Streptococcus suis: an emerging zoonotic pathogen

Review

Streptococcus suis: an emerging zoonotic pathogen Zhao-Rong Lun, Qiao-Ping Wang, Xiao-Guang Chen, An-Xing Li, Xing-Quan Zhu

Streptococcus suis is a major porcine pathogen worldwide, and can be transmitted to human beings by close contact with sick or carrier pigs. S suis causes meningitis, septicaemia, endocarditis, arthritis, and septic shock in both pigs and human beings, and mortality is high. Human infection with S suis occurs mainly among certain risk groups that have frequent exposure to pigs or pork. Outbreaks of human S suis infection are uncommon, although several outbreaks have occurred in China in recent years. In July, 2005, the largest outbreak of human S suis infection occurred in Sichuan province, China, where 204 people were infected and 38 of them died. There have been 409 cases of human S suis infection worldwide, most of which have occurred in China, Thailand, and the Netherlands, and these infections have led to 73 deaths. This review provides background information on the biology and molecular characteristics of this Gram-positive bacterium, and describes the clinical signs, pathology, epidemiology, diagnosis, and treatment of human infection with S suis.

Introduction Streptococcus suis is an important pathogen associated with a wide range of diseases in pigs, including meningitis, septicaemia, pneumonia, endocarditis, and arthritis.1 S suis can be transmitted to human beings by direct contact. The first human case of S suis was reported in Denmark in 1968.2 Human infection with S suis has become a serious zoonosis and has been reported in many countries with intensive swine production. More than 200 cases were reported worldwide before 2005, most of them from European and Asian countries and regions.3 In July, 2005, a large outbreak of human S suis infection occurred in Sichuan province, China, accompanied by several sporadic cases in other provinces. This was the third reported outbreak of human S suis infections that has occurred in China, with two earlier outbreaks occurring in Jiangsu province in 1998 and 1999. In the past 8 years in China, at least 237 people have been infected with S suis and 53 of them died.4–6 The repeated intensive outbreaks of human S suis infection have raised great public concern worldwide regarding S suis as an emerging zoonotic agent.

Biological features S suis is a Gram-positive facultative anaerobe, is coccoid or ovoid, and occurs as single cells, in pairs, or in short chains.7 Based on the capsular polysaccharides, 35 serotypes have been identified (types 1–34 and 1/2),7–11 but serotypes 32 and 34 have since been proven to be Streptococcus orisratti.12 Serotype 2 is most commonly associated with diseases in pigs and human beings, and is the most frequently reported serotype worldwide.13–15 Except for two human S suis infection cases caused by type 1 and one case of septicaemia caused by type 14, all other human S suis infections are attributed to type 2.16,17 The natural habitat of S suis is the upper respiratory tract, particularly the tonsils and nasal cavities, as well as the genital and alimentary tracts of pigs.18,19 S suis type 2 colonises the palatine tonsils of clinically ill and apparently healthy pigs, and is usually transmitted http://infection.thelancet.com Vol 7 March 2007

nasally or orally.20 Carriers of S suis are infectious to other pigs and are important in the transmission of this bacteria in herds.14 S suis type 2 is resistant to various environmental conditions. It can survive for 10 min at 60°C, 2 h at 50°C, and 6 weeks in carcasses at 10°C.21 At 0°C, this organism can survive for 1 month in dust and for over 3 months in faeces, whereas at 25°C, it can survive for 24 h in dust and for 8 days in faeces.21 However, S suis type 2 can be killed easily with 5% bleach at 1:799 dilution.21 S suis is sensitive to antibiotics, including penicillin, ceftriaxone, cephalosporin, ampicillin, and amoxicillin. Penicillin G is commonly used to treat or control infections caused by S suis. However, penicillin-resistant strains have been isolated,22,23 and strains highly resistant to other commonly used antibiotics have also been reported.24 The genome of S suis, which has been completely sequenced, contains 20 074 917 bp with a G+C content of 41·3%.25 Although the functions of 20–30% of the genes are unknown, many genes that may play a part in the pathogenesis of S suis infection have been studied, including polysaccharide production, capsular transport, iron-restriction factors, suilysin, virulence-associated proteins, various enzymes, arginine deiminase system, and IgG binding proteins.26–31 Studies on virulence factors of S suis are beginning to reveal the mechanism of this bacteria’s pathogenesis. The virulence of S suis differs among serotypes and between different strains of the same serotype. Most studies on the virulence of S suis have been done with serotype 2. Several virulence factors or candidates have been described, including capsule,28,32 muramidaserelease protein and extracellular protein factor,33–37 suilysin,38–43 and adhesins.44–46

