FRANK L. BRYAN Center f o r Disease Control U.S. Public Health Service Atlanta, Georgia

Transcription

1 CUISTRIDXIM PERFRINGENS IN RELATION TO mxr PRODUCTS+ FRANK L BRYAN Center f o r Disease Control US Public Health Service Atlanta, Georgia Neat and p o u l t r y products, p a r t i c u l a r l y r o a s t beef and turkey, a r e f r e q u e n t l y incriminated as v e h i c l e s of Clostridium perfringens foodborne outbreaks ( t a b l e ) Such outbreaks are u s u a l l y a s s o c i a t e d w i t h foods prepared in food s e r v i c e establishments where l a r g e volumes of food a r e prepered s e v e r a l hours o r a day o r more i n advance of serving and h e l d during t h e intervening period a t temperatures t h a t are conducive t germination of spores and m u l t i p l i c a t i o n of vegetative c e l l s Typical outbreaks that have occurred i n t h e United S t a t e s a r e i l l u s t r a t e d i n t a b l e Factors, uncovered during epidemic i n v e s t i g a t i o n s (and indicated i n t a b l e ), t h a t c o n t r i b u t e t o outbreaks of C perfringens foodborne i l l n e s s include f a i l u r e t o cogked foods, holding foods a t warm ( b a c t e r i a l incubating) temperatures, preparing foods a day o r more i n advance of serving, and inadequate reheating (Bryan, 9) A summary of contributory f a c t o r s involved i n 59 outbreaks is i l l u s t r a t e d i n t a b l e Before these f a c t o r s can influence growth o r s u r v i v a l of C perfringens Clostridium perfringens i n meat, however, t h e meat must become contamlnated i s a normal i n h a b i t a n t of the intestinal t r a c t of man and o t h e r animals When enrichment procedures are used, it i s n o t unusual t o f i n d a l l f e c a l specimens from people and most from animals p o s i t i v e f o r C perfringens It i s a l s o found i n high numbers i n s o i l and d u s t Data on t h i s s u b j e c t has been reviewed by Smith and Holdeman (968) and by Bryan (969) Animal carcasses become contaminated from Fntestinal contents o r from soil o r dust; i n addition, meat can become contaminated when handled by workers Cross contamination, which is enhanced when both contaminated and uncontaminated meat i s processed on the same equipment by t h e same people, a l s o occurs As a r e s u l t of such contemlnation, meat f r e q u e n t l y harbors perfringens Several i n v e s t i g a t o r s have reported on t h e i s o l a t i o n of E perfringens i n various r a w meat and p o u l t r y products ( t a b l e 4 ) These data i n d i c a t e t h a t C perfringens can be expected t o be present on raw meat f r o m t i m e t o time * Presented a t t h e 5th Annual R e c i p r o c a l k a t Conference of t h e American Meat Science Association, 9

2 TABU MEAT AND RELATED PRODUCTS WHICH WERF: ATTRIBUTED AS BEING VEHICLES OF OUTBREAKS OF REPOEiTED (CONFIF~IVEDAND UNCONFIRMED) CLOSTRIDIUM PERFmGENS FOODBORNE ILWESS, Beef 9 Veal Year Pork Chicken Turkey 6 4 Other meat 5 She llfi sh Fish Other foods 5 8 unknown Food Total Total

3 TABLE Number ill REPORTS OF OUTBEiEAKS OF CIOSTRIDIUM PERFRINGENS FOODBORNE ILLNESS THAT HAVE APPEARED IN US LITERATUREL Vehicle Contributory factors Place References > Creamed chicken, chicken croquettes serving, f a i l u r e t o cooked foods, inadequate reheating Restaurants 8 Turkey serving, f a i l u r e t o cooked foods, inadequate reheating Train meal H a r t e t a l (96) 4 Meat and c h i l i bean combination Failure t o properly r e f r i g e r a t e cooked foods Picnic Dunham ( 96) 8 t o 9 Creamed turkey State institution Kemp e t a l (96) 55 Shrimp salad Prepered a day before serving, f a i l u r e t o cooked foods Sorority house kjebb and Wiley (96) 4 Roast beef Holding foods a t warm temperatures Restaurant H a r t (96) 5 Rmst beef Scout dinner :<art (96) 9 Smoked ham Family dinner S a r t ( 96) - e - (cont hu

