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Shigella
CHAPTER ELEVEN
Shigella Steven L. Percival*, David W. Williams** *
Professor of Microbiology and Anti-infectives, Surface Science Research Centre and Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool, UK Professor of Oral Microbiology, Tissue Engineering & Reparative Dentistry, School of Dentistry, Cardiff University, Heath Park, Cardiff, UK **
BASIC MICROBIOLOGY Shigellae are Gram-negative, non-motile rod-shaped bacteria. As a group they do not produce gas from carbohydrates and they reside in the family Enterobacteriaceae demonstrating very similar characteristics to Escherichia coli. Unlike other members of the Enterobacteriaceae group, shigellae are non-lactose fermenting on MacConkey agar or desoxycholate citrate agar after an incubation period of 24 hours (h). Shigellae, by definition, are non-motile and do not decarboxylate lysine or hydrolyze arginine. Except for Shigella sonnei, certain serovars within the other species, and certain strains within these serovars, they do not produce gas from glucose or decarboxylate ornithine, nor do they use sodium acetate or produce indole from tryptophan.
NATURAL HISTORY Kiyoshi Shiga first documented Shigella in 1898 (Shiga, 1898). However, there is evidence that Ogata (1892) in Japan and Chantemesse and Widal (1888) in France may have actually isolated Shigella much earlier. The genus name Shigella was published in 1919 (Castellani and Chalmers, 1919). Numerous publications on Shigella occurred after this date with a significant paper on its grouping documented in 1954 (Enterobacteriaceae Subcommittee, 1954; Rowe and Gross, 1981). Shigella, based on both biochemical and serological evidence, can be classified into 4 major serological groups, namely: Group A, Shigella dysenteriae, which includes at least 10 serotypes; Group B, Shigella flexneri, includes six serotypes; Group C, Shigella boydii, which includes 15 serotypes; and Group D, Shigella sonnei, which includes only one serotype. The type species is S. dysenteriae 1.
METABOLISM AND PHYSIOLOGY Shigellae are facultatively anaerobic organisms that grow poorly under anaerobic conditions. The optimal temperature for the growth of Shigella is 37 C, in media Microbiology of Waterborne Diseases ISBN 978-0-12-415846-7, http://dx.doi.org/10.1016/B978-0-12-415846-7.00011-1
Ó 2014 Elsevier Ltd. All rights reserved.
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containing 1% peptone as carbon and nitrogen source (Holt et al., 1994). Shigellae are killed at a temperature of 55 C within 1 h (Rowe, 1990). Whilst shigellae are able to tolerate extremely acidic conditions (pH 2.5) for short periods they prefer to grow at neutral or slightly alkaline pH (pH 7.0–7.4).
CLINICAL FEATURES Apart from also occurring in chimpanzees and monkeys, bacillary dysentery is specifically a human disease characterized by a type of diarrhoea in which the stools contain blood and mucus. In extreme cases, it becomes associated with heavy inflammation of the colonic mucosa. Shigellosis, principally a self-limiting disease in healthy adults, has been known to cause fatalities particularly in young children (Salyers and Whitt, 1994). Shigellae are transmitted by the direct faecal–oral route, with infected individuals typically excreting 105–109 shigellae per g of wet faeces, with symptomless carriers excreting 102–106 per g (Dale and Mata, 1968; Thomas, 1955). Because of this, food can potentially be contaminated through the soiled fingers of patients or carriers. The transfer of shigellae by flies breeding on faeces has been established as a very important transmission route during some outbreaks. In a study of endemic shigellosis in Bangladesh, 2.1% of children aged 5 years and under, were found to be asymptomatic carriers (Hossain et al., 1994). Similar results were reported from Mexico where 55% of infants, 2 years of age and under, infected with Shigella were asymptomatic (Guerrero et al., 1994). The severity of disease due to Shigella depends on the virulence of the infecting strain, aside from the host’s immune system. The disease caused by S. sonnei tends to be mild and of short duration whereas that caused by S. flexneri tends to be more severe. Shigella boydii and S. dysenteriae produce disease of varying severity, but S. dysenteriae has often caused epidemics of severe infections. The infective dose for Shigella is generally quite low when compared with other pathogens such as E. coli and Vibrio cholera. The median infective dose (ID50) for Shigella is around 104 cells (Du Pont et al., 1972) in healthy adults compared to V. cholera, which is around 107 cells or higher. Shaughnessy et al. (1946) found that a dose of 108 organisms of S. flexneri were required to induce disease in volunteers who had previously ingested 2 g of sodium bicarbonate. The incubation period following ingestion of Shigella ranges from 36–72 h, but can be as short as 12 h, with frank dysentery appearing within 2 days. Symptoms of shigellosis usually develop suddenly, often as abdominal colic followed by watery diarrhoea, which may be accompanied by fever and malaise. Some individuals go on to develop abdominal cramps, tenesmus and the frequent passage of small volumes of stool (bloody mucus). Symptoms of dysentery can last for about 4 days. In severe cases, symptoms lasting up to 10 days have been documented. Patients who are recovering
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from infection often continue to excrete Shigella for a month following infection. There is documented evidence that some patients can still excrete Shigella for over a year following recovery (Du Pont et al., 1970). This carriage may be more important under conditions of poor hygiene. Shigellae are known to produce an exotoxin, initially described as a neurotoxin, but it also has a fluid transuding effect on the intestinal mucosa. To date, the role of the toxin in the pathogenesis of dysentery is uncertain. Shigella dysenteriae type 1 is responsible for many cases of haemolytic uraemic syndrome (HUS; which was first described in 1955; Gasser et al., 1955), accompanying outbreaks of dysentery and in some parts of the world is one of the commonest forms of acute renal failure in children. Although an invasive disease, infecting shigellae usually do not reach tissue beyond the lamina propria and, therefore, they very rarely cause bacteraemia or systemic infections except under very special circumstances (Struelens et al., 1985).
Pathogenicity and Virulence The two main virulence factors of Shigella are their invasive techniques and toxigenic properties; however, the exact role of the toxin produced by Shigella has yet to be defined. As with most enteric pathogens the first step in the invasion of host cells by shigellae, as demonstrated in HeLa cells, is attachment. In the case of Shigella this process does not seem to be mediated through interaction with a specific receptor (Clerc and Sansonetti, 1987). However, there is mounting evidence suggesting that the invasion plasmid antigen (Ipa) D may be involved as an adhesive. The proteins, IpaB and IpaC, encoded by genes located on the virulence plasmid, have been found on the bacterial surface, suggesting some importance in the pathogenicity of Shigella (Menard et al., 1994). It has been suggested that these two proteins are essential for phagocytosis. It is thought that the proteins rupture phagocytic vesicles allowing intracellular spread (ICS). ICS is mediated by two proteins, IcsA (also called VirG; Bernardini et al., 1989) and IcsB, which facilitate cell death and inflammatory response in the host cells. The process of cell death, induced by these proteins is as yet unknown, but seems to be independent of the production of Shiga toxin (Salyers and Whitt, 1994). Shigella dysenteriae is known to produce the aforementioned Shiga toxin, encoded on the chromosome, which belongs to the family of A1/B5 toxins. This Shiga toxin, whose main action is on blood vessels, is only released during cell lysis and is not actively secreted from the cell (Rowe, 1990).
