Bacillus and Other Aerobic Endospore-Forming Bacteria


TAXONOMY Back to top

Bacillus was defined in 1920 as a genus of gram-positive, aerobic sporeformers, but since

1995 three strictly anaerobic and seven asporogenous Bacillus species have been proposed.

This undermining of the definition has occurred because 16S rRNA gene sequence analysis

has permitted the recognition of genus boundaries, whereas genera were previously defined

phenotypically, as pragmatic collections of species sharing key (i.e., diagnostic) features.

Many new species have been delineated largely on the basis of 16S rRNA gene sequence

similarity and DNA-DNA relatedness—phenotypic descriptions may be brief, and routine

phenotypic characters for distinguishing some species are very few and of little practical

value.

With the accumulation of 16S rRNA gene sequence data, Bacillus has been divided; 14 new

genera containing species originally allocated to Bacillus have been published since 1990,

and together with Bacillus itself the species in these genera now number 388. In addition, 38

genera containing aerobic endospore formers not originally allocated to Bacillus have been

described. Sporosarcina was proposed in 1936, but the other 37 genera have been proposed

since 1990, and together they contain 109 species. Following some mergers, there are now

53 genera of aerobic endospore formers overall, and over 520 species. Although seven

named families containing aerobic endospore formers now lie within the order Bacillales of

the class “Bacilli,” in the phylum Firmicutes, only the

families Bacillaceae and Paenibacillaceae contain species that may be of clinical interest.

The clinical bacteriologist need not, therefore, be greatly concerned at this taxonomic

expansion, because for the medically relevant species it does not represent taxonomic

upheaval. Bacillus is still the largest genus, with 162 species (90), and it continues to

accommodate most of the best-known names such as Bacillus subtilis (the type species), B.

anthracis, B. cereus, B. licheniformis, B. megaterium, B. pumilus, and B.

thuringiensis. Relatively few other familiar names, some of which are of potential clinical

interest, have been transferred to newer genera: Brevibacillus brevis (91), Geobacillus

stearothermophilus (92; important as a thermophilic contaminant and autoclave test

organism), Lysinibacillus sphaericus (2), and Paenibacillus polymyxaand Paenibacillus

macerans. However, several new Bacillus and Paenibacillus species have been proposed on

the basis of single isolates of unknown significance from clinical sources: B. idriensis and B.

infantis from neonatal sepsis (82); P. konsidensis, P. massiliensis, P. sanguinis, and P.

timonensis from blood cultures (83,116); B. massiliensis and P. provencensis isolated from

cerebrospinal fluid (CSF) (56, 117); P. turicensis from a CSF shunt (14); and P. urinalis from

urine (117). “Paenibacillus hongkongensis,” now classified in a new genus of aerobic

endospore formers as Cohnella hongkongensis (74), was isolated from a case of

pseudobacteremia in a boy with neutropenic fever.

DESCRIPTION OF THE GENERA Back to top

Notwithstanding the handful of strictly anaerobic and asporogenous members

of Bacillus, those species likely to be isolated in a clinical laboratory are rod-shaped,

endospore-forming organisms that may be aerobic or facultatively anaerobic, and young

cultures are usually gram positive but sometimes gram variable or clearly gram negative.

They are mostly catalase positive and may be motile by means of peritrichous flagella. Most

species are mesophilic, but there are some thermophilic and psychrophilic species. A large

number of the other, newer genera comprise small numbers of species that are unlikely to be

encountered in a clinical laboratory, as many of them are from exotic and extreme

environments.

EPIDEMIOLOGY AND TRANSMISSION Back to top

Most aerobic endospore formers are saprophytic organisms living in the natural environment,

and many species are very widely distributed. Some species, however, are opportunistic or

obligate pathogens of animals, including humans, other mammals, and insects. The main

habitats are soils of all kinds, ranging from acid to alkaline, nonsaline to highly saline, hot to

cold, and fertile to desert, and the water columns and bottom deposits of fresh and marine

waters. They have been isolated from air at high altitude, from subterranean waters, and

from volcanic and permafrost soils. Endospores readily survive distribution in soils, dusts,

and aerosols from natural environments to a wide variety of other habitats such as manmade

environments, and they may be carried across the globe by wind. The resistance of the

spores to heat, radiation, disinfectants, and desiccation also results in aerobic endospore

formers being frequent contaminants in the operating room, on surgical dressings, in

pharmaceutical products, and in foods. Dried foods such as spices, milk powders, and

farinaceous products are often quite heavily contaminated with spores, and when water

becomes available during food preparation these spores may germinate, leading to spoilage

or food poisoning. B. anthracis is, to all intents and purposes, an obligate pathogen of

animals and humans. Its close relative B. cereus is well established as an opportunistic

pathogen, and other aerobic endospore formers can also be opportunistic pathogens

occasionally. Three members of the B. cereus group—B. anthracis, B. cereus, and B.

thuringiensis—are regarded by many as pathovars of a single species, and there is evidence

of extensive horizontal gene transfer within the B. cereus group (18).

Anthrax was the first example of an infection of humans and animals proven as caused by a

bacterium, and this disease remains the most widely recognized clinical condition caused by

a Bacillus species. It is primarily a disease of domestic or wild animals, and prior to the

availability of an effective veterinary vaccine in the late 1930s, anthrax was one of the

foremost causes worldwide of mortality in cattle, sheep, goats, and horses. Humans almost

invariably contract anthrax directly or indirectly from animals. Over the past half century

there has been a marked decline in the incidence of anthrax in both animals and humans;

the use of veterinary and human vaccines, improvements in factory hygiene, sterilization

procedures for imported animal products, and the increased use of man-made alternatives to

animal hides or hair have all contributed to this. Nevertheless, the disease continues to be

endemic in many countries, particularly those that lack efficient vaccination policies. It is still

common in several sub-Saharan African countries, western China, some Mediterranean

countries, small pockets in Canada and the United States, and certain countries of central

Asia and central and South America. National vaccination programs have led to a progressive

global reduction in livestock cases over the last 30 years, but there are concomitant

problems of diminishing veterinary experience and a public ignorance of the disease; the

former problem may lead to individual outbreaks taking longer to recognize and control, and

the latter to the sale and slaughter of affected animals (140). Direct animal-to-animal

transmission (i.e., excluding scavengers feeding on carcasses of animals with anthrax) is

very rare. Because B. anthracis spores remain viable in soil for many years and their

persistence does not depend on animal reservoirs, B. anthracis is exceedingly difficult to

eradicate from an area of endemicity, and regions of nonendemicity must be constantly on

the alert for the arrival of B. anthracis in imported animal products. Anthrax is not

contagious, and transmission to humans is usually restricted to direct contact with infected

animals, or products from infected animals; however, there have been reports of person-toperson

transmission of cutaneous anthrax, including a case of a mother with a cutaneous

lesion on her finger infecting her 1-year-old child, and a case of transmission of cutaneous

abdominal lesions from one brother to another brother who shared a bed (146).

Contaminated fomites, including such oddities as a communal loofah, or infection of an

injection site by contamination of the skin or by syringe have also rarely been implicated

(86), as has person-to- person, nosocomial spread from an umbilical infection (151).