4 Number ill Vehicle Contributory factors Place Reference 9 Turkey salad serving, f a i l u r e t o cooked foods Nursing home S e l t z e r e t al (s) 55 Creamed chicken Holding foods a t warm temperatures Church dinner (restaurmt caterer) Fleming ( m ) 55 Roast beef and gravy serving, failure t o cooked foods, inadequate reheating Welfare i n s t i t u t i o n luncheon Werrin end Witte (96 5 Turkey serving, f a i l u r e t o codked foods, holding foods a t w a r m temperatures, inadequate reheating School Condit and Proctor (9 Lamb stew p i e Leftover food, f a i l u r e School Agar and Ploeger (964 Nelson e t a l (966) School McCroan and Mixson to cooked foods, inadequate reheating serving, failure t o codked fads (9 (Continu

5 TABLE Number ill (CONTINUED) Vehicle Contributory factors Place Reference (965) Turkey a la king serving, failure t o cooked foods, W d e q u a t e reheating, holding foods a t warm temperatures School Herron e t al 4 Turkey Failure t o properly refrigerate cooked foods, inadequate reheating Restaurant banquets (three ) Peterson e t al 66 Beef gravy Leftover food, f a i l u r e t o cooked foods School Evans and P r e i z l e r (9 Helstad e t el (96) 4 Chicken salad serving, failure t o cooked foods Luncheon Goldblatt e t al 56 Chicken salad Luncheon Houglum and Fleming ( 84 Prime r i b au j u s Holding foods a t warm temperatures Hot e banquet Francis e t a l (968) 9 Roast beef Contamination by equipment a f t e r cooking, holding foods a t w a r m temperatures Hot e l banquet Schachner e t a l - (966 (96 L- (96 (Continu

6 TAELE Nmber ill (CONTINUED) Vehicle Contributory factors Place Reference $ Mushroom gravy Holding foods a t warm temperatures M i l i t a r y base Robinson and Meseer (9 6 Braised beef serving, failure t o properly refrigerate cooked foods, inadequate reheating School Armes e t a l ( % ~ ) 59 Turkey with gravy serving, f a i l u r e t o cooked foods, inadequate reheating School Bryan e t a l (9) N Roast beef Holding foods a t w a r m temperatures inadequate reheating F a s t food r e s t a u r a n t B r y a n and Kilpatrick ( 88 Spaghetti and meat sauce Prepared two days b e f x e serving, failure t o cooked foods, inadequate reheating School dinner Deshaye e t a l (9) Other outbreaks have been reported t o n a t i o n a l agencies responsible f w surveillance f foodborne diseases

7 9 TABLE FACTORS THAT CONTRIBUTE TO OUTBREAKS O F CLQSTRIDIUM PERFRINGENS FOODBOIWE ILLNESS^ Factor Percent Inadequate holding temperature (room, r e f r i g e r a t o r, warmer) Failure t o cooked foods 8 Holding foods a t warm ( b a c t e r i a l incubating) temperatures 46 Preparing foods a day o r more before serving 44 Inadequate reheating of cooked, c h i l l e d foods 8 Use of l e f t o v e r foods Based on 59 outbreaks that were reported t o t h e Center f o r Disease Control from 96 through 9

8 Number of samples RAW FED MEATS - Beef 5 54 Number positive 5 Frozen bone les s Carcasses 4 Imported-Gr B r i t Retail Abattoirs Steak and mince Tripe Hamburger - Veal Carcasses % 4 6 Frozen boneless Carcasses Pork Retail Abattoirs Sausage H N fl 9N ll Lamb and Mutton Carcasses Imported-Gr B r i t Abattoir Frozen boneless Liver Market Abattoir Hospital Black pudding 4 4 li Percent positive Reference 5

9 ABI;E 4 (CONTINUED) Food POULTRY Chicken Turkey FISH Herring MEAT, POULTFX, FISH (no breakdown ) Number of samples Number Percent positive 5 6 H N positive H N 4 a Reference5 44 (4) H = hemolytic; N = non-hemolytic ( ) = heat-resistant strains; percentages a r e l e a s t s i g p i f i c a n t because both heat-sensitive and h e a t - r e s i s t a n t s t r a i n s cause foodborne i l l n e s s Without enrichment Enrichment method 5 [ l ]Hall and Angelotti (965); [ Hobbs e t a l (95); [] Hobbs and [5 Sylvester and Green Wilson (95); [4 B r y a n and Kilpatrick (96); [6 McKillop (959); E Messer e t a l (9); [8 Canada and (964); [9 Bryan and McKinley ( l E x [ l o ] Zottola and Busta ; ill Christian and King (9); [I Strong e t a l (96) (s fii;