Lancet Infect Dis 2007; 7: 201–09 Published Online January 12, 2007 DOI:10.1016/S14733099(07)70001-4 State Key Laboratory of Biocontrol and Center for Parasitic Organisms, School of Life Sciences, Zhongshan (Sun Yat-Sen) University, Guangzhou, China (Prof Z R Lun PhD, Q P Wang MPA, A X Li PhD); Institute of Tropical Medicine, Southern Medical University, Guangzhou, China (Prof X G Chen MD); and Department of Parasitology, College of Veterinary Medicine, South China Agricultural University, Guangzhou, China (Prof X Q Zhu PhD) Correspondence to: Professor Zhao-Rong Lun, Center for Parasitic Organisms, School of Life Sciences, Zhongshan (Sun Yat-Sen) University, Guangzhou 510275, China [email protected]

Identification S suis is able to grow in anaerobic or aerobic conditions, but is unable to grow in 6·5% NaCl solution.47 Colonies of S suis are small (0·5–1·0 mm diameter), greyish or transparent, and slightly mucoid.1 Most S suis strains 201

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Number of cases (%) Meningitis2,3,6,49,50,56,69–101 Septicaemia and septic shock*17,50,69,72,91,100–106

264 (72·5%) 88 (24·2%)

Arthritis†107–110

4 (1·1%)

Endocarditis†110–113

4 (1·1%)

Pneumonia†85,110,114

3 (0·8%)

Peritonitis†115 Total

1 (0·3%) 364 (100%)

*More than 80% of patients with septic shock died. †Data on these types were not available for the Sichuan outbreak.

Table 1: Types of infection in patients infected with S suis

produce narrow zones of α-haemolysis on sheep blood agar plates. S suis type 2 colonies produce α-haemolysis on sheep blood agar plates and β-haemolysis on horse blood agar plates.1 Presumptive identification based on four biochemical tests (Voges-Proskauer, salicin, trehalose, and 6·5% NaCl) can be successful for almost all capsular types of S suis.48 However, biochemical characteristics are so variable that identification is often difficult and may require a combination of biochemical reactions, followed by confirmative serotyping.49,50 The latter method is based on capsular polysaccharide antigens by use of one or more of the following techniques: capsular reaction,7–11,51 capillary precipitation,7 or a co-agglutination test.52 PCR is a rapid technique used to detect specific serotypes or strains of S suis in animal carriers, or to identify strains obtained from infected or healthy pigs, or even sick human beings for clinical diagnosis or epidemiology studies. PCR based on the S suis-specific 16S ribosomal RNA (rRNA) region and a species-specific probe (serotypes 1–31) targeting 16S rRNA gene can be used to identify S suis strains.53,54 A PCR procedure based on a 688 bp fragment within the glutamate dehydrogenase gene (gdh) of S suis type 2 was reported to efficiently amplify a specific fragment from all S suis strains tested.55 A multiplex PCR assay was also developed for this purpose for differentiating the strains.55 Type 2-specific PCR has been established for detection of S suis type 2 in human infection.56 Additionally, immunocapture method,9 fluorescent antibody techniques,57,58 whole-cell antigen-based indirect ELISA,59 and purified capsular polysaccharide antigen-based indirect ELISA60 have been developed. Phylogenetic analysis of 35 serotypes based on sequences of 16S rRNA gene and a viable region of the chaperonin 60 gene also revealed that serotypes 32 and 34 are distant from other serotypes,61,62 and were identified as S orisratti.12 Molecular methods such as RFLP,63 genome fingerprinting,64 pulsed-field gel eletrophoresis,65–67 and multilocus sequence typing68 have been used to study the genetic diversity of S suis strains, the colonial relations between the strains, and pathogenicity of particular clones. 202

Clinical signs in human infection Human infections with S suis are most frequently manifested as purulent meningitis, but reports of septic shock with multiple organ failure, endocarditis, pneumonia, arthritis, and peritonitis have also been reported (table 1). Differences in clinical signs among patients infected with S suis have been observed. In the acute form of meningitis, symptoms include high fever, headache, chills, nausea, vomiting, and vertigo, followed by one or more of the following: hearing loss, walking ataxia, coma, neck stiffness, petechia, articular pain, peripheral and facial paralysis, severe myalgia, ecchymosis, rashes, and rhabdomyolysis.56,69–71,116 In the acute form of toxic septic shock, besides high fever, chills, headache, vomiting, vertigo, and abdominal pain, other clinical signs were also observed, such as hypotension, tachycardia, liver dysfunction, subcutaneous haemorrhage (purpura fulminans; figure 1), disseminated intravascular coagulation, acute renal failure, and acute respiratory distress syndrome (table 2).17,69,71,119 Hearing loss is the most common sequela after recovery from purulent meningitis, whereas death often follows septic shock.