Survival in the Environment Despite the public health significance of shigellae, their presence and persistence in the environment is not well documented when compared to other species in the family
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Enteriobacteriaceae. Humans are the only important reservoir of Shigella. Excretion of shigellae in stools is highest during the acute phase of dysenteric illness. During this phase the environment is contaminated and the organisms can survive for weeks in cool and humid locations (Rowe and Gross, 1981). The bacteria can survive for 5–46 days when dried on linen and kept in the dark, and for 9–12 days in soil at room temperatures (Roelcke, 1938). Although shigellae tolerate a low pH (<3) for short periods, they soon perish; but they will remain alive for days if specimens are kept alkaline and are prevented from drying (Rowe, 1990). Of all shigellae, S. sonnei appears to be most resistant to harsh conditions and this is certainly the case when compared with S. dysenteriae and S. flexneri. It has been shown that S. sonnei can survive for over 3 h on fingers and up to 17 days on wooden toilet seats (Huchinson, 1956). In a study by McGarry and Stainforth (1978), S. dysenteriae was shown to survive for up to 17 days in biogas plant effluent (11–28 C), but less than 30 h in the biogas plant itself (14–24 C). Shigella may be spread in aerosol droplets, possibly generated by flushing toilets and spray irrigation systems. A study by Newson (1972) showed that by flushing a suspension (1010 cells) of S. sonnei, an aerosol of about 39 bacteria per cubic metre of air was produced and that the Shigella could be recovered from the splashes and survive for up to 4 days. The effectiveness of sewage treatment plants in inactivating Shigella is limited. However, research has shown that Shigella removal is very similar to that of E. coli.
Survival in Water and Epidemiology Shigellosis outbreaks in water have been reported (Mandell et al., 1995; CDC, 1996; Alamanos et al., 2000; Simchen et al., 1991; Egoz et al., 1991; Samonis et al., 1994; Morera et al., 1995; Maurer et al., 2000; Alamonos et al., 2000). Whilst Shigella has been identified in surface waters, little is known about the distribution, survival and transmission of Shigella in surface waters. Dissemination of Shigella is highly significant in developing countries as a mode of transmission. As a rule, drinking water will not contain Shigella unless it is untreated or if there are problems with the water treatment process (Green et al., 1968). There have been studies on the survival of Shigella in water (Feachem et al., 1980). From this and a number of other studies, it has been found that survival of Shigella depends upon concentrations of other bacteria, nutrients, oxygen and temperature. Within clean water, survival times are less than 14 days at temperatures >20 C, but in waters <10 C, Shigella has been shown to survive for weeks. McFeters et al. (1974) showed that Shigella died more slowly in well water at 9–12 C than bacteria such as Salmonella and Vibrio cholera. Talayeva (1960) found that S. flexneri survived for up to 21 days in clean river water at temperatures of 19–24 C, up to 47 days in autoclaved river water, up to 9 days in well
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water, up to 44 days in autoclaved tap water and up to 6 days in polluted well water. Contrary to this McGarry and Stainforth reported in 1979 that S. dysenteriae could survive for 93 days in sterilized water at 11–28 C. Shrewsbury and Barson (1957) found that S. dysenteriae could survive for between 2.5 and 29 months in sterile but faecally contaminated water at 21 C. Infections with Shigella are often acquired by drinking water contaminated with human faeces or by eating food washed with contaminated water. Food borne outbreaks of shigellosis occur, especially in the tropics and less frequently in developed countries (Coultrip et al., 1977). In addition to contamination from faeces by food-handlers who have poor hygiene, flies may sometimes act as vectors in tropical countries (Khalil et al., 1994). There is evidence for Shigella infection acquired by swimming in sewage-contaminated recreational waters (Rosenberg et al., 1976; Makintubee et al., 1987; Sorvillo et al., 1988). In developed countries, infections are usually associated with recent travel to countries with insufficient sanitary facilities (Parsonnet et al., 1989; Lu¨scher and Altwegg, 1994). Outbreaks of Shigella infections have occurred in day-care centres associated with direct person-to-person transmission by the faecal–oral route, which are facilitated by the low infectious dose (10–200 organisms) necessary to induce infection. Shigellae are often the cause of laboratory-acquired infections (Aleksic et al., 1981; Grist and Emslie, 1989). Natural disasters and wars are frequently associated with shigellosis outbreaks and mass encampments become ‘breeding places’ for infection, causing a high incidence of illness and fatalities (Centers for Disease Control, 1994b; Sharp et al., 1995). Saeed et al. (2009) studied the interactions between S. dysenteriae or S. sonnei and Acanthamoeba castellanii. The study demonstrated that S. dysenteriae or S. sonnei grew and survived in the presence of the protozoa for more than 3 weeks. The authors concluded that the relationship between S. dysenteriae and S. sonnei with A. castellanii was symbiotic, and indicated that the amoebae may serve as a transmission reservoir for Shigella in water. Studies with volunteers have shown that fewer than 200 viable cells are needed to readily produce shigellosis (Crockett et al., 1996). A number of outbreaks, primarily food related, have been due to Shigella. These have included consumption of poi (Lewis et al., 1972), tuna (Bowen, 1980) and contaminated salads. In fact during 1961–1975 there were 10 648 cases (72 outbreaks) of shigellosis reported in the USA principally due to the consumption of contaminated salads (Black et al., 1978). The contamination of food is possibly the most important route of transmission of Shigella (Barrel and Rowland, 1979). Shigella dysenteriae 1 has caused major epidemics in Central America (1969–70), Bangladesh (1972) and East Africa (since 1991), whereas S. boydii is mainly prevalent in South Asia and the Middle East. In Europe and North America, S. sonnei is by far the most predominant species causing infections, followed by S. flexneri (Aleksic et al., 1987;
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Lee et al., 1991; Centers for Disease Control, 1994a). Infections due to S. boydii and S. dysenteriae are almost exclusively imported by travellers or foreign-born citizens returning from visits to their home countries (Aleksic et al., 1987). In the UK and the rest of Europe, S. dysenteriae, common during the First World War, is now rare. Between 1920 and 1930, both S. flexneri and S. sonnei were endemic and approximately equal in causing incidents, but by 1940 S. sonnei had become dominant, increasing in incidence annually to a peak of over 49 000 (99% of all shigellae notified) in 1956. The incidence of Sonne dysentery (caused by S. sonnei) then declined steadily in the UK to an annual average of about 3000 notified cases between 1970 and 1990. However, the numbers rose sharply in 1991 where there were several widespread community outbreaks and these continued to rise to a peak of 17 000 cases in 1992. The incidence has since fallen but there were still more than 4550 cases in 1995. Infections due to other shigellae, usually imported, have remained constant during the last decade at approximately 800–900 a year. Similar changes have taken place in the USA. Until 1968, S. flexneri and S. sonnei were equally common, but S. sonnei now accounts for 65% of cases and S. flexneri for about 30%. In tropical areas, shigellosis is endemic. It has been estimated that 5 million cases of shigellosis require hospital treatment; of these, about 600 000 die every year. There is general agreement in the literature that the maintenance of endemic shigellosis has little or no relationship to water quality, but that it is strongly related to water availability and associated hygienic behaviour. However, there will always be specific exceptions to this; for instance, Sultanov and Solodovnikov (1977) considered that the maintenance of dysentery was due to the widespread use of polluted surface water for domestic purposes. Some epidemics of bacillary dysentery are waterborne. An outbreak of 2000 cases of shigellosis due to S. sonnei occurred in 1966 in Scotland, UK when the chlorination plant on a town’s water supply failed (Green et al., 1968). During 1961–75, 38 waterborne outbreaks of shigellosis were reported in the USA (Black et al., 1978). Most of these outbreaks involved semi-public or individual water systems and were usually the result of inadequate or interrupted chlorination of water contaminated by faeces. Such waterborne epidemics are usually dramatic, but they can be terminated very quickly when the water supply is adequately treated. Rahman et al. (2011) isolated five bacterial strains serotyped as S. flexneri 2b from a freshwater lake in Bangladesh. The isolates possessed the ipaH virulence gene and a megaplasmid. He et al. (2012) investigated a shigellosis outbreak by comparing the source of drinking water, consumption of untreated water and food in an elementary school in China. The study concluded that the outbreak of shigellosis was caused by drinking untreated water from a polluted well.