10 It should a l s o not be s u r p r i s i n g t o f i n d C perfringens I n cooked meat and poultry products because i t s spore8 a r e present on t h e r a w products and t h e s e cpores can survive the heat generated during ordinary cooking procedures and because recontamination from workers or from equipment that contact cooked meat is a l i k e l y p o s s i b i l i t y (Bryan and Kilpatrick, 9) Several i n v e s t i g a t o r s have found C perfringens in cooked meat and p o u l t r y products ( t a b l e 5 ) "hue, i f such-cooked products a r e h e l d a t temperatures t h a t do not prevent t h e gruwth of C perfringens, spores w i l l germinate and vegetative c e l l s w i l l multiply; i f g i c n enough t i m e, numbers s u f f i c i e n t t o cause illness w i l l develop By serotyping i s o l a t e s from r a w and cooked meat and from kitchen equipment, evidence shows t h a t strains of C perfringens present on r a w meat o r i n s e r t e d into the meat by thermopgs survived cooking and can be found on o r in cooked meat Also, workers can be t h e source of t h e serotypes present on cooked, s l i c e d meat ( B r y a n and Kilpatrick, 9) Several f a c t o r s permit t h e development of l a r g e numbers o f i n cooked meat and p o u l t r y products: C perfringens It r e q u i r e s s e v e r a l amino a c i d s (arginine, leucine, isoleucine, methionine, phenylalanine, threonine, valine, tryptophane, h i s t i d i n e, c y s t h e, glutamic acid, tyrosine, a s p a r t i c acid, and sme s t r a i n s serine and a l a n i n e ) and s e v e r a l v i t a m b s (adenine, b i o t i n, n i c o t i namide, pantothenate, pyridoxal, and some s t r a i n s r i b o f l a v i n and u r a c i l ) f o r growth (Boyd e t a l, 948; Fuchs and Bonde, 95) Foods t h a t do not contain t h e s e amino a c i d s and vitamins a r e not s u i t a b l e f o r i t s growth These n u t r i e n t s are a v a i l a b l e i n meat, poultry, f i s h, legumes and milk It r e q u i r e s a high water a c t i v i t y, u s u a l l y a b w e a, 96 (Hobbs, 965; Gough and Alford, 965; Strong et 9) Most meat and p o u l t r y products have aw values above t h i s l e v e l It grows within the ph range of 5 t o 9, b u t rapid growth occurs only between ph 55 t o 5 (F'uchs and Bonde, 95; Smith, 96; Barnes e t a l, 96) Most meat products are within t h i s ph range 4 I t does not compete well i n t h e presence of o t h e r microorganisms (Smith and Holdeman, 968; Kafel and A y r e s, 969) When meat i s cooked, however, most competitive and amensal f h r a are k i l l e d ; t h i s gives h e a t - r e s i s t a n t C perfringens spores an opportunity f o r germination and gives the r e s u l t i n g c e l l s an opprtunity f o r rapid, unmolested m u l t i p l i c a t i o n when t h e temperature becomes favorable 5 I t r e q u i r e s a low oxidation-reduction p o t e n t i a l ( E h ) t o i n i t i a t e growth ptimm Eh t o i n i t i a t e growth i s from -45 t o - mv; t h e h i g h e s t i s from + l t o +l mv (Read and O r r, 94; Hanke and When meat c)r gravy i s Bailey, 945; Barnes and Ingram, 956 ) cmked, oxygen i s driven out and t h e s e f m d s become anaembic C perfringens enough t o support t h e grcrwth of - e,

11 TABLE 5 - INCIDENCE OF C PERF HINGENS IWE A I N PROCX;:;I~:ll FOOIX Food PROCESSEX) MEATS Requires f u l l cooking Requires light cooking Requires no cooking Steak and mince Sausage Number of samples Tripe Black pudding Roast ( c o l d ) 5 Cold meats 6 BBQ pork sandwiches Roast beef Cooked chickens 5 46 Cooked f urther processed chickens Turkey Wkg Turkey stock PROCESSED FISH Hospital cooked Kipper Smoked haddock Smoked salmon Number positive 4 4 H N 4 H N 4 H N 4 H 4N 9 H N Percent positive ( ) FROZEN FOODS ROME PREPARED FOODS 65 scampi DMYDRATED SOUPS, GRAVIES, SAUCES AND SPAGHETTI COMMERCIALLY PREPARED Reference 5 ( Continued )

