(Symposium on Food Microbiology end Public Health: Paper I)

OUTBREAKS OF PARATYPHOID B FEVER ASSOCIATED WITH IMPORTED FROZEN EGG. I. EPIDEMIOLOGY

BY K. W. NEWELL

Epidemiological Research Laboratory, Central Public Health Laboratory, Colindale

C o N T E N T s

1. The epidemic . 2. The outbreaks 3. The sporadic cases . 4. The caws and excreters 6. Investigation of bakeries 6. Imported frozen egg 7. Discussion . 8. Acknowledgements . 9. Reference .

PAGE 462 463 464 464 464 467 468 469 470

1. THE EPIDEMIU IN AUGUST 1954 a number of strains of Salmonella paratyphi B isolated from patients and excreters in different administrative areas of North-west London, were found by the Central Enteric Reference Laboratory to belong to phage type 3a var. 2. This type is uncommon. Only 13 strains have been identified since January 1949, and only one of these was in the past three years.

Table 1. Distribution of incidents caused by a. speci$c type of Salmonella paretyphi B

Suspected month Administrative Outbreak (0) Number of cmes area where Single case (S) of infection A r >

infection occurred Clinical Symptomless

July 1954 Harrow M. B . 0 5 2 September 1954 Harrow M.B. S 1 0

Barnet U.D. S 1 0 Edinburgh S 1 0 Fulham M.B. 0 2 0 Camberwell M.B. S 1 0 Sheffield C.B. s, s 2 0 Windsor M.B. 0, s 10 6* St. Pancras M.B. S 1 0 Watford R.D. S 1 0 Sheffield C.B. s, s 1 1 Basingstoke M.B. 0 2 2 Paddington M.B. 0 3 0

November 1954 Richmond M.B. 0 4 3 Chelsea M.B. S 1 0 Hendon M.B. s, s 2 0

Totals 6, 0 14, S 38 14

* Including a case where only a serological diagnosis was made.

October 1954

Food microbiology and public health 463

Between the beginning of August 1954 and the end of December 1954, fifty-one strains of this type were identified: 38 from clinical cases and 13 from symptomless excreters. The distribution of these cases is shown in Table 1. Thirty-seven of these patients and excreters were from six small outbreaks (an outbreak being defined as 2 or more related caaes or excreters). Fourteen were single cases or excreters not known to be associated with each other or with the outbreaks.

2. THE OUTBREAKS

The Harrow outbreak I n August strains were isolated from five cases and two symptomless excreters

in four families in North-west London. They lived in three administrative areas and, although they were a t first thought to be unassociated, detailed investigation showed that they had all eaten chocolate Bclairs filled with imitation cream from a bakery in Harrow M.B. on 24 July. Two of the families ate cakes from this bakery every week, but the other two families ate these cakes only rarely.

The Fulharn outbreak Strains were isolated in September from two patients, in different families, who

had become ill within a day of each other. The only connection between them wt t~ that they had eaten cream cakes from a bakery in Fulham M.B. on 18 September. One patient had bought cakes late on this day a t a reduced price and had kept them for 24 hours. Four to six hours later she had diarrhoea and vomiting lasting for 12 hours. She then recovered and developed her main illness on 23 September. The second patient became ill on 24 September.

The Windsor outbreak Ten people from Windsor, Egham and Beaconsfield became ill between 13 and

30 October. They had all eaten cakes from one bakery in Windsor M.B. between 8 and 23 October; no other connection was found. Two family contacts of the patients and three of the retail staff of the bakery were found to be symptomless excreters and one pastry cook had serological evidence of recent infection.

The Basingstoke outbreak Two children in different families became ill between 4 and 6 November and

two family contacts were found to be symptomless excreters. Between 17 and 23 October both families had eaten cakes from the same bakery.

The Paddington outbreak In October two children in different families sharing one house in Willesden M.B.

ate cakes from a bakery in Paddington M.B. a week before the onset of their illness.

464 K . W. Newell

Later the strain was isolated from a child in Wembley M.B. who had been in close contact with one of the children.

The Richmond outbeak In November there were four cases in three families in South London; the dates

of onset were from 1 to 7 December. Three symptomless excreters were found among family contacts. In the 14 days preceding their illness they had all eaten cakes from different retail shops of a bakery which distributed its products over a large part of South London. The cakes eaten were made in a small branch of this firm in Richmond M.B.

3. THE SPORADIC CASES

The fourteen single cases unconnected with the known outbreaks were also investigated. The patients were asked to remember the foods they had eaten during the three beeks before the onset of illness and, where possible, the foods and the shops supplying them were examined. All the single cases had eaten cakes during the incubation period of their illness, although in some cases the history was vague or confused by purchases a t many different shops a t the relevant times.