Figure 1: Clinical signs of subcutaneous haemorrhage found in a patient infected with S suis Reproduced from Yu et al117 with the permission of Centers for Disease Control and Prevention.

Pathology There are many descriptions of the pathological and histopathological lesions in pigs infected with S suis.1 The most common gross lesions are congestion of the meninges, lymph nodes, and lungs, and the most common histopathological finding is within the choroidal plexus. Evidence of encephalitis, oedema, and congestion of the brain may be present. In the central nervous system, lesions associated with meningitis and choroiditis may be observed, including oedema of the leptomeninges and the dura mater, hyperaemic meningeal blood vessels, and an increased quantity of cerebrospinal fluid (CSF). The most characteristic histopathological lesion of acute S suis meningitis is a diffuse neutrophilic infiltrate. An increased amount of CSF has also been reported in http://infection.thelancet.com Vol 7 March 2007

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human meningitis cases by lumbar puncture.70,119 By necropsy examination of patients who died from septic shock syndrome or meningitis syndrome, Zhu and colleagues50 reported gross lesions, including widespread haemorrhage, especially in stomach and adrenal glands, leptomeningeal congestion, oedema of cerebrum, hyperaemia of myocardium, disseminated intravascular coagulation, and lack of coagulation of whole blood, as well as septicaemia. Additionally, degeneration or necrosis of hepatocytes and kidney cells was observed.50 The pathological characteristics of the organs of sick pigs and of patients were similar.50 Number of cases (%) High fever

81 (100%)

Subcutaneous haemorrhage

75 (93%)

Disseminated intravascular coagulation

75 (93%)

Acute renal failure

66 (82%)

Chill

64 (79%)

Hypotension

62 (77%)

Vomiting

54 (67%)

Abnormal liver function

51 (63%)

Diarrhoea

42 (52%)

Headache

40 (49%)

Table 2: Clinical indications of 81 cases with septic shock syndrome71,100,117,118

S suis does not usually cause outbreaks of human infection. Sporadic cases have been reported in many countries that have intensive swine industry, after the first S suis human case described in Denmark in 1968.2 To date, most of the human infection cases have occurred in northern Europe and Asia (table 3 and table 4; figure 2). The total number of cases worldwide is well over 400. China, Thailand, and the Netherlands are responsible for 69%, 11%, and 8% of the total cases reported, respectively. Two large outbreaks of human infection were reported in rural regions of Jiangsu province during the summers of 1998 and 1999, with 25 reported cases, 14 of whom died from septic shock syndrome and meningitis.4,125 In July, 2005, the largest outbreak of S suis human infection occurred in Sichuan province of China. This outbreak caused 204 human infections and 38 deaths because of lack of appropriate or timely treatment. Sporadic cases were reported at the same time in other provinces and regions of the country, including four (one death) in Guangdong province and ten in Hong Kong. The causes of the two S suis human infection outbreaks in Jiangsu province as well as the S suis human infection outbreak in Sichuan province in 2005 have been reported by several groups.72,101,117 After a careful epidemiological analysis, these outbreaks were concluded to be closely related to a large outbreak of S suis infection in pigs, since all the 233 human cases occurred in the endemic regions of pig infection, and approximately 80 000 pigs