12 4 - TABLE 5 H (CONTINUED) hemolytic; N = non-hemolybic ( ) = h e a t - r e s i s t a n t strains; percentages are l e a s t s i g n i f i c a n t because both heat-sensitive and h e a t - r e s i s t a n t s t r a i n s cause foodborne illness Without enrichment Enrichment method 5 [l] Hall and Angelotti (965); f McKillop (959); Bryan and Kilpatrick (9); [4 Christian and K i n g (9); [ 5 ] L i l l a r d (9); [6 Zottola and Busta (9;); E Bryan and McKinley (9); [8 Hobbs e t a l ( ) ; (9 Nakamura and Kelly (968); [lo] Strong e t a l ( 9 6 r -

13 5 6 Its heat-resistant spores can survive boiling f o r t o 6 hours (Hobbs e t al, 958; Barnes e t al, 96; H a l l e t, * a, 96; Hobbs, 965; Nakamura and Converse, 96;r; Weiss and Strong, 96; Roberts, 968) Several investigators have observed i t s survival i n cooked meat products Barnes e t al, 96; Woodburn and Kim, 966; Strong and Ripp, 96 - H i g h temperatures a l s o heat shock, or a c t i v a t e, i t s spores, causing, a higher yield of vegetative c e l l s fromheated spore cultures than from unheated spore cultures (Barnes e t a 96 ) 8 Its temperature range f o r growth has been reported between 546' and lof (Solberg and E l k i n d, 9; Collee e t a l, 96) I n beef, however, it did not commence t o grow u n t i l temperatures of 6 5 O o r 6 8 O F were reached (Barnes e t a l, 96; Hall and Angelotti, 965) Optimum growth occurs between log t o FF (Boyd e t a l, 948) A large volume of hot cooked meat, even i f refrigerated, w i l l s t a y within t h e growth range f o r C perfrinaens f o r several hours ( B r y a n e t al, 9) A t opt-temperatures the generation time f o r C perfringens has been reported t o be as short a s 85 minutes; Tt averaged minutes (Arbuckle, 96) A l l of these f a c t o r s a r e i n t e r r e l a t e d If a l l a r e optimum f o r C perfringens, rapid growth w i l l occur a f t e r an i n i t i a l l a g On t h e ocher hand, i f any one f a c t o r i s not optimum, the r a t e of multiplication w i l l be decreased Combinations of these f a c t o r s a t sub-optimal levels may prevent growth even i f each f a c t o r alone a t such levels would permit growth under otherwise optimum conditions Freezing and refrigerated storage is detrimental t o vegetative c e l l s of C perfringens and freezing t o a l e s s e r extent, i s detrimental t o i t s spores TBarnes e t al, 96; Canada e t al, 964; Strong and Canada, 964; Woodburn and Kim,TgG; Strong and Ripp, 96) These organisms, however, can be found in frozen foods s o freezing o f f e r s no assurance of s a f e t y (Bryan and Kilpatrick, 9; Bryan e t al, 9) Also, large volumes of foods t h a t have been stored in r e f r i g e r a t o r s overnight, and not adequately reheated, have frequently been vehicles of outbreaks (table ) A review of the f a c t o r s t h a t contribute t o outbreaks ( t a b l e s, ), shows that t h e way t o prevent C perfringens foodborne i l l n e s s from-meat products i s t o hold them a t temperatures too cold or too hot t o permit multiplication or not long enough t o permit organisms t o multiply; and t o reheat chilled food, just before serving, t o a temperature l e t h a l f o r vegetative cells of C perfringens (Bryan, 969) Thus, t o prevent C perfrinaens foodborne i l l n e s s, cooked meat and poultry should be hanzled in the following ways ( B r y a n and Kilpatrick, 9; Bryan e t a l, 9; Bryan and McKinley, 9): They should be eaten within hours af'ter cooking If they a r e held a t warm temperatures t o be served later, hold i n warmers or steam t a b l e s (which have a i r or water temperatures above

