A total of 615 strains of Salmonella enterica serovar Enteritidis (SE), received from 1991-1995 at
the Onderstepoort Veterinary Institute (OVI), were phage typed. Most SE isolates (54,7%) originated
from poultry followed by humans (28 ,5 %) and poultry eggs (9,6 %). Phage type 34 was the most
prevalent (40,5 %) of all isolates, followed by phage type 4 (33 ,8 %). Other phage types identified
were 1, 1 b, 4a, 7, 7a, 9a, 14, 24, 24var and 35 (in total 2,4 % of isolates). Most isolates of SE were
received from the Western Cape Province (47,4 %) and Gauteng (22,3 %). In poultry phage type 4
was dominant, but in humans, eggs, goats, ducks, sheep, pigs and rabbits, phage type 34 was the
dominant type. It appeared as if the poultry-associated epidemic of SE in South Africa that occurred
from 1991-1995 originated in the Western Cape Province during 1991 amongst poultry and then
spread from there to humans and eggs and then to the rest of the country, where it emerged during
1993. Results indicate that phage type 34 was the dominant phage type from 1991-1993, but during
1994-1995 its presence declined. During this latter period the presence of phage type 4 increased.
This may suggest that two smaller epidemics consisting of the two different phage types might have
been responsible for the epidemic that occurred from 1991-1995.The articles have been scanned in colour with a HP Scanjet 5590; 600dpi. 
Adobe Acrobat v.9 was used to OCR the text and also for the merging and conversion to the final presentation PDF-format.mn201

Dicks, L.M.T.

Mare, L.

Van der Walt, M.L.

The articles have been scanned in colour with a HP Scanjet 5590; 600dpi. 
Adobe Acrobat v.9 was used to OCR the text and also for the merging and conversion to the final presentation PDF-format.A total of 615 strains of Salmonella enterica serovar Enteritidis (SE), received from 1991-1995 at
the Onderstepoort Veterinary Institute (OVI), were phage typed. Most SE isolates (54,7%) originated
from poultry followed by humans (28 ,5 %) and poultry eggs (9,6 %). Phage type 34 was the most
prevalent (40,5 %) of all isolates, followed by phage type 4 (33 ,8 %). Other phage types identified
were 1, 1 b, 4a, 7, 7a, 9a, 14, 24, 24var and 35 (in total 2,4 % of isolates). Most isolates of SE were
received from the Western Cape Province (47,4 %) and Gauteng (22,3 %). In poultry phage type 4
was dominant, but in humans, eggs, goats, ducks, sheep, pigs and rabbits, phage type 34 was the
dominant type. It appeared as if the poultry-associated epidemic of SE in South Africa that occurred
from 1991-1995 originated in the Western Cape Province during 1991 amongst poultry and then
spread from there to humans and eggs and then to the rest of the country, where it emerged during
1993. Results indicate that phage type 34 was the dominant phage type from 1991-1993, but during
1994-1995 its presence declined. During this latter period the presence of phage type 4 increased.
This may suggest that two smaller epidemics consisting of the two different phage types might have
been responsible for the epidemic that occurred from 1991-1995.mn201

UPSpace at the University of Pretoria

Onderstepoort Journal of Veterinary Research, 67: 129-133 (2000) Phage types of Salmonella enterica serovar Enteritidis isolated in South Africa from 1991-1995 L. MARE1, M.L. VAN DER WALT1 and L.M.T. DICKS2 ABSTRACT MARE, L., VAN DER WALT, M.L. & DICKS, L.M.T. 2000. Phage types of Salmonella enterica serovar Enteritidis isolated in South Africa from 1991-1995. Onderstepoort Journal of Veterinary Research, 67:129-133 A total of 615 strains of Salmonella enterica serovar Enteritidis (SE) , received from 1991-1995 at the Onderstepoort Veterinary Institute (OVI) , were phage typed . Most SE isolates (54,7 %) originated from poultry followed by humans (28 ,5 %) and poultry eggs (9,6 %) . Phage type 34 was the most prevalent (40,5 %) of all isolates, followed by phage type 4 (33 ,8 %). Other phage types identified were 1, 1 b, 4a, 7, 7a, 9a, 14, 24, 24var and 35 (in total 2,4 % of isolates). Most isolates of SE were received from the Western Cape Province (47,4 %) and Gauteng (22,3 %). In poultry phage type 4 was dominant, but in humans, eggs, goats, ducks, sheep, pigs and rabbits, phage type 34 was the dominant type. It appeared as if the poultry-associated epidemic of SE in South Africa that occurred from 1991-1995 originated in the Western Cape Province during 1991 amongst poultry and then spread from there to humans and eggs and then to the rest of the country, where it emerged during 1993. Results indicate that phage type 34 was the dominant phage type from 1991-1993, but during 1994-1995 its presence declined. During this latter period the presence of phage type 4 increased. This may suggest that two smaller epidemics consisting of the two different phage types might have been responsible fo r the epidemic that occurred from 1991-1995. Keywords: Phage typing, Salmonella enterica serovar Enteritidis, South Africa INTRODUCTION The Salmonella surveillance data of the World Health Organization revealed that the prevalence of Salmo-nella enterica serovar Enteritidis (SE), increased dramatically from 1980-1989 in North and South America, Europe and Africa (Anonymous 1993) . During 1990 SE was isolated the most often from human samples in the UK, USA and Canada. At that stage the worldwide increase in the prevalence of SE was regarded as a pandemic. The main source of human infections was contaminated food, especially from poultry and eggs of domestic fowls (Schroeter, Ward, Rowe, Protz, Hartung & Helmuth 1994). Given the preference of many people to eat raw, or under-cooked eggs, this food was regarded as a major source of infection (Humphrey, Greenwood, Gilbert, Rowe & Chapman 1989) . 1 Onderstepoort Veterinary Institute, Private Bag X01 , Onderste· poort, 0110 South Africa 2 Department of Microbiology, University of Stellenbosch, Pri-vate Bag X1, Matieland, 7602 South Africa Accepted for publication 12 April2000-Editor The first recorded poultry-associated outbreak of SE in South Africa was in 1991 in the Western Cape Province. The Onderstepoort Veterinary Research Institute (OVI) has recorded data on the prevalence of salmonellas in South Africa since 1977, and for the period from 1977-1990 only 35 isolates of SE had been identified, mostly from cattle and pigs, but none from poultry and eggs. From 1991, a marked in-crease in the prevalence of SE infection in poultry and other sources was observed, and based on this, it is concluded that these outbreaks of SE infection in South Africa were linked to the pandemic in the rest of the world. 129 Salmonella enterica serovar Enteritidis isolated in South Africa Serotyping of Salmonella does not provide any infor-mation on the epidemiological relationships of strains isolated from a common outbreak. For th is reason additional methods for the epidemiological differen-tiation of Salmonella strains were developed. Phage typing has been used widely to study the distribution of Salmonella serovars. This phage-typing scheme had been developed specifically for SE (Ward, De Sa & Rowe 1987). This paper reports on the results obtained in the phage typing of 615 South African SE isolates received at the OVI from 1991-1995. MATERIALS AND METHODS Bacterial strains and phage typing A total of 615 isolates of SE (Table 1) isolated from various sources and which originated from eight of the nine provinces of South Africa were phage-typed at the OVI. These isolates were identified according to the biochemical identification methods described by Brenner (1984) and serotyped according to the Kauffmann-White scheme (Kauffmann 1972). Phage typing was done according to the method described by Ward et al. (1987) . Ten typing phages were used which differentiated 53 phage types. RESULTS AND DISCUSSION The prevalence of SE infections in South Africa reached a peak during 1993 and 1994, but de-creased markedly during 1995 (Fig. 1). From 1996 onwards, this trend continued for the following years (Anonymous 1995). The pattern of the SE epidemic closely resembled those reported from overseas countries, i.e. a sharp increase in the number of cases from which SE was isolated, followed by a stable period of 2-3 years and then a definite de-crease (Brown, Baggesen, Hansen, Hansen & Bis-gaard 1 994) . 