4. THE CASES AND EXCRETERS

Phage type 3a var. 2 of Salm. paratyphi B was isolated from the faeces of forty-six people, the blood of two, the urine of one, the sputum of one and the synovial fluid of one person. Serological evidence of recent infection was found in one person who had no symptoms. More females than males were affected, and more than half of those affected were younger than sixteen years.

5. INVESTIGATION OF BAKERIES

The six bakeries suspected of being the places wheSe the food was contaminated were investigated P 8 weeks after the possible date of infection. A blood specimen and 1, 2 or 3 faecal specimens were taken from all baking and retail staff. No excreters of Salm. paratyphi B were found in the baking staff, although serological examination of a pastry cook in the Windsor outbreak indicated a recent infection. This bakery supplied two retail shops where the patients had bought cakes. Three women working in one of the retail shops were found to be symptomless excreters of this organism.

No members of the staffs of the six bakeries admitted having any past history of gastro-intestinal illness and those absent or on leave were found to show no evidence of recent infection.

Salm. paratyphi B was not isolated from the cakes, fillings, machines or materials a t the time of the examinations, and no pathogens were found in Moore’s swabs (Moore, 1948) placed in the drains and lavatories of two of the bakeries.

The investigations in two of the bakeries are given in detail, although similar investigations were made in the others.

Food microbiology and public health 465

Harrow bakery In Harrow, all those who worked in the bakery were questioned and specimens

were taken 6 weeks after the suspected date of infection. Samples of filled and unfilled cakes and cream powder were examined. Cream from chocolate Bclairs showed 4,800,000 colonies/g including Escherichia coli type I , but no Salmonella were found, and the cream powder before reconstitution had only small numbers of organisms.

Sampling was repeated a week later. The production of chocolate Bclairs had been discontinued and samples of another type of cake and filling were taken a t each stage of their preparation. The cake ingredients were imported frozen egg, margarine, sugar and flour. No Salmonella or E. wli type I were found in the margarine and flour, which had low bacterial counts. The 3 oz sample of imported frozen egg, which was taken from a thawed opened tin, had a colony count of 722,OOO/g and E. wli type I but no Salmonella were found. The ingredients were mixed in a machine and a sample then showed a colony count of 47,000/g including E . wli type I and small numbers of Salm. typhi-murium. The cake mix was placed on trays and the mixing machine was washed and refilled with margarine, sugar and flour as the base of a cream. After mixing, a sample had a colony count of 61,00O/g including E. coli type I and small numbers of Salm. typhi-murium. The baked cake was filled with this mixture and the final product contained Salm. typhi-murium.

Sampling was again repeated a week later. A sample of a cake mix in the mixer before egg was added had a colony count of less than lOO/g and after the addition of imported frozen egg of more than 1O,OOO,OOO colonies/g. Further imported frozen egg samples gave colony counts of 7,000,000/g from an opened tin and 610,000 colonies/g, including E. coli type I and small numbers of Salm. aberdeen, from an unopened tin.

Chocolate Bclairs were again being manufactured, but now their cream had colony counts of less than lOO/g. The colony counts of the mixes a t this bakery were interesting, as they decreased as investigations continued. The differences between the colony counts of cake mixes at different times may have been due to the way the mixing machine had been washed. Mixtures containing imported frozen egg were expected to have a high colony count the count of the raw egg was high, but the colony count of mixtures which did not contain egg varied and seemed to depend upon the ingredients of the preceding mixture in the machine. The colony counts of cream and cream bases decreas4 as investigations were concentrated upon the machine, and the staff may have taken more care in washing it after it had been used.

When sampling was carried out during manufacture, mixes passing through the machine contained Salmonella; this might have been due to a contaminated machine or to the earlier use in the machine of mixes containing imported frozen egg, the only ingredient sampled separately which was found to contain Salmonella. In the earlier examinations of frozen egg the number of coli-amogenes organisms was high and it is possible that Salmonella may have been present, masked by an overgrowth of other organisms. Washings from the machine were examined once and they were found to have high colony counts, but no Salmonella were isolated.

466 K . W. Newel1

Further samples of faeces taken from the staff of the bakery did not show Salmonella, except from a van driver who ate the cakes frequently and who was found to be excreting Salm. aberdeen.

The discovery of Salm. aberdeen in a van driver and in an unopened tin of imported frozen egg may have been coincidental, but as this is one of the less common Salmonella species, and the van driver was a regular eater of the cakes, it is possible that he may have become infected with the organism from an earlier tin of imported frozen egg, with cakes as the vehicle of infection.

The batch number and the shipment of the imported frozen egg used at the bakery at the relevant time were unfortunately unobtainable. The tins used on the suspected day of contamination were similar to those used during the investi- gations, but there was then no reason t o suspect that they were of the same batch, or that the imported egg was the probable source of infection.