The continued existence of B. anthracis in the ecosystem appears to depend on a periodic

multiplication phase within an animal host, and so it is generally regarded as an obligate

pathogen. Its environmental presence thus reflects contamination from an animal source at

some time and persistence of spores, rather than replication within the soil. However, some

authorities believe that self-maintenance may occur within certain soils, and germination

of B. anthracis spores and genetic exchange between vegetative cells growing in grass

rhizosphere have been demonstrated (119). In human and animal specimens the organism is

usually sought only when the case history suggests that it is reasonable to suspect anthrax.

B. anthracis has been subjected to military research, development, and occasional

deployment in several different countries over many years, following attacks on livestock

during World War I, and it has remained high on the list of agents that could be used in

biological warfare or bioterrorism. Few reports of laboratory-acquired infections exist, but a

major outbreak occurred in April 1979 in the city of Sverdlovsk, USSR (now Yekaterinburg,

Russia), in the Urals as a result of the accidental release of spores from a military production

facility. Although the natural disease is readily controllable, the 2001 bioterrorism-related

anthrax outbreak in the United States increased the public concern about this disease

(see chapter 12).

CLINICAL SIGNIFICANCE Back to top

The majority of aerobic endospore-forming species apparently have little or no pathogenic

potential and are rarely associated with disease. The principal exceptions to this are B.

anthracis, the agent of anthrax, and B. cereus, but a number of other species, particularly B.

licheniformis and B. pumilus, have been implicated in food poisoning and other human and

animal infections.

Bacillus anthracis

Human anthrax has traditionally been classified as either (i) nonindustrial, resulting from

close contact with infected animals or their carcasses after death from the disease, or (ii)

industrial, as acquired by those employed in processing wool, hair, hides, bones, or other

animal products. Dependent on the route of infection, there are three major clinical forms of

anthrax: cutaneous, inhalation, and ingestion or oral-route anthrax. Anthrax meningitis can

develop as a complication of any of these forms, or occasionally in the absence of any of

them (57, 121).

Cutaneous anthrax accounts for about 99% of naturally acquired human anthrax cases

worldwide; an estimated 2,000 cases are reported annually. Infection typically occurs when

spores are inoculated through a break in the skin, although case reports and animal studies

suggest that preexisting lesions are not necessary for infection (60); infections following

insect bites have been reported. Following an incubation period of usually 2 to 6 days (but

with extremes of a few hours to 3 weeks) a small papule appears, progressing over the next

24 h to a ring of vesicles, with subsequent ulceration and formation of a characteristic

blackened eschar. Subsequent eschar formation may become thick and surrounded by

extensive edema. Fever, pus, and pain at the site are normally absent; their presence

probably indicates secondary bacterial infection. Before the availability of antimicrobial

therapy, 10 to 20% of untreated cases of cutaneous anthrax were fatal. Less than 1% of

cases are fatal today, and they are mainly due to obstruction of the airways by the edema

that accompanies lesions on the face or neck or as a result of progression of the cutaneous

disease into systemic infection. Eschars take several days to evolve, and even with effective

antimicrobial therapy they may take several weeks to resolve.

Ingestion anthrax is not uncommon in regions of endemicity worldwide where socioeconomic

conditions are poor and people eat raw or undercooked meat of anthrax-infected animals

that have died suddenly; asymptomatic infections and symptomatic infections with recovery

may not be uncommon (124). It takes two forms: oral or oropharyngeal infection, in which

the lesion is in the buccal cavity or on the tongue, tonsils, or posterior pharyngeal wall, and

gastrointestinal anthrax, in which ulcerations develop anywhere within the tract, but

primarily in the mucosae of the terminal ileum or cecum. Oropharyngeal symptoms include

sore throat, dysphagia, and regional lymphadenopathy, followed by severe edema of neck

and chest. Intestinal anthrax causes nausea, vomiting, anorexia, abdominal pain, mild

diarrhea, and fever; this can progress to bloody diarrhea, hematemesis, and massive ascites

(140). Mortality rates range widely, owing to the nonspecific nature of the early symptoms

and late initiation of antimicrobial therapy.

Between 1900 and 2001, only 18 cases of naturally acquired inhalation anthrax were

recorded in the United States, with 16 (89%) being fatal (16), and figures in the United

Kingdom show a similar picture. Recently, however, anthrax has occurred in persons using

contaminated imported animal hides for drum making. A case of inhalation anthrax in an

African drum maker in 2006 was the first naturally occurring case of inhalation anthrax in the

United States since 1976; the hides from west Africa were contaminated with B.

anthracisspores. Two cases of cutaneous anthrax, in a drum maker and a family member,

occurred in the United States in 2007 (23), and there was a fatal case of inhalation anthrax

in a drum maker in the United Kingdom in 2008 (3). Both cutaneous and inhalation anthrax

have also been associated with the handling or playing of goatskin drums contaminated with

spores of B. anthracis (40). Among the 22 cases of the anthrax outbreak in the United States

in late 2001, in which spores were delivered in mailed letters, early recognition and

treatment of the 11 patients with confirmed inhalation anthrax resulted in a 65% survival

rate (9).

The inhaled spores are ingested by macrophages, but the role of macrophages thereafter is

unclear, as they may be bactericidal towards germinated spores but also be crippled by

lethal and/or edema toxin and so allow bacterial outgrowth (31). The replacement of the

older name for this form of the disease, “pulmonary anthrax,” with the newer name

“inhalation anthrax” is a reflection of the fact that active infection occurs in the lymph nodes

rather than the lungs themselves. Analysis of 10 of the cases associated with the

bioterrorism events of 2001 (71) revealed a median incubation period of 4 days (range, 4 to

6 days). All of the patients with inhalation anthrax had severe illness and were hospitalized.

Their clinical presentation included fever or chills, fatigue or malaise, minimal or

nonproductive cough, dyspnea, and nausea or vomiting; some had chest pain and sweats. All

patients had abnormal chest radiographic images, with pleural effusion, infiltrates, or

mediastinal widening.

Regardless of the form of the disease, the generalized symptoms that may initially be mild

(fatigue, malaise, fever, and/or gastrointestinal symptoms) can rapidly develop into a

fulminant state following lymphohematogenous spread from a primary lesion, with symptoms

of dyspnea, cyanosis, severe pyrexia, and disorientation, followed by circulatory failure,

shock, coma, and death (71). Depending on the host, there is a rapid buildup of the bacteria

in the blood over the last few hours to terminal levels of 107 to 109/ml in the most

susceptible species. Enhanced clinical and laboratory expertise and conducting prospective

surveillance are critical components of rapid anthrax diagnosis and for response

preparedness, should B. anthracis be used in bioterrorist attacks (52).

Bacillus cereus Group

Bacillus cereus is a ubiquitous organism, and clinical isolates are phylogenetically diverse

(68); it is a wide-ranging opportunistic pathogen of humans and other animals and an

important cause of foodborne illness. B. cereus caused 21 (2%) mean annual total foodborne

outbreaks and 160 (1%) mean annual total foodborne illnesses between 2001 and 2005 in

the United States as reported through the Foodborne Diseases Active Surveillance Network

(FoodNet) of the Centers for Disease Control and Prevention’s (CDC’s) Emerging Infections

Program. However, this probably underrepresents the true burden of illness, since outbreaks

involving less commonly identified pathogens, such as B. cereus, are less likely to have a

confirmed etiology because these organisms are not always considered in clinical,

epidemiological, and laboratory investigations of foodborne disease outbreaks (24).

