T H E I R I S H J O U R N A L M E D I C A L S C I E N C E

TI-IE O F P I C I A L J O U R N A L OF T H E ROYAL A C A D E M Y OF M]~DICINE I N I R E L A N D

OF

SIXTH SEI~IES. NO. 405. NOVEMBER, 1959.

SALMONELLA FOOD POISONING TRACED TO DUCK EGGS.

RICHARD STOKES, M.B., D.P.H., Asst. C.M.O., Co. Wexford.

I NSTANC~ES of human Salmonella infection t ransmit ted by infected eggs have been repor ted in the l i terature on numerous occasions since Le Coq (1906) suggested the possibility of transmission of infection

through the medium of eggs. Scott (1930) described 3 personal cases and cited 7 other instances of

S. t yph imur ium infection in which the circumstant ia l evidence was sufficiently s t rong to incriminate duck eggs. Two years la ter (1932) he invest igated 3 cases of gastro-enteri t is which followed the consumption of duck eggs. He succeeded in isolating the same organism (S. typhi- murium) f rom the pat ients and f rom eggs f rom the corresponding flock of ducks. S. t yph imur ium was also isolated f rom post mor tem speci- mens of spleens, ovaries, and intestines of one flock of ducks.

Gordon and Buxton (1945 a) isolated S. t yph imur ium f rom the blood and faeces of a pa t ient who died of gastro-enteri t is following consump- tion of a f r ied duck egg. Agglut inins of S. t yph imur ium were found in the sera of 4 ducks f rom which the egg was obtained. The same vi phage type of S. t yph imur ium was cul tured f rom the yolk and shell of three of the eggs.laid by these ducks, and also f rom the ovary of two of the flock as well as f rom the intestine of a th i rd duck.

Eedy (1950) repor ted a case of food poisoning due to the consumption of a boiled duck egg ; S. t yph imur ium vi phage Type v was isolated f rom the urine and faeces of the pa t ien t and f rom 8 out of 47 eggs f rom the responsible flock of ducks. The drake was the only one f rom which a positive rectal swab was isolated.

Miller (1952) repor ted two cases of acute bacterial food poisoning following consumption of a raw duck egg. The same vi phage type of S. t yph imur ium was isolated f rom 2 out of 9 eggs laid by 6 ducks and f rom the intestinal t rac t of one duck, f rom the ovary of a second duck and f rom both the intestinal t rac t and ovary of a third. Miller has also recorded the case of a woman who suffered a severe a t tack of acute gastro-enteri t is a few hours a f t e r eating a f r ied duck egg. The same vi phage type of S. t yph imur ium was isolated f rom a cloacal swab of one of the suspected flock. A similar vi phage s t ra in was isolated f rom a f a r m e r who had eaten a home-made ice cream which included duck eggs f rom the same flock. All but one of the 50 ducks in the flock gave positive agglut inat ion tests.

482 I R I S H J O U R N A L OF M E D I C A L S C I E N C E

Garrod and McIlroy (1949) described a hospital outbreak of 60 cases amongst pat ients and nurses who cat a " Queen of pudding " sweet, which contained 300 duck eggs. The same vi phage type was isolated f rom the cases and f rom the ducks which laid the infected eggs.

In the above extracts f rom the literatulre there is ample evidence of the importance of duck eggs as a source of human Salmonella infection.

The following experience of the author is of some interest especially as it is the first bacteriologically proved case of human Salmonella infection t ransmit ted by infected duck eggs to have been reported in ]~ire.

I n A u g u s t , 1957 a case of h u m a n sa lmone l lo s i s was repor ted to t he W e x f o r d P u b l i c H e a l t h D e p a r t m e n t . T he p rev ious h i s t o r y of the p a t i e n t was i n v e s t i g a t e d in a n effort to d i scover t he l ike ly source. T he pa t i en t , a m a n aged 52 years , l ived a lone b u t worked on a n e i g h b o u r i n g f a rm, where he h a d all h i s mea l s , excep t occas iona l ly on a S u n d a y m o r n i n g w h e n he h a d b r eak fa s t a t home . On S u n d a y 18.8. '57 he h a d b r e a k f a s t a t home , cons i s t i ng o f sausages , bread, bu t t e r , t ea a n d two fr ied duck eggs, w h i c h he b r o u g h t h o m e f rom h i s e m p l o y e r ' s f a r m on S a t u r d a y n igh t . L u n c h was a t h i s e m p l o y e r ' s house . T h i s cons i s t ed o f beef, vege tab le a n d p o t a t o a n d was sha r ed by five o the r pe r sons who did n o t become ill. " T ea " cons i s t ed of tea , b read , b u t t e r a n d sweet cake, b u t no eggs.

Monday , 19 .8 . ' 58 - -He fel t well excep t t h a t he h a d occas iona l " g r i p y " a b d o m i n a l pa in . H e c a m e to work as usua l . Shor t ly before b r e a k f a s t (8.30 a .m.) he h a d one b o u t of d ia r rhoea . He a te b reakfas t , cons i s t i ng of tea , b read , b u t t e r a n d one boi led d u c k egg. He c o n t i n u e d to work d u r i n g t he d a y a n d d id n o t feel bad ly , excep t t h a t he h a d e r a m p y a b d o m i n a l p a i n a n d odd b o u t s of d ia r rhoea . He h a d l u n c h as usua l . T o w a r d s t e a (6 p .m.) he d id n o t feel so well (hot, swea t ing , nausea ) b u t d id n o t v o m i t ; g r i py a b d o m i n a l pa ins , t e n e s m u s a n d d i a r rhoea b e c a m e m o r e severe, t e m p e r a t u r e 102°F. H i s doc tor adv i sed i m m e d i a t e a d m i s s i o n to hosp i ta l , b u t he d id n o t go un t i l t h e fol lowing m o r n i n g .

On a d m i s s i o n (20.8.'58) he was feel ing ve ry ill, w i t h severe c r a m p y a b d o m i n a l p a i n a n d c o n s t a n t d i a r rhoea . T e m p e r a t u r e 103°F. A s p e c i m e n of faeces was sen t for e x a m i n a - t i on for en ter ic p a t h o g e n s , a n d t he p a t i e n t p u t on s u l p h a g u a n i d i n e a n d S te ra tha l . Af t e r a b o u t 48 h o u r s h i s t e m p e r a t u r e se t t l ed a n d t he a b d o m i n a l p a i n a n d d i a r rhoea ceased, b u t he s t i l l fe l t weak . F r o m t h e n on h i s recovery was u n e v e n t f u l .

Report on specimens of faeces: 21.8. '57. S. T y p h i m u r i u m iso la ted (Dubl in)

2.9. '57 . . . . {Cork) 20.9. '57 ,, ,, No' g r o w t h deve loped

Several fo l low.up s p e c i m e n s of faeces a n d u r i n e u p to Sept . '58 were n e g a t i v e for en te r i c pa thogens . T he p a t i e n t ' s s e r u m a n t i b o d y t i t r e h a d been e x a m i n e d in A u g u s t , 1957, b u t was n e g a t i v e on 8.1758, a n d aga in on 14.11.'58. The s e rum of five o t h e r pe r sons who h a d p a r t a k e n of t h e s ame food as t h e p a t i e n t showed no S. t y p h i m i r i u m a g g l u t i n i n s a n d s p e c i m e n s o f faeces were also n e g a t i v e for en ter ic p a t h o g e n s . Al l t hese i nd iv idua l s , however , c l a imed t h e y d id n o t ea t duck eggs.

The p a t i e n t ' s h i s t o r y sugges t ed t h e poss ib i l i ty t h a t t h e two fr ied d u c k eggs m i g h t be t he source of h i s infec t ion . T h e eggs were la id b y 2 of a flock of 13 ducks k e p t on t h e f a rm. T h e b i rds al l a p p e a r e d h e a l t h y , a n d the re was no h i s t o ry o f a n y u n d u e m o r t a l i t y or i l lness . S pec i mens o f b lood were t a k e n f rom all 13 ducks , a n d i n d i v i d u a l ducks were m a r k e d b y n u m b e r e d leg r ings . T h e r e s u l t a n t s e r u m a n t i b o d y levels a g a i n s t S. t y p h i m u r i u m ( H = i ) are s h o w n in Tab le 1. E i g h t gave t i t r e s o f d i agnos t i c s ignif icance, a n d 5 were nega t ive . Spec imens o f faeces f rom al l 13 were e x a m i n e d for en ter ic p a t h o g e n a n d al l were nega t ive . U n f o r t u n a t e l y , on ly one egg (2408} was ava i l ab le for e x a m i n a t i o n as t h e flock d i s con t i nued l ay i ng un t i l t h e fol lowing Apri l . Th i s s ingle spec imen was n e g a t i v e for Sa lmone l l a o rgan i sms . Two ducks (2413 a n d 2404) d ied d u r i n g Sept . 1 9 5 7 - - b o t h , it is c la imed , due to acc idents .

