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1、VECTOR-BORNE AND ZOONOTIC DISEASESVolume XX, Number XX, 2019 Mary Ann Liebert, Inc.DOI: 10.1089/vbz.2018.2399Streptococcus suis Meningitis: Epidemiology, Clinical Presentation and TreatmentMaria Hlebowicz, Pawe Jakubowski, and Tomasz SmiataczAbstractStreptococcus suis, a prevalent porcine pathogen,
2、may sporadically cause infections in humans, and has recently emerged as a cause of zoonoses in some professionals. The aim of this article was to review available data on epidemiology, etiopathogenesis, diagnostics, and management of the most common form of S. suis infection, purulent meningitis. L
3、iterature data show that S. suis is an important etiological factor of purulent meningitis, especially in subjects being occupationally exposed to contact with pigs and/or pork meat. Owing to growing incidence of S. suis meningitis, a history of such exposure should be verified in each patient prese
4、nting with typical meningeal symptoms. Whenever S. suis was confirmed as the etiological factor of purulent meningitis, therapeutic protocol should be adjusted appropriately, to avoid patients exposure to potentially ototoxic antimicrobial agents and corticosteroids. Considering the biphasic charact
5、er of S. suis meningitis and its frequently atypical outcome, all individuals with this condition should be optimally supervised by a multi- disciplinary team, including an ENT specialist.Keywords: Streptococcus suis, meningitis, therapy, diagnostics, occupational diseaseIntroductionStreptococcus su
6、is, a prevalent porcine pathogen, may sporadically cause infections in humans, and has recentlyemerged as a cause of zoonoses in some professionals. Pa- tients infected with S. suis typically present with meningitis, arthritis, and/or sepsis. Main risk groups for S. suis infection are subjects being
7、 occupationally exposed to pigs and/or pork, for example, farmers, butchers, meat sellers, foresters, and hunters.The aim of this article was to review available data on epidemiology, etiopathogenesis, diagnostics, and manage- ment of the most common form of S. suis infection, purulent meningitis.Mi
8、crobiology of S. suisS. suis is a heterogeneous Gram-positive bacterium. This facultative anaerobe, spherical or ovoid in shape, typically presents in pairs or as short chains. Another specific feature ofS. suis is the presence of alpha hemolysis on selective media enriched with horse blood (Staats
9、et al. 1997, Feng et al. 2014). The lack of growth in 6.5% NaCl agar, negative result of Voges-Proskauer test, and synthesis of acid from trehaloseor salicin are sufficient to consider an alpha-hemolytic Gram- positive coccus as a S. suis isolate (Goyette-Desjardins et al. 2014, Okura et al. 2016).
10、However, more accurate identifi- cation requires additional biochemical tests: for arginine dihydrolase (positive result), production of acid from lac- tose, sucrose, and inulin (positive result) and synthesis of acid from glycerol, mannitol, and sorbitol (negative result) (Goyette-Desjardins et al.
11、 2014, Okura et al. 2016).S. suis is a very common swine pathogen, isolated from upper airways (predominantly tonsils and nasal cavity), gas- trointestinal tract, and genitals of pigs. Markedly less often,S. suis may be also isolated from other species like horses, dogs, and cats. Apparently, some p
12、orcine strains of S. suis have evolved and become potent human pathogens, as well (Staats et al. 1997, Gottschalk and Segura 2000, Huang et al. 2005). Although to this date, a total of 35 various serotypes ofS. suis have been identified based on the heterogeneity of their capsular antigens, it is se
13、rotype 2 (SS2) that plays a crucial role in the pathogenesis of human infections (Gottschalk et al. 2007, Wertheim et al. 2009). Other serotypes, less often isolated from humans, are SS1, SS4, SS5, SS14, SS16, and SS24 (Arends and Zanen 1988, Mai et al. 2008, Nghia et al. 2008, Haleis et al. 2009, K
14、erdsin et al. 2009, 2011, Gus- tavsson and Ramussen 2014). However, this serotype-basedDownloaded by East Carolina University from at 03/13/19. For personal use only.Department of Infectious Diseases, Medical University of Gdansk, Gdansk, Poland.1STREPTOCOCCUS SUIS MENINGITIS5Downloaded by East Caro
15、lina University from at 03/13/19. For personal use only.classification raises some controversies. Some authors who documented the presence of S. suis-like strains, which although satisfied the previously mentioned biochemical taxonomic criteria, were shown to be genetically distinct entities (Hill e
16、t al. 2005, Tien le et al. 2013, Ishida et al. 2014, Baig et al. 2015, Nomoto et al. 2015, Okura et al. 2016). Hence, molecular methods have been used increasingly to ultimately confirm the identity of presumable S. suis isolates (see, Okura et al. 2016). Using a molecular approach, namely multilocu
17、s sequence typing, SS2, the most common cause of human infections among S. suis serotypes, has been classified into at least 16 sequence types (STs), some of which form clonal complexes (King et al. 2002, Goyette-Desjardins et al. 2014).A number of S. suis virulence factors have been identified to d
18、ate. They can be classified into four main categories: (1) surface/secreted elements, (2) enzymes/proteases, (3) tran- scription factors/regulatory systems, and (4) transporters/se- cretion systems (Feng et al. 2014). Based on the profile of their virulence factors, S. suis strains are classified as
19、 highly pathogenic, weakly pathogenic (hypovirulent), and non- pathogenic (avirulent) (Feng et al. 2014). The most promi- nent and best characterized virulence factors of S. suis are surface and secreted elements: capsular polysaccharides, muramidase-released protein, and a 38 kDa surface protein, s
20、uilysin (SLY) (Wilson et al. 2007). Although the list of confirmed and putative virulence factors is extensive (see, Fittipaldi et al. 2012, Segura et al. 2017) and at least 37 of them are claimed to be critical, the role of many still has not been verified appropriately.Epidemiology of S. suis Infe
21、ctionsS. suis was first identified as an etiological factor of human infections in 1968 (Wertheim et al. 2009), and since then a total of *1600 cases of zoonoses caused by this pathogen have been reported in *30 countries in Europe (Austria, Belgium, Croatia, Denmark, France, Germany, Greece, Hungar
22、y, Ireland, Italy, the Netherlands, Poland, Portugal, Spain, Sweden, and United Kingdom), Asia (China, Hong Kong, India, Japan, Korea, Laos, Philippines, Singapore, Taiwan, Thailand, and Vietnam), North America (Canada and United States), South America (Argentina, Chile, and French Guiana), Australi
23、a, and New Zealand (Shneerson et al. 1980, Robertson 1986, Yen et al. 1994, Kay et al. 1995, Michaud et al. 1996, Staats et al. 1997, Spiss et al. 1999, GeffnerSclarsky et al. 2001, Kopic et al. 2002, Ibaraki et al. 2003, Rosenkranz et al. 2003, Teekakirikul and Wiwanitkit 2003, Suankratay et al. 20
24、04, Huang et al. 2005, Hui et al. 2005, Lopreto et al. 2005, Willenburg et al. 2006, Yu et al. 2006, Gottschalk et al. 2007, Camporese et al. 2007, Lun et al. 2007, Lee et al. 2008, Ma et al. 2008, Mai et al. 2008, Manzin et al. 2008, van de Beek et al. 2008, Fittipaldi et al. 2009, Wertheim et al.
25、2009a, 2009b, Feng et al. 2010, Huh et al. 2011, Nghia et al. 2011, Demar et al. 2013, Koch et al. 2013, Zalas-Wiecek et al. 2013). Although a majority of these cases were sporadic infections, two outbreaks of S. suis SS2 epidemics were reported from China (Huang et al. 2005, Ye et al. 2006, Yu et a
26、l. 2006, Lun et al. 2007, Feng et al. 2009, 2010, Ma et al. 2009), and this bacterium was shown to occur endemically in Thailand and Vietnam (Teekakirikul and Wiwanitkit 2003, Suankratay et al. 2004, Mai et al. 2008,Wertheim et al. 2009a, 2009b, Kerdsin et al. 2009, 2011, Nghia et al. 2011, Ngo et a
27、l. 2011). All this points to S. suis as a potential public health threat.Relatively more frequent occurrence of human S. suis in- fections in Asian countries points to a potential geographical tropism of this pathogen that probably should be attributed not only to the specific climate but also to th
28、e leading role of pork industry and popularity of pork dishes in this area (see Risk Factors, Risk Groups, and Routes of Infection section) (Feng et al. 2014). Most European cases of S. suis infections in humans were reported from the Netherlands (n = 41), the United Kingdom (n = 15), and Denmark (n
29、 = 12), and zoo- noses caused by this pathogen occurred only sporadically in the remaining countries (Wertheim et al. 2009a). One specific feature of the European isolates of S. suis is their predilection to the meninges and frequent involvement in the etiology of purulent meningitis (Feng et al. 20
30、14). S. suis infections have been relatively rarely documented in the United States and Canada, two potent players in the global swine market (Donsakul et al. 2003, Heidt et al. 2005, Gottschalk et al. 2007). Recent evidence suggests that the latter phenomenon may be at least partially explained by
31、different structure of the Northern American S. suis STs. Although most S. suis found in Asia and Europe were highly virulent ST1 isolates, the intermediate-virulence ST25 and ST28 strains seem to prevail in the United States and Canada (Goyette-Desjardins et al. 2014, Athey et al. 2015).Risk Factor
32、s, Risk Groups, and Routes of InfectionLiterature evidence suggests that the principal risk group for S. suis infection are individuals exposed to pigs and pork meat, usually in an occupational setting. The following groups can be identified as particularly predisposed to S. suis infection: farmers,
33、 slaughterhouse workers, butchers, and meat sellers (Dupas et al. 1992, Staats et al. 1997, Charland et al. 2000, Lalonde et al. 2000). However, there is also ev- idence of occupational S. suis infection in which wild boars were the source of the pathogen, for example, for foresters and hunters (Ros
34、enkranz et al. 2003). The susceptibility to infection does not seem to be age and sex specific, as zoo- noses caused by S. suis were reported in 30- to 70-year-old subjects, both men and women (Feng et al. 2014).The aim of a casecontrol study conducted in Vietnam (Nghia et al. 2011) was to identify
35、the risk factors for S. suis meningitis using a subset of 100 patients with this type of infection and a group of matched hospital (n = 303) and community controls (n = 300). The study identified con- sumption of dishes containing undercooked, raw pork, swine intestines, and porcine blood, occupatio
36、nal exposure to pigs and pork, and presence of skin injuries while dealing with pigs and pig meat as independent risk factors for S. suis in- fection (Nghia et al. 2011). According to some authors, the incidence of S. suis zoonoses is higher in summer (Ma et al. 2008). Others showed that swine indus
37、try workers constitute up to 60% of patients infected with this pathogen (Hui et al. 2005), and researchers from the Netherlands demonstrated that occupational exposure to pigs is associated with up to 1000-fold increase in the risk for S. suis infection (Halaby et al. 2000). However, there are also
38、 published reports on the occurrence of S. suis infections in subjects who have never had any contact with swine or consumed the high-risk rawDownloaded by East Carolina University from at 03/13/19. For personal use only.pork dishes (Kopic et al. 2002, Manzin et al. 2008, van de Beek et al. 2008, Fi
39、ttipaldi et al. 2009).Nevertheless, the abovementioned findings, as well as the evidence from many published case reports, imply that typ- ically S. suis zoonoses result from a wound infection or in- gestion of pork contaminated with this pathogen. This was also confirmed in a recent meta-analysis b
40、ased on three studies with a total of 1454 cases reported, which identified raw pork consumption, exposure to pigs or pork, pig-related occupation, and male sex as significant risk factors for S. suis infection (Rayanakorn et al. 2018).Regarding the route of transmission, a growing body of evidence
41、suggests that S. suis can be an airborne pathogen.S. suis was shown to survive in feces for up to 104 days (Clifton-Hadley and Enright 1984), and an airborne trans- mission of this pathogen has been demonstrated in experi- mental studies in pigs (Berthelot-Herault et al. 2001, Madsen et al. 2001). T
42、hose findings were more recently confirmed by Bonifait et al. (2014), who detected S. suis in the aerosol from the swine confinement buildings and in the nasal swabs from 58% of pork producers, taken before the work shift.Purulent Meningitis as the Most Common Form of S. suis Infection in HumansAcco
43、rding to literature, the most common forms of zoo- notic S. suis infections are meningitis and sepsis (Suankratay et al. 2004, Wertheim et al. 2009b). The first reported case ofS. suis meningitis was diagnosed in Denmark in 1968 (Staats et al. 1997). Since then, meningitis was shown to be the most c
44、ommon presentation of this infection in both Europe and Asia (84.6% and 75.2%, respectively), and sepsis turned out to be the second most common of S. suis-related zoonoses (15.4% and 18.6%, respectively) (Huang et al. 2005). Other, less often reported clinical forms of S. suis infection include ent
45、eritis, arthritis, endocarditis, pneumonia (predominantly an opportunistic one), spondylodiscitis, endophthalmitis, uveitis, and peritonitis (Huang et al. 2005). Also in a large retrospective analysis of patients from Hong Kong hospital- ized owing to S. suis infection, primary clinical manifesta- t
46、ions were meningitis (48%), sepsis (38%), and endocarditis (14%) (Ma et al. 2008).S. suis can be also an etiological factor of streptococcal toxic shock-like syndrome (STSLS). A few cases of STSLS caused by S. suis have been described in various countries thus far, primarily in pig farmers (Gomez et
47、 al. 2014, Ya- manaka et al. 2015, Mancini et al. 2016, Kim et al. 2018). According to literature, this condition, characterized by shock, multiorgan failure, rapidly progressive soft-tissue in- fection, and high fatality, may be caused by some S. suis isolates that release more proinflammatory cyto
48、kines than others (Ye et al. 2009).Usually, S. suis infection starts with the typical meningeal signs, such as fever, headache, nausea, and vomiting, and neurological symptoms, such as dizziness, balance disorders, and limb trembling. The results of central nervous system imaging are normal in most
49、cases. The diagnosis of purulent meningitis can be confirmed based on cerebrospinal fluid (CSF) examination and CSF and blood culturing. Most pa- tients respond well to broad-spectrum intravenous antibiotics such as penicillin, ampicillin, amikacin, or cefotaxime. Usually a spectacular improvement of general and neuro-logical status is observed within a few days/week