Epidemiology S suis is distributed worldwide and is most adapted to domesticated pigs, but is also occasionally recovered from wild boars, horses, dogs, and cats.1,120 S suis type 2 colonises the palatine tonsils of clinically ill and apparently healthy pigs.20 The symptomless carrier therefore represents a potential source of infection to herds or to human beings. Piglets are most susceptible, but infection can occur at any age.1 Predisposing factors are found in pigs raised in suboptimum conditions (eg, poor housing with inadequate ventilation). The situation can be further aggravated if pigs are raised under conditions that cause stress and subsequent immune suppression.1 Human infection is mainly caused by direct contact with carrier pigs, sick pigs, or raw pork contaminated with S suis via wounds on skin or mucosa of the mouth and nasal cavity.102 Therefore, human infection usually occurs in those people whose jobs are associated with pigs or pork, such as pig farmers, abattoir workers, meat-processing workers, and veterinarians.2,72,102,118,119,121 The infection rate of these people has been estimated to be 1500 times higher than that of the general population.2 Individuals who are immunosuppressed, including those who have had their spleens removed, are at increased risk, and human infection cases have been reported in such individuals.102,122–124 In some cases, hunters become infected when they come into contact with wild boars.119 Human S suis infection has been thought of as an occupational disease in some high-income countries. http://infection.thelancet.com Vol 7 March 2007

Cases

Deaths* (%)

283

54 (19·1%)

Thailand69,98,99,128

47

12 (26%)

Netherlands2,84,98,129

34

1 (3%)

China

4–6,71,72,77,87,97,110,125–127

UK 86,107,130

6

Germany70,119,131–133

6

1 1

Spain3,134

6

0

France49,82,102,135

5

1

Croatia16,136

4

2

Denmark2

3

0

Belgium80,85,137

2

1

Japan56,88

2

0

Italy94

2

0

USA138

1

0

Argentina92

1

0

Austria95

1

0

Canada139

1

0

Hungary140

1

0

Greece119

1

0

New Zealand105

1

0

Singapore116

1

0

Sweden79

1

Total

409

0 73 (17·8%)

*Percentage given only if number of cases is >20.

Table 3: Human beings infected with S suis worldwide, by country

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Cases

Deaths* (%)

Sichuan province5

204

38 (18·6%)

Hong Kong77,87,110,126

48

1 (2%)

Jiangsu province6,71,72

25

14 (56%)

Guangdong province141

4

1

Taiwan97,142

2

0

Total

283

Diagnosis and treatment Presumptive diagnosis of human S suis infection is based on clinical signs and microscopic lesions. Confirmation of infection is achieved by isolation of the infectious agents and the recognition of microscopic lesions in tissues. Epidemiology history, such as information about direct contact with sick pigs, is very useful for final confirmation. The detailed clinical signs and microscopic lesions have been discussed in previous sections. In addition to clinical information, the initial routine laboratory examination is essential for diagnosis of this disease.6,70,119 Patients infected with S suis display elevated white blood cell counts at 13·8–26·6×10⁹/L (81–95% neutrophils) and high C-reactive protein concentrations of 130–236 mg/L (normal value <10 mg/L).70,73,119 In some cases, high activities of alanine aminotransferase and aspartate aminotransferase were detected because of liver damage.119 Examination of patient’s CSF usually revealed turbidity, accompanied by polymorphonuclear pleocytosis (white blood cell count of 1·25–3·24×10⁹/L), and very low concentrations of protein and glucose.70,73,119 Gram stain of CSF, blood, and sometimes joint fluid, can show pairs or short chains of Gram-positive coccoid rods. The identification of the isolated infectious agent S suis is done by biochemical and serological procedures, and sometimes by molecular techniques. Type 2-specific PCR procedures that can identify S suis have been reported for the detection of S suis infection in human beings.56 S suis is sensitive to many antibiotics. Once the infectious agent of S suis is verified, antibiotic treatment, accompanied with other associated treatments, is very effective.

54 (19·1%)

*Percentage given only if number of cases is >20.

Table 4: Human S suis infection in China, by region

were estimated to be infected by S suis in this province at that time.50,72,143 Almost all the human patients had a history of direct contact with infected pigs or pork. Of the 205 patients investigated, 199 (97%) had contact with sick pigs, and among these 199 patients, 134 (67%) had slaughtered sick pigs and 100 (50%) had skin cuts.72,143 In another report, Du and colleagues6 mentioned that eight people who ate well-cooked pork from sick pigs did not develop clinical signs, indicating that people who ate properly cooked pork are unlikely to be at a risk of transmission. No person-to-person transmission occurred in these two outbreaks in Jiangsu province,6 or in the outbreak of human S suis infection in Sichuan province.117,143 Person-to-person transmission is unlikely to occur without very close contact with infected materials such as infected blood. To date, data from all epidemiological surveys on these outbreaks in China strongly indicate that direct contact with sick pigs is necessary for S suis infection.

USA 1 2

Canada

0 cases <10 cases >20 cases >200 cases

36 5 4 7 8 9 12 11

USA

10 13

Japan

China

Jiangsu Sichuan Hong Kong

Thailand Singapore

Argentina New Zealand

Figure 2: Countries or regions where S suis human infection cases have been reported 1=Sweden; 2=Denmark; 3=UK; 4=Belgium; 5=Germany; 6=Netherlands; 7=France; 8=Hungary; 9=Austria; 10=Croatia; 11=Italy; 12=Spain; 13=Greece.

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Therapeutic treatment varies between patients, depending on the clinical signs. After confirmation of infection, patients are commonly treated with penicillin G, accompanied by one or more other antibiotics including ceftriaxone, gentamicin, chloramphenicol, and ampicillin. The dosage of antibiotic varies. For less severely ill patients, intravenous administration of 4 million units of penicillin G every 6 h or 2 g ceftriaxone every 12 h for at least 10 days is effective.73,119 For severe cases, intravenous administration of 2 g ceftriaxone every 6 h or 2 g ceftriaxone every hour is not always effective,17,102 and multiple antibiotics are usually given. Antibiotic treatment consisting of 2 g ceftriaxone, 6 g ampicillin, and 240 mg gentamicin per day for 14 days was given to a 51-year-old man.70 Zhang and colleagues71 treated 22 patients with intravenous administration of high doses of penicillin G at 12–14 million units per day and dexamethasone 10–15 mg per day in combination with chloramphenicol or other antibiotics. For severely ill patients who developed septic shock syndrome, antibiotic treatment had limited effect.71 Additional intensive supportive care and treatments, such as maintenance of blood glucose concentrations at 4–6 mmol/L, selective digestive-tract decontamination, strategies for prevention of iatrogenic infection, and intravenous immunoglobulin against shock were required.71,144 Septic shock syndrome may lead to severe damage of organs, including liver, kidneys, and circulatory system, and therefore, mortality can be high (more than 70%) despite adequate treatments.

Prevention and control Because the main infectious sources are sick pigs, prevention of transmission to human beings depends on the control of sick animals. Various types of vaccines have been developed for pigs, with varied protective efficacy. Vaccination with purified capsule vaccine failed to protect swine from S suis type 2.145 Mice immunised with purified suilysin vaccine from S suis type 2 were completely protected against challenge with the virulent S suis type 2 strain from which the vaccine originated.42 However, this vaccine could not effectively protect immunised pigs against S suis type 2.43 In other experiments, vaccination with virulent, avirulent, or formalin-killed virulent S suis type 2 gave variable results.1 The vaccine commonly used in the pig industry, however, remains the inactivated autogenous vaccine generated from virulent strains isolated from sick pigs.146 One of the disadvantages of autogenous vaccines is the absence of safety and efficacy data. Therefore, each new batch of an autogenous vaccine should be tried out on animals and critically assessed before it is used on a larger scale. Although the use of inactivated autogenous vaccine is empirical, this vaccine can protect healthy pigs from S suis infection and prevent the spread of this disease in herds during outbreaks of S suis infection. Outbreaks of human S suis infection mainly occur in low-income countries with intensive pig production. http://infection.thelancet.com Vol 7 March 2007

In these countries, control of S suis infection in pigs is compromised because of poor husbandry conditions, including dirty, moist, and poorly ventilated housing, and contaminated drinking water or food. Therefore, improvement of pig-raising conditions and vaccination of pigs are both effective methods to decrease the outbreak of S suis infection, which in turn reduces the risk of human infection. At present, there is no S suis vaccine for human beings. Therefore, in serious outbreak situations, strict controls on animal trading and slaughtering are essential measures for curbing transmission from pigs to human beings. Furthermore, increasing awareness of the disease within populations that are at high risk is also expected to help avoid human infection. Education should be extended to everyone who prepares and cooks pork, including those doing so in their homes. Those with open wounds should wear gloves when handling raw or uncooked pork, and all those who prepare pork should wash their hands and clean their utensils thoroughly after contact. Adequate cooking is also essential. WHO recommends that pork should be cooked to reach an internal temperature of 70°C or until the juices are clear rather than pink.

Conclusions S suis is an increasingly important pathogen, causing meningitis, septicaemia, arthritis, and endocarditis in both pigs and human beings. S suis can naturally colonise the respiratory tract, especially the tonsils, of pigs. Carriers play an important role in the transmission of S suis within herds and sometimes to human beings. Although the virulence factors of S suis are yet to be firmly established, various methods for identification of strains of S suis have been developed, comprising biochemical, serological, molecular, and other techniques. These methods are helpful in identifying the infectious agent, and can help people take quick measures to control outbreaks of S suis infection in both pigs and humans beings. People infected with S suis present with various clinical signs. Purulent meningitis has been the most frequently observed manifestation in patients. Septic shock occurs in some patients and causes high mortality. Pathological changes in infected patients are often found, and they are similar to those seen in pigs. Quick diagnosis and adequate treatment are vital to decrease the damage to patients caused by S suis. Antibiotic treatments are effective when associated supportive measures are taken. Sporadic human infections by S suis have been reported worldwide. However, outbreaks of human infection are infrequent. The recent outbreaks of human S suis infection in China might have been caused by the following factors: (1) poor pig-raising houses, which make pigs susceptible to S suis outbreaks; (2) pig farmers or butchers who have direct contact with sick pigs or raw pork; (3) eating undercooked pork from sick pigs; 205

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Search strategy and selection criteria Literature searches were done predominantly using the following databases: Medline (PubMed; http://www.ncbi. nlm.nih.gov), CNKI (http://www.cnki.net), Wanfang Data (http://www.wangan.calis.edu.cn), WHO (http://www.who. int/en), and ScienceDirect (http://www.sciencedirect.com). Search terms included were “Streptococcus suis”, “Streptococcus suis infection”, “human Streptococcus suis infection”, “human Streptococcus suis infection and epidemiology”, and “Zhulianqiujun”. Relevant articles or book chapters in English and Chinese were mostly considered but some references in other languages were also considered. The final search date was August, 2006.

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(4) delayed diagnosis and treatment; (5) highly virulent strains of S suis type 2 involved in the outbreaks; and (6) poor coordination and cooperation among the responsible government departments. The key to preventing people from acquiring S suis infection is the avoidance of direct contact with sick pigs or infected carrier pigs. For high-risk groups, the wearing of gloves and respirators is essential when in close contact with sick pigs or raw pork. In endemic regions, education on S suis and human S suis infection is helpful in increasing awareness of human S suis infection both in patients and physicians.

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Conflicts of interest We declare that we have no conflicts of interest.

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Acknowledgments We thank Y C Zhong, J Wang, and R L Owen for their critical review of the manuscript. The authors’ laboratories were supported in part by grants from the Ministry of National Education (DPCKSCU/IRT0447), Sun Yat-Sen (Zhongshan) University (#3253280), the Natural Science Foundation of Guangdong Province (#036606 and #04105510), the National Science Foundation of China (#30570245) to ZRL, the China National Science Funds for Distinguished Young Scientists (#30225033) to XQZ, and the Department of Scientific and Technology of China (2003BA712A03-07) to XGC. References 1 Staats JJ, Feder I, Okwumabua O, Chengappa MM. Streptococcus suis: past and present. Vet Res Commun 1997; 21: 381–407. 2 Arends JP, Zanen HC. Meningitis caused by Streptococcus suis in humans. Rev Infect Dis 1988; 10: 131–37. 3 Geffner Sclarsky DE, Moreno MR, Campillo Alpera MS, Pardo Serrano FJ, Gomez GA, Martinez-Lozano MD. Streptococcus suis meningitis. An Med Interna 2001; 18: 317–18. 4 Wang YH, Dong DP, Xie Q, Wang DX, Han LZ, Ni YX. Analysis of infectious syndrome caused by Streptococcus suis type 2. Jiangsu Med J 2005; 31: 419–20 (in Chinese). 5 Ministry of Health of People’s Republic of China. Report of human Streptococcus suis in Sichuan (in Chinese). http://www.moh.gov.cn/ newshtml/10317.htm (accessed Dec 12, 2006). 6 Du YP, Qian WJ, Xu GB. Investigation on 8 human cases with meningitis caused by Streptococcus suis type 2. Chin J Prev Med 2000; 34: 305 (in Chinese). 7 Gottschalk M, Higgins R, Jacques M, Mittal KR, Henrichsen J. Description of 14 new capsular types of Streptococcus suis. J Clin Microbiol 1989; 27: 2633–36. 8 Gottschalk M, Higgins R, Jacques M, Beaudoin M, Henrichsen J. Characterization of six new capsular types (23 through 28) of Streptococcus suis. J Clin Microbiol 1991; 29: 2590–94.

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