B. cereus is the etiological agent of two distinct food poisoning syndromes. The diarrheal

type is characterized by abdominal pain and diarrhea 8 to 16 h after ingestion of

contaminated food; it is associated with a wide diversity of foods, from meats and vegetable

dishes to pastas, desserts, cakes, sauces, and milk. The emetic type is characterized by

nausea and vomiting 1 to 5 h after eating the offending food; oriental rice dishes are

predominant sources, although occasionally other foods such as pasteurized cream, milk

pudding, pastas, and reconstituted formulas have been implicated. One emetic outbreak

followed the mere handling of contaminated rice in a children’s craft activity, and fulminant

liver failure associated with the emetic toxin has been reported (94). B. cereus spores are

very adherent to surfaces and are widespread in food preparation environments, and they

can survive many cleaning and normal cooking procedures. These are key factors for both

syndromes; under conditions of improper food storage after cooking, the spores germinate

and the vegetative cells multiply.

The toxigenic basis of B. cereus food poisonings and other B. cereus infections have been

much elucidated over the last three decades. In diarrheal illness, one or more enterotoxins

are produced by vegetative cells in the small intestine, following the ingestion of spores or

vegetative cells; the toxins are believed to cause diarrhea by damaging the integrity of ileal

epithelial cell membranes. B. cereus produces a range of protein toxins, of which three have

been implicated in diarrheal illness: hemolysin BL (Hbl) and nonhemolytic enterotoxin (Nhe),

both of which are three-component toxins restricted to the B. cereus group, and the singlecomponent

β-barrel, pore-forming cytotoxin K (CytK). These toxins may act synergistically,

but there is evidence that Nhe is the most dominant in diarrheal illness (128). The emetic

illness is an intoxication caused by a highly heat-, proteolysis-, and acid-resistant toxin

preformed in the food—hence its rapid onset. The toxin, cereulide, is a small ring-formed

dodecadepsipeptide produced at the end of logarithmic growth, and its genetic determinants

are borne on a plasmid related to the pXO1 virulence plasmid of B. anthracis (41). Cereulide

production by B. cereus has not been demonstrated at temperatures below 12°C, but the

related and psychrotolerant species Bacillus weihenstephanensis may produce detectable

cereulide at 8°C (135). Gherlardi et al. (53) used PCR amplification of toxin genes in

conjunction with randomly amplified polymorphic DNA (RAPD)-PCR and multiplex RAPD-PCR

to trace the source of two outbreaks of food poisoning.

Bacillus cereus is an important ocular pathogen, causing a rapidly progressive

endophthalmitis that is refractory to treatment. Cases are, fortunately, infrequent; they

usually occur after penetrating trauma of the eye but sometimes follow hematogenous

spread or, occasionally, eye surgery. Significant loss of vision, and often loss of the eye

itself, can occur within 24 to 48 h (101). B. cereus keratitis associated with contact lens wear

has also been reported (109). Other B. cereus infections occur mainly, though not

exclusively, in persons predisposed by neoplastic disease, immunosuppression, alcoholism

and other drug abuse (including cases associated with contaminated heroin), the presence of

catheters (65) or implants such as fluid shunts, or some other underlying condition such as

diabetes, and fatalities occasionally result. Reported conditions include bacteremia,

septicemia, fulminant sepsis with hemolysis, meningitis (following allogenic stem cell

transplants in two cases) (58), brain hemorrhage, ocular infections including

panophthalmitis, ventricular shunt infections, endocarditis (1), pneumonia (47),

pseudomembranous tracheobronchitis, exacerbation of bronchiectasis, empyema, pleurisy,

peritonitis in a dialysis patient, lung abscess, brain abscess, liver abscess, osteomyelitis,

salpingitis, urinary tract infection, and primary cutaneous infections. El Saleeby et al. (42)

found an association between tea drinking and invasive B. cereus infection in

immunocompromised children. Ko et al. (84) reported the emergence of a β-lactamdependent

strain associated with prolonged administration of β- lactams via an indwelling

catheter in a neutropenic patient. Strains of B. cereus have been isolated in association with

periodontitis (63). Wound infections, often of open fractures (38), and mostly in otherwise

healthy persons, have been reported following surgery (associated, in one report, with

contaminated incontinence pads), road traffic and other accidents, scalds, burns, plaster

fixation, drug injection, and close-range gunshot and nail bomb injuries; some became

necrotic and gangrenous (32). Fatal neonatal meningitis was caused by a blank firearm

injury; blank cartridge propellants are commonly contaminated with the organism. Neonates

also appear to be particularly susceptible to B. cereus, especially with umbilical stump

infections, and cases of meningitis have been associated with the use of catheters and

manual ventilation balloons (44). Respiratory tract infections have also been associated with

contaminated ventilation systems among neonates and in a pediatric intensive care unit

(73). Several cases of B. cereus pneumonia in metal workers and welders have been

reported, including fatal infections (67). Infection of these metal workers may be related to

welding-fume exposure, demonstrated to suppress pulmonary defenses in animal studies.

Interestingly, the isolate from one of these cases was found to harbor a plasmid (pBCXO1)

that was 99.6% similar to the pXO1 virulence plasmid of B. anthracis, while other isolates

were also found to harbor either pXO1 virulence genes or both pXO1 and pXO2 virulence

genes (67); the role of these pXO1 or pXO2 plasmid genes, if any, in the virulence of these

isolates is not known. Additional atypical B. cereus strains, originally identified as B.

anthracis due to the presence of pXO1 and pXO2 plasmids, have also been isolated in

association with fatal infections of chimpanzees and a gorilla in Ivory Coast and Cameroon

(79, 85). A nosocomial outbreak of B. cereus infection related to catheter use was associated

with reused towels (35), and a hospital pseudo-outbreak was associated with contaminated

ethanol used as a skin disinfectant. B. cereus also causes infections in domestic animals. It is

a well-recognized agent of mastitis and abortion in cattle, particularly when animals are in

winter housing, and can cause these conditions in other livestock.

Strains of B. thuringiensis commonly carry genes for B. cereus enterotoxins, and assays

have demonstrated that enterotoxin production occurs, but the cereulide synthetase gene

has not been detected in this species (6, 105). B. thuringiensis is well known as an insect

pathogen, preparations of certain strains are widely used as biopesticides, and transgenic

crop plants that express the insecticidal crystal toxin genes have been developed, but there

is as yet no evidence of infections directly associated with the use of this organism as an

insecticide. Occupational exposure to the organism has been connected with presence of the

organism in feces but without gastrointestinal symptoms. A review of the safety of using B.

thuringiensis as a biopesticide on crop plants found that the main pesticide strains assayed

produced low titers of enterotoxin (13). There have been few reports of gastroenteritis

outbreaks in which B. thuringiensis was implicated (98, 128). However, cases of such illness

caused by B. thuringiensis may have been attributed to B. cereus, as the former may not

produce its characteristic insecticidal toxin crystals when incubated at 37°C, owing to the

loss of the plasmids carrying the relevant genes. There have been reports of wound, burn,

and ocular infections with B. thuringiensis, and in a fatal case of pulmonary disease and

bacteremia in a neutropenic patient, there was evidence that membrane-damaging toxins

contributed to the infection (54). Experimental B. thuringiensisendophthalmitis has been

achieved in rabbits (17).

Other Species

Reports of infections with non-B. cereus group species are comparatively rare but very

diverse, and there have been several hospital pseudoepidemics associated with contaminated

blood culture systems. B. licheniformis has been reported from prosthetic-valve endocarditis,

pacemaker wire infection, ventriculitis following the removal of a meningioma, brain

abscesses, septicemia following arteriography, bacteremia associated with indwelling central

venous catheters, bacteremia during pregnancy with eclampsia and acute fibrinolysis,

peritonitis in patients undergoing continuous ambulatory peritoneal dialysis (CAPD) and in a

patient with volvulus and small-bowel perforation, ophthalmitis, and corneal ulcer after

trauma. An outbreak of bacteremia among patients with blood malignancies was related to

nonsterile cotton wool used during skin disinfection (106). B. licheniformis bacteremia has

been reported for an immunocompetent man and has twice been reported in association with

Munchausen’s syndrome: one case followed self-inoculation with organic drain cleaner (61),

and in another case following self-inoculation with soil, B. pumilus and Paenibacillus

polymyxa were also isolated (51). B. licheniformis can cause foodborne diarrheal illness, and

in a case associated with an infant fatality, lichenilysin A, a heat-stable cyclic lipopeptide, has

been implicated (99). This organism is frequently associated with bovine abortion and has

been shown to have a tropism for the bovine placenta; it has also been associated with

abortion in water buffalo and occasionally with bovine mastitis. As with such B.

cereus infections, these types of B. licheniformis infection are associated with wet and dirty

conditions during winter housing, particularly when the animals lie in spilled silage, and in

one outbreak a water tank contaminated with B. licheniformis was implicated.

The name B. subtilis was often used in the past for any clinical isolate, but since 1970 there

have been reports of infection in which this species appears to have been identified

accurately. They include cases of pneumonia, bacteremia, and septicemia associated with

neoplastic disease; breast prosthesis and ventriculo-atrial shunt infections; isolations from

surgical wound drainage sites; endocarditis in a drug abuser; meningitis following a head

injury; bacteremia associated with trauma; bacteremia in cancer patients; cholangitis

associated with kidney and liver disease; and isolation from dermatolymphangioadenitis

associated with filarial lymphedema. Two cases of severe hepatotoxicity followed the

ingestion of nutritional supplements contaminated with B. subtilis (130). Administration of an

oral probiotic preparation marketed for the treatment or prevention of intestinal disorders,

and allegedly containing B. subtilis, led to a fatal septicemia in an immunocompromised

patient; subsequently, the organism concerned was identified as Bacillus clausii (127). These

authors reported another B. clausii infection, cholangitis in polycystic kidney disease, in a 15-

year-old French boy who had undergone a renal transplant, but the source of the organism

was unclear. B. subtilis has also been associated with cases of bovine mastitis and ovine

abortion. B. subtilis has been implicated in foodborne illness: vomiting has been the

commonest symptom, but with accompanying diarrhea frequently reported, the onset

periods have been short (ranging from 10 min to 14 h; median, 2.5 h), the bacterial loads of

the organism were high (105 to 109 CFU/g), and the implicated foods were often prepared

dishes in which meat or fish was served with cereal-based components such as bread,

pastry, rice, or stuffing. Bacillus amyloliquefaciens, a close relative of B. subtilis, is widely

used industrially for enzyme and amino acid production, but human consumption of Ltryptophan

manufactured in an organism genetically engineered from a strain of this species

was associated with a large epidemic of eosinophilia-myalgia syndrome with 37 deaths; the

causative agent has not been identified with certainty (100). Environmental strains of this

species producing a heat-stable, nonprotein toxin have been isolated in association with

building-related health problems (100).

Organisms identified as B. circulans have been isolated from cases of bacteremia in cancer

patients, meningitis, CSF shunt infections, endocarditis, a wound infection in a cancer

patient, a bite wound, endophthalmitis, peritonitis in a patient undergoing CAPD (12), and

epidemic endophthalmitis associated with a contaminated product used during cataract

surgery. It must be noted, however, that many isolates previously regarded as B.

circulans might have been wrongly identified (see comments on B. circulans below).B.

coagulans has been isolated from corneal infection, bacteremia, and bovine abortion. B.

pumilus has been found in cases of cutaneous, pustule, and rectal fistula infections, central

venous catheter infection in an immunocompetent child (10), bacteremias in

immunosuppressed patients (106), bacteremia in a patient with Munchausen’s syndrome

(51), and repeated contamination of a blood platelet screening procedure; it has also been

found in association with bovine mastitis. Toxigenic strains of B. pumilus have been isolated

in association with foodborne illness and from clinical and environmental specimens, and a

heat-stable cyclic lipopeptide, pumilacidin, was implicated in a rice-associated food poisoning

outbreak (50). Lysinibacillus sphaericus has been implicated in a fatal lung pseudotumor,

bacteremia, and meningitis. B. megaterium (eight isolates), B. pumilus (six), Brevibacillus

brevis (five), B. licheniformis (two), and B. subtilis (one) isolated from chewing tobacco were

found to produce potent exogenous virulence factors that caused plasma exudation and

tissue dysfunction in an animal model (118). B. megaterium caused a delayed-onset lamellar

keratitis following laser-assisted eye surgery (114).

Bacillus brevis has been isolated from corneal infection and implicated in several incidents of

food poisoning; since those reports, the species was split (see “Taxonomy” above) and

transferred to the new genusBrevibacillus. Strains of one of the newer species, Brevibacillus

agri, were isolated in association with an outbreak of waterborne illness in

Sweden; Brevibacillus centrosporus was isolated from a bronchoalveolar lavage fluid

sample, Brevibacillus parabrevis was found in a breast abscess, and both species have been

isolated from human blood (93). Brevibacillus laterosporus has been reported in association

with a severe case of endophthalmitis.

Paenibacillus alvei has been isolated from cases of meningitis, endophthalmitis, a prosthetic

hip infection in a patient with sickle cell anemia, wound infections, and, in association

with Clostridium perfringens, a case of gas gangrene. P. macerans has been isolated from a

wound infection following removal of a malignant melanoma, from a brain abscess following

penetrating periorbital injury, from a catheter-associated infection in a leukemic patient, and

from bovine abortion, and P. polymyxa has been isolated from bacteremia in a patient with

cerebral infarction, a bacteremic case of Munchausen’s syndrome (51), and ovine

abortion. Paenibacillus popilliae has been reported from endocarditis, and Paenibacillus

larvae has been reported from infection of a CSF shunt system.

Single isolations of several new Bacillus and Paenibacillus species from clinical specimens,

but of unknown significance, are mentioned in “Taxonomy” above.

COLLECTION, TRANSPORT, AND STORAGE OF

SPECIMENS Back to top

Bacillus species normally survive transport in freshly collected specimens or in a standard

transport medium. Local transport of specimens (for no longer than a few hours) can be

done at room temperature or at 2 to 8°C for most specimens, including serum. Generally, if

specimens such as stool, sputum, pleural fluid, blood, and material on swabs are to be

shipped overnight or longer, they should be sent at 2 to 8°C, while fresh tissue and serum

samples should be shipped frozen. Formalin-fixed tissues can be sent at room temperature

primarily for detection using immunohistochemistry and (although they are much less

suitable) PCR. For blood specimens with which PCR will be used to detect B. anthracis DNA,

collection tubes containing EDTA or citrate as an anticoagulant are preferable to those

containing heparin.

All the clinically significant isolates reported to date are of species that grow, and often

sporulate, on routine laboratory media at 37°C. It seems unlikely that many clinically

important but more fastidious strains are being missed for the want of special media or

growth conditions. Maintenance is simple if spores can be obtained, but it is a mistake to

assume that a primary culture or subculture on blood agar will automatically yield spores if it

is stored on the bench or in the incubator. It is best to grow the organism on nutrient agar

(or Trypticase soy agar) containing 5 mg/liter manganese sulfate for a few days, and

refrigerate when microscopy shows that most cells have sporulated. For most species,

sporulated cultures on slants of this medium, sealed after incubation, can survive in a

refrigerator for years. Alternatively, cultures (preferably sporulated) can be frozen or

lyophilized.

Safety Aspects

Clinical specimens for isolation of Bacillus species other than B. anthracis can be handled

safely on the open bench without special precautions. Efforts should be made to avoid

methods that produce aerosols. Any procedures that have the potential to generate aerosols

should be done in a microbiological safety cabinet. Biosafety level 2 practices, containment

equipment, and facilities are recommended for activities using clinical materials and

diagnostic quantities of infectious cultures.

Isolation and presumptive identification of B. anthracis can be performed safely in the

routine clinical microbiology laboratory, provided that normal good laboratory practice is

observed. Preexposure vaccination is not recommended for laboratory personnel doing

routine processing of clinical or environmental specimens in general diagnostic laboratories

(26); however, biosafety level 3 facilities are recommended for all such work (140). When

working with pure cultures of B. anthracis, direct and indirect contact of broken skin with

cultures and contaminated laboratory surfaces, accidental parenteral inoculation, and, rarely,

exposure to infectious aerosols are the primary hazards to laboratory personnel. Laboratories

that frequently centrifuge B. anthracissuspensions should use an aerosol-tight rotor that can

be repeatedly autoclaved (26).

Human infectious doses have not been established for B. anthracis; the U.S. Department of

Defense estimates that a 50% lethal dose for humans is 8,000 to 10,000 spores, but this is

largely based on data from nonhuman primate studies. When collecting clinical specimens for

suspected anthrax, appropriate personal protective equipment should be used, such as

disposable gloves, disposable apron or overalls, and boots which can be disinfected after

use; for dusty samples that might contain many spores, the use of a face shield and/or a

respirator should be considered. Full details of personal protective equipment and of

disinfection and decontamination are given in Annexes 1 and 3 of the WHO Anthrax in

Humans and Animals guidelines (140). It should be noted that although hand washing with

soap and water or with chlorhexidine gluconate, and the use of hypochlorite- releasing

towels, may reduce endospore contamination of the skin, waterless rubs containing ethanol

are ineffective at removing endospores. Preexposure vaccination recommendations by

Advisory Committee on Immunization Practices (ACIP) for laboratory exposures are

addressed in “Vaccination” below.

Bacillus anthracis is defined as a select agent and is included on both the Department of

Health and Human Services/CDC and U.S. Department of Agriculture/APHIS select agent

lists. Thus, possession of the agent in the United States requires registration of the

laboratory with either the CDC or APHIS. When B. anthracis is identified by a laboratory, the

identification of this agent must be reported to the CDC or APHIS immediately and a

APHIS/CDC Form 4 (Report of the Identification of a Select Agent or Toxin) submitted within

7 days. Other authorities should be notified as required by federal, state, or local laws.

When B. anthracis is isolated in an unregistered laboratory, the organism must either be

destroyed on-site by a recognized sterilization or inactivation process or be transferred to a

registered laboratory within 7 days. Shipping of this agent requires completion of the

APHIS/CDC Form 2 (Request to Transfer Select Agents and Toxins) and prior approval from

either the CDC or APHIS (see http://www.selectagents.gov for additional information of

select agent regulation in the United States).

Specimens from Patients Suspected To Have Anthrax

In all cases, specimens from possible sources of infection (carcass, hides, hair, bones, etc.)

should be sought in addition to patient specimens. Leakproof containers, to be placed in

secondary containers for “double-bagging,” and then secure, outer containers for carriage

are needed. A blood smear may reveal the capsulated rods or, if treatment has started,

capsule “ghosts.” Postmortem blood collected by venipuncture (a characteristic of anthrax is

nonclotting blood at death) should be examined by smear (for capsule) and culture.

Guidelines for clinical evaluation of persons with possible anthrax can be found

athttp://www.cdc.gov/mmwr/preview/mmwrhtml/mm5043a1.htm.

Cutaneous Anthrax

The edge of an eschar should be lifted and two specimens of vesicular fluid collected

(preferably prior to initiation of antimicrobial therapy) by rotating swabs beneath it; one is

for a smear for visualizing the capsule, Gram stain, and culture, and the other is for PCR. For

immunohistochemical (IHC) analysis of cutaneous lesions, a full-thickness punch biopsy

specimen fixed in 10% buffered formalin from a papule or vesicle lesion and including

adjacent skin should be taken. Biopsies should also be taken from both vesicle and eschar if

present (122).

Inhalation Anthrax

Anthrax will be suspected only if the patient’s history suggests it. Chest radiographs and

chest computed tomography scans are recommended. In addition to imaging studies, obtain

blood cultures prior to antimicrobial therapy. Pleural fluid, if present, should be obtained for

Gram stain, culture, and PCR. Serology is also useful for the diagnosis of cases when culture

fails owing to previous treatment. Collect acute- and convalescent-phase serum samples 2 to

4 weeks apart for serologic testing. Pleural and/or bronchial biopsy samples can be tested by

immunohistochemistry. Postmortem, the approach given for ingestion anthrax should be

followed (see below).

Ingestion Anthrax

As with the inhalation form, anthrax is suspected only if an adequate history of the patient is

known. Specimens from oral lesions may be collected in the same way as for the cutaneous

disease (140). Premortem, obtain blood cultures before antimicrobial therapy. Ascites fluid, if

present, should be collected for Gram stain, culture, and PCR. A stool or rectal swab, and

material from any oropharyngeal lesions, should also be collected for Gram stain, culture,

and PCR. Acute- and convalescent-phase serum samples, with the first obtained within 7

days of onset and the convalescent-phase sample obtained 2 to 3 weeks later, should be

collected for serologic testing. Postmortem blood collected by venipuncture should be

examined by smear (for observation of capsule) and culture. Any hemorrhagic fluid from the

nose, mouth, or anus should be cultured. If these are positive, no further specimens are

needed. Again, if negative, specimens of peritoneal or ascitic fluid, spleen, and/or mesenteric

lymph nodes, aspirated by techniques avoiding spillage of fluids, may be collected for smear

and culture.

Anthrax Meningitis

Collect CSF and blood specimens for cultivation, capsule staining, and PCR; specimens

should also be subjected to antigen detection testing, if available.

Specimens from Animals Suspected To Have Died of Anthrax

Although the organism is rapidly destroyed by putrefaction in the intact carcass, the carcass

of an animal that died of anthrax still generally yields positive cultures from appropriate

specimens, such as blood from a peripheral vein, or from snips of tissue such as from the tip

of an ear, as sporulation will still occur in some tissues; however, hemorrhagic exudate is

preferred to aspirated blood or tissue specimens for direct demonstration of the capsulated

organism using Gram, Giemsa, or polychrome methylene blue (M’Fadyean) staining.

DIRECT EXAMINATION Back to top

The first examination of smears and cultures in many clinical laboratories is done with the

Gram stain. In the past, it was regarded as of limited value in anthrax diagnosis, because the

capsule is not seen. Notwithstanding this, if large numbers of gram-positive bacteria are

observed in a patient’s blood at death, then B. anthracis should be suspected. As in the 2001

bioterrorism incident in the United States, such preparations can be very useful (Fig. 1a). In

other circumstances and in animals in particular, the blood or other specimen may not be

collected soon after death and before putrefactive organisms appear; B. anthracismay then

be indistinguishable without the use of the proper capsule stain.



In addition to culturing B. anthracis, there are molecular and antigen-based detection

methods available for direct detection in clinical and environmental samples. These detection

methods may provide additional information. Several methods, including a B. anthracisspecific

Laboratory Response Network (LRN) PCR assay, IHC assays, and serology, were

useful for confirmation of cases during the 2001 bioterrorism-associated outbreak and more

recent cases associated with drum making using B. anthracis-contaminated hides

(23, 66,112, 113, 122).

The IHC assay, as performed at the CDC, uses the same antibodies as the direct fluorescentantibody

(DFA) assay (specific to cell wall antigen or the capsule) to detect B. anthracis in

formalin-fixed, paraffin-embedded tissues. This method was particularly useful in the

diagnosis of cutaneous cases during the 2001 bioterrorism-associated outbreak. Skin biopsy

samples from cutaneous lesions from 8 of 10 patients were positive for both the capsule and

cell wall antigens (122). The most widely used and available detection method in the U.S.

public health system is the LRN PCR (66). In addition to being widely used in 2001, this

assay and the IHC assay were used in 2007 to diagnose two cutaneous anthrax cases in a

drum maker and his child (23).

At the CDC, a positive PCR result on any clinical specimen from a patient collected from a

normally sterile site (such as blood or CSF) or a lesion of other affected tissue (skin,

pulmonary, reticuloendothelial, or gastrointestinal) is regarded as a supportive or

presumptive diagnostic test. It is considered sufficient to provide a probable diagnosis but is

not confirmatory in itself. The principal reason for such stringent guidelines on the use of

PCR approaches and the value of their results towards providing a confirmatory diagnosis is

based on the possibility that environmental contamination of a non-anthrax-related lesion

could result in a positive result; this is especially the case with the use of some previously

published PCR primers for capsule and chromosomal genes that can produce false positives

with reactions to soil microbiota. This is quite similar to the recommendations that are

included in the 2008 WHO guidelines (140), in which PCR can be used for identification of an

isolate but is not recommended for testing of specimens.

There are numerous reports on the use of alternative technologies for the detection of B.

anthracis, such as mass spectrometry, flow cytometry, time-resolved fluorescent assays,

high-performance liquid chromatography, and even the use of engineered B cells to detect B.

anthracis (5, 69, 115, 149, 152). Two recent studies focused on detecting the anthrax

toxins, which are highly expressed during infection, in specimens instead of directly detecting

the bacilli (15, 133). One reported on an immunoassay using highly fluorescent europium

nanoparticles to detect protective antigen (PA), while the other reported detection of lethal

factor (LF) by taking advantage of its metalloprotease activity, which cleaves specific

peptides. The LF protein was captured by monoclonal antibodies and then incubated with a

synthetic peptide substrate whose cleavage products were detected by matrix-assisted laser

desorption ionization–time of flight (MALDI-TOF) mass spectrometry (15). These and other

novel approaches may allow for detection of B. anthracis infection earlier in the course of the

disease and thus allow for more successful treatment.

ISOLATION Back to top

Isolation from Human Specimens

Fresh specimens from patients should be inoculated onto plates of blood agar in the normal

way. Enrichment procedures are generally inappropriate for isolations from clinical

specimens. However, when seeking B. cereusin stools several days after a food poisoning

episode, nutrient or tryptic soy broth with polymyxin (100,000 U/liter) may be added to a

heat-treated specimen. Heat treatments at 70°C for 30 min or 80°C for 10 min are widely

used for aerobic endospore formers in general, but 62 to 65°C for 15 to 20 min is more

suitable for B. anthracis; temperatures above 70°C are not recommended for this species

(142). There is no effective enrichment method for B. anthracis in old animal specimens or

environmental samples, and isolation from these is best attempted using polymyxinlysozyme

EDTA-thallous acetate (PLET) agar (80; see also chapter 17). Aliquots (0.1 ml) of

the undiluted suspension and 1:10 and 1:100 dilutions of a heat-treated suspension of the

specimen are spread across PLET plates, which are read after incubation for 36 to 40 h at

37°C. Creamy white, domed, circular colonies, 1 to 3 mm, are subcultured onto (i) blood

agar plates to test for gamma phage and for hemolysis and (ii) directly or subsequently in

blood to look for capsule production using either the M’Fadyean stain or India ink negative

stain (the latter is less reliable, because the ink coagulates the blood and makes

interpretation difficult); 2.5 ml of blood (preferably defibrinated horse blood, but horse or

fetal calf serum is satisfactory) is inoculated with a pinhead quantity of growth from the

suspect colony, incubated statically for 6 to 18 h at 37°C, and then stained. A

differential/selective chromogenic medium is marketed by R&F Laboratories, Downers Grove,

IL (R&F Anthracis chromogenic agar), and it has undergone some independent evaluation

(72), but another study (97) found PLET to be more sensitive and selective.

Several media have been designed for the isolation, identification, and enumeration of B.

cereus organisms. They exploit the organism’s egg yolk reaction (phospholipase C) positivity

and acid-from-mannitol negativity; pyruvate and polymyxin may be included for selectivity.

Three satisfactory formulations are MEYP or MYP (mannitol, egg yolk, polymyxin B agar;

MEYP, Oxoid, Basingstoke, United Kingdom; MYP, Difco, BD, Franklin Lakes, NJ), PEMBA

(polymyxin B, egg yolk, mannitol, bromthymol blue agar; Oxoid), and BCM (Bacillus

cereusmedium; LabM, Bury, United Kingdom) (see chapter 17). There are more recent

formulations that reveal phospholipase C positivity using specific chromogenic substrates

rather than natural egg yolk: Bacillus cereusgroup plating medium (Biosynth Chemistry and

Biology, Staad, Switzerland, also available as Cereus-Ident-Agar from Heipha, Eppelheim,

Germany) and Bacillus cereus/Bacillus thuringiensis chromogenic plating medium (R&F

Laboratories).

There are no selective media for other Bacillus species, but spores can be selected for by

heat treating part of the specimen as described above; however, this is not appropriate for

fresh clinical specimens, where spores are usually sparse or absent. Vegetative cells of both

sporeformers and non-sporeformers are killed by heat treatment, but the heat-resistant

spores not only survive but also may be heat shocked into subsequent germination; another

part of the specimen is cultivated without heat treatment in case spores are very heat

sensitive or absent.

In specimens submitted for food poisoning investigations, or for isolation of B. anthracis from

old carcasses, animal products, or environmental specimens, the organisms will mostly be

present as spores. Heat treatment, as described above, will both heat shock the spores and

effectively destroy non-spore-forming contaminants. A variety of approaches are used to

process dry or solid samples prior to heat treatment. Direct plate cultures are then made on

blood, nutrient, or selective agars, as appropriate, by spreading up to 0.1-ml volumes from

undiluted sample and 10- and 100-fold dilutions of the treated sample.

Isolation from Animals Suspected To Have Died of Anthrax

Anthrax should be considered as the possible cause of death in herbivorous animals that

have died suddenly and unexpectedly, especially if hemorrhage from the nose, mouth, or

anus has occurred, and if death has taken place at a site with a history of anthrax—perhaps

even several decades before. PCR-based approaches are becoming more widely used for

direct detection of B. anthracis in veterinary specimens.

Carcasses 1 to 2 Days Old

Due to the nonclotting nature of blood in animals that have died of anthrax infection, it is

usually possible to aspirate a few drops of blood from a peripheral vein for (i) a M’Fadyeanstained

smear and (ii) direct plate culture on blood agar.

In pigs, the enormous terminal bacteremia seen in herbivores may not develop, and the

capsulated rods may not be visible in blood smears. When cervical edema is present, smears

and cultures should be made of fluid aspirated from the enlarged mandibular and

suprapharyngeal lymph nodes. Intestinal anthrax of pigs may be obvious only at necropsy,

when rods are usually visible in stained smears made from mesenteric lymph nodes.

Older Putrefying Carcasses

The organism may not be visible in smears 2 to 3 days following death, as it competes poorly

with putrefactive organisms; culture is then necessary for diagnostic confirmation. Sections

of tissue, or any blood-stained material, should be collected, and spleen or lymph node

specimens should be taken if the animal has been opened. With putrefied and very old

carcasses, swabs of the nostrils, nasal turbinates, and eye sockets are likely to yield B.

anthracis, but the best specimens may be samples of contaminated soil taken from beneath

the head and tail.

Isolation of B. anthracis from Bioterrorism-Related Specimens

In 1999, an LRN was established in the United States by the CDC in partnership with the

Association of Public Health Laboratories, Federal Bureau of Investigation, and Department of

Defense to provide the public health laboratory response to acts of bioterrorism (103). This

network links local (sentinel) laboratories to laboratories with more specialized testing and

increased biosafety capacity at the state (reference) and federal (national) levels. There are

reference level laboratories in all 50 states able to detect agents, includingB.

anthracis, rapidly. State public health laboratories are part of the LRN and are able to

provide guidance, or the LRN can be accessed using the Internet

(http://www.bt.cdc.gov/lrn/). If unable to reach the state public health laboratory during

nonbusiness hours, LRN consultations may be requested by calling the CDC Emergency

Operations Center at 770-488-7100 . State and territorial public health

laboratory contact information and sentinel laboratory guidelines are also available on the

American Society for Microbiology website at www.asm.org. For general questions there is a

24-h hotline number, 800-CDC-INFO ( 800-232-4636 ), and an e-mail

address, cdcinfo@cdc.gov. Although initially limited to the United States, there are now over

150 national and international locations, including laboratories within Canada, Australia,

Germany (U.S. military base), Japan (U.S. military base), South Korea (U.S. military base),

and the United Kingdom, capable of providing a rapid response to acts of biological

terrorism, emerging infectious diseases, and other public health threats and emergencies.

Isolation of B. anthracis from Environmental and Animal

Product Specimens

Tests for the presence of B. anthracis may be requested for diverse specimens, such as

animal products (e.g., wool, hides, hair, and bonemeal) from regions of endemicity, soil or

other materials from old burial sites or tannery or laboratory sites due for redevelopment, or

other environmental materials associated with outbreaks (e.g., sewage sludge). Detection in

such specimens may mean searching for rather few spores of B. anthracis among those of

many other species, especially other members of the B. cereus group. Some environmental

specimens may contain substances that inhibit germination and growth of B. anthracis (140).

At present, there is no enrichment method for B. anthracis, and culture by the selective agar

techniques described above is the best approach. PCR-based methods are being used

increasingly for the direct detection of B. anthracis in clinical and environmental samples

(125), but it is still advisable to confirm positive results by conventional methods.

IDENTIFICATION Back to top

Remember that these organisms do not always stain gram positive; some are gram variable,

gram positivity is readily lost in older cultures, and some species or strains are frankly gram

negative. Before attempting to identify to the species level, it is important to establish that

the isolate really is an aerobic endospore former and that other inclusions are not being

mistaken for spores. Phase contrast (at a magnification of ×1,000) should be used if

available, as it is superior to spore staining and more convenient. Spores are larger, more

phase bright, and more regular in shape, size, and position than other kinds of inclusions

such as polyhydroxybutyrate (PHB) granules (Fig. 2d), and sporangial appearance is valuable

in identification (Fig. 2). For spore staining, flood a heat-fixed smear with 10% aqueous

malachite green for up to 45 min (without heating), followed by washing and counterstaining

with 0.5% aqueous safranin for 30 s; spores are green within pink-red cells at a

magnification of ×1,000 (Fig. 1d). A Gram-stained smear showing cells with unstained areas

suggestive of spores can be stripped of oil with acetone-alcohol, washed, and then stained

for spores.



Bacillus and related genera contain facultative anaerobes as well as strict aerobes, which can

be a valuable characteristic in identification. For example, B. licheniformis and B.

subtilis, which have very similar colonial (Fig. 3j) and microscopic (Fig. 2e) morphologies,

are facultatively anaerobic and strictly aerobic, respectively. Likewise, the two large-celled

species B. cereus and B. megaterium (Fig. 2b and d) are facultatively anaerobic and strictly

aerobic, respectively.

The most widely used diagnostic schemes use traditional phenotypic tests, or miniaturized

tests of the API 20E and 50CHB kits used together (90) (bioMerieux, Marcy l’Etoile, France).

The API 20E and 50CHB kits can be used for the presumptive distinction of B. anthracis from

other members of the B. cereus group within 48 h. bioMerieux also offers identification cards

for Bacillus and related genera for the VITEK and VITEK Compact automated identification

systems. As many new species have been proposed since these schemes were established,

updated API and VITEK databases have been prepared. Biolog Inc. (Hayward, CA) also offers

aBacillus database. The effectiveness of such kits can vary with the genera and species of

aerobic endospore formers concerned, but they are improving with continuing development

and enlarged databases. The many proposals for new species, often on the basis of single

isolates, make the satisfactory expansion of such databases problematic; for a database to

be effective in identifying a particular species, its entry for that species needs to reflect the

characterization of at least 10 authentic strains from a range of sources, but this requirement

can be very difficult, even impossible, to fulfill. It is stressed that the use of these kits should

always be preceded by the basic characterization tests described below.

Other approaches include chemotaxonomic fingerprinting by fatty acid methyl ester profiling,

pyrolysis mass spectrometry, and Fourier transform infrared spectroscopy. All these

approaches have been successfully applied either across the genera or to small groups. As

with genotypic profiling methods, large databases of authentic strains are necessary; some

of these are commercially available, such as the Microbial Identification System software

(Microbial ID Inc., Newark, DE) database for fatty acid methyl ester analysis.

For diagnostic purposes, the aerobic endospore formers comprise two groups: the reactive

ones, which give positive results in various routine biochemical tests and which are therefore

easier to identify, and the nonreactive ones, which give few, if any, positive results in such

tests. Nonreactive isolates tend to dominate the identification requests sent to reference

laboratories. Table 1 shows reactions for some species belonging to the former group, and

the phenotypic test scheme outlined above may be used in conjunction with it.



Identification and Detection of B. anthracis

It is generally easy to distinguish virulent B. anthracis from other members of the B.

cereus group. B. anthracisisolates are characterized by typical microscopic appearance (Fig.

1b and 2a) and colonial morphology (Fig. 3a): colonies are white or gray, nonhemolytic or

only weakly hemolytic, susceptible to the diagnostic gamma phage (inquiries about gamma

phage should be addressed to the Diagnostics Systems Division, USAMRIID, Fort Detrick,

Frederick, MD), generally susceptible to penicillin, nonmotile, and able to produce the

characteristic capsule as shown by M’Fadyean staining (Fig. 2a) or India ink staining (Fig.

1b). As an alternative to culture in blood, the capsule of virulent B. anthracis can be

demonstrated on nutrient agar containing 0.7% sodium bicarbonate, incubated overnight

under 5 to 7% CO2 (candle jars perform well). Colonies of the capsulated organism appear

mucoid, and the capsule can be visualized by M’Fadyean or India ink staining of smears or by

DFA staining (Fig. 1c; see below).

In addition to phenotypic analysis, molecular and antigenic detection assays are available for

the rapid identification of B. anthracis. The LRN PCR (restricted to LRN laboratories; see

above) targets three distinct loci on the B. anthracis chromosome, pXO1 virulence plasmid,

and pXO2 virulence plasmid. Using several loci increases specificity and allows for the

detection of avirulent strains (lacking pXO1 or pXO2). The anthrax toxin genes (pagA, lef,

and cya) are located on pXO1, while the genes required for capsule

biosynthesis (capBCA) are located on pXO2. Isolates lacking pXO2 or both plasmids are

mostly found in the environment and are frequently mistaken for B. cereus, due to the lack

of a capsule, and discarded. These genes have been widely used as B. anthracis-specific

gene targets; however, there have been recent reports of these genes in species other

than B. anthracis (8, 55, 67). Recently several laboratories have developed specific PCR

assays for B. anthracis that target chromosomal genes such

as rpoB, gyrA, and plcR (39, 70, 111).

A two-component DFA assay has been and is currently used to identify encapsulated

vegetative cells of B. anthracis (33, 45). This assay uses two different monoclonal antibodies

specific for a B. anthracis cell wall antigen and the B. anthracis capsule (Fig. 1c). Neither

antigen is 100% specific for B. anthracis; however, onlyB. anthracis has been found to be

positive for both antigens, and thus, the assay is 100% specific when both cell wall and

capsule components are used together. It was heavily used at the CDC during the 2001

bioterrorism-associated outbreak for the rapid (<4-h) identification of isolates (33).

Tetracore Inc. (Gaithersburg, MD) has produced a rapid (yielding a result within 15 min)

immunochromatographic test (RedLine Alert) utilizing an antibody specific for one of the B.

anthracis S-layer proteins. This assay has been approved by the Food and Drug

Administration (FDA) for use on nonhemolyticBacillus species colonies cultured on sheep

blood agar plates. Manufacturer’s data suggest that the test was 98.6% sensitive when

tested on 145 B. anthracis isolates and 45 nonhemolytic, non-B. anthracis isolates; however,

such identification of B. anthracis is only considered presumptive, and this test should not be

used as a stand-alone test.

An immunochromatographic field assay has been developed by the U.S. Naval Medical

Research Center (NMRC), Silver Spring, MD, to detect PA in samples of blood or tissue

exudates (Bacillus anthracisimmunochromatographic field assay). Inquiries from veterinary

and public health authorities should be directed to the NMRC by calling 301-319-

7409 or in writing to the Naval Medical Research Center, 503 Robert Grant Ave., Silver

Spring, MD 20910 (J. Czarnecki, NMRC, personal communication, 2007). The assay has been

used to detect B. anthracis in animals, even several days after death. The assay has a high

sensitivity for the detection of B. anthracis in an infected animal and has a high specificity

(regarded as 100%; 95% confidence interval, 98.5 to 100%) for detection of the organism in

cattle (104). Among 10 recently vaccinated bovines in one study, the assay yielded no falsepositive

reactions.

Identification of Bacillus cereus and B. thuringiensis

Colonies of B. cereus and relatives are very variable but readily recognized (Fig. 3a to c):

they are characteristically large (2 to 7 mm in diameter) and vary in shape from circular to

irregular, with entire to undulate, crenate or fimbriate edges; they have matte or granular

textures. Smooth and moist colonies are not uncommon, however. The optimum growth

temperature is about 37°C, with minima and maxima of 15 to 20°C and 40 to 45°C,

respectively. Although colonies of B. anthracis and B. cereus can be similar in appearance,

those of the former are generally smaller and nonhemolytic, may show more spiking or

tailing along the lines of inoculation streaks, and are very tenacious compared with the

usually more butyrous consistency of B. cereus and B. thuringiensis colonies, so that they

may be pulled into standing peaks with a loop. Bacillus mycoides produces characteristic

rhizoid or hairy-looking, adherent colonies which readily cover the whole agar surface.

The key characteristics for recognizing and distinguishing the B. cereus group are colonial

morphology (Fig. 3ato c); large cells often in chains, producing ellipsoidal spores not swelling

the sporangia (Fig. 2b and c), usually within 48 h and often apparent after 24 h; facultative

anaerobes; and positive egg yolk reaction (i.e., lecithinase). Negative or very weak

hemolysis and lack of motility distinguish B. anthracis and B. mycoides fromB. cereus and B.

thuringiensis. Bacillus cereus, B. mycoides, B. thuringiensis, and, to a lesