Streptococcus suis, an important pig pathogen and emerging zoonotic agent—an update on the worldwide distribution based on serotyping and sequence typing

Figures & data

Table 1 Worldwide distribution of serotypes for reported clinical S. suis cases of infection in pigs by country from 1 January 2002 to 31 December 2013

Country	Clinical cases	Predominant serotypes^a (frequency in %)	Reference
Worldwide	4711	2 (27.9%)	9 (19.4%)	3 (15.9%)
North America	3162 (67.1%)	2 (24.3%)	3 (21.0%)	1/2 (13.0%)
Canada	3 065	2	3	1/2	25, 29
United States	97	3	2	7	55
South America	125 (2.7%)	2 (57.6%)	1/2 (9.6%)	14 (8.8%)
Brazil	125	2	1/2	14	56,57
Asia	659 (14.0%)	2 (44.2%)	3 (12.4%)	4 (5.6%)
Mainland China	639	2	3	4	30,58–60
South Korea	20	3	4	2, 8, 22	61
Europe	765 (16.2%)	9 (61.0%)	2 (18.4%)	7 (6.7%)
Netherlands	99	9	2	7	62
Spain	666	9	2	7	63–65

^a Only the three most predominant serotypes, which were identified by co-agglutination (or an equivalent method using reference antisera), are shown in this table.

Table 2 Worldwide distribution of reported clinical S. suis cases of infection in humans by country until 31 December 2013

	Reported cases	Confirmed serotypes^a	Unconfirmed^c or unknown serotypes^d
Country		2	14	Others^b		Reference
Worldwide	1642	1227 (74.7%)	33 (2.0%)	5 (0.3%)	377 (23.0%)
North America	8 (0.5%)	7 (87.5%)	1 (12.5%)	0	0
Canada	5	4	1	—	—	7,20,94,95
United States	3	3	—	—	—	96–98
South America	9 (0.5%)	2 (22.2%)	0	1 (11.1%)	6 (66.7%)
Argentina	4	1	—	1	2	74,77,99,100
Chile	4	—	—	—	4	75,76
French Guiana	1	1	—	—	—	101
Asia	1481 (90.2%)	1133 (76.5%)	29 (2.0%)	3 (0.2%)	316 (21.3%)
Cambodia	13	13	—	—	—	102
Mainland China	245	245	—	—	—	16,103–107
Hong Kong	69	53	—	—	16	12,82,108–113
Japan	11	10	—	—	1	114–118
Laos	1	—	—	—	1	Unpubl.^e
Philippines (United States)	1	—	—	—	1	119
Singapore	3	—	—	—	3	120–122
South Korea	4	—	—	—	4	123–126
Taiwan	7	2	2	—	3	21,22,127
Thailand	553	292	21	2	238	11,13,23,26,45,73,128–143
Vietnam	574	518	6	1	49	10,72,144–149
Europe	140 (8.5%)	84 (60.0%)	3 (2.1%)	1 (0.7%)	52 (37.1%)
Austria	1	—	—	—	1	150
Belgium	4	3	—	—	1	151–154
Croatia	2	—	—	—	2	44
Denmark	8	6	1	—	1	9,155–159
France	19	8	—	—	11	160–177
Germany	9	8	—	—	1	19,92,178–184
Greece	2	—	—	—	2	185,186
Ireland	1	—	—	—	1	187
Italy	3	2	—	—	1	188–190
Netherlands	51	39	1	1	10	14,191–199
Poland	1	—	—	—	1	200
Portugal	1	—	—	—	1	201
Serbia	5	—	—	—	5	202
Spain	13	4	—	—	9	203–214
Sweden	1	1	—	—	—	215
United Kingdom	19	13	1	—	5	216–230
Oceania	4 (0.2%)	1 (25.0%)	0	0	3 (75.0%)
Australia	3	—	—	—	3	231,232
New Zealand	1	1	—	—	—	91

^a Serotypes were identified by co-agglutination (or an equivalent method using reference antisera) or by PCR specific reaction for serotype 2 (and 1/2) or for serotype 14 (and 1).

^b Serotypes other than serotypes 2 and 14. See main text and Table 3 for details.

^c Serotypes were determined based on biochemical identification so are reported as ‘unconfirmed’.

^d Strain serotype was not mentioned in the publication and is thus considered as ‘unknown’.

^e Wertheim H, unpublished data (2014).

Table 3 Clinical manifestations of reported clinical S. suis cases of infection in humans by serotypes confirmed by co-agglutination

Confirmed serotypes	Reported cases	Clinical manifestations
Meningitis	Septic shock^a	Other^b	Unknown^c
2	867	590 (68.1%)	233 (26.9%)	25 (2.9%)	19 (2.2%)
14	28	14 (50.0%)	6 (21.4%)	—	8 (28.6%)
4	1	1	—	—	—
5	1	—	—	1	—
16	1	—	—	1	—
21	1	1	—	—	—
24	1	—	1	—	—

^a Septic shock includes bacteremia, sepsis, septicemia and streptococcal toxic shock-like syndrome cases.

^b Other clinical manifestations such as endocarditis, septic arthritis, pneumonia, peritonitis, pulmonary edema, myocarditis, etc.

^c Clinical manifestations were either not specified or could not be associated with a particular serotype.

Table 4 Studies exploring human carriage and exposure to S. suis in risk groups

Study (reference)	Technique employed/target	Risk groups	Positive carriage or exposure (positive/tested)	Serotypes found
Serological
New Zealand, 1989^Citation235	Indirect ELISA/serotype 2 whole bacteria	Pig farmers	15/70 (21.4%)	—
Meat inspectors	11/107 (10.3%)
Dairy farmers	9/96 (9.4%)
Netherlands, 1999^Citation236	Western blot/serotype 2 MRP/EF	Veterinarians	MRP: 6/100 (6.0%)	—
	EF: 2/100 (2.0%)
Pig farmers	MRP: 2/190 (1.1%)
	EF: 1/190 (0.5%)
United States, 2008^Citation237	Indirect ELISA/serotype 2 whole bacteria	Pig workers	7/73 (9.6%)	—
Upper respiratory tract colonization (isolation)
Italy, 1989^Citation238	Tonsil swabs	Slaughterhouse workers	2/10 (20%)	2
Mexico, 2001^Citation233	Tonsil swabs	Slaughterhouse workers	4/69 (5.8%)	2, 27, NT^a
Germany, 2002^Citation181	Pharyngeal swabs	Slaughtering and meat processing workers	7/132 (5.3%)	2

^aNon-typable strain (NT).

Figure 1 Worldwide distribution of the most important S. suis serotype 2 sequence types isolated from both clinical pig and human cases of infection.

Table 5 Determined sequence types of reported clinical S. suis cases of infection in pigs from 1 January 2002 to 31 December 2013

Country	Serotypes^a	ST	ST complex	Number of cases	Reference
North America
Canada	2	1	1	2	240
		25	25	28	52,240
		28	28	18	52
		145	25	1	MLST Database
	23	80	Unrelated	1	51
	24	68	Unrelated	1	51
	25	69	Unrelated	1	51
	27	72	Unrelated	1	51
	28	75	Unrelated	1	51
	29	92	Unrelated	1	51
	30	77	Unrelated	1	51
	31	70	Unrelated	1	51
	Not specified	13	13/149	Not specified	51
United States	2	1	1	3	52
		25	25	28	52
		28	28	33	52
Europe
Denmark	4	54	53/54	1	51
	5	53	53/54	1	51
	6	55	Unrelated	1	51
	8	87	87	1	51
	9	82	Unrelated	1	51,240
	10	78	Unrelated	1	51
	11	91	Unrelated	1	51
	12	74	Unrelated	1	51
	13	71	Unrelated	1	51,241
	16	73	Unrelated	1	51
Finland	2	37	Unrelated	1	51
	Not specified	27	27	Not specified	51
		38	Unrelated	1	51
France	2	1	1	4	242
		140	Unrelated	1	MLST Database
		141	1	1	MLST Database
		142	28	1	MLST Database
		143	1	1	MLST Database
		144	1	1	MLST Database
		229	25	1	MLST Database
		230	25	1	MLST Database
	14	231	Unrelated	1	MLST Database
	15	81	Unrelated	1	MLST Database
Germany	1/2	100	Unrelated	1	243
	2	1	1	5	243
		25	25	1	243
		28	28	2	243
		97	Unrelated	1	243
	3	95	Unrelated	1	243
	7	29	29	7	240,243
		89	16	1	243
	9	93	Unrelated	1	243
		96	Unrelated	1	243
		98	16	2	243
		99	16	1	243
Italy	2	1	1	1	86
	9	138	Unrelated	1	MLST Database
Netherlands	1	1	1	4	62,240
		13	13/149	2	51,62
		149	13/149	1	62
		156	1	1	62
	1/2	1	1	1	62,240
	2	1	1	21	62,240
		20	147	19	62
		29	29	1	62
		134	1	1	MLST Database
		146	1	1	MLST Database
	3	15	16	1	62
		35	27	1	51
	4	17	147	3	62
	7	29	29	5	62
		135	29	1	MLST Database
		136	16	1	62
		150	Unrelated	1	62
		153	Unrelated	1	MLST Database
		218	Unrelated	1	62
	8	87	87	1	62
		198	16	1	62
	9	1	1	2	62,240
		15	16	1	62
		16	16	38	62
		136	16	2	62
		148	1	1	62
		151	16	1	62
		152	16	1	MLST Database
		154	16	1	MLST Database
		155	16	1	62
		182	Unrelated	1	62
		184	Unrelated	1	MLST Database
		189	Unrelated	1	62
		220	Unrelated	1	62
	15	81	Unrelated	1	51
	Not specified	183	Unrelated	1	MLST Database
Spain	1	1	1	2	244MLST Database
	1/2	1	1	2	244MLST Database
		28	28	1	MLST Database
		64	94	1	51
	2	1	1	31	244
		5	1	1	51
		27	27	1	MLST Database
		28	28	1	MLST Database
		86	1	1	MLST Database
		124	1	1	244
	3	14	147	1	51
		15	16	1	51
		27	27	1	MLST Database
		89	16	1	51
	4	16	16	1	51,240
	5	17	147	1	51
	9	16	16	2	51,240
		59	123	1	51
		123	123	8	244
		125	123	9	244
		361	Unrelated	1	MLST Database
		367	Unrelated	1	MLST Database
	14	1	1	1	244MLST Database
	15	65	Unrelated	2	51
	27	65	Unrelated	2	51
United Kingdom	1	1	1	5	240,242MLST Database
		12	11	1	51
		13	13/149	1	51
	1 or 14	10	1	1	51
	2	1	1	37	240,242MLST Database
		2	1	5	51
		9	1	1	51
		25	25	7	MLST Database
		28	28	5	MLST Database
		29	29	1	MLST Database
		30	28	1	MLST Database
	3	27	27	2	51
		29	29	1	MLST Database
		31	28	2	51
		33	27	1	51
		42	Unrelated	1	51
	4	23	87	3	51
	5	39	Unrelated	1	MLST Database
		44	Unrelated	1	51
	7	29	29	6	MLST Database
		34	225	1	51
		83	29	1	51
	8	1	1	1	MLST Database
	9	46	Unrelated	1	51
		48	Unrelated	2	51
		50	Unrelated	1	51
	11	88	Unrelated	1	51
	14	1	1	14	MLST Database
	15	43	43/52	1	51
		45	Unrelated	1	51
		49	Unrelated	1	51
		52	43/52	1	51
	16	41	Unrelated	2	51MLST Database
		47	Unrelated	1	51
	28	21	87	1	51
	Not specified	40	Unrelated	1	MLST Database
		51	Unrelated	1	MLST Database
		90	Unrelated	1	MLST Database
Asia
Mainland China	2	1	1	49	59,245,246
		7	7	216	59,241,242,245–247
		25	25	1	246
		28	28	31	59,245,246
		86	1	1	245
		117	27	27	MLST database
		162	28	1	245
		223	1	1	MLST Database
		228	7	1	MLST Database
		242	1	1	MLST Database
		244	7	1	MLST Database
		245	28	1	MLST Database
		289	1	1	59
		290	Unrelated	1	MLST Database
		352	Unrelated	1	MLST Database
		353	Unrelated	1	MLST Database
		354	Unrelated	1	MLST Database
		355	Unrelated	1	MLST Database
		418	Unrelated	1	MLST Database
		419	Unrelated	1	MLST Database
	3	224	Unrelated	1	MLST Database
	7	129	29	1	MLST Database
		225	225	1	MLST Database
		335	Unrelated	1	MLST Database
		420	Unrelated	1	MLST Database
	9	222	Unrelated	1	MLST Database
		226	226/227	1	MLST Database
		227	226/227	1	MLST Database
		239	239/241	1	MLST Database
		241	239/241	1	MLST Database
		417	Unrelated	1	MLST Database
	11	260	Unrelated	1	MLST Database
		263	Unrelated	1	MLST Database
	13	262	Unrelated	1	MLST Database
	27	258	Unrelated	1	MLST Database
	31	261	27	1	MLST Database
		265	27	1	MLST Database
	Not specified	29	29	1	59
		118	Unrelated	1	59
		156	1	2	59
		264	Unrelated	1	MLST Database
		266	Unrelated	1	MLST Database
		267	Unrelated	1	MLST Database
		303	Unrelated	1	MLST Database
		383	Unrelated	2	MLST Database
		421	Unrelated	1	MLST Database
		422	Unrelated	1	MLST Database
Japan	1	1	1	1	53,248
	2	1	1	5	53,248
		28	28	48	53,248
		324	28	1	248
	3	108	94	1	53
		117	27	1	53
	7	29	29	1	53
		118	Unrelated	1	53
	11	108	94	1	53
Vietnam	9	390	Unrelated	1	MLST Database

^a Serotypes were identified by co-agglutination (or an equivalent method using reference antisera), by PCR or, sometimes, by undefined methods.

Table 6 Determined sequence types of reported clinical S. suis cases of infection in humans from 1 January 2002 to 31 December 2013

Country	Serotype^a	ST	ST complex	Number of cases	Reference
North America
Canada	2	25	25	3	53,242
	14	6	1	1	51
United States	2	1	1	1	53
		25	25	1	98
South America
Argentina	2	1	1	1	Unpubl.^b
French Guiana	2	1	1	1	101
Europe
France	2	20	147	2	53,242
Italy	2	1	1	1	86
		134	1	2	86,188
Netherlands	2	1	1	14	62,240
		20	147	11	62,240
		134	1	1	62
		146	1	1	62
	14	6	1	1	51
Spain	2	3	1	1	204
United Kingdom	2	1	1	1	53
	14	2	1	1	MLST Database
Asia
Cambodia	2	1	1	13	102
Mainland China	2	1	1	11	242,247
		7	7	210	242,240,247
	14	1	1	1	241
Hong Kong	2	1	1	14	51,249
		9	1	12	51,249
		25	25	1	249
Japan	2	1	1	7	53,116
		28	28	1	116
Thailand	2	1	1	123	53
		25	25	17	53,129
		28	28	4	53,129
		101	225	1	128
		102	25	2	53
		103	25	6	53,129
		104	225	45	53
		126	1	3	129
	5	181	Unrelated	1	133
	14	11	11	1	53
		105	1	19	130,132
		127	1	1	132
	24	221	221/234	1	133
Vietnam	2	1	1	56	10,240
		107	1	1	10
	14	105	1	1	10
	16	106	Unrelated	1	146

^a Serotypes were identified by co-agglutination (or an equivalent method using reference antisera) or by PCR. However, it is impossible to distinguish between serotypes 1 and 14 and serotypes 1/2 and 2 by PCR, so serotypes remain to be confirmed.

^b Gottschalk M, unpublished data (2014).

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