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Godoy et al. (2011) investigated a waterborne outbreak in Lleida, Spain, following consumption of mains water, bottled water and spring water. The waterborne outbreak was caused by S. sonnei following contamination of the public water supply. Chen et al. (2001) reported on an outbreak of gastroenteritis which affected 730 students. Shigella sonnei and Entamoeba histolytica were isolated from the stool specimens of patients. Environmental investigations revealed that the source of infection was contamination of underground well water by sewage from a toilet. The outbreak ended with the closure of the well water supply. To avoid such problems, institutions and other groups that maintain their own wells, including schools and summer camps, need to be vigilant about maintenance and check for potential contamination.
EVIDENCE FOR GROWTH IN A BIOFILM Little is known about Shigella and its ability to form and survive in biofilms, which suggests the need for further research.
METHODS OF DETECTION Culturable Techniques In pure cultures, Shigella form circular, glistening, translucent or slightly opaque colonies on nutrient agar. It is able to grow on blood agar but with no haemolysis. The colony size varies with small colonies developed by S. dysenteriae, but most Shigella serovars produce colonies of 1–2 mm after 18–24 h of incubation at 37 C. Shigella sonnei may develop as smooth and larger, flatter colonies showing an irregular edge, often referred to as phase 1 colonies. ‘Phase 2’ colonies are associated with the loss of the 12 0000-14 0000 kDa virulence plasmid and a change of the antigenic specificity. Phase 2 strains still grow homogeneously in broth culture, but they may partially sediment after boiling at 100 C or autoagglutinate in 3.5% NaCl solution (Rowe, 1990; Bockemu¨hl, 1992). On Leifson’s deoxycholate citrate agar, Salmonella-Shigella agar, or xylose-lysine-deoxycholate and on MacConkey agar, shigellae grow as colourless, translucent, smooth colonies of 1–2 mm after 18–24 h of incubation at 37 C. After prolonged incubation (>48 h), growth of S. sonnei becomes pinkish due to delayed fermentation of lactose and sucrose. For the isolation of shigellae, a freshly passed stool specimen during the acute stage of illness is the material of choice. If present, mucus or bloodstained portions should be selected for culture and, if desired, for microscopic examination for the presence of faecal
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leucocytes. If the specimens cannot be cultured within 2–4 h, they should be preserved in a transport medium. Shigellae are easily overgrown by the concomitant aerobic intestinal flora. Enrichment of stool specimens in Gram-negative broth (Hajna) or selenite broth for about 6 h at 37 C can be tried. After growth on an appropriate agar, Shigella species can be identified by biochemical reactions, combined with agglutination in group- or serovar-specific antisera for shigellae.
Molecular Techniques Maheux et al. (2011) used a rapid, procedure combined with a DNA enrichment method (dubbed CRENAME – concentration and recovery of microbial particles, extraction of nucleic acids, and molecular enrichment), coupled to a Shigella-specific real-time PCR (RT-PCR) assay targeting the tuf gene, to detect Shigella in water. The authors compared this to the US Environmental Protection Agency (EPA) culture-based Method 1604 on MI agar in terms of analytical specificity, ubiquity, detection limit and rapidity. The CRENAME method provided an easy and efficient approach to detect Shigella. The authors concluded that the Shigella-specific RT-PCR assay was comparable to US EPA Method 1604 on MI agar in terms of analytical specificity and detection limit. However, CRENAME provided significant advantages in terms of speed and ubiquity. Hsu et al. (2007) developed a sensitive method for detection of S. sonnei in water. Thirty-three S. sonnei and 72 non-S. sonnei isolates were tested and one primer pair was found capable of specifically amplifying a 369-bp insertion sequence 1 (IS1) fragment from all S. sonnei isolates and one S. dysenteriae ATCC strain by PCR. PCR assays have been proposed to monitor the presence of Shigella. The uid chromosomal region was used to confirm the presence of Shigella species by Cleuziat and Robert-Baudouy (1990). Other genes, such as tuf (elongation factor Tu) or clpB (Cleuziat et al., 1990) and heat shock protein F84.1 have also been used to detect Shigella (Maheux et al., 2009; Clark et al., 2011. Clark et al. (2011) evaluated five oligonucleotide primers sets (ETIR, SINV, exoT, VS1 and ipaH2) for their potential applicability in qPCR assays to detect contamination from bacterial pathogens that included E. coli O157:H7, Salmonella typhimurium, Campylobacter jejuni, Pseudomonas aeruginosa, and S. flexneri. Zhou et al. (2011) investigated an oligonucleotide-based microarray using the sequences of 16S-23S rDNA internal transcribed spacer regions (ITS) and the gyrase subunit B gene (gyrB). Hsu et al. (2010) developed a procedure to detect Shigella species and Enteroinvasive Escherichia coli (EIEC) from environmental water samples using membrane filtration followed by nutrient broth enrichment, isolation using selective culture plates, and
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identification of the invasion plasmid antigen H (ipaH) gene by PCR. Of the 93 water samples from nine reservoirs and one watershed examined, 76 (81.7%) water samples tested culture positive for Shigella and five water samples were positive (5.4%) for Shigella. Maheux et al. (2009) evaluated nine different PCR primer sets to detect Shigella in water. Of the nine PCR primer sets tested, only the primer set targeting the tuf gene amplified DNA from all Shigella strains tested. Theron et al. (2001) developed a rapid seminested PCR method for the detection of virulent Shigella species in ‘spiked’ environmental water samples. A set of primers specific for the invasion plasmid antigen gene (ipaH) in Shigella species was used. The PCR procedure coupled with an enrichment culture detected as few as 1.6 S. flexneri organisms in pure culture.
ANTIMICROBIAL CONTROL In the literature, there is little information regarding the effectiveness of disinfectants on Shigella in relation to control in water. Wang et al. (2011) investigated ultraviolet (UV) light exposure, chlorine or UV followed by chlorine in municipal wastewater for the inactivation of E. coli, S. dysenteriae and toxicity formation. Positive results were achieved using all disinfection procedures. In addition, ozone has been shown to have positive effects on the inactivation of Shigella (Selma et al., 2007). Most cases of Shigella dysentery due to S. sonnei are mild and do not require any antibiotic treatment. Oral salt rehydration therapy is generally the best treatment regime. If antibiotics need to be administered, ampicillin, tetracycline, cotrimoxazole or ciprofloxacin are an appropriate choice. Antibiotics are usually administered because they shorten the duration of illness and decrease the relapse rate (Hruska, 1991). The first reported case of multiple-drug resistant Shigella in Japan occurred in 1956. To date, Shigella is acquiring resistance against many different drugs, constituting a major concern. For example, between 1979 and 1982 the percentage of resistant S. sonnei strains isolated in a hospital in Madrid increased from 39.6 to 97.9% for ampicillin, from 34.4 to 96.9% for co-trimoxazole (SXT), from 6.3 to 18.0% for tetracycline and from 1.6 to 15.1% for chloramphenicol (Lopez-Brea et al., 1983). The first SXT-resistant strain of S. dysenteriae type 1 in Bangladesh was isolated in 1982 (Shahid et al., 1985), with SXT resistance also evident in Finnish travellers (Heikkila¨ et al., 1990). Antibiotic therapy for the treatment of shigellosis should always be based on proper antibiotic susceptibility testing. If this is not possible, blind therapy should include a quinolone as the majority of strains are susceptible.
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RISK ASSESSMENT Health Effects: Occurrence of Illness, Degree of Morbidity and Mortality, Probability of Illness Based on Infection • Shigella can be classified into four major serological groups. Group A, S. dysenteriae, Group B, S. flexneri, Group C, S. boydii, and Group D, S. sonnei, which includes only one serotype. Shigella sonnei accounts for most cases in the developed world. • Shigella infection is characterized by watery or bloody diarrhoea, abdominal pain, fever and malaise. Symptoms of dysentery can last for about 4 days but in severe cases up to 10 days has been documented. Shigellosis is principally a self-limiting disease in otherwise healthy adults; it has been known to cause fatalities, particularly in malnourished infants. • Shigella dysenteriae type 1 is responsible for many cases of HUS. • The severity of disease depends on the virulence of the infecting strain, aside from the host’s immune system. The disease caused by S. sonnei tends to be mild and of short duration, whereas that caused by S. flexneri tends to be more severe. • Children and infants generally suffer a higher rate of infection and more severe disease course.
Exposure Assessment: Routes of Exposure and Transmission, Occurrence in Source Water, Environmental Fate • Shigellosis is specifically a human disease that is transmitted by the direct or indirect faecal–oral route. • Infections with Shigella species are often acquired by drinking water contaminated with human faeces or by eating food washed with contaminated water. Transfer of shigellae by flies has been very important during some outbreaks. • Helped by the low infectious dose (10–200 organisms) necessary to induce infection, person-to-person contact in day-care centres, institutions and other places where hygiene may not be the best have resulted in outbreaks. • Shigella can be found in surface waters and also within contaminated drinking water and this is significant as a mode of transmission in developing countries. • Within clean water, survival times are less than 14 days at temperatures >20 C, but in waters of less than 10 C, they have been shown to survive for weeks. They do not survive at acidic pH. • Shigella sonnei appears to be more resistant to detrimental environmental conditions than S. dysenteriae and S. flexneri. Shigella dysentaeriae has been shown to survive for at least 6 days in septic tank effluent.
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Risk Mitigation: Drinking Water Treatment, Medical Treatment • Drinking water treatment that includes disinfection is sufficient to remove Shigella. Waterborne outbreaks have generally resulted from inadequate treatment. • Most cases of Shigella dysentery (i.e., S. sonnei) are mild and do not require any antibiotic treatment. Treatment by means of rehydration oral salts is all that is required. Ampicillin, co-trimoxazole, tetracycline or ciprofloxacin are appropriate antibiotic choices.
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Crockett, C.S., Haas, C.N., Fazil, A., et al., 1996. Prevalence of shigellosis in the US: consistency with dose-response information. Int. J. Food Microbiol. 30, 87–99. Dale, D.C., Mata, L.J., 1968. Studies of diarrheal disease in Central America. XI. Intestinal bacterial flora in malnourished children with shigellosis. Am. J. Trop. Med. Hyg. 17, 397–403. DuPont, H.L., Hornick, R.B., Snyder, M.J., Libonati, J.P., Formal, S.B., Gangarosa, E.J., 1972. Immunity in shigellosis. I. Response of man to attenuated strains of Shigella. J. Infect. Dis. 125 (1), 5–11. DuPont, H.L., Hornick, R.B., et al., 1972. Immunity in shigellosis. II. Protection induced by live oral vaccine or primary infection. J. Infect. Dis. 125, 12–16. Du Pont, H.L., Gangarosa, E.J., Reller, L.B., et al., 1970. Shigellosis in custodial institutions. Am. J. Epidemiol. 92, 172–179. Egoz, N., Shmilovitz, M., Kretzer, B., et al., 1991. An outbreak of Shigella sonnei infection due to contamination of a municpal water supply in northern Israel. J. Infect. 22, 87–93. Enterobacteriaceae Subcommittee Reports, 1954. Int. Bull. Bacteriol. Nomencl. Taxon. 4, 1–94. Feachem, R.T.G.A., Bradley, D.J., Garelick, H., Mara, D.D., 1980. Health aspects of exceta and sullage management: A state of the art review. Appropriate technology for water supply and sanitation. The World Bank, Transportation, Water and Telecommunications Department, Washington, D.C vol. 2. Gasser, C., Gautier, E., Siebenmann, R.E., Oechslin, R., 1955. Ha¨molytisch-ura¨mische Syndrome: bilaterale Nierenrindennekrosen bei akuten erworbenen ha¨molytischen Ana¨mien. Schweiz. Med. Wochenschr. 85, 905–909. Godoy, P., Bartolome´, R., Torres, J., et al., 2011. Waterborne outbreak of Shigella sonnei caused by consumption of public supply water. Gac. Sanit. 25 (5), 363–367. Green, D.M., Scott, S.S., Mowat, D.A.E., et al., 1968. Waterborne outbreak of viral gastroenteritis and Sonne dysentery. J. Hyg. 66, 383–392. Grist, N.R., Emslie, J.A.N., 1989. Infections in British clinical laboratories, 1986–7. J. Clin. Pathol. 42, 677–681. Guerrero, L., Calva, J.J., Morrow, A.L., Velazquez, F.R., et al., 1994. Asymptomatic Shigella infections in a cohort of Mexican children younger than two years of age. Pediatr. Infect. Dis. J. 13, 597–602. Heikkila¨, E., Siitonen, A., Jahkola, M., Fling, M., et al., 1990. Increase of trimethoprim resistance among Shigella species. J. Infect. Dis. 161, 1242–1248. He, F., Han, K., Liu, L., et al., 2012. Shigellosis outbreak associated with contaminated well water in a rural elementary school: Sichuan Province, China, June 7–16, 2009. PLoS One. 7 (10), e47239. Hendricks, C.W., 1971. Enetric bacterial metabolism of stream sediment eluates. Can. J. Microbiol. 17, 551–556. Hossain, M.A., Hasan, K.Z., Albert, M.J., 1994. Shigella carriers among non-diarrhoeal children in an endemic area of shigellosis in Bangladesh. Trop. Geogr. Med. 46, 40–42. Hruska, J.F., 1991. Gastrointestinal and intraabdominal infections. In: Reese, R.E., Betts, R.F. (Eds.), A practical approach to infectious diseases, third ed. Little, Brown, Boston, pp. 305–356. Hsu, B.M., Wu, S.F., Huang, S.W., et al., 2010. Differentiation and identification of Shigella spp. and enteroinvasive Escherichia coli in environmental waters by a molecular method and biochemical test. Water Res. 44 (3), 949–955. Hsu, W.B., Wang, J.H., Chen, P.C., et al., 2007. Detecting low concentrations of Shigella sonnei in environmental water samples by PCR. FEMS Microbiol. Lett. 270 (2), 291–298. Huchinson, R.I., 1956. Some observations on the method of spread of Sonne dysentery. Monthly Bulletin of the Ministry of Health and the public health laboratory service 15, 110–118. Khalil, K., Lindblom, G.B., Mazhar, K., Kaijser, B., 1994. Flies and water as reservoirs for bacterial enteropathogens in urban and rural areas around Lahore, Pakistan. Epidemiol. Infect. 113, 435–444. Lee, L.A., Shapiro, C.N., et al., 1991. Hyperendemic shigellosis in the United States: a review of surveillance data for 1967–1988. J. Infect. Dis. 164, 894–900. Lewis, J.N., Loewenstein, M.S., Guthrie, L.C., Sugi, M., 1972. Shigella sonnei outbreak on the island of Maui. Am. J. Epidemiol. 96, 50–58. Lopez-Brea, M., Collado, L., Vicente, F., Perez-Diaz, J.C., 1983. Increasing antimicrobial resistance of Shigella sonnei. J. Antimicrob. Chemother. 11, 598.