300 -,-__________ ____ -----, 250 - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - r-- - - - - - - - - - - - - - -~ -.2! ca '0 .!!l 200 __ _______ __________ _ _ o 150 - -- - ------- - ------- - -... Q) ~ 100 _ __________ ___ ______ _ :::l Z 5: -----------n ---I I 1991 1992 1993 Years ------n----I I 1994 1995 FIG. 1 The number of Salmonella Enteritidis isolates received at the OVI from 1991-1995 130 Most of the 615 samples (54,7%) received over the 5-year period were of poultry origin (Table 1). It is assumed that these samples were representative of the presence of SE for this period. During this period the awareness towards SE was very high among animal health officials, and many poultry and egg producers in the country had instituted SE screen-ing programmes. Consequently, a large number of isolates were sent to the OVI for identification . A to-tal of 9,6 % samples were from eggs, probably due to the more intensive screening programme of many egg producers. Samples originating from other animals were repre-sented at very low numbers (Table 1). It is believed that these samples represented a spillover of infec-tion from poultry to the other species. Although 28,5 % of all strains isolated were from humans, it is believed that this finding is not representative from this source for the period under review. The reason is that in the majority of human diarrhoea cases in South Africa, an aetiological diagnosis of the cause is not made routinely. Hence, very few isolates of SE were made on a routine basis from humans during the study period . However, in the Western Cape Province, the Red Cross Childrens' Hospital was very active from 1991-1995 in the study of the causes of diarrhoea amongst children, and most of the human SE strains originated from that area. A small number of the human SE isolates were from cases of diar-rhoea in Pretoria, Gauteng. The prevalence of SE was the highest in the West-ern Cape (47,4 % of all isolates) (Table 2), followed by Gauteng (22,3 %), with much lower rates in the rest of the country. During 1991, only two SE isolates (phage type 34) were isolated in the Western Cape Province, and in 1992, 56 isolates were isolated from poultry and one from a human (phage type 34), in the Western Cape Province. Only from 1993 was the organism isolated from other parts of the country and from a wider source range. In the Western Cape Province, phage type 34 was the dominant strain isolated from egg and poultry samples, but in the rest of the country, phage type 4 was the dominant one from these sources. The rea-son for this difference is difficult to explain. A possi-ble explanation may be that the phage type 34 strain that was dominant in poultry in the Western Cape Province during the first part of the epidemic, was not responsible for the outbreaks in poultry during the latter part of the epidemic in Gauteng and other prov-inces. In total , the most dominant phage type among poultry was phage type 4, followed by phage type 34 (Table 3). For all other strains, including those iso-lated from eggs, phage type 34 was the most domi-nant. In strains isolated from humans, phage type 14 and phage type 4 (both 48/175) were present in equal numbers with, phage type 34 (59/175) being the most predominant. L. MARE, M.L. VAN DER WALT & L.M.T. DICKS TABLE 1 Source of SE isolates from 1991-1995 Number of SE isolates Source 1991 1992 1993 1994 1995 Total % Poultry 2 56 106 131 42 337 54,7 Humans - 1 69 79 26 175 28,5 Eggs - - 51 8 - 59 9,6 Feed - - 7 6 - 13 2,1 Goats - - - 10 - 10 1,6 Environment - - - 6 - 6 1,0 Cattle - - - 3 1 4 0,6 Ducks - - 3 - - 3 0,5 Sheep - - 2 - - 2 0,3 Jackal - - - 2 - 2 0,3 Parrots - - - 1 - 1 0,2 Rabbit - 1 - - - 1 0,2 Ostriches - - - 1 - 1 0,2 Pigs - - - 1 - 1 0,2 Total 2 58 238 248 69 615 100 TABLE 2 Distribution of SE isolates in the nine provinces of South Africa Province Total number of SE Percentage (%) Presence of phage types 4 and 34 in poultry and eggs isolates received of total number of Number of Number of isolates phage type 4 isolates phage type 34 isolates Western Cape 292 47,4 6 145 Gauteng 137 22,3 47 3 Mpumalanga 50 8,1 39 0 Kwazulu-Natal 47 7,7 21 3 Free State 41 6,7 23 9 North West 34 5,5 14 3 Northern Province 10 1,6 1 5 Eastern Cape 4 0,7 4 0 Northern Cape 0 0 0 0 Total 615 100 155 168 TABLE 3 Phage types of SE occurring in the various sources Phage types Sources Total 4 34 14 7 Untypable Other" Poultry 149 121 10 23 24 10 337 Humans 48 59 48 0 16 4 175 Eggs 6 47 0 1 5 0 59 Feed 1 2 6 0 4 0 13 Goats 0 10 0 0 0 0 10 Ducks 0 2 0 0 0 1 3 Ostriches 0 0 0 0 1 0 1 Environment 1 1 1 0 3 0 6 Cattle 2 2 0 0 0 0 4 Jackal 0 1 0 0 1 0 2 Sheep 0 2 0 0 0 0 2 Pigs 0 1 0 0 0 0 1 Parrots 1 0 0 0 0 0 1 Rabbit 0 1 0 0 0 0 1 Percentage 33,8 40,5 10,6 3,9 8,8 2,4 100 Totals 208 249 65 24 54 15 615 a Other phage types: 1, 1 b, 4a, 7a, 9a, 24, 24var, 35 131 Salmonella enterica serovar Enteritidis isolated in South Africa 140,,--------------------------------------------------------~ 120 III 100 ,S! III '0 .!!l 80 ... ~ 60 E :::l Z 40 20 o -+-'=-----------~ 1991 mllill!I34 1992 1993 1994 1995 Years ~ 14 • Other mllill!I Untypable mllill!I * I FIG. 2 The prevalence of the various phage types of Salmonella enterica serovar Enteritidis (SE) Isolates that could not be phage typed at the Onderstepoort Veterinary Institute Other: Phage types 1, 1 b, 4a, 7a, 9a, 14b, 24, 24var and 35 No consistent pattern in the distribution of the domi-nance of a specific phage type during the period 1993-1995 was observed (Fig. 2). From 1991-1993 phage type 34 was the most prevalent, followed by phage type 4 and 14, while from 1994-1995 its num-bers decreased, and phage type 4 became the most prevalent, followed by phage type 34. A similar vari-ation in the distribution of the dominant source of samples was not observed amongst the species, for poultry remained the most important source (Table 1), followed by humans. Thus, from 1993-1994 a change from phage type 34 to 4 as the most preva-lent phage type occurred, although no change in the dominant source of the isolates was recorded. The most probable explanation for these results is that from 1991-1993 phage type 34 was the most domi-nant phage type in poultry and eggs, and that most of the strains originated from the Western Cape Prov-ince. The epidemic in the Western Cape Province subsided, and in the rest of the country another epi-demic among poultry and eggs occurred, caused by a phage type 4 strain. If poultry and eggs are ex-cluded, phage type 34 strains remained dominant in all parts of the country for the entire study period. Phage type 34 is not internationally recognized as an important or very prevalent phage type, nor is it believed to be very virulent. It is present in very low numbers in other countries, and has been reported from Japan, Spain and Argentina (Caffer & Eiguer 1994; Anonymous 1993). It is not known what fac-tors contributed to the large number of this phage 132 type encountered in South Africa. In addition, it is not known from where it originated, but it is related to phage type 4. A possible explanation for its high prevalence in South Africa is that initially a phage type 4 strain did enter the country, and that it mutated to phage type 34, to emerge in 1991 in poultry in the Western Cape Province. Reports from Europe, in-cluding such countries as Germany (Schroeter et al. 1994), Italy (Fantasia & Filetici 1994) and the United Kingdom (Khakhria, Duck & Lior 1991), indicate that phage type 4 is the most frequently encountered (Khakhria et al. 1991). Apart from phage type 4, none of the prominent phage types found in other coun-tries were dominant in South Africa. It is believed the laboratory at the OVI received dur-ing the period 1991-1995 SE isolates of poultry ori-gin that were representative of the presence of this organism in this species. Therefore, the distribution and prevalence of the phage types in the country are believed to be representative of the situation for this period. The data show that: • It appeares as if the epidemic of SE infections originated in poultry in the Western Cape Province in 1991, the infection probably spread to humans in the Western Cape Province in 1992, and then to eggs, other sources, and to the rest of the coun-try, where it emerged in 1993. • Phage type 34 was the most prevalent phage type among all strains isolated. • Phage type 4 was more prevalent than phage type 34 in poultry. • Phage type 34 was more prevalent during the period 1991-1993, but its numbers subsequently subsided and phage type 4 became more preva-lent for the period 1994-1995. REFERENCES ANONYMOUS. 1993. Report on Salmonella in eggs. Advisory Committee on the Microbiological Safety of Food, United King-dom. ANONYMOUS. 1995. Salmonella enteritidis phage type 34 and holidays abroad. Communicable Disease Report Weekly, 5. BRENNER, D.J. 1984. Enterobacteriaceae, in Bergey's Manual of Systematic Bacteriology. Vol. 1, edited by N.R. Krieg & J.G. Holt. Baltimore/London: Williams & Wilkens. BROWN, D.J., BAGGESEN, D.L., HANSEN, H.B., HANSEN, H.C. & BISGAARD, M. 1994. The characterization of Danish iso-lates of Salmonella enterica serovar Enteritidis by phage typ-ing and plasmid profiling : 1980-1990. APMIS, 102:208-214. L. MARE, M.L. VAN DER WALT & L.M.T. DICKS CAFFER, M.1. & EIGUER, T. 1994. Salmonella enteritidis in Ar-gentina. International Journal of Food Microbiology, 21 :15-19. FANTASIA, M. & FILETICI , E. 1994. Salmonella enteritidis in Italy. International Journal of Food Microbiology, 21 :7-13. HUMPHREY, T.J., GREENWOOD, M. , GILBERT, R.J. , ROWE, B. & CHAPMAN, P. 1989. The survival of salmonellas in shell eggs cooked under simulated domestic conditions. Epidemi-ology and Infection, 103:35-45. KAUFFMANN , F. 1972. Serological examination of Salmonella species. Kauffmann-White Scheme, 1 st ed. Baltimore: Wil-liams & Wilkens. KHAKHRIA, R., DUCK, D. & LlOR, H. 1991 . Distribution of Sal-monella enteritidis phage types in Canada. Epidemiology and Infection, 106:25-32. SCHROETER, A., WARD, L.R., ROWE, B., PROTZ, D., HAR-TUNG, M. & HELMUTH, R. 1994. Salmonella enteritidis phage types in Germany. European Journal of Epidemiology, 10:645-648. WARD, L.R., DE SA, J.D.H. & ROWE, B. 1987. A phage-typing scheme for Salmonella enteritidis. Epidemiology and Infection, 99:291-294. 133 

Phage types of Salmonella enterica serovar Enteritidis isolated in South Africa from 1991-1995

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Phage types of Salmonella enterica serovar Enteritidis isolated in South Africa from 1991-1995

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