Fulham bake y

Similar investigations were made a t the Fulham bakery. The imitation cream in the original container was sterile and imported frozen egg from an unopened tin had colony counts of more than 50,00O,OOO/g. A cake mix containing this egg had a colony count of more than 4,000,000/g and Salm. thompson was isolated. No fillings were being made at the time of the investigation, but the same machine was normally used for mixing both cakes and fillings. The mixing machine bowls were washed in cold water but they were not washed after each mix. The imported frozen egg was in a tin of the same shape as that used in Harrow, and later it was found that the tin examined was of the same batch and shipment as those used on the suspected date of contamination.

Other bakeries In October in another bakery in Harrow, a sample was taken from an unopened

tin of imported frozen egg, as part of the investigation of a single case. Salm. thompson was isolated. This tin was found later to be of the same batch and shipment as the tin sampled in Fulham. No other tins could be obtained for examination.

In five of the bakeries a common mixing machine was used for cake mixes and for fillings. In one of the five bakeries the machine was washed only when the first mix would affect the quality of the one following. Contamination of imitation cream with cake mix was not thought to affect its quality. In two bakeries the machine was washed in cold water under a tap without soap or detergent. In a further two it was washed in a sink with hot water and detergent, but not regularly after each mix. In the sixth bakery a separate mixing machine was used for fillings. Here ‘butter cream’ made in a cake-mixing machine was used to dilute proprietary cream and a common savoy bag was used for piping out the outer part of the cake and later for its filling.

A comparison was made of the ingredients wed at the relevant times in the six bakeries associated with outbreaks. There were four different suppliers of flour,

Food microbiology and public health 467

four of white fat, three of margarine and three of chocolate. Three different brands of imitation cream were used in five bakeries, and one bakery had not used imitation cream at all during the four months before the probable date of contamination. The only common ingredient was imported frozen egg, and in each bakery associated with an incident there were common utensils or machines used for products containing imported frozen egg and for uncooked fillings. AU the bakeries used the egg in a cake mixture which was subsequently cooked; this egg was not used in any uncooked products in this series of bakeries.

6. IMPORTED FROZEN EGG

Imported frozen egg was supplied in 22 lb or 44 lb tins. In each suspected bakery 22 lb tins were used at the time the patients would probably have been infected. I n four bakeries the shape of the tins and the cardboard cartons they were packed in were thought to be unusual and this helped to determine the &te on which they were used. In the other two bakeries the staff could remember the unusual tins, but could not remember the date when they were used. Invoices confirmed the fact that the unusual tins were supplied a t the relevant times. The unusual 22 Ib tins were of an upright type, rather like a one-gallon petrol tin. They had small press-in caps in one corner of the top and were hand-made. There were no batch numbers on the tins or the cartons and two tins were packed side by aide in a cardboard carton.

In the Windsor bakery English frozen egg was used until four days before the probable date of infection of the first cases. Imported frozen egg in this unusual pack was then used for three weeks, followed by English frozen egg. All the persons affected in this outbreak were thought to have been infected in this thme-week period.

In Basingstoke the only consignment of imported frozen egg packed in this way and delivered to the town was received at the bakery four days before the suspected date of infection of the patients. The wholesaler supplying the tins had not supplied egg to this bakery in the preceding six months nor did he supply any in the following month.

Three wholesalers supplied the imported frozen egg to the six suspected bakeries. With their co-operation an attempt was made to trace back to the shipment all tins of the unusual type used by the bakeries at the relevant times. In five of the bakeries the imported frozen egg was found to have been part of a small shipment unloaded in the Port of London in July 1954 from the S.S. Shillong. The imported frozen egg used in the Harrow bakery, where the first outbreak occurred, was not thought to have been part of this shipment and it had not been possible to find out from which ship it was unloaded. It was packed, however, in tins of this unusual shape.

The ‘Shillong’ shipment of imported frozen egg was distributed by four wholesalers from July to November 1954. The three firms which supplied the suspected bakeries together distribute about 10% of the imported frozen egg coming into this country.

468 K . W. Newel1

The fourth firm distributed another 12% of the imported frozen egg imports, but this firm was mainly supplied with 44 lb tins from this shipment.

The S.S. Shillong carried 196 tons of egg packed in three different ways: in 44 lb machine made tins; in 22 lb tins of the type described, packed in pairs in cardboard cartons, and in 22 lb tins of a similar shape, but packed in single cartons. They all contained stored chilled eggs packed in four factories in December 1953. Two of the factories were at one time owned and operated by British and American companies and were aid to be large and well equipped for packing eggs. The third factory had not packed eggs for some time before December 1953 and the fourth factory had not been known to have been used for egg packing before. Less than one-third of the tins were of 22 lb. The importers were of the opinion that the two larger factories probably packed only 44 lb tins while the two other factories packed 22 lb tins, one in double and one in single cartons.

Invoices were examined at all the bakeries in four of the administrative areaa where outbreaks occurred, to find out the number that used imported frozen egg in the relevant month, and the proportion of those that used imported frozen egg of the ‘Shillong’ shipment in the unusual tin. The findings are shown in Table 2.

Table 2. Distribution of imported frozen egg

Administrative area 7

Total no.

Fulhm M.B. 37 Windaor M.B. 9 Besingstoke M.B. 3 Paddington M.B. 20 Totale 69

Bakeries L

\

No. using imported frozen egg in

No. using unusual 22 Ib cans from

relevant month ‘ShilIong’ ehipment 10 1* 4 3 1

10 1 1

25 6

* Two other bakeries may have used 22 lb tins of unusuel type from the ‘Shillong’ shipment.

In these areas, four outbreaks were connected with 4 of the 6 bakeries known to have been supplied with 22 lb tins of unusual shape from the ‘Shillong’ shipment. Another of the bakeries in Windsor, unconnected with an outbreak, supplied cakes to a single cme. The other thirteen single cases had eaten cakes in areas where the suspected batch of imported frozen egg had been distributed. Two patients ate cakes regularly from a bakery using this batch of egg, three sometimes ate cakes from a bakery using this egg and the remaining eight may have done so.

7. DISCUSSION

The epidemiological evidence suggests that the series of outbreaks described were connected with cream cakes made in bakeries. No carriers or excreters were found among the staff making the cakes, although in one bakery serological evidence of

Food microbiology and public health 469

recent infection was found in one pastry cook, and three of the persons selling cakes in one of the two shops associated with cases in the Windsor outbreak were symptomless excreters.

The distribution of the incidents and the short period of time in which they occurred made it appear probable that some common vehicle was responsible. The only common factor found in all the bakeries contaminated was imported frozen egg packed in an unusual manner. Every bakery used this egg a t the time the cakes were thought to have been contaminated, and in two bakeries this was the drily time that the suspected batch was used in that area. Though Salm. paratypki B was not found, the six samples of egg examined had high colony counts and contained E. coli type I and, in two samples, Salmonella. Fifty-seven tins packed in a different manner, probably in a different factory, but shipped at the same time, were also examined. They gave low colony counts, and yielded neither E. coli nor Salmonella. It is probable, therefore, that one batch of imported frozen egg was the vehicle by which these bakeries were contaminated.

Imported frozen egg will keep for only 3 or 4 days after it has been thawed, and as the smallest pack is 22 lb it cannot be used economically in the home or in small bakeries. This may be the main reason why these incidents were connected with larger firms which used machines.

Investigations at the bakeries concerned in these incidents showed that there was a considerable risk of contamination of uncooked products with Salmonella when any contaminated ingredient was used in a cake mix. In most small bakeries and in some larger ones the same machines are used for food which is to be sold cooked and uncooked. There are often inadequate facilities for washing utensils, and cake-mix and cake-filling bowls may be washed in the same water, sometimes without hot water, soap or detergent.

Savoy bags are often used to dispense many different products. They are difficult to wash and they are not washed frequently. All the bakeries visited on this investigation had Savoy bags in continuous use and no member of the staffs could remember their ever having been boiled. In some bakeries they were washed under a tap daily and only discarded when their nozzles began to wear.

The risk of contamination of an uncooked cake filling would appear to be high should any infected person or contaminated article gain entry to a bakery, and this risk may well increase with the size and complexity of bakery equipment.

Phage-typing has made it possible to connect a series of patients and outbreaks which otherwise would have to be considered as single sporadic illnesses. When this has been done attempts can be made to find a common food vehicle and the possible source of contamination. An early investigation into scattered outbreaks of this type is only possible when there is a central bureau where changes in incidence of different phage types can be observed.

8. ACKNOWLEDGEMENTS I wish to thank Dr. Betty C. Hobbs and the staff of the Food Hygiene Laboratory for the bacteriological examinations of food and egg, and Dr. E. S . Anderson and

470 K . W. Newell

the staff of the Central Enteric Reference Laboratory for the phage-typing. I should also like to thank the seven Public Health Laboratories, the five Hospital Laboratories, the Medical Officers of Health and Sanitary Inspectors of twenty administrative areas, the staffs of the bakeries and the egg wholesalers, for the information, help and co-operation which they so readily gave.

9. REFERENCE

MOOBE, B. (1948). The detection of typhoid carriers in towns by means of sewage ezeminotion. Mon. BuU. Minist. Huh Lab. Sew. 7, 341.

(Received 5 July, 1955)