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Lu¨scher, D., Altwegg, M., 1994. Detection of shigellae, enteroinvasive and enterotoxigenic Escherichia coli using the polymerase chain reaction (PCR) in patients returning from tropical countries. Mol. Cell. Probes. 8, 285–290. Maheux, A.F., Picard, F.J., Boissinot, M., et al., 2009. Analytical comparison of nine PCR primer sets designed to detect the presence of Escherichia coli/Shigella in water samples. Water Res. 43 (12), 3019–3028. Maheux, A.F., Bissonnette, L., Boissinot, M., et al., 2011. Rapid concentration and molecular enrichment approach for sensitive detection of Escherichia coli and Shigella species in potable water samples. Appl. Environ. Microbiol. 77 (17), 6199–6207. Maheux, A.F., Picard, F.J., Boissinot, M., Bissonnette, L., et al., 2009. Analytical comparison of nine PCR primer sets designed to detect the presence of Escherichia coli/Shigella in water samples. Water Res. 43, 3019–3028. Makintubee, S., Mallonee, J., Istre, G.R., 1987. Shigellosis outbreak associated with swimming. JAMA 236, 1849–1852. Mandell, G.M., Bennett, J.E., Dolin, R., 1995. Principles and practice of infectious diseases, fouth ed. Churchill Livingstone Inc., New York, USA. 2033–2035. Maurer, A., Stu¨rchler, D., 2000. A waterborne outbreak of small round structured virus, campylobacter and shigella co-infections in La Neuveville, Switzerland, 1998. Epidemiol. Infect. 125, 325–332. McFeters, G.A., Bissonnette, G.K., Jezeski, J.J., et al., 1974. Comparative survival of indicator bacteria and enteric pathogens in well water. Appl. Microbiol. 27 (5), 823–829. McGarry, M.G., Stainforth, J. (Eds.), 1978. Compost, fertilizer and Biogas production from human and farm wastes in the people’s rebublic of China. International Development Research Centre, Ottawa. Menard, R., Sansonetti, P., Parsot, C., 1994. The secretion of the Shigella flexneri Ipa invasins is activated by epithelial cells and controlled by IpaB and IpaD. EMBO J. 13, 5293–5302. Morera, M.A., Espejo, E., Coll, P., et al., 1995. Epidemic outbreak of shigellosis following water intake. Enferm. Infec. Microbiol. Clin. 13, 160–165. Newson, S.W.B., 1972. Microbiology of hospital toilets. Lancet 2, 700–703. Ogata, M., 1892. Zur a¨tiologie der Dysenterie. Zentralbl. Bakteriol. Parasitenkd Infektionskr. Hyg. 11, 264–272. Parsonnet, J., Greene, K.D., Gerber, A.R., et al., 1989. Shigella dysenteriae type 1 infections in US travellers to Mexico, 1988. Lancet 2, 543–545. Rahman, M.Z., Azmuda, N., Hossain, M.J., et al., 2011. Recovery and characterization of environmental variants of Shigella flexneri from surface water in Bangladesh. Curr. Microbiol. 63 (4), 372–376. ¨ ber die Resistenz verschiedener Ruhrkeime. Z. Hyg. Infektionskr. 120, Roelcke, K., 1938. U 307–314. Rosenberg, M.L., Hazlet, K.K., Schaefer, J., et al., 1976. Shigellosis from swimming. J. Am. Med. Assoc. 236, 1849–1852. Rowe, B., 1990. Shigella. In: Parker, M.T., Collier, L.H. (Eds.), Topley & Wilson’s Principles of bacteriology, virology and immunity, eighth edn, vol. 2. Edward Arnold, London, pp. 455–468. Rowe, B., Gross, R.J., 1981. The genus Shigella. In: Starr, M.P., Stolp, H., et al. (Eds.), 1981. The Prokaryotes, vol. II. Springer-Verlag, Berlin, Heidelberg and New York, pp. 1248–1259. Saeed, A., Abd, H., Edvinsson, B., Sandstro¨m, G., 2009. Acanthamoeba castellanii an environmental host for Shigella dysenteriae and Shigella sonnei. Arch. Microbiol. 191 (1), 83–88. Salyers, A.A., Whitt, D.D., 1994. Bacterial pathogenesis: a molecular approach, first edn. ASM Press, Washington, DC. Samonis, G., Elting, L., Skoulika, E., et al., 1994. An outbreak of diarrhoeal disease attributed to Shigella sonnei. Epidemiol. Infect. 112, 235–245. Selma, M.V., Beltra´n, D., Allende, A., Chaco´n-Vera, E., Gil, M.I., 2007. Elimination by ozone of Shigella sonnei in shredded lettuce and water. Food Microbiol. 24 (5), 492–499. Shahid, N.S., Rahaman, N.M., et al., 1985. Changing pattern of resistant Shiga bacillus (Shigella dysenteriae type 1) and Shigella flexneri in Bangladesh. J. Infect. Dis. 152, 1114–1119. Shaughnessy, D.J., Olson, R.C., Bass, K., et al., 1946. Experimental human bacillary dysentery. J. Am. Med. Assoc. 132, 362–368.
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Sharp, T.W., Thornton, S.A., et al., 1995. Diarrheal disease among military personnel during Operation Restore Hope, Somalia, 1992–1993. Am. J. Trop. Med. Hyg. 52, 188–193. Shrewsbury, J.F.D., Barson, G.J., 1957. On the absolute viability of certain pathogenic bacteria in a synthetic well water. J. Pathol. Bacteriol. 74, 215–220. Shiga, K., 1898. u¨ber den Dysenteriebacillus (Bacillus dysentericus). Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. 24, 817–828, 870–4, 913-18. Simchen, E., Jeeraphat, S., Shihab, S., Fattal, B., 1991. An epidemic of waterborne Shigella gastroenteritis in Kibbutzim of western Galilee in Israel. Int. J. Epidemiol. 20, 1081–1087. Sorvillo, F.J., Waterman, S.H., Mascola, L., Waterman, S.H., 1988. Shigellosis associated with recreational water contact. Am. J. Trop. Med. Hyg. 38, 613–617. Struelens, M.J., Patte, D., Kabir, I., et al., 1985. Shigella septicemia: prevalence, presentation, risk factors, and outcome. J. Infect. Dis. 152, 784–790. Sultanov, G.V., Solodovnikov, Y.P., 1977. Significance of water factor in epidemiology of dysentery. Zhurnal Mikrobiologii Epidemiologii Immunobiologii 6, 99–101. Talayeva, J.G., 1960. Survival of dysentery bacteria in water according to the results of a reaction with haptenes. Microbiol. Immunol. 4, 314–320. Theron, J., Morar, D., Du Preez, M., et al., 2001. A sensitive seminested PCR method for the detection of Shigella in spiked environmental water samples. Water Res. 35 (4), 869–874. Thomas, S., 1955. The numbers of pathogenic bacilli in faeces in intestinal diseases. J. Hyg. 53, 217–224. Wang, X., Hu, X., Hu, C., Wei, D., 2011. Sequential use of ultraviolet light and chlorine for reclaimed water disinfection. J. Environ. Sci. (China) 23 (10), 1605–1610. Zhou, G., Wen, S., Liu, Y., et al., 2011. Development of a DNA microarray for detection and identification of Legionella pneumophila and ten other pathogens in drinking water. Int. J. Food Microbiol. 145 (1), 293–300.
Shigella Steven L. Percival*, David W. Williams** *
Professor of Microbiology and Anti-infectives, Surface Science Research Centre and Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool, UK Professor of Oral Microbiology, Tissue Engineering & Reparative Dentistry, School of Dentistry, Cardiff University, Heath Park, Cardiff, UK **
BASIC MICROBIOLOGY Shigellae are Gram-negative, non-motile rod-shaped bacteria. As a group they do not produce gas from carbohydrates and they reside in the family Enterobacteriaceae demonstrating very similar characteristics to Escherichia coli. Unlike other members of the Enterobacteriaceae group, shigellae are non-lactose fermenting on MacConkey agar or desoxycholate citrate agar after an incubation period of 24 hours (h). Shigellae, by definition, are non-motile and do not decarboxylate lysine or hydrolyze arginine. Except for Shigella sonnei, certain serovars within the other species, and certain strains within these serovars, they do not produce gas from glucose or decarboxylate ornithine, nor do they use sodium acetate or produce indole from tryptophan.
NATURAL HISTORY Kiyoshi Shiga first documented Shigella in 1898 (Shiga, 1898). However, there is evidence that Ogata (1892) in Japan and Chantemesse and Widal (1888) in France may have actually isolated Shigella much earlier. The genus name Shigella was published in 1919 (Castellani and Chalmers, 1919). Numerous publications on Shigella occurred after this date with a significant paper on its grouping documented in 1954 (Enterobacteriaceae Subcommittee, 1954; Rowe and Gross, 1981). Shigella, based on both biochemical and serological evidence, can be classified into 4 major serological groups, namely: Group A, Shigella dysenteriae, which includes at least 10 serotypes; Group B, Shigella flexneri, includes six serotypes; Group C, Shigella boydii, which includes 15 serotypes; and Group D, Shigella sonnei, which includes only one serotype. The type species is S. dysenteriae 1.
