-

.

.

-

.

-

.

.

.

.

2

-

.

. 42

18

-

.

!

.

!

1

.

82

. 1950

. -

-

.

Turkey

.

-

-

.

Duck

!

. .

.

-

-

.

.

1

-

-

-

9

-

1

-

-

-

4

-

5

1

-

3

-

-

-

1

477

8

9

29

I0

17

2447

109

53

89

14

40

I 4 -

I

-

1

*Excluding Salm. paratyphi 13, Salm. pullorum, Salm. lcallittarton, Sabn. abortusovis. pattern. I n b o t h these incidents the chicken was c o o k e d a n d cut up the day b e f o r e and then k e p t for s o m e h o u r s a t a m b i e n t t e m p e r a t u r e . P h a g e typing results w e r e available for I5 o u t b r e a k s ; in seven the strains of Staph. aureus b e l o n g e d to g r o u p lII, in five to group l/III, in two to g r o u p l a n d in one o u t b r e a k the strains were u n t y p a b l e . In seven o u t b r e a k s strains o f Staph. aureus were examined for the p r o d u c t i o n o f enterotoxin, I n the three o u t b r e a k s m e n t i o n e d above and in three other outb r e a k s the strains p r o d u c e d e n t e r o t o x i n A and in o n e family o u t b r e a k the strains p r o d u c e d e m e r o t o x i n C ( S i m k o v i c o v a & Gilbert, 1970).

258

P U B L I C H E A L T H VOL. 84 NO. 5

Gonyaulax tamarensis toxin In an outbreak of shellfish poisoning due to the toxin of the dinoflagellate Gon tamarensZ~ 70 persons became ill after eating mussels; this outbreak has already been discussed under shellfish and other fish. Clostridiwn welchii Just under one-quarter of the cases of food poisoning in which the causal agent was known was due to CI. welchii. There were, however, 20 fewer incidents and about 500 fewer cases than in 1967; the decrease was mainly in general outbreaks. In five outbreaks more than 100 persons were ill and in five between 50 and I00 persons; most of the larger outbreaks were associated with meals in industrial canteens, schools or other institutions. The vehicles of infection, which were established with reasonable certainty in 39 of the 49 outbreaks, were all meat or poultry dishes, in most cases precooked and reheated. In most of the incidents the strains of CI. welchii isolated from the patients were said to be heat-resistant, but in three outbreaks heat-sensitive strains (surviving not more than I0 minutes at 100°C) were obtained. Outbreaks due to heat-sensitive 13-haemolytic strains of CI. welchff have previously been reported (Sutton & Hobbs, 1968); the organisms may survive cooking if the size of the joint is such that heat penetration is slow and the cooling period long or in frozen poultry or other frozen meat that is insufficiently thawed before cooking (Mead, 1969), or in meat contaminated during storage after being cooked (McKillop, 1959). Chemical In an outbreak due to copper sulphate twenty factory workers had vomiting, diarrhoea or nausea after drinking tea brewed with water from a corroded geyser; some patients vomited within a few minutes of drinki~ag the tea and others had diarrhoea but no vomiting. The copper content of a sample of tea from the brew pan was 30 p.p.m. The geyser had not been serviced/~orsome years and showed considerable copper corrosion (Nicholas, 1968). Ten persons became ill after drinking a proprietory beverage served from a dispenser unit at a caf6; chemical analysis revealed 110 p.p.m, by weight of cadmium and 25 p.p.m, of iron. A cadmium-plated steel clamp, used for holding the cover in place, had fallen into the stainless steel container and the acid beverage had attacked the cadmium and steel. The manufacturers have now replaced cadmium-plated clamps by those made of stainless steel (Settle, 1970). Discussion In 1968, 73 % of reported cases of food poisoning in which the causal organism was identified ~ere due to salmonell~e; this represent~ an increase compared with I967 and 1966 when the rates were 66% and 65°~ respectively (Vernon, 1967). The commonest serotype was Salm. typhimurium, which was isolated in

FOOD POISONING AND Sahnonella INFECTIONS

259

41 7o of cases of salmonellosis, a slightly lower proportion than in previous years. In interpreting these figures it must be remembered that reported isolations probably include only a small part of all Sahnonella infections that occur. Conclusions about the distribution of different serotypes, their sources and their importance have, therefore, to be guarded. The epidemiology of Sahn. typhimurium infections and the relative importance of different sources can only be determined with the aid ~of phage-typing (Anderson, 1969). Most human infection with Sahn. typhimurium is probably acquired through eating meat and meat products (Anderson, 1968). Poultry appears to be becoming increasingly important as a source of salmonellosis (Royal Society of Health, 1969). Chicken or turkey was established as the vehicle of infection in 15 Salmonella outbreaks in 1968 compared with four outbreaks in 1967. Three outbreaks were due to Sahn. tvphimurium, 4 to Sahn. montevideo, 3 to Sah~7. virchow, 2 to Sabn. panama, 2 to Sahn. enteritidis and 1 to Sahn. muenchen. Eight outbreaks, in which altogether over 400 persons were affected, were associated with spit-roasted chicken. Frozen chicken may already be infected with salmonellae and cooking on a rotary spit may not bring the centre of the bird to a temperature sufficient to destroy the bacteria; contamination of the cooked chicken may occur from utensils, containers, surfaces and also from raw to cooked birds by the hands of the staff. The introduction of infected meat and poultry into the kitchen is always a hazard and the risk is even greater when the method of cooking may not render the meat safe. Clearly, measures for the reduction of Sahnonella infection are required at all stages of production from the breeder flock to the table, including the reduction of contamination of animal feeding stuffs.

Summary An analysis is presented of reports of food poisoning, including salmonellosis, received by the Public Health Laboratory Service from public health and hospital laboratories and by the Department of Health and Social Security from medical officers of health. In 1968, 246 general outbreaks, 546 family outbreaks and 4292 sporadic cases were recorded; 10,511 persons were affected, slightly fewer than in 1967, and 44 patients died. In 78 ~ of cases the causal organism was ~identified; in nearly three-quarters of the cases due to a known cause and in all except two of the deaths the causal organisms were salmonellae. A particular food was incriminated in a third of the general outbreaks but in only 2 ~ of family outbreaks.

References ArCOERSON, E. S. (1968). Br. reed. J. iii, 333. ANDERSON, E. S. (1969). In Bacterial Food Poisoning, p. 47. Ed. Joan Taylor. London: Royal Society o f Health. BARROW, G. I. & MILLER, D. C. (I969). Lancet, ii, 421. CLARK, R. B. (1968). Lancet, fi, 770.

260

PUBLIC HEALTH VOL. 84 NO. 5

COCrmURN, W. C. & VERNON,E. (1969). In Bacterial Food Poisoning, p. 5. Ed. Joan Taylor. London: Royal Society of Health. F~NAND~S, M. T. (1968). Med Offr, 120, 352. GLEN, A. D. G. & ROWLANDS, D. F. (1969). Ned. Offr, 122, 75. HILL, R. J. (1969). Environm. Hlth, 77, 345. HOBBS, B. C. & GILBERT, R. J. (1970). Chemy. Ind. (Rev.) 215. Lancet (1969). Meat for the dog. (Annot.) ii, 832. MCCOLLUM, J. P. K., PEARSON, R. C. M., INGHAM, H. R., WOOD, P~ C. & DEWAR, H. A. (1968). Lancet ii, 767. MCKILLOP, E. J. (1959). J. Hyg., Camb. 57, 31. MEAD, G. C. (1969). J. appL Bact. 32, 86. NICHOLAS, P. O. (1968~). Lancet, H, 40. PAYNE, D. J. H. (I 969a) PubL Hlth, Lond. 84, 5. PAYI~, D. J. H. (1969b). In Bacterial Food Poisoning, p. 117. Ed. Joan Taylor. London: Royal Society of Health. PENNINGTON,J. H., BROOKSBANK,•. H., POOLE, P. M. & SEYMOUR,E. (1968). Br. reed. d. iv, 804. PRESTON,F . S. (1968). Aerospace Med. 39, 519. P o n u c HEALTH LAnORATORYSERVtC• (1964). MG;~. Bull. Minist. Hlth, 23, 189. Royal Society of Health Journal (1969). 89, 52. RowE, B., GILES, C. & BROWN, G. L. (1969). Br. reed. J. iii, 561. SEMPLE, A. B., TURNER, G. C. & L o r r y , D. M. O. (1968). Br. reed. J. iv, 801. SEaTtLE, H. L. (1970). Meal. Offr, 123, 24. StMKOWCOVA, MAODA & GmSERT, R. J. J. Med. MicrobioL In the press. STATIYrORY INSTRUMENT (1969). No. 871. Food and drugs. Food Hygiene. The Meat (Sterilisation) Regulations 1969. London: H.M.S.O. SUTTON, P,. G. A. & HOBBS, B. C. (1968). J, Hyg., Camb. 66, 135. TAYLOR, JOAN (~ McCoY, J. H. (1969). In Food-borne-Infections and Intoxications, p. 3. Ed. H. Riemann. New York: Academic Press. VERNON, E. (1967). Non. Bull. Minist. Hlth, 26, 235. VERNON, E. (1969). PubL Hlth, Lond. 83, 205.