14 6 49) only as long 88 the internal temperature of the food does not drop below OF If the temperature drops below loof, reheat the food If they are held cold to later be served cold, rapidly cool them to below 65OF, then cool to and hold at or below 45OF until served One method of rapid cooling for meat and poultry is to slice them and pile to a depth no higher than inches on cold pans, and then place in refrigerator or freezer Another method is to cut roasts into smaller portions (such as l/4-pound pieces) and place in double plastic bags which are surrounded by ice, then refrigerate Methods of rapidly cooling stock and gravy are to immerse pans which hold them into ice or cold water baths or to mix in a mechanical mixer for an hour, then refrigerate 4 If they ere held cold to be served hot later, the same procedures a8 described in item should be used; in addition, heat the chilled meat to an internal temperature of at least 69~ and boil stock or gravy If these precautions would be taken in all food service establishments, one of the most commonly occurring foodborne diseasesthe disease that accounts for most reported cases of such illness in the United States would become a rareity

15 REFERFNCES Agar, E and E Ploeger 9 4 Clostridium perfringens outbreak-washington (U S ) Morbidity M o r t a l i t y Weekly Report :4 Center f o r Disease Control, Atlanta, Georgia Arbuckle, R E 96 The influence of temperature on t h e growth of Indiana S t a t e University Library, Clostridium perfringens M S Thesis Bloomington, Indiana Armes, W H, Jr, C B Tucker, W M Arnold, J N Barrick, G S Lovejoy, D R Daffron and R C Rendtorft 969 Clostridium e r f r i n ens f m d for poisoning (U S ) Morbidity Mortality Weekly Report 8 Disease Control, Atlanta, Georgia Barnes, E M, J E Despaul and M Ingram 96 The behavior of a food poisoning s t r a i n of Clostridium welchii in b e e f J Appl B a c t e r i o l 6 :45 Barnes, E M and M Ingram 956 The e f f e c t of redox p o t e n t i a l n t h e growth of Clostridium w e l c h i i strains i s o l a t e d from horse muscle J Appl B a c t e r i o l 9: Boyd, M J, M A Logan and A F T y t e l l 948 The growth requirements of Clostridium perfringens (welchii) BP6K J Biol Chem 4: Bryan, F L 969 What the s a n i t a r i a n should h o w about Clostridium perfrinrens foodborne illness J M i l k Food Technol :8 Bryan, F L 9 Emerging foodborne d i s e a s e s P a r t Factors t h a t contribute t o outbreaks and t h e i r c o n t r o l J M i l k Food Technol ( ~press n ) Bryan, F L and E G Kilpatrick 9 Clostridium perfrinrens r e l a t e d t r o a s t beef cooking, storage, and contamination i n a fast food s e r v i c e r e s t a u r a n t h e r J Public Health 6:869 Bryan, F L and T W McKinley 9 P r e v e n t i m of foodborne i l l n e s s by time-temperature c o n t r o l of thawing, cooking, c h i l l i n g, and reheating turkeys i n school lunch kitchens ( I n press ) B r y a n, F L, T W McKinley and B Mixson 9 Use of time-temperature evaluations i n d e t e c t i n g t h e responsible vehicle and contributing f a c t o r s of fdodborne d i s e a s e outbreaks J Milk Food Technol 4:56 Canada, J C and D H Strong l i v e r s J Food S c i :86 g64 Clostridium perfringens i n bovine

16 H a l l, H E, R, Angelotti, K H, L e w i s and M J Foter 96 C h a r a c t e r i s t i c 6 of Clostridium r f k i n ens strains associated with food and foodborne disease J Ba*:@?4 z Hanke, M E and J H Bailey 945 Oxidation-reduction p o t e n t i a l w e l c h i i and o t h e r c l o s t r i d i a Proc-Soc E- requirements of M e d 59:6 Bid Hart, C J, W W Sherwood and E Wilson 96 A food poisoning outbreak aboard a common c a r r i e r Public Health Reports 5:5 Hart, J C 96 Clostridium food poisming-connecticut, 96 ( U S ) Center f o r Disease Control, Morbidity Mortality Weekly Report :6, Atlanta, Georgia Helstad, A G, A D Mandel and A S Evans 96 Thermostable Clostridium e r f r i n ens as cause of food poisoning outbreak Public Health Report %Fi+ Herron, J T, W L Bunch, Jr, M C hwson and J M Cairns 965 (U S ) Morbidity Mortality Weekly Report 4 :85 Center f o r Disease Control, Atlanta, Georgia Hobbs, B C 965 Clostridium welchii as a food poisoning organism J Appl B a c t e r i o l 8:4 Hobbs, B C, 965 Contamination of meat supplies Clostridium welchii and toxoplasma Mon Bul M i n i s t Health Public Health Lab S e w ( G B r i t ) 4:45 Hobbs, B C, M E Smith, C L Oakley and G H Warrack welchii food poisoning J Hyg 5:5 95 Clostridium Hobbs, B C and J G Wilson 95 Contamination of wholesale meat supplies with salmonellae and heat r e s i s t a n t Clostridium welchii Mon B u l M i n i s t Health Public Health Lab Serv I G B r i t ) B Hobbs, G, D C C a m, B B Wilson and J M Shewan 965 The incidence f organisms of t h e genus Clostridium i n vacuum packed f i s h in t h e United Kingdom J Appl B a c t e r i o l 8:65 Houghlum, A J and D S Fleming Mortality Weekly Report 6:6 Georgia 96 G a s t r o e n t e r i t i s (US) Morbidity Center f o r Disease Control, Atlanta, Kemp, G E, R Proctor and A S Browne 96 Foodborne d i s e a s e i n California w i t h s p e c i a l reference t o Clostridium perfringens (welchii ), Public Health Reports :9 Kafel, S and J C A y r e s b a ~ t e r i a i n canned hams 969 The antagonism of enterococci c m Ahvr- J Appl B a c t e r i o l :

17 9 Canada, J C, D H Strong and L G S c o t t 964 Response of Clostridium perfringens spores and vegetative c e l l s t o temperature v a r i a t i o n Appl Microbiol l: Christiansen, L N and N S 9 and sendwiches a t r e t a i l o u t l e t s The microbial content of some salads J Milk Food Technol 4:89 Collee, J G, J A Knowlden and B C Hobbs 96 Studies on the growth, sporulation and carriage of Clostridium welchii with s p e c i a l reference t o food poisoning strains J Appl ~ a c t e r m : 6 Condit, P K and R L Proctor 965 (U S ) Morbidity Mortality Weekly Control, A t l a n t a, Georgia f o r Disease Deshaye, J V, C A Bartleson, C D Leaf, H Anundson, T Mason, C V Hall and B J Francis 9 Clostridium e r f r l n enswashington ( U S ) Morbidity Mortality Weekly Report :l *Center,l f o r Disease Control, Atlanta, Georgia- ~ Dunham, V L 96 Foodborne Clostridium rfrin ens outbreakcalifornia (U S ) Morbidity Mortality Weekly Report %enter f o r Disease Control, Atlanta, Georgia- 966 Heat - r e s i s t a n t Clostridium perfringens Evans, A S and J P r e i z l e r (U S ) Morbidity Mortality Weekly Report 5 :, outbreakwashington Center f o r Disease Control, Atlanta, Georgia 8 Fleming, D S 96 Probable Clostridium perfringens food poisoning-minnesota (U S,) Morbidity Mortality Weekly Report :6,68 Center f o r Disease Control, Atlanta, Georgia Francis, B J, J A Bessey, S A Davis, R Olson and E Ploeger 968 Food poisoningspokane, Washington ( U S o ) Morbidity Mortality Weekly Report : Center f o r Disease Control, Atlanta, Georgia F uchs, A R and G J Bonde 95 The n u t r i t i m a l requirements of Clostridium perfringens J Gen Microbiol 6 : Goldblatt, E L, J R Thompson, R Anderson and C L Rodemacher 966 GastroenteritisOregon ( U S ) Morbidity Mortality Weekly Report l5:46 Center f o r Disease Control, Atlanta, Georgia Gough, B J and J A Alford 965 Effect of curing agents on t h e growth and s u r v i v a l of food-poisoning strains of Clostridium perfringens J Food S c i :5 H a l l, H E and R Angelotti 965 Clostridium perfringens i n meat and meat products Appl Microbiol :5

18 L i l l a r d, H S 9 Occurrence of Clostridium p e r f r i w e n s i n b r o i l e r processing and f'urther processing operations J Food S c i 6:@ *',;sser, W, J T Peeler, R e B Read, Jr, J E Campbell, H E H a l l and H Haverlsnd 9 Microbiological q u a l i t y survey o f some selected market foods in two socioeconomic areas Bacteriol Froc, 9:U 9 5 Human food poisoning due t o growth of Clostridium perfrwens (E welchii) i n freshly cooked chickens: Preliminary note J Bacteriol 5:9 McClung, L S McCroan, J E and B W Mixson 965 Clostridium perfringens food poisoninggeorgia (U S ) Morbidity Mortality Weekly Report 4 :8, 9 Center for Disease Control, Atlanta, Georgia McKillop, E J 959 Bacterial contamination of h o s p i t a l food w i t h special reference t o Clostridium welchii food pdisoning J Hyg 5: Nakmmra, M and J, D Converse 96 Heat resistance of spores of Clostridium w e l c h i i J Hyg 65 :59 Nakamura, M and K D Kelly 968 Clostridium p e r f r i w e n s i n dehydrated soups and sauces J Food Sci :44 Nelson, K E, E A Agar, J R Marks and I m u e l food poisoning R e p o r t of an outbreak 966 C l o s t r i d i u m h e r J Epidemiol Peterson, D e R, H W Anderson and R Detels 966 Three outbreaks o f foodborne disease w i t h dual etiology Public Health Reports 8:899 Reed, G B and J H Orr 94 Cultivation of anaerobes and oxidationreduction potentials J Bacteriol 45:9 Roberts, T A 968 Heat and radiation resistance and activation of spores of Clostridium welchii J Appl Bacteriol : Robinson, J A and M Messer 969 Clostridium e r f r i n ens food poisoning (U S ) Morbidity Mortality Weekly Report%enter for Disease Control, A t l a n t a Georgia Schachner, C S, T Fodor and Reisberg 968 Clostridium perfringens food poisoningnew York City (U S ) Morbidity Mortality Weekly Report C :45 Center f o r Disease Control, A t l a n t a, Georgia Seltzer, J, F Rumney and M Mattarazzo 96 C l o s t r i d i u m perfringens (U S ) Morbidity Mortality Weekly Report food poisoningcalifornia :4 Center f o r Dieease Control, Atlanta, Georgia

19 Smith, L D, S 96 Clostridium perfringens food poisoning I n : Microbiological Quality of Foods (Slanetz, L W, C Chichester, A R Gaufin and J Ordal, E d ) pp -8 Academic Press, New York, N Y Smith, L D S 9 Factors a f f e c t i n g t h e growth of Clostridium perfringens In: Proc SOS/O rd International Cong Food S c i Technol I n s t Food Technologists Chicago, I l l i n o i s Smith, L D S and L V Holdeman 968 The pathogenic anaerobic b a c t e r i a University of Chicago Press, Chicago, I l l i n o i s Solberg, M and B Elkind 9 Effect of processing and storage conditions on t h e microflora of Clostridium perfringensinoculated f r a n k f u r t e r s J Food S c i 5:l6 Strong, D H and J C Canada 964 Survival of Clostridium Perfringens in frozen chicken gravy J Food S c i 9:49 Strong, D H, J C Canada and B B G r i f f i t h s 96 Incidence of Clostridium perfringens in American foods Appl Microbiol :4 Strong, D H, E F Foster and C L Duncan 9 Influence of water a c t i v i t y on t h e growth of Clostridium perfringens Appl Microbiol 9:98 Strong, D H and N M Ripp 96 E f f e c t of cookery and holding on hams and turkey r o l l s contamineted with Clostridium perfringens Appl Microbiol 5 : Sylvester, P K and J Green 96 The incidence of h e a t - r e s i s t a n t Clostridium w e l c h i i in some raw meat s u p p l i e s Med O f f r 5:89 Webb, R W and N H Wiley 96 An outbreak of food poisoning caused by Clostridium perfringens Student Med :@ Weiss, K F and D H Strong 96 Some p r o p e r t i e s of h e a t - r e s i s t a n t and h e a t - s e n s i t i v e strains o f Clostridium perfringens J B a c t e r i d 9: Werrin, M and E J Witte 96 Clostridium perfringens food poisoning-philadelphia (U S ) Morbidity Mortality Weekly Report :8 Centcr f o r Disease Control, A t l a n t a, Georgia Woodburn, M and C H Kim 966 Survival of Clostridium e r f r i n ens during baking and holding of turkey s t u f f i n g Appl Microbiol -4