METABOLISM AND PHYSIOLOGY Shigellae are facultatively anaerobic organisms that grow poorly under anaerobic conditions. The optimal temperature for the growth of Shigella is 37 C, in media Microbiology of Waterborne Diseases ISBN 978-0-12-415846-7, http://dx.doi.org/10.1016/B978-0-12-415846-7.00011-1
Ó 2014 Elsevier Ltd. All rights reserved.
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containing 1% peptone as carbon and nitrogen source (Holt et al., 1994). Shigellae are killed at a temperature of 55 C within 1 h (Rowe, 1990). Whilst shigellae are able to tolerate extremely acidic conditions (pH 2.5) for short periods they prefer to grow at neutral or slightly alkaline pH (pH 7.0–7.4).
CLINICAL FEATURES Apart from also occurring in chimpanzees and monkeys, bacillary dysentery is specifically a human disease characterized by a type of diarrhoea in which the stools contain blood and mucus. In extreme cases, it becomes associated with heavy inflammation of the colonic mucosa. Shigellosis, principally a self-limiting disease in healthy adults, has been known to cause fatalities particularly in young children (Salyers and Whitt, 1994). Shigellae are transmitted by the direct faecal–oral route, with infected individuals typically excreting 105–109 shigellae per g of wet faeces, with symptomless carriers excreting 102–106 per g (Dale and Mata, 1968; Thomas, 1955). Because of this, food can potentially be contaminated through the soiled fingers of patients or carriers. The transfer of shigellae by flies breeding on faeces has been established as a very important transmission route during some outbreaks. In a study of endemic shigellosis in Bangladesh, 2.1% of children aged 5 years and under, were found to be asymptomatic carriers (Hossain et al., 1994). Similar results were reported from Mexico where 55% of infants, 2 years of age and under, infected with Shigella were asymptomatic (Guerrero et al., 1994). The severity of disease due to Shigella depends on the virulence of the infecting strain, aside from the host’s immune system. The disease caused by S. sonnei tends to be mild and of short duration whereas that caused by S. flexneri tends to be more severe. Shigella boydii and S. dysenteriae produce disease of varying severity, but S. dysenteriae has often caused epidemics of severe infections. The infective dose for Shigella is generally quite low when compared with other pathogens such as E. coli and Vibrio cholera. The median infective dose (ID50) for Shigella is around 104 cells (Du Pont et al., 1972) in healthy adults compared to V. cholera, which is around 107 cells or higher. Shaughnessy et al. (1946) found that a dose of 108 organisms of S. flexneri were required to induce disease in volunteers who had previously ingested 2 g of sodium bicarbonate. The incubation period following ingestion of Shigella ranges from 36–72 h, but can be as short as 12 h, with frank dysentery appearing within 2 days. Symptoms of shigellosis usually develop suddenly, often as abdominal colic followed by watery diarrhoea, which may be accompanied by fever and malaise. Some individuals go on to develop abdominal cramps, tenesmus and the frequent passage of small volumes of stool (bloody mucus). Symptoms of dysentery can last for about 4 days. In severe cases, symptoms lasting up to 10 days have been documented. Patients who are recovering
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from infection often continue to excrete Shigella for a month following infection. There is documented evidence that some patients can still excrete Shigella for over a year following recovery (Du Pont et al., 1970). This carriage may be more important under conditions of poor hygiene. Shigellae are known to produce an exotoxin, initially described as a neurotoxin, but it also has a fluid transuding effect on the intestinal mucosa. To date, the role of the toxin in the pathogenesis of dysentery is uncertain. Shigella dysenteriae type 1 is responsible for many cases of haemolytic uraemic syndrome (HUS; which was first described in 1955; Gasser et al., 1955), accompanying outbreaks of dysentery and in some parts of the world is one of the commonest forms of acute renal failure in children. Although an invasive disease, infecting shigellae usually do not reach tissue beyond the lamina propria and, therefore, they very rarely cause bacteraemia or systemic infections except under very special circumstances (Struelens et al., 1985).
Pathogenicity and Virulence The two main virulence factors of Shigella are their invasive techniques and toxigenic properties; however, the exact role of the toxin produced by Shigella has yet to be defined. As with most enteric pathogens the first step in the invasion of host cells by shigellae, as demonstrated in HeLa cells, is attachment. In the case of Shigella this process does not seem to be mediated through interaction with a specific receptor (Clerc and Sansonetti, 1987). However, there is mounting evidence suggesting that the invasion plasmid antigen (Ipa) D may be involved as an adhesive. The proteins, IpaB and IpaC, encoded by genes located on the virulence plasmid, have been found on the bacterial surface, suggesting some importance in the pathogenicity of Shigella (Menard et al., 1994). It has been suggested that these two proteins are essential for phagocytosis. It is thought that the proteins rupture phagocytic vesicles allowing intracellular spread (ICS). ICS is mediated by two proteins, IcsA (also called VirG; Bernardini et al., 1989) and IcsB, which facilitate cell death and inflammatory response in the host cells. The process of cell death, induced by these proteins is as yet unknown, but seems to be independent of the production of Shiga toxin (Salyers and Whitt, 1994). Shigella dysenteriae is known to produce the aforementioned Shiga toxin, encoded on the chromosome, which belongs to the family of A1/B5 toxins. This Shiga toxin, whose main action is on blood vessels, is only released during cell lysis and is not actively secreted from the cell (Rowe, 1990).
Survival in the Environment Despite the public health significance of shigellae, their presence and persistence in the environment is not well documented when compared to other species in the family
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Enteriobacteriaceae. Humans are the only important reservoir of Shigella. Excretion of shigellae in stools is highest during the acute phase of dysenteric illness. During this phase the environment is contaminated and the organisms can survive for weeks in cool and humid locations (Rowe and Gross, 1981). The bacteria can survive for 5–46 days when dried on linen and kept in the dark, and for 9–12 days in soil at room temperatures (Roelcke, 1938). Although shigellae tolerate a low pH (<3) for short periods, they soon perish; but they will remain alive for days if specimens are kept alkaline and are prevented from drying (Rowe, 1990). Of all shigellae, S. sonnei appears to be most resistant to harsh conditions and this is certainly the case when compared with S. dysenteriae and S. flexneri. It has been shown that S. sonnei can survive for over 3 h on fingers and up to 17 days on wooden toilet seats (Huchinson, 1956). In a study by McGarry and Stainforth (1978), S. dysenteriae was shown to survive for up to 17 days in biogas plant effluent (11–28 C), but less than 30 h in the biogas plant itself (14–24 C). Shigella may be spread in aerosol droplets, possibly generated by flushing toilets and spray irrigation systems. A study by Newson (1972) showed that by flushing a suspension (1010 cells) of S. sonnei, an aerosol of about 39 bacteria per cubic metre of air was produced and that the Shigella could be recovered from the splashes and survive for up to 4 days. The effectiveness of sewage treatment plants in inactivating Shigella is limited. However, research has shown that Shigella removal is very similar to that of E. coli.
Survival in Water and Epidemiology Shigellosis outbreaks in water have been reported (Mandell et al., 1995; CDC, 1996; Alamanos et al., 2000; Simchen et al., 1991; Egoz et al., 1991; Samonis et al., 1994; Morera et al., 1995; Maurer et al., 2000; Alamonos et al., 2000). Whilst Shigella has been identified in surface waters, little is known about the distribution, survival and transmission of Shigella in surface waters. Dissemination of Shigella is highly significant in developing countries as a mode of transmission. As a rule, drinking water will not contain Shigella unless it is untreated or if there are problems with the water treatment process (Green et al., 1968). There have been studies on the survival of Shigella in water (Feachem et al., 1980). From this and a number of other studies, it has been found that survival of Shigella depends upon concentrations of other bacteria, nutrients, oxygen and temperature. Within clean water, survival times are less than 14 days at temperatures >20 C, but in waters <10 C, Shigella has been shown to survive for weeks. McFeters et al. (1974) showed that Shigella died more slowly in well water at 9–12 C than bacteria such as Salmonella and Vibrio cholera. Talayeva (1960) found that S. flexneri survived for up to 21 days in clean river water at temperatures of 19–24 C, up to 47 days in autoclaved river water, up to 9 days in well
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water, up to 44 days in autoclaved tap water and up to 6 days in polluted well water. Contrary to this McGarry and Stainforth reported in 1979 that S. dysenteriae could survive for 93 days in sterilized water at 11–28 C. Shrewsbury and Barson (1957) found that S. dysenteriae could survive for between 2.5 and 29 months in sterile but faecally contaminated water at 21 C. Infections with Shigella are often acquired by drinking water contaminated with human faeces or by eating food washed with contaminated water. Food borne outbreaks of shigellosis occur, especially in the tropics and less frequently in developed countries (Coultrip et al., 1977). In addition to contamination from faeces by food-handlers who have poor hygiene, flies may sometimes act as vectors in tropical countries (Khalil et al., 1994). There is evidence for Shigella infection acquired by swimming in sewage-contaminated recreational waters (Rosenberg et al., 1976; Makintubee et al., 1987; Sorvillo et al., 1988). In developed countries, infections are usually associated with recent travel to countries with insufficient sanitary facilities (Parsonnet et al., 1989; Lu¨scher and Altwegg, 1994). Outbreaks of Shigella infections have occurred in day-care centres associated with direct person-to-person transmission by the faecal–oral route, which are facilitated by the low infectious dose (10–200 organisms) necessary to induce infection. Shigellae are often the cause of laboratory-acquired infections (Aleksic et al., 1981; Grist and Emslie, 1989). Natural disasters and wars are frequently associated with shigellosis outbreaks and mass encampments become ‘breeding places’ for infection, causing a high incidence of illness and fatalities (Centers for Disease Control, 1994b; Sharp et al., 1995). Saeed et al. (2009) studied the interactions between S. dysenteriae or S. sonnei and Acanthamoeba castellanii. The study demonstrated that S. dysenteriae or S. sonnei grew and survived in the presence of the protozoa for more than 3 weeks. The authors concluded that the relationship between S. dysenteriae and S. sonnei with A. castellanii was symbiotic, and indicated that the amoebae may serve as a transmission reservoir for Shigella in water. Studies with volunteers have shown that fewer than 200 viable cells are needed to readily produce shigellosis (Crockett et al., 1996). A number of outbreaks, primarily food related, have been due to Shigella. These have included consumption of poi (Lewis et al., 1972), tuna (Bowen, 1980) and contaminated salads. In fact during 1961–1975 there were 10 648 cases (72 outbreaks) of shigellosis reported in the USA principally due to the consumption of contaminated salads (Black et al., 1978). The contamination of food is possibly the most important route of transmission of Shigella (Barrel and Rowland, 1979). Shigella dysenteriae 1 has caused major epidemics in Central America (1969–70), Bangladesh (1972) and East Africa (since 1991), whereas S. boydii is mainly prevalent in South Asia and the Middle East. In Europe and North America, S. sonnei is by far the most predominant species causing infections, followed by S. flexneri (Aleksic et al., 1987;
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Lee et al., 1991; Centers for Disease Control, 1994a). Infections due to S. boydii and S. dysenteriae are almost exclusively imported by travellers or foreign-born citizens returning from visits to their home countries (Aleksic et al., 1987). In the UK and the rest of Europe, S. dysenteriae, common during the First World War, is now rare. Between 1920 and 1930, both S. flexneri and S. sonnei were endemic and approximately equal in causing incidents, but by 1940 S. sonnei had become dominant, increasing in incidence annually to a peak of over 49 000 (99% of all shigellae notified) in 1956. The incidence of Sonne dysentery (caused by S. sonnei) then declined steadily in the UK to an annual average of about 3000 notified cases between 1970 and 1990. However, the numbers rose sharply in 1991 where there were several widespread community outbreaks and these continued to rise to a peak of 17 000 cases in 1992. The incidence has since fallen but there were still more than 4550 cases in 1995. Infections due to other shigellae, usually imported, have remained constant during the last decade at approximately 800–900 a year. Similar changes have taken place in the USA. Until 1968, S. flexneri and S. sonnei were equally common, but S. sonnei now accounts for 65% of cases and S. flexneri for about 30%. In tropical areas, shigellosis is endemic. It has been estimated that 5 million cases of shigellosis require hospital treatment; of these, about 600 000 die every year. There is general agreement in the literature that the maintenance of endemic shigellosis has little or no relationship to water quality, but that it is strongly related to water availability and associated hygienic behaviour. However, there will always be specific exceptions to this; for instance, Sultanov and Solodovnikov (1977) considered that the maintenance of dysentery was due to the widespread use of polluted surface water for domestic purposes. Some epidemics of bacillary dysentery are waterborne. An outbreak of 2000 cases of shigellosis due to S. sonnei occurred in 1966 in Scotland, UK when the chlorination plant on a town’s water supply failed (Green et al., 1968). During 1961–75, 38 waterborne outbreaks of shigellosis were reported in the USA (Black et al., 1978). Most of these outbreaks involved semi-public or individual water systems and were usually the result of inadequate or interrupted chlorination of water contaminated by faeces. Such waterborne epidemics are usually dramatic, but they can be terminated very quickly when the water supply is adequately treated. Rahman et al. (2011) isolated five bacterial strains serotyped as S. flexneri 2b from a freshwater lake in Bangladesh. The isolates possessed the ipaH virulence gene and a megaplasmid. He et al. (2012) investigated a shigellosis outbreak by comparing the source of drinking water, consumption of untreated water and food in an elementary school in China. The study concluded that the outbreak of shigellosis was caused by drinking untreated water from a polluted well.
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Godoy et al. (2011) investigated a waterborne outbreak in Lleida, Spain, following consumption of mains water, bottled water and spring water. The waterborne outbreak was caused by S. sonnei following contamination of the public water supply. Chen et al. (2001) reported on an outbreak of gastroenteritis which affected 730 students. Shigella sonnei and Entamoeba histolytica were isolated from the stool specimens of patients. Environmental investigations revealed that the source of infection was contamination of underground well water by sewage from a toilet. The outbreak ended with the closure of the well water supply. To avoid such problems, institutions and other groups that maintain their own wells, including schools and summer camps, need to be vigilant about maintenance and check for potential contamination.
EVIDENCE FOR GROWTH IN A BIOFILM Little is known about Shigella and its ability to form and survive in biofilms, which suggests the need for further research.
METHODS OF DETECTION Culturable Techniques In pure cultures, Shigella form circular, glistening, translucent or slightly opaque colonies on nutrient agar. It is able to grow on blood agar but with no haemolysis. The colony size varies with small colonies developed by S. dysenteriae, but most Shigella serovars produce colonies of 1–2 mm after 18–24 h of incubation at 37 C. Shigella sonnei may develop as smooth and larger, flatter colonies showing an irregular edge, often referred to as phase 1 colonies. ‘Phase 2’ colonies are associated with the loss of the 12 0000-14 0000 kDa virulence plasmid and a change of the antigenic specificity. Phase 2 strains still grow homogeneously in broth culture, but they may partially sediment after boiling at 100 C or autoagglutinate in 3.5% NaCl solution (Rowe, 1990; Bockemu¨hl, 1992). On Leifson’s deoxycholate citrate agar, Salmonella-Shigella agar, or xylose-lysine-deoxycholate and on MacConkey agar, shigellae grow as colourless, translucent, smooth colonies of 1–2 mm after 18–24 h of incubation at 37 C. After prolonged incubation (>48 h), growth of S. sonnei becomes pinkish due to delayed fermentation of lactose and sucrose. For the isolation of shigellae, a freshly passed stool specimen during the acute stage of illness is the material of choice. If present, mucus or bloodstained portions should be selected for culture and, if desired, for microscopic examination for the presence of faecal
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leucocytes. If the specimens cannot be cultured within 2–4 h, they should be preserved in a transport medium. Shigellae are easily overgrown by the concomitant aerobic intestinal flora. Enrichment of stool specimens in Gram-negative broth (Hajna) or selenite broth for about 6 h at 37 C can be tried. After growth on an appropriate agar, Shigella species can be identified by biochemical reactions, combined with agglutination in group- or serovar-specific antisera for shigellae.
Molecular Techniques Maheux et al. (2011) used a rapid, procedure combined with a DNA enrichment method (dubbed CRENAME – concentration and recovery of microbial particles, extraction of nucleic acids, and molecular enrichment), coupled to a Shigella-specific real-time PCR (RT-PCR) assay targeting the tuf gene, to detect Shigella in water. The authors compared this to the US Environmental Protection Agency (EPA) culture-based Method 1604 on MI agar in terms of analytical specificity, ubiquity, detection limit and rapidity. The CRENAME method provided an easy and efficient approach to detect Shigella. The authors concluded that the Shigella-specific RT-PCR assay was comparable to US EPA Method 1604 on MI agar in terms of analytical specificity and detection limit. However, CRENAME provided significant advantages in terms of speed and ubiquity. Hsu et al. (2007) developed a sensitive method for detection of S. sonnei in water. Thirty-three S. sonnei and 72 non-S. sonnei isolates were tested and one primer pair was found capable of specifically amplifying a 369-bp insertion sequence 1 (IS1) fragment from all S. sonnei isolates and one S. dysenteriae ATCC strain by PCR. PCR assays have been proposed to monitor the presence of Shigella. The uid chromosomal region was used to confirm the presence of Shigella species by Cleuziat and Robert-Baudouy (1990). Other genes, such as tuf (elongation factor Tu) or clpB (Cleuziat et al., 1990) and heat shock protein F84.1 have also been used to detect Shigella (Maheux et al., 2009; Clark et al., 2011. Clark et al. (2011) evaluated five oligonucleotide primers sets (ETIR, SINV, exoT, VS1 and ipaH2) for their potential applicability in qPCR assays to detect contamination from bacterial pathogens that included E. coli O157:H7, Salmonella typhimurium, Campylobacter jejuni, Pseudomonas aeruginosa, and S. flexneri. Zhou et al. (2011) investigated an oligonucleotide-based microarray using the sequences of 16S-23S rDNA internal transcribed spacer regions (ITS) and the gyrase subunit B gene (gyrB). Hsu et al. (2010) developed a procedure to detect Shigella species and Enteroinvasive Escherichia coli (EIEC) from environmental water samples using membrane filtration followed by nutrient broth enrichment, isolation using selective culture plates, and
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identification of the invasion plasmid antigen H (ipaH) gene by PCR. Of the 93 water samples from nine reservoirs and one watershed examined, 76 (81.7%) water samples tested culture positive for Shigella and five water samples were positive (5.4%) for Shigella. Maheux et al. (2009) evaluated nine different PCR primer sets to detect Shigella in water. Of the nine PCR primer sets tested, only the primer set targeting the tuf gene amplified DNA from all Shigella strains tested. Theron et al. (2001) developed a rapid seminested PCR method for the detection of virulent Shigella species in ‘spiked’ environmental water samples. A set of primers specific for the invasion plasmid antigen gene (ipaH) in Shigella species was used. The PCR procedure coupled with an enrichment culture detected as few as 1.6 S. flexneri organisms in pure culture.
ANTIMICROBIAL CONTROL In the literature, there is little information regarding the effectiveness of disinfectants on Shigella in relation to control in water. Wang et al. (2011) investigated ultraviolet (UV) light exposure, chlorine or UV followed by chlorine in municipal wastewater for the inactivation of E. coli, S. dysenteriae and toxicity formation. Positive results were achieved using all disinfection procedures. In addition, ozone has been shown to have positive effects on the inactivation of Shigella (Selma et al., 2007). Most cases of Shigella dysentery due to S. sonnei are mild and do not require any antibiotic treatment. Oral salt rehydration therapy is generally the best treatment regime. If antibiotics need to be administered, ampicillin, tetracycline, cotrimoxazole or ciprofloxacin are an appropriate choice. Antibiotics are usually administered because they shorten the duration of illness and decrease the relapse rate (Hruska, 1991). The first reported case of multiple-drug resistant Shigella in Japan occurred in 1956. To date, Shigella is acquiring resistance against many different drugs, constituting a major concern. For example, between 1979 and 1982 the percentage of resistant S. sonnei strains isolated in a hospital in Madrid increased from 39.6 to 97.9% for ampicillin, from 34.4 to 96.9% for co-trimoxazole (SXT), from 6.3 to 18.0% for tetracycline and from 1.6 to 15.1% for chloramphenicol (Lopez-Brea et al., 1983). The first SXT-resistant strain of S. dysenteriae type 1 in Bangladesh was isolated in 1982 (Shahid et al., 1985), with SXT resistance also evident in Finnish travellers (Heikkila¨ et al., 1990). Antibiotic therapy for the treatment of shigellosis should always be based on proper antibiotic susceptibility testing. If this is not possible, blind therapy should include a quinolone as the majority of strains are susceptible.
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RISK ASSESSMENT Health Effects: Occurrence of Illness, Degree of Morbidity and Mortality, Probability of Illness Based on Infection • Shigella can be classified into four major serological groups. Group A, S. dysenteriae, Group B, S. flexneri, Group C, S. boydii, and Group D, S. sonnei, which includes only one serotype. Shigella sonnei accounts for most cases in the developed world. • Shigella infection is characterized by watery or bloody diarrhoea, abdominal pain, fever and malaise. Symptoms of dysentery can last for about 4 days but in severe cases up to 10 days has been documented. Shigellosis is principally a self-limiting disease in otherwise healthy adults; it has been known to cause fatalities, particularly in malnourished infants. • Shigella dysenteriae type 1 is responsible for many cases of HUS. • The severity of disease depends on the virulence of the infecting strain, aside from the host’s immune system. The disease caused by S. sonnei tends to be mild and of short duration, whereas that caused by S. flexneri tends to be more severe. • Children and infants generally suffer a higher rate of infection and more severe disease course.
Exposure Assessment: Routes of Exposure and Transmission, Occurrence in Source Water, Environmental Fate • Shigellosis is specifically a human disease that is transmitted by the direct or indirect faecal–oral route. • Infections with Shigella species are often acquired by drinking water contaminated with human faeces or by eating food washed with contaminated water. Transfer of shigellae by flies has been very important during some outbreaks. • Helped by the low infectious dose (10–200 organisms) necessary to induce infection, person-to-person contact in day-care centres, institutions and other places where hygiene may not be the best have resulted in outbreaks. • Shigella can be found in surface waters and also within contaminated drinking water and this is significant as a mode of transmission in developing countries. • Within clean water, survival times are less than 14 days at temperatures >20 C, but in waters of less than 10 C, they have been shown to survive for weeks. They do not survive at acidic pH. • Shigella sonnei appears to be more resistant to detrimental environmental conditions than S. dysenteriae and S. flexneri. Shigella dysentaeriae has been shown to survive for at least 6 days in septic tank effluent.
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Risk Mitigation: Drinking Water Treatment, Medical Treatment • Drinking water treatment that includes disinfection is sufficient to remove Shigella. Waterborne outbreaks have generally resulted from inadequate treatment. • Most cases of Shigella dysentery (i.e., S. sonnei) are mild and do not require any antibiotic treatment. Treatment by means of rehydration oral salts is all that is required. Ampicillin, co-trimoxazole, tetracycline or ciprofloxacin are appropriate antibiotic choices.
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