I n N o v e m b e r , 1957, I p u r c h a s e d t he flock o f l l , a n d kep t t h e m p r i v a t e l y for f u r t h e r i n v e s t i g a t i o n s (see Tab le 1). Spec imens of faeces were e x a m i n e d for en ter ic p a t h o g e n s , w i th n e g a t i v e r e su l t s f r om all ava i l ab le ducks on 23.1, '58 a n d 29.4. '58 a n d also as pa r t of pos t m o r t e m e x a m i n a t i o n on each duck .

Eggs: The first s p e c i m e n s ob t a i ned (except for one n e g a t i v e spec imen in Sept . 1957) was on 29.4. '58. F r o m t h e n un t i l 30.6. '58 a to t a l o f 62 eggs f rom t h e flock wore e x a m i n e d for ev idence of S; t y p h i m u r i u m , or o t he r en ter ic p a t h o g e n s , w i t h n e g a t i v e resu l t s . Al l eggs were i n c u b a t e d a t 37°C. for one week a n d t h e n cu l tu res were m a d e f rom the ou ts ide of shel l , t h e whi te , t he yolk , a n d po r t ions of t he shell i tself. On 30.6. '58 16 fu r t he r eggs were s u b m i t t e d for e x a m i n a t i o n ; 14 were nega t ive , b u t two yolks

S A L M O N E L L A FOOD P O I S O N I N G 483

yielded a good g rowth of a non-lactose fe rmente r on McConkey's solid medium. A suspension of bo th organisms gave posit ive agglut ina t ion wi th s tandard sera. They also gave the accepted carbohydra te fe rmenta t ion tes ts for the Salmonel la group. The cul tures were later confimned by Dr. J o a n Taylor as S. t y p h i m u r i u m O = 1, 4, 5, 12 : t t : i ; 1, 2 and phage type 1 (a) by Dr. E. S. Anderson. Three fur ther eggs submi t t ed for examina t ion in Ju ly , 1958 were negat ive for S. t yph imur ium.

Four of the flock died between J a n u a r y and April , 1958. On pos tmor t em examina t ion all in ternal organs were heavily infected wi th tuberculosis . Cultures were made f rom livers, spleens, gallbladders, ovaries and hear ts and were all negat ive for S. t yph imur ium. The remain ing 7 were killed off dur ing October, 1958. On post-mortem all showed evidence of tuberculosis. The usual rout ine culture of internal organs was negative, except for the spleen of duck 2414, which gave a pure g rowth of Salmonella on McConkey's medium; s ta ined smears showed Gram negative bacilli ; suspensions of the g rowths gave posit ive agglu t ina t ion wi th O and H anti-sera. They also gave the typical Salmonella sugar reaction. The organism was again confirmed as S. t y p h i m u r i u m 0 - - 4 , 5, 12 ; H = i ; 1, 2 and phage type 1 ( a ) - - the same type and s t ra in as t ha t isolated f rom the egg.

I n the above inves t iga t ion there is conclusive evidence t h a t one or more members of the flock of 13 ducks were chronic carriers of S. t y p h i m u r i u m infection and were p roduc ing eggs which contained the same organisms, and were in fact responsible for acute food poisoning in a m a n who ate two fried eggs which had been laid by the flock.

There arc other points of interest in connection with the investiga- tion :

1. W h a t was the source of the ducks ' infection? The ducks had been obtained f rom an approved poul t ry station and

as there was no history of any unusual mor ta l i ty in the flock as ducklings or later, it is most likely tha t the infection was contracted dur ing the adul t life of the birds. The general hygiene of the f a rm was none too good : it was heavily infested with rats, due, it was claimed, to a neigh- bouring dog kennel in which the dogs were fed with meat f rom emer- gency slaughtered and other animal earcases collected f rom the sur- rounding areas.

Numerous surveys have been made of Salmonella infection among rats and mice. Khali l (1938) found 7.3 per cent. of 750 rats t r apped in par t s of Liverpool to be infected. Ker r in (1928) found an incidence of 11 per cent. in rats in Aberdeen; Metcalfe, Brown and Pa rke r (1958) found an incidence of Salmonella infection in 4.4 per cent. of brown rats in the por t of Manchester, but failed to isolate any Salmonella organism f rom 279 black rats.

Ludtam (1954) reported an examinat ion of rats t rapped and poisoned in various types of premises in the Not t ingham area between 1949-1954. He found 4-4 per cent. of 518 rats positive for Salmonella. In September, 1953, Salmonellae were isolated f rom 4 pe r cent. of 94 rats f rom a butcher ' s by-product factory. I n the last months of 1953 the incidence rose to 40 per cent. of 60 rats examined; and in the first 4 months of 1954 the incidence was still 27-6 per cent. of 29 rats. At the t ime when the high incidence occurred, the fac tory was overloaded with mater ia l f rom slaughter-houses, large accumulations of bones and meat being piled in open sheds and often wai t ing for some weeks before disposal. I t is general ly found that the greatest incidence is in ra ts cap tured in the vicini ty of abbatoirs, knackeries and butchers ' by-product factories.

Welch et al. (1941) found that Salmonella may smwive in ra t faeces, at room tempera tu re for at least 148 days.

I t is suggested tha t the ducks in question were infected by eating rodent faeces a n d / o r urine with their feed. In an effort to substantiate

484 I R I S H JOURNAL OF MEDICAL S CIEN CE

the above, a very small number of rats f rom the fa rm were examined for evidence of Salmonella infection, with negative results.

2. Why, if the patient had been eating duck eggs (boiled and fried) from the flock for twelve months, was there no at tack of food-poisoning previously, or not even a mild gastro-intestinal upset ?

(a) I t may be postulated that the ducks had become infected only a short time previously so that he was the first and only victim, as they ceased to lay almost immediately.

(b) The element of chance. Not all eggs laid by a carr ier bird con- tain the infective organisms. I t has been estimated as between 1 per cent. and 4 per cent. (Wilson 1946). (In the present series only 2 eggs were positive out of 82 examined.)

(c) The number of organisms present in the egg : Large numbers of Salmonella organisms appear to be necessary to

cause an attack of food poisoning. McCullough and Eisele (1951) carried out a very large number of feeding tests on human volunteers. The number of bacteria required to produce symptoms varied between about 150,000 and 10 billion, depending on the serotype involved, e.g. Sal- monella Newpor t - -o f 16 people fed with doses of 152,000 to 385,000 bacteria, only two became ill; with 1,350,000 organisms three out of six were ill. Extensive experiments as to the effect of cooking on Salmonella- infected egg mixtures were carried out in connection with the M.R.C. investigation into the bacteriology of sprayed dried eggs (Special Report, Se~'.ies No. 260). In many cases it was not possible to isolate Salmonella organisms af ter using freshly rehydra ted egg to prepare scrambled eggs and omelettes. I t was possible in a proport ion of cases, especially if the organisms were present in large numbers before cooking.

Neely and Nelson (1951) found that an egg yolk and cornflour mixture contaminated with large numbers of Salmonella was not sterilised by heating to 100 ° C. for 10 minutes, followed by 60 ° C. for 20 minutes. Heat ing the same mixture at 100 ° C. for 30 minutes sterilised it. They emphasised that no method of cooking duck eggs can be recommended which does not result in coagulation of the yolk. Sterilisation of duck eggs is incomplete if they are fr ied on one side only for 4 or 5 minutes. F ry ing on both sides for a similar time usually renders them safe for human consumption. Boiling for 10 minutes has been claimed to be a safe method for cooking duck eggs, but Clareburg and Burger (1950) recommend that large duck eggs should be boiled for 14 minutes or boiled for 10 minutes and left for a fu r the r 5 minutes before eating.

There would seem to be two factors involved in the sterilisation of eggs and their products by cooking: (i) the adequacy of the cooking, and (ii) the extent of the bacterial infection in the food beforehand.

.One or more of the above factors may explain the absence of earlier infection in the patient.

3. Two fu r the r points of interest are the value of blood testing in ident i fying infected birds, and its possible relationship to ovarian activity. Is the level of serum antibody ar~ indication of the degree of infectivity ?

Warrack and Dalling (1933) showed the diagnostic significance of agglutination tests on ducks' blood in detecting infected ducks. They

SALMONELLA FOOD POISONING 485

also noted that the t i tre of agglutinin in a par t icular duck may vary considerably over a relatively short period (3 months). Repeated blood agglutination tests on 30 ducks showed that negative birds stay negative and positive reactors stay positive. They suggested this as a possible means of differentiating between infected and non-infected ducks.

Gordon and Garside (1944) showed that the organism may be demon strated post mortem in the tissues of ducks which had given a negative agglutination tests on ducks' blood in detecting infected ducks. They Gordon and Buxton (1945 b). They were able to associate the variation in t i tre with ovarian activity. Ducks reacting positively might later become negative when the ovaries become inactive, even though in the same case S. typhimurium had been isolated from tissues.

The t i tre of serum antibody level in 7 of the flock under review was estimated in all 4 ti tres between 2.9.'57 and 29.9.'58 (see Table 1, p. 486).

Since the birds ceased to lay in September, 1957 and ~Iuly, 1958, we may regard these dates as representing the end of ovarian activity for the respective seasons. As they were not laying on 10.2758 and were in full lay on 6.6.'58, these dates might be regarded as phases of ovarian inactivity and activity respectively.

I t may be seen from the Table that while the sera of ducks No. 8364, 2410, and 2414 showed a variation in ant ibody level corresponding with ovarian activity, none reverted to negative dur ing the inactive phase. Duck No. 2136 did not show a corresponding type of variation. Three of the birds (Nos. 2139, 2145, and 2415) which had negative tests on 15.9.'57 later gave titres of diagnostic significance. As all the flock were kept together, the possibility of cross infection could not be elimi- nated in this case. I t is also of interest that it was f rom the spleen of the duck with the highest agglutination level (2414) that the organism was isolated. I t is not known if the infected egg/eggs were laid by the samc duck or if the infected egg/eggs eaten by the patient were from this duck.

Originally an a t tempt was made to individualise the eggs by the use of a separate laying cage for each duck. This seemed to upset the birds and considerably reduced the output of eggs--a mat ter that was all- important to the completion of the investigation, so the cages were abandoned.

Discussion.

So far, we have been considering an isolated incident of Salmonella food poisoning. Let us now consider food poisoning in its broader implications. In this discussion it is intended to deal mainly with food poisoning due to Salmonella infection. However, in so doing wc are dealing with 90-95 per cent. of cases o f food poisoning due to known causes. Food-borne infection due to contamination with Salmonella organisms occurs in all parts of the world. The incidence varies in different countries, but in genera] dur ing the past 10-15 years there is a well-marked increase. In fact, in some countries, notably Great Britain, it has now become a major Public Heal th problem. Previous to 1942, in England, the number of incidents reported rarely reached 100 per annum. From then on, a sharp increase was noticed in the number of

TA

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1.

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k N

o.

8734

2139

2145

2410

2414

2415

2136

2406

..

2408

..

2412

..

2403

..

2404

..

2413

..

Dat

e

15.9

.'57

fH

1/25

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Neg

.

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oo

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5.9.

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1/4o

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1/

640

0 1/

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Neg

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H

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20

o 1/

8o

23.1

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: H

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100

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10.2

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Date

6.6.

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0

1/10

H

1/

640

O 1

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H

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320

O 1

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0 1/

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758

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10.4

758

:

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26.9

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.

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.

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.

Neg

.

Neg

.

Neg

.

Neg

.

Neg

.

FAECES

Dat

e

23.1

.'58

Neg

.

Neg

.

Neg

.

Neg

.

Neg

.

Neg

.

Neg

.

Neg

.

Neg

.

Dat

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18.4

.'58

Neg

.

Neg

.

Neg

.

Reg

.

Neg

.

Neg

.

Neg

.

EG

GS

Dat

e D

ate

Dat

e

29.4

.'58

13.5

.'58

5.6.

'58

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.

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. O

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. N

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fH

1/25

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. ]

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. (1

1)

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. (4

) 5~

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. (2

) N

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(4)

©

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. !

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. (3

) N

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(4)

! N

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(3)

Neg

. (3

)

Neg

. !

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. (2

) N

eg.

(4)

L-~

Neg

. [

Neg

. (3

) N

eg.

(4)

O

Neg

. }

Neg

. (2

) N

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(3)

As

wel

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abo

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5 ot

her

mis

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1958

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-Six

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pos.

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-

Die

d 13

.1.'5

8

Die

d 29

.1.'5

8

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d 25

.9,'5

7 D

ied

30.9

.'57

Neg

.

Neg

.

Neg

.

Neg

.

mur

ium

).

15.7

.'58-

-Thr

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ggs

exam

ined

--

Neg

. 20

.10.

'58-

-S.

Typ

him

uriu

m i

so.

late

d fr

om

sple

en

of

Duc

k 24

14.

Q

SALMONELLA FOOD POISONING 487

reported incidents. This coincided with the importation of sprayed dried eggs from the U.S.A., tbe Argentine and Australia. In 1943 there were 244 reported outbreaks; in 1945, 433; in 1947, 846; in 1949, 1,369, and by 1955 the extremely high figure of 5,269. The figures for 1956 and 1957 were 4,323 and 4,218 respectively; the latter were made up of 96 general outbreaks; 323 family outbreaks and 3,799 sporadic cases. Besides, there were 2,625 reported incidents in which no cause was discovered. About 90 per cent. of these were isolated sporadic eases. In a report Food Poisoning in England and Wales in 1954 pub- lished by the Public Health Laboratory Service, the authors comment that " most of the outbreaks for which no cause was found were small outbreaks reported so late to the M.O.H. that no investigation was worth carrying out "

In interpreting the above figures it must be remembered that food poisoning was made notifiable under the English Food Hygiene Regula- tions issued in 1938. In 1939 the Emergency Public Health Laboratory Service was set up. This expanded during the war years and became the Public Health Laboratory Service in 1946. The Ministry for Health published a memorandum in 1949, which was brought up to date in January, 1958, giving directions as to the investigations and notifications in case of food poisoning outbreaks. These factors have helped to make the Medical Officer of Health and medical practitioner more conscious of the problem of food poisoning, and may account for a proportion of the increased incidence. I t is most unlikely that they have been respon- sible for any large share of the increase between the figures in England today and those of 15-20 years ago.

While the morbidity rate is high, the disease is associated with a relatively low mortality, e.g., in England in 1939 when there were 83 outbreaks the total number of food poisoning deaths was 30. In 1947 there were 846 outbreaks and 61 deaths, and in 1956 with 4,323 incidents there were only 35 deaths. However, the Chief M.O. of the Ministry of Health in his 1956 annual report comments: " At a time when the deaths from infectious diseases are falling rapidly, the 30 to 40 deaths from Salmonella infection each year assume a significance they would not have had 20 years ago ".

Since Gaertner (1888) fil~t identified a specific bacillus as a cause of food poisoning, the bacteriology has become steadily more complicated. Almost 400 distinct serotypes have now been differentiated by the analysis of the somatic and flagellar antigens according to the Kauffman- White scheme.

One type, S. typhimurium, is more common than all the rest together. i t accounted for 83 per cent. of all isolations from human cases in England and Wales between 1949 and 1954. The next commonest are S. enteritidis ; S. thompson; S. newport; S. dublin, and numerous others whose prominence in any particular year depends on the particular strain being involved in a special outbreak. It is noteworthy that Salmonella heidelberg, which was first isolated in England in 1953 (11 times) had in 1954 risen to second place (269 cases) after Salmonella typhimurium, which is still responsible for 66 per cent. of all Salmonellae isolations (Report, 1958).

During the past 20 years or so, much patient bacteriological and

488 I R I S H J O U R N A L OF M E D I C A L S C I E N C E

epidemiological work has been done on the distr ibution of Salmonella in man and animal. I t is now well established that man can contract infection f rom animal sources, and a fa i r ly close paral lel ism has been demonstrated between sero-types isolated f rom human cases of Sal- monellosis and those predominat ing in local animals and poultry. There is also abundant laboratory evidence tha t near ly all members of the group are capable of establishing in some animal or bird a harmless carr ier state while retaining the capaci ty to produce disease in other animals of the same or different species. Numerous surveys have shown that Salmonella food poisoning would appea r in fact to be derived mainly from a widespread prevalence of chronic Salmonellosis in poul t ry, pigs, cattle, as well as rodents (rats and mice), domestic pets (cats and dogs) and even human beings. I t is impossible to review here the exten- sive l i terature repor t ing such surveys, but an a t tempt will be made to summarise the data in general terms.

Poultry seem to be the commonest reservoir of Sahnonellae. Ducks are especially significant, as Salmonella infection may be widespread on duck farms. The organism invades the genital t rac t (ovary and ovi- duct) with infection of the individual egg, while f rom a d i r ty infected shell contaminated by bacteria in the dejecta of an infected bird or dur ing passage through the cloaca, the organism may penet ra te to the interior of the egg or remain virulent on the surface for several months. The pa r t p layed by duck eggs as a source of human Salmonellosis is well established. Reference has a l ready been made earlier in this pape r to a few of the numerous outbreaks traced to duck eggs. Dur ing the years 1950-1952 inclusive, the Medical Research Council carried out a survey of the incidents of Salmonellae in nat ive English duck eggs (Anon. 1954). This revealed that 0.15 per cent. of 13,562 eggs were infected. These were derived f rom 10 out of 590 different farms. I t was esti- mated that this would amount to about 187,000 infected duck eggs on the marke t in any par t icu la r year. S. t yph imur ium was the commonest type isolated.

Salmonellae infection of fowl, a l though even more common, are much less f requent ly a source of human food poisoning, as two of the com- monest strains, S. pul lorum (the cause of white diarrhoea in chicks) and S. gal l inarum (cause of fowl typhoid) are pract ical ly non-pathogenic for man. I t appears f rom experiments that ovarian infection seldom occurs in the hen with s trains other than S. pul lorum. A few eases of human Salmonella infection in the l i tera ture suggest tha t occasionally the infection may be pr imar i ly in the yolk.

Wa t t (1945) described an outbreak of food poisoning due to S. monte- video aboard a merchant vessel in which 28 out of a crew of 70 were affected. The outbreak was due to the consumption of a mayonnaise p repared f rom raw hen eggs.

Crowe (1946) described an outbreak of 23 eases of S . typhimur ium infection following the consumption of an artificial bu t te r mixture in the manufac ture of which was included a hen egg. The circumstant ia l evidence was sufficiently strong to incriminate the egg as the source of the infection in 23 out of 27 persons at risk.

Blythe Brooke et al. (1950) repor ted typh imur ium infection in a 2-year old boy, probably due to a hen egg.

SALMONELLA FOOD POISONING 489

Bernstein (1952) examined 3,648 English home produced and imported hen eggs, but failed to isolate any Salmonellae.

Watts and Mander (1953) isolated only S. pullorum from 3,312 Australian hen eggs.

Numerous Salmonella types other than S. pullorum and gallinarum have been isolated from hens or their eggs in U.S.A. S. typhimurium, S. thompson, S. enteritidis are some of the strains isolated.

Carter et al. (1950) examined samples of pooled contents of 2,964 hen eggs and isolated 6 serotypes. One was S. para-typhoid B, and 5 others S. puIlorum.

Turkeys and geese also suffer from Salmonella infection and have been the cause of food poisoning. Percira and Blaxland (1955) recorded an extensive outbreak among the birds on a turkey farm in Wiltshire. The farmer and his wife were infected after examining some of the birds post mortem. Many other birds such as pigeons, pheasants, parrots, budgerigar, finches, etc. may also be infected.

The risk of human infection from bulk egg preparations (e.g. liquid egg, frozen egg, spray-dried egg) is considerably greater than from shell eggs. In this, one infected egg can infect a complete batch. The inci- dence of Salmonellae in spray-dried whole egg powder has been assayed by many workers in different countriees. An extensive survey of the incidence of spray-dried eggs imported into England from U.S., Canada and the Argentine between February, 1943, and August, 1945, was carried out by the Medical Research Council (Special Report Series 260). 7,584 samples were examined. I t revealed an incidence of 9.9 per cent. infected with 33 different serotypes.

The extensive use of these mixtures in Great Britain resulted in the introduction of 28 new types of Salmonellae. Eighteen of these had been reported as having been found in human cases and carriers in North and South America (Edwards and Brunner), and also to be common pathogens of fowl in the same areas.

Murdock (1954) examined liquid egg mixtures of Northern Ireland home-produced eggs. The samples were taken as the mixture passed from the homogenizer to the receptacle cans. Salmonellae were isolated 21 times from batches representing 1,010 hen's eggs (2.1 per cent.) and 12 times from 249 batches of duck eggs (48.2 per cent.) S. typhimurium was the serotype usually found.

A more comprehensive survey was undertaken by the Public Health Laboratory Services (1955). From a total of 1,649 samples of untreated or chilled liquid English hen eggs, 0-5 per cent. were infected with Salmonellae (5 with typhimurium; 3 with pullorum and one with me~e- gridis). Of 65 samples of duck eggs, two were infected with S.typhi- murium. Of 316 samples of mixed hen and duck eggs 4 were infected with S. typhimurium (Anon. 1955).

Bulk preparations of Chinese eggs are also commonly infected. Smith and Hobbs (1955) isolated Salmonellae from 27 per cent. of 128 cans. The strains isolated were S. pullorum; S. thompson; S. aberdeen and S. typhimurium only twice.

During 1955 and 1956 Public Health Laboratory Services examined almost 20,000 samples of home and imported eggs, and egg products (Report, 1958). Samples were examined from 11 different countries.

490 IRISH JOURNAL OF MEDICAL SCIENCE

The proportion of samples contaminated was often quite high, up to 50 per cent. in some batches. The only product free from contamina- tion was pasteurised dried egg from Poland.

The most highly contaminated were frozen whole egg, flaked, powdered and frozen albumen from China; and frozen whole egg frola Australia and from the United Kingdom. Excluding S. pullorum, the predominant Salmonellae in Chinese eggs and albumen were Salmonella thompson; S. potsdam; S. aberdeen and S. newport, and in the Australian and British eggs S. typhimirium. In addition, some samples of Chinese eggs and albumen were shown to contain para-typhoid B, probably from human contamination at source. Eight different phage types of the latter were found. Analysis of the phage types occurring in cases of S.para-typhoid B outbreaks during 1955-56 in England showed that the 8 phage types isolated from the Chinese eggs had been isolated from 80 per cent. of the incidents.

Pigs. I t was generally considered that S. cholcra-suis was the most important cause of pig Salmonellosis. In some countries surveys have supported this view, but in others a variety of sero-types have been isolated among which typhimurium is the commonest.

Scott (1940) in Great Britain examined batches of mesenteric glands and spleens from apparently healthy pigs. From a total of 1,000 pigs he isolated Salmonellae 41 times (3.8 per cent). The commonest were cholera-suis (10) ; typhimurium (9) ; Salmonella thompson (7) ; Salmonella newport (6) and Salmonella enteritidis (4).

A more extensive survey was carried out by the Medical Research Council in 1944-45 Report, 260). Pooled lymph nodes were obtained from several abattoirs in different parts of England. Each lot contained lymph nodes from 5 pigs: 133 different strains were isolated from a total of 5,285 pigs (2.5 per cent).

Since all but three of the sero-types had been isolated from dried eggs imported into England and since it was known that some dried egg was used for pig feeding, it was considered that fresh Salmonella infections were introduced into pigs through the medium of dried eggs. Surveys in other countries have shown an even higher incidence.

In an extensive sampling of food purchased on the open market in Illinois (Felsanfeld, 1950), Salmonellae were found in 17"6 per cent. of 102 specimens of hamburger hash. The incidence was considerably lower in federally inspected meat (14.3 per cent. of 573 samples of pork). The Salmonellae involved apparently originating in the animals them- selves were sero-types commonly involved in human infections.

Cattle. Although apparently less common as a reservoir of Sal- monella infection than poultry or pigs, cattle are nevertheless an impor- tant source. For many years Salmonellae have been known to cause disease in cattle. The earlier references mention S. enteritidis and S. typhimurium as the commonest causal organisms. More detailed ex- amination of the flagellar antigens of some strains of S. enteritidis from cattle showed that the organism was not S. enteritidis but S. dublin. This latter type is widely distributed throughout the world and is the com- monest type affecting cattle. Many surveys have shown a wide variation in the incidence, type and distribution in different countries.

Field (1948) reported extensive studies carried out in Wales. He

SALMONELLA FOOD POISONING

T A B L E 2

Faeces and bile from individual cattle yielding Salm. dublin

491

I r i s h N o n - I r i s h " "

F a e c e s ( s e p a r a t e b e a s t s )

T o t a l P o s i t i v e P e r c e n t a g e

1,254 / 126 - 10 .0 I 8 5 5 1 32 3"7

B i l e ( s e p a r a t e b e a s t s )

T o t a l P o s i t i v e P e r c e n t a g e

" 1 1 8 - - 4 3"4 2 1 8 1 0 . 5

T A B L E 3

Area incidence (Irish) of Salm. dublin in cattle faeces

C o r k

N - O i - O f - s p e c i m e n s . . 1 - - 2 2 0 - - P o s i t i v e 18

. . . . 8-2 P e r e e n t a g e . .

B a t c h e s * . . . . ~ - 2 3 - - - P o s i t i v e . . . . I I . 2 P e r c e n t a g e . .

D u b l i n

65 10.2

34 50-0

D r o g h e d a

107 4 3.7

6 4

66,7

, W a t c r f o r d

148 12

8.1

19 5

26-3

L i m e r i c k

55 10 18-2

6 4

66-7

B e l f a s t

85 17 20.7

10 7

79 .0

Incidence of Salm, in healthy cattle in Northern Ireland (C. R. 2$furdock, 1953)

T A B L E 4

County incidence of 595 samples

C o u n t y

A n t r i m . . . . D o w n . . . . A r m a g h . . . . T y r o n e . . . . D e r r y . . . . F e r m a n a g h . . . .

TOTAL

S a m p l e s of f aeces

. . 1 8 0 • . 117 . . 72 • . 114 . . 90 . . 22

. . 595

P o s i t i v e for S a l m . d u b l i n

16 20 19

8 6 5

74

P e r c e n t •

8•9 17-1 26 .4

7 .0 6-7

22.7

12-4

T A B L E 5

Incidence in Northern Ireland Cattle as compared with Eire

H o m e - b r e d

F a e c e s T o t a l P o s i t i v e fo r

S a l m . d u b l i n

382 4 0

P e r C e n t .

10.5

T o t a l

1 0 6

I m p o r t e d

F a e c e s P o s i t i v e for S a l m . d u b l i n

26

P e r cen t •

24 .5

* T h e t e r m " b a t c h " r e f e r s t o s a m p l e s o f f a e c e s c o l l e c t e d f r o m t h e s l a u g h t e r h o u s e a t o n e t i m e a n d e x a m i n e d i n d i v i d u a l l y .

492 IRISH JOURNAL OF MEDICAL SCIENCE

diagnosed Salmonella infection on 20 farms. S. dublin was the organism isolated except for S. typhimurium on one farm.

Ritchie and Clayton (1951) reported an investigation carried out during 1949-50 on presumed healthy cattle slaughtered at a Birkenhead abattoir. They isolated S. dublin from 10 per cent. of the faeces and 3-4 per cent. of bile samples of Irish cattle, and from 3"7 of faeces and 0"5 per cent of bile samples of non-Irish cattle (see Table 2). S. dublin was also isolated from 12.4 per cent. of liver swabs of Irish cattle, but was not isolated from 171 swabs of non-Irish cattle.

Murdock and Gordon (1953) confirmed the high incidence in Irish cattle in a survey carried out in 1950-52. They isolated S. dublin from faeces of 86 of 1,000 Irish cattle.

More recently (Report, 1955) a survey was carried out in England to ascertain the incidence of Salmonellae in carcasses of cattle and pigs, which had been passed for human consumption. From cattle 42 strains of S. dublin and three strains of S. typhimurium were isolated. S. dublin was obtained from bile, liver, spleen, mesenteric glands and faeces. From the peritoneal swabs of 1,518 carcasses no Salmonella organisms were isolated. Negative results were also obtained from the liver and spleen of 494 calves. From pigs S. dublin was isolated 9 times ; S. typhimurium 3 times and S. anatum once.

Bischoff (1953) recorded that in Hamburg during 1950-53 Salmonellae were isolated from 849 of 9,645 carcasses of different animal species slaughtered for food. S. dublin accounted for the majority of the strains.

Rodents (rats and mice). Salmonellosis is enzootic and occasionally reach epizootie proportions in rats and mice. As already mentioned the incidence of infection varies depending on the availability of in- fected material. The organism can survivc for long periods in faeces under normal conditions. The unwarranted use of S. enteritidis variety Danysz as a rodent poison may lead to human Salmonellosis through pollution of meat or other foods by rodent excreta.

Domestic Pets (eats and dogs). Wolff et al. (1948) drew attention to the high infection rate amongst dogs in the U.S.A. and the potential risk to humans. Many sero-types have been isolated from faeces of clinically normal dogs and not infrequently two or more types from thc same animal.

Cruickshank and Smith (1949) examined faeces from 500 healthy dogs and found 5 positive for Salmonellae. From a similar number of h(,althy cats hi, found 7 positive. The' organisms isolated included S. typhimurium ; S. anatum ; S. montevideoand S. para-typhoid B. They made the interesting calculation based on dog lieences issued in Great Britain that if the-,above was a fair sample, there would be from 20,000 to 30,000 dogs excreting Salmonellae at any one time. The number of eats would probably bc in excess of this figure. A similar position in /;;ire, where there were 258,750 licenced dogs at the end of 1957, wouht mean that there would be about 2,500 dogs excreting Salmon(;llac.

Another possible if rather unusual source is o~'gauic fertilisers. These are derived from human and animal sources, and widely advert isedand rce()mmcnded by experts. Those of human origin arc usually dried

SALMONELLA FOOD POISONING 493

sludge from sewage works. Those of animal origin are manufactured from an.imal remains, bone, hoof, and horn, meat and blood.

Walker (1957) examined 123 samples of organic fertilisers, purchased mainly in retail shops in the county of Kent: 50 (40 per cent.) were positive for Salmonellae. Bone meal was the most heavily contaminated (28 samples). Thirty-four different types of Salmonellae were isolated.

Since bone meal may also be used in animal feeding stuffs, its use may be responsible for some of the unexplained animal infections.

Certain ticks, fleas (Xenopsilla Cheopis) and flies may also be possible vectors in the spread of Salmonellosis.

The question of the human carrier requires special consideration, especially in view of the undue prominence sometimes given to it. The finding of a human Salmonella carrier amongst the food preparation staff is often accepted as the proved source of a particular outbreak. He may, in fact, be just another victim instead of the source. Salmonellae organisms are excreted under the following conditions: (i) during an acute attack; (ii) following an acute attack either for a short period (temporary carrier) or for a prolonged period (chronic carrier); (iii) by a symptomless chronic carrier. Numerous investigations following acute outbreaks have shown that Salmonellae organisms can be isolated readily after an acute attack, but their presence diminishes in a more or less orderly fashion during the following weeks, except for a very small number which might persist longer or even go on to be chronic carriers.

Kwantes (1952) followed up 112 cases following an acute outbreak of S. typhimurium food poisoning. The number of faeces positive at the end of each week were 112, 60, 34, 16, 9, 9, 3 (end of the 9th week).

Miller, Nicol and Ramsden (1955) investigated the clearance rate of 563 cases of S. bovis~morbificans. Only 14 were still excreting after 4-5 weeks and these were further reduced to four after 13-14 weeks.

Taylor (]950) has suggested that the percentage of carriers in a population is low and in an industrial area it has been estimated as 1 per cent. (Grant, 1951).

An investigation carried out by the Public Health Laboratory Services on 9,829 persons showed that 24 (0-24 per cent.) were positive for Salmonellae. (Savage, 1956.)

Although in general the incidence of chronic Salmonellae carriers is low, in a community where the incidence of acute food poisoning is high, the number of individuals excreting the organism at any one time may be considerable.

There is no doubt that some human food poisoning has arisen from food contaminated by infected food handlers, who in the main are unaware of their carrier state. In many other cases it is derived either from a food-producing animal or bird, or as a secondary infection from any of the other sources already mentioned. While we have little pre- cise information on the relative importance of these different modes of spread, undoubtedly infected food-producing animals and poultry con- stitute a serious hazard to human health.

Almost any food under suitable conditions of temperature and humidity can act as a vehicle of Salmonella infection. In England and Wales the vehicle of infection is recovered in only about 40 per cent. of outbreaks, so that no definite conclusion on the relative importance of

494 IRISH JOURNAL OF MEDICAL SCIENCE

the different foods can be drawn. However, food incorporating infected meat (especially beef and pork) are serious sources of human food poisoning. Processed and made-up meat such as meat pie, stew's, sausages, brawn, pressed beef, re-heated and cold meats are particularly common sources. Statistics published by the Public Health Laboratory Services show that from 1950-1955 there were 1,807 general outbreaks and family outbreaks of food poisoning in which the causal food was named. Meat and meat products were held to be responsible in 1,255 of these. It is therefore evident that the hygienic handling of meat is one of the main problems in the prevention of food poisoning. Meat is a food which must be viewed in its whole range from farm to consumer, and especially in its handling in t h e abattoir. We have already seen from various surveys that Salmonellae organisms may be isolated from a significant proportion of carcasses passed for human consumption. IIobbs (1953) demonstrated a high instance of C1. Welehii infection in raw meat in an abattoir. The organism was isolated from 20 per cent." of pork samples, from 24 per cent. of beef samples and from 14 per cent. of veal. In rccent years a considerable increase has been noted in the number of isolations of this organism from food poisoning episodes of the general outbreak variety. The risks of dissemination of infected meat from the abattoir cannot be wholly controlled by increased routine meat inspections because many of these infections can be detected only by laboratory examination. The general hygiene of the abattoir is of the utmost importance. Many very serious outbreaks of food poison- ing have been traced to unhygienic conditions in abattoirs during a time of over-taxation of accommodation, with relaxation ()t! normal con- ditions of disposal of animal carcasses and waste products.

Such circumstances, during a labour controversy, gave rise to a large typhimurium outbreak in Sweden in ]953. There were 7,717 notified cases and 90 deaths. (Lundbeck et al. (1955).)

Under somewhat similar conditions an outbreak occurred in Essex involving 3,000-4,000 customers of every retail butchec's shop in the affected area (Camp, 1947). The source was one or two infected pigs admitted to thc abattoir. Contamination of many other carcasses occurred because of the very unhygienic condition prevailing in the slaughter-house, including the use of wiping clothes dipped in a common bucket of water. Although the prime vehicle was raw meat, corned bee[ became secondarily infected, as a result of the two types of meat being handled together in butchers' shops.

Proper lairage facilities for animals awaiting slaughter is also of importance, if serious cross-infection is to be prevented. Mcl)onagh and Smith (1958) examined rectal swabs from 171 pigs in Iairag(;. Immediately after arrival, only 5 were excreting Salmonella (2-9 per cent.). Fur ther examination at the end of 7 days showed that the per- centage infected had risen to ]3"5. So the problem involves the contro] of lairage, the handling, transport and storage of carcasses. The subse- quent prevention of contamination of meat and meat products is closely related to the hygienic control of food premises and their personnel. The most important of these are the bulk food manufacturer and the communal eating establishment. In modern times more and more food preparation is escaping from the domestic kitchen into the hands of the

SALMONELLA FOOD POISONING 495

bulk commercial manufacturer. There is also a very marked increase in the number of people eating outside their homes in professional cater- ing establishments where defects in hygienic control may affect a large number of people. Prepared foods such as meat-pies are passing from production by a few to production on an extensive scale, thus creating new problems and the need for a much higher sanitary standard of safety. Methods comparatively harmless in the domestic kitchen are fraught with grave risk when practised in the communal kitchen. Meat and other food must of necessity be cooked beforehand and served cold or re=heated. There is also the difilculty of ensuring that the tempera- ture reached at the centre of a large mass of meat is sufficiently high to destroy infective organisms. A further difficulty is the storage of cooked meat at sufficiently low temperatures to prevent bacterial mul- tiplication. The butcher's shop is not to be forgotten, where sometimes there is ample opportunity for meat to become contaminated.

Eggs and their products are a highly potent source of Salmonella infection. Egg mixtures raise problems quite distinct from findings from flocks and from single eggs. These are widely distributed and used by the bakers and confectioners in the manufacture of products which subsequently may not receive effective heat treatment. Numerous outbreaks have been traced to these mixtures. They are also suspect sources in many outbreaks traced to sweetmeats; trifles, custards, etc. In recent times the association between Chinese egg mixtures and para- typhoid B. outbreaks has been noteworthy. These are mainly associated with the consumption of cream cakes, in the manufacture of which Chinese albumen has been used or very closely associated.

There are numerous reports in the literature of infection spread by milk and milk products. Infection may be primarily in the milk of those animals acutely infected with Salmonellae or may be infected by the faeces of a carrier animal, or human source. S. dublin is the usual sero-type involved. The outbreaks are usually of an explosive nature. In countries where pasteurisation of milk supplies is practised, milk and milk products do not usually constitute a serious source of human in- fection with Salmonellae.

While the foregoing are the main types of foods involved in food poisoning episodes, there are numerous others which may well be of equal importance under adverse conditions of preparation and storage.

Of interest in this respect is an account by Scott Thompson (1955) of a number of outbreaks of para-typhoid B. infection in South Wales. At first special attention was directed to synthetic cream in a number of bakeries, but the epidemiological evidence exonerated this source. Flour was the only substance which was common to all bake-houses in- volved. Although it seemed to be a very unlikely substance to harbour paratyphoid bacilli, i t was shown that these organisms could remain viable for nearly a year in flour and multiply freely in slightly damp sacks.

Before concluding, I would like to review briefly the position regard- ing food poisoning in ]~ire.

The incidence would seem to be in sharp contrast to the experience in many other countries, especially our near neighbours, England. Food poisoning as such is not notifiable under our Food Hygiene Regula-

496 I R I S H JOURNAL OF MEDICAL S CIEN CE

tions. Salmone]losis is, however, a notifiable infectious disease under the Infectious Disease Regulations, 1948. During the years 1948-1957, inclusive, a total of 117 cases was notified to Local Authorities. Seventy- seven of these occurred in County Boroughs : all in Dublin, except for two in Limerick and one in Cork. Seven notifications were from urban areas and thir ty-three from rura l areas. The distribution in both urban and rural areas was fair ly uniform, practically all isolated cases with two notable exceptions. Eight cases were notified from one dispensary district in Co. Roscommon (1953) and 14 cases f rom Co. Wate r fo rd (1955). One was a family outbreak which was not traced to any par- t icular source. The other is interesting in tha t it occurred following a threshing in a rural farm. Meat f rom a beef joint which had been cooked one or possibly two days previously was served cold for dinner and tea. Four teen employees all became ill. S. enteritidis was isolated from their stools and also from some of the " left over " meat. The source of the meat infection was not discovered, but rodent contamina- tion was suggested. The major i ty of the isolated cases were diagnosed following routine examination of faeces in hospitals and were traced to no par t icular source. Li t t le reference is made to food poisoning in the Annual Reports of C.M.O.s. The 1955 Report for Dublin City refers to three large outbreaks which occurred in canteens attached to three large business firms. Ful l investigation did not pin down any par t icular food. We may be fair ly certain that the number of repor ted cases does not represent the total incidence of food poisoning in ]~ire. First ly, cases are only notifiable af ter the isolation of a Salmonella organism. Secondly, only a small number of persons suffering from " diarrhoea and enteritis " seek medical advice, and of those who do, scant if any, bacteriological investigation is carried out in many cases. The large explosive outbreak in a canteen or other communal eating establish- ment is often times due to contamination by a toxin-producing staphy- lococcus or C1. Welchii infection. The Salmonella organism has a much higher incidence in the family outbreak and sporadic case. In England Salmonellae organisms are isolated from 95 to 99 per cent. of family outbreaks and sporadic cases, but only from about 50 per cent. of the larger general outbreaks. The increasing incidence of the C1. Welchii isolations in the la t ter has already been mentioned.

In the course of preparat ion of this paper I have had numerous per- sonal communications from C.M.O.s and other associated personnel. All seem to agree that there is a much higher incidence of food poison- ing than is generally realised. Many have related experiences of quite substantial outbreaks in which af ter full investigation no apparen t cause could be found. Others admit that although no source was dis- covered their investigation was not sufficiently searching or there was no investigation at all.

The Incidences of reported outbreaks are also relatively few.McWeeney (1909) investigated an outbreak which occurred amongst the inmates of an insti tution in the South of Ireland. Of 197 pupils at risk, 73 were infected with S. enteritidis with 9 deaths. He succeeded in isolating from the meat supply to the insti tution the same organism. The animal responsible, a K e r r y heifer, was slaughtered in a private establishment and was killed because of its fai lure to thrive. O'Kel ly (1922) investi-

SALMONELLA FOOl) POISONING 497

gated an outbreak of S. enteritidis in an institution nearDubl in; 148 boys out of a total of 170 in one block of the institution were affected. The cause of the outbreak was infected milk which was contaminated ei ther direct ly f rom an employee who suffered from an attack of gastro- enterit is five days previously or from contamination by flies f rom the servants ' lavatory. O'Kelly and IIayes (1946) investigated an outbreak in three institutions in a Midland town which was traced to a cow in- fected with S. enteritidis. The same organism was grown from samples of milk from the cow, which died shortly afterwards. The next repoz'ted outbreak has already being mentioned that reported by Crowe (1946) due to an infected egg. Moore and Mullancy (1949) reported that an outbreak of food poisoning in which 50 people were involved was due to milk from an infected sick cow which later died. S. dublin was the organism involved. A second cow apparent ly " h e a l t h y " in the herd was also found to be excreting S. dublin in her milk and faeces. The same organism was la ter isolated from the water supply on this farm.

Mullaney (1955) describes numerous outbreaks of Salmonella infec- tion in cattle, pigs, horses and dogs. In one dairy herd of 35 cows 4 died, 2 ra ther suddenly. Several others were affected but recovered. The outbreak was due to S. dublin.

The same organism was also responsible for an outbreak amongst pigs. Out of a batch of 20 store pigs 12 died. Fu r th e r reference is made to a valuable colt which died ra ther suddenly of Salmonellosis. S. typhi- murium was isolated on p.m. from heart, blood, l iver and spleen. A second incident occurred amongst 20 weened foals : 12 were affected and 5 died, again from S. dublin infection. He also mentions an outbreak in two kennels in one of which 22 dachshunds (all the dogs in the kennel) died, f rom S. dublin infection.

The investigations of Ritchie and Clayton (1951) on Irish and non- Ir ish cattle slaughtered in a Birkenhead abat toir has already been mentioned. A more detailed analysis is shown on Table 2. From this we see the incidence of Salminella-positive cattle expoI~ted through different Ir ish ports. I t may be presumed that in the main the cattle in each case were from the surrounding countryside. The generally high incidence of S. dublin in Ir ish as against non-Irish cattle is note- worthy. Murdoch (1954) did a somewhat similar type of survey on Nor thern I re land cattle and a number of cattle f rom ]%ire which were legally imported and retained for at least two months before being sold as fa t cattle (Table 5). Of 382 N.I. cattle 40 were positive for S. dublin. Of imported cattle (t~ire) 26 (24.5 per cent.) were postive for S. dublin: The area incidence in N.I. cattle is shown in Table 4.

In the Annual Reports of the Minister of Agricul ture the post mortem findings of dead animals and poul t ry refer red for examination are re- corded. In 1953-54 Report out of 87 duck carcasses there were 4 Sal- monella isolations. In 1955-56 Report out of about 8,000 fowl examined 82 were due to Salmonellae other than pullorum. Out of 116 swine 2 were due to Salmonella. In 1956-57 Report out of 197 pig carcasses examined 11 were diagnosed as Salmonella scpticacmia.

Other than the above we have little definite information as to the amount of Salmonella infection amongst the well-known common reset-

498 IRISH JOURNAL OF MEDICAL SCIENCE

voirs discussed earlier in this paper. Experience in other countries shows that the main source of human food poisoning is of animal origin. As far as I am aware, other than the routine blood testing in connection with B.W.D. and fowl typhoid eradication schemes, there has been no worth-while investigation as to the incidence of Salmonellae sero-types commonly involved in human infection amongst poultry and their pro- duets. The high incidence of S. typhimurium infection amongst samples of Northern Ireland liquid egg mixtures is of interest. A similar survey in ]~ire would seem to be worth while.

Tile findings of Ritchie, Clayton and Murdoch would suggest that there is much latent Salmonella infection in Irish cattle. Mullaney's survey of his experiences would also seem to suggest that at least Sal- monella infection can be responsible for serious outbreaks of disease in animals. We have no information on the possible incidence in pigs, rodents, domestic pets (eats and dogs), organic fertilisers, or animal feeding stuffs (bone and meat meal). According to 1956-57 Annual Report of the Minister for Agriculture there were 1,288 tons of meat and bone meal and 2,062 tons of fish meal imported into Nire under lieenee during the year covered by the Report.

While the recorded incidence of Salmonella infection in l~ire is low, I think there is evidence to suggest that much more is occurring than is apparent at first sight. Many of the smaller type of outbreak in which Salmonellae are usually involved are not being notified or fully investi- gated, so that the souree remains obscure. It is suggested that more thorough investigation of isolated sporadic eases is necessary. Wider exploration is indicated, not only amongst the family contacts, but also amongst associated domestic animals and poultry. In this type of in- fection direct medical supervision is necessary. Routine enquiries by a Health Inspector alone are scarcely adequate. In many cases of Salmonella infection in humans, investigation of this type would un- doubtedly reveal many reservoirs of infection amongst poultry and animals.

Salmonellosis is a disease of both man and animals. Methods for prevention and control form a common ground for investigation and co-operation between the veterinary and medical professions and others concerned with public health. As Sehofield (1945) has said: " Today we recognise no boundary line separating animal from human Sal- monellae, but rather is there an ever-growing recognition of the great importance of the so-called animal strain in human infection."

As long ago as 1295 Sir William Savage postulated that if Salmonella infection could be controlled, food poisoning would cease to be a Public Health problem. He thought that the key to the control of Salmonella infection lay in the discovery and eradication of animal reservoirs from which these organisms were probably spread, and reached human food. While this hypothesis still holds good, our knowledge of the widespread distribution of these organisms in the animal world makes the prospects envisaged by Savage of preventing Salmonella food poisoning by eradi- cating them very remote. The best and only course seems to be to inter- pose between the animal reservoir of infection and human food any- thing that will destroy the Salmonella organism or at least inhibit their multiplication. As has been seen, the important matters in this con-

S A L M O N E L L A F O O D P O I S O N I N G 499

nec t ion are carefu l and hygien ic control of aba t to i r practices, sc rupulous c leanl iness in food p r e p a r a t i o n and d i s t r ibu t ion , especial ly when food is to be ea ten cold or uncooked. Cooking at adequate t e m p e r a t u r e s a nd for a sufficient per iod of t ime to des t roy bac te r i a ; a n d s torage a t tem- pe ra tu res sufficiently low to p r e v e n t the i r mul t ip l ica t ion .

The greates t s ingle fac tor in the se rv ing of clean food in a c a t e r i ng es tab l i shment is the m e n t a l a t t i t ude of the people working there. Unless there is a genera l awareness of the impor t ance of personal a n d g e n e r a l hyg iene serious accidents wil l occur. H i g h e r s t andards should be en- couraged by educa t ion r a t h e r t h a n the law. I t is essential t h a t both m a n a g e m e n t and staff should apprec ia te the impor tance of the i r f u n c t i o n in the c o m m u n i t y and should be tho rough ly imbued with the p r inc ip l e s of food hygiene.

References.

Anon {1954}. Man. Bull. Minst. Hlth. Lab. Serv., 13, 38. Anon. (155). Ibid., 14, 65. Berdstein, A. (1952). Ibid., 14, 64. Bischoff, H. 195). Berl. Munch. Tierarstl. Wschr., 66, 406. Blyth Brooke C.OS. et al. {1950). Man. Bull. Minst. Hlth. 9, 128. Camp, F. E. (1947). 1bid., 6, 89. Carter, M. J. et al. (1950). Pub. Hlth. Rep. Wash. 65, 778. Clareburg and Burger, H. C. {1950). Food Res., 15, 340. Crowe, M. {1946). J. Hyg. (Land.), 44, 342. Cruickshank, J. C. and Smith, H. W. {1949). Brit. Med. J., ii, 1254. Edwards, J. R. and Brunner, D. W. (1943}. J. infect. Dis., 72, 58. Eedy, B. N. (1950). Mo~. Bull. Minst. Hlth. Lab. Serv. 9, 213. Felsenfeld, O. et al. {1950). J. Amer. Vet. Med. Assn., 116, 17. Field, H. I. {1948). B. Vet. J. 104, 251,294, 323. Gaertner, A. H. (1888}. K.-BI. arztl. Vet., Thuringen 17, 573. Garrod, L. P. and McIlroy, M. B. (1949). Brit. Med. J., ii, 1259. Gibbons, N. E. and Moore, R. L. (1944). Canad. J. Res. Sect. F. 22, 48. Gordon, R. F. and Buxton A. {1945a}. Man. B. Minst. Hlth. Lab.Serv., 4, 46. Gordon, R. F. and Buxton, A. (1945b). J. Hyg. (Land.), 44, 179. Gordon, R. F. and Garside {1944). J. Camp. Path., 54, 61. Grant, J. (1951). Med. O~cer, 85, 117. Hobbs et al. (1953). J. Hyg. (Land.), 51, 75. Kwantes, W. (1952). Man. Bull. M. Hlth. Lab. Serv., 11,239. Khalil, A. M. {1938). J. Hyg. (Land.}, 38, 75. Kerrin, J. C. {1928}. J. Path. Bact., 31, 588. Lundbeck, H. et al. {1955). J. appl. Bact., 18, 535. Le Coq. A. {1906). Cit. Lancet (1946), 1, 887. Ludlam, G. B. {1954). M. B. Health Lab. Serv., 13, 196. McDonagh, V. P. and Smyth, M. G. (1955). J. Hyg. {Land.), 56, 271. McCullough, N. B. and Eisele, C. W. (1951). J. Infect. Dis., 88, 278. McWeeney, E. J. {1909}. Brit. Med. J., i, 1171. Metcalfe Brown and Parker {1957}. Lancet, ii, 1277. Miller, A. A. (1952). Brit. Med. J. , ii, 125. Miller, Nicol and Ramsden (1955). Rep. Publ. Hlth. Med. Subj. Land., No. 96. Moore, 1~. and Mullaney, P. E. 0949}. Irish Vet. J., 3, 384. Mullaney, P. E. (1955). Ibid., 9, 202. Murdock, C. R. and Gordon, W. A. M. (1953). M. Bull. Min. Hlth. Lab. Serv., 12, 72. Murdock, C. It. 0954}. Ibid., 13, 43. Neely, R. A. and Nelson, M. G. (1951). Ibid., 10, 96. O'Kelly, W. D. (1922). J. Hyg. (Land.), 21, 114. O'Kelly, W. D. and Hayes, R. (1946}. Irish J. Med. Sci., 6th Series, 249. Pereira, M. S. and Blaxland, J. D. (1955). Man. Bull. M. Hlth. lab. Serv., 14, 52. Report 260 (1947). B . M . R . C . Spec. Report Series No. 260. Report (1955). Man. B. Minst. Hlth. Lab. Serv., 14, 132. Report (1958}. Man. B. Minst. Hlth. Lab. Serv., 17, 50. Ritchie and Clayton (1951). Ibid., 10, 272. Scott, W. M. (1930}. Brit. Med. J., ii, 56. Scott, W. M. (1932). J. Path. Bact., 35, 655. Scott, W. M. {1940). J. Hyg. {Land.), 21, 25S.

500 I R I S H J O U R N A L O F M E D I C A L S C I E N C E

Savage and Prince Whi te (1925). Med. Res. C. Sp. Rap. Ser., 92, 48. Schofield, F. W. (1945). Canad. J . Comp. Med., 9, 62. Smith, M. E. and Hobbs , B. C. (1955). Men. B. M. Health Lab. Se~v., 14, I54. Savage (1956). Cir. Brit. Meal. J . , ii, 321. Taylor, J. (1950). Publ. Hlth. Lend., 63, 168. Thompson Scott (1953). Men. Bull. M. Hlth. Lab. Serv., 12, 187. Walker, J. H. C. (1957). Lancet, ii, 283. Warrack, G. H. and Dal l ing T. (1933). Brit. Vet. J . , 89, 483. Watt , J . (1945). Publ. Hlth. Rap. Wash., 60, 835. Watts , P. S. and Mander, S. (1953). Men. B. Minst . Hlth. Lab. Serv., 12, 127. Welch, H. etal. (1941). Amer. J . Pub. Hlth., 31,332. Wilson, J . E. (1946). Vet. Rec., 58, 269. Wolff, A. H. , etal. (1948). Amer. J . Publ. Hlth., 38, 403. Statist ics relat ing to food poisoning in Eng land and Wales taken f rom var ious Men.

B. Minst . Health Lab. Serv.

Acknowledgments. I wish to grateful ly acknowledge and place on record m y indebtedness to the following

in connect ion wi th th i s pape r : - Mr. Brendan Whi t ty , M.Sc., M.R.C.V.S., The Veter inary College, Ballsbridge, Dublin,

who is responsible for all the bacteriological and serological work in connect ion wi th the inves t iga t ion and also the post m o r t e m examina t ion of the ducks.

Wi thou t his encouragement and assistance th is inves t iga t ion could no t have been carried out or b roug h t to a successful conclusion.

Dr. J o a n Taylor, Director, Sahnonel la ge f . Lab., Colindale, to w h o m I am great ly indebted for her mos t helpful personal communica t ions wi th commen t s and advice.

Dr. E. S. Anderson of the Salmonella Lab., Colindale for his personal in teres t and communica t ions and for carrying out the t yp i ng of all organisms isolated.

Dr. H. Aughney, C.M.O., Wexford for her interest , encouragement and advice a t all t imes.

Prof. T. Murphy, U.C.D., for his cri t icism of the paper and his valuable help in locat ing numerous references.

The m a n y C.M.O.'s f rom w h o m I have had personal communica t ions , especially Dr. M. O'Farrel l , Co. Water ford and Dr. M. F lynn , Co. Wes tmea th .

Discassion. Professor MURPHY. I t h ink you will agree t ha t the a moun t of work which Dr. Stokes

has pu t in to th is paper is incredible. I would like to welcome Mr. W h i t t y and I a m delighted t ha t he has been able to come here. I t is a very good th ing to see some people in the I r i sh Public Heal th Service coming forward wi th mater ia l of th is type and indeed, Wexford have done more t han their share in pu t t i ng forward mater ia l for this Section. I hope tha t Dr. Stokes will publ i sh th i s in the Journa l of the Academy in due course. His invest igat ion of the outbreak was very thorough. Dr. Corboy recently gave a ta lk to the D.P .H. class on th is and I have taken these figures f rom her. I n 1957 there were 103 million subs tan t ia l meals and 171 mill ion snacks supplied each week th rough canteens, etc., in Eng land and Wales. Here the same increase in canteens is t ak ing place. The increased use of made-up dishes is undoub ted ly ano ther factor in the increased incidence and the very active Publ ic Heal th Labora to ry Service in Bri ta in is another factor which is picking up more cases of food poisoning. He ment ioned the rout ine medical examina t ion of food handlers but , generally speaking, they are get t ing away f rom this. Unless it is a thorough bacterial examina t ion it is no use at all. Even rout ine bacterial examina t ion will not pick up all of t h e m and it is very expensive for the results obtained. The approach should be th rough the food handlers themselves. We should educate t hem and make them aware of the seriousness of the mat te r .

Mr. WHITTY. I wish to t h a n k you for the inv i ta t ion to a t t end your meet ing to-n ight and it has been a very pleasant experience for me. I am glad to have been associated wi th Dr. Stokes in th is invest igat ion. There is a lot of the detective in h is buy ing these ducks and following them up to the conclusion. I a m very glad t ha t there is a cer ta in amoun t of associat ion between the s is ter professions, the medical and the veter inary. We have a lot in common and I hope th i s col laborat ion will extend f rom now on.

Professor O'KELLY. YOU would really w a n t to read th i s paper before you could speak about it. I t is in teres t ing t ha t the s t imulus for it was one case. Isola ted cases are occurring regular ly bu t they are no t notified and in m a n y cases a doctor is no t called. When the Ministry of Hea l th in Eng land decided no t to publ i sh the n u m b e r of cases f rom food poisoning bu t only the n u m b e r of incidents they pointed out t ha t one

SALMONELLA F001) POIS()NING 501

outbreak which was runn ing th rough the count ry was from a central place t ha t was sending out pork pies all a round the country . The outbreak t h a t occurred in Sweden was peculiar. I was in Got tenberg at the t ime and the inspectors said t ha t the condi t ions in the aba t to i r were very unhygienic. They said tha t rats were responsible for it. I t was a paratyi)hoid B infection. Wi th regard to eggs a tlhing which migh t be considered is the quest ion of fertile eggs as against infertile ones.

Dr. AUGHNEY. We have really had great fun out of all this but it has definitely been home-work for Dr. Stokes. Iit was all done after hours. The co-operation which we received f rom the poul t ry in t ruc t ress was mos t helpful and [ feel t ha t we should have ~tssociated wi th these people long ago. I would also like to acknowledge Mr. W h i t t y ' s work on our behalf. I t is not by any means the first t ime tha t he has helped us.

Dr. ()'FLA:NA(,~AN. I weuld like to t h a n k Mr. Stokes very much for coming along and reading th i s paper. One th ing tha t I t h ink is impor t an t in these food processing p lan ts which is often overlookcd is the wate r supply. Where canning is concerned and wate r is required for cooling they often just shove the i r tubes into any old s tream and use it for co(fling fluid and tha t has been the cruise of con tamina t ion in many cases, Was the type found in the pa t ien t and the duck the same?

Dr. ()'~E(]AN. I would like to add m y t r ibu te to Dr. Stokes and Mr. Whi t ty for a very exhaus t ive paper . I a m sure Dr. Stokes got a lot of sat isfact ion out of br inging th is to such a sa t isfactory conclusion. H o w did he persuade the farmer to allow h im to get blood f rom the ducks before he bought them. The notif ication of infectious diseases fs the only th ing we ask our colleagues in General Medicine to do and they do not do it ior us. W h y arc we not told of these outbreaks of food poisoning? Eggs are not allowed into th i s count ry and it is one of the th ings we have got to be thankfu l for. I t has prevented Salmonella from being introduced into the country. W h y if S. dublin is so common amongs t cat t le do we no t get more of it amongs t the humans? One thing tha t m a y help us is the artificial manures . Most of ours is well sterilised before it leaves the factory. I n Eng land it m a y jus t be crushed bu t no t s~r i l i sed . The food hygiene regula, t ions do no t app ly to canteens in th i s country .

Dr. C~ow~:. I would like to congratulate Dr. Stokes on his presentat ion. The only th ing he did not lind was hew the ducks came to be involved, l i e raised the point as to why the m a n did not get infected sooner. I t seems tha t only one duck was involved at a t ime and it is possible tha t he had eggs f rom the other ducks. A number of these ducks had tuberculosis . He ment ioned tha t some s laughter house products were near the farm. Could the ducks have eaten th i s and got Salmonella f rom this or else the tuberculosis? I n 1937 vhe law was passed in Germany tha t duck eggs could only be sold wi th a label t ha t they m u s t he boiled for eight minutes . In the Netherlands they went even fur ther and tr ied to get Salmenella-free flocks of ducks. Mr. F lynn has taken samples of ducks eggs here for the last few years. We have done about 50 bu t so far have not yet get any positives, The last outbreak of Salmonella here tha t we knew of was in 1947. In 1909 Pro fe~or McWeency a t t r ibu ted the ou tbreak to the fact tha t the calf was sick before it was s]aughtered and he made the suggestion tha t they should do away wi th pr iva te s laughter houses.

Dr. COWELr,. I t appears to me tha t Dr. Stokes allowed the rats t(~ get away too easily. F r o m m y knowledge of the coun t ry ra t s and ducks are very tolerant to one another . I was wonder ing whether th i s farm could no t be fur ther invest igated for rats. A great deal of work seems to have been done in t rac ing the Salmonella in other animals and poul t ry bu t ra ts seem to have taken very li t t le pa r t in it and I was wondering if he could do more work on rodents. F r equen t ly one hears people saying tha t they do no t like duck eggs as they disagree wi th them. This usual ly means they give them a t u m m y upset and diarrhoea. Could these be mi ld ly infected people?

Dr. STO~ES (replying). They gave up the examina t ion of food handlers because they usual ly move a round so much. [ do no t t h i n k the ducks got over to the ra ts very of ten as the neighbours were not friendly. Some day we migh t be able to do more work on ra ts bu t I t h ink Mr. W h i t t y did enough for us on th i s occasion. The quest ion of fertile and non-fert i le eggs has been invest igated bu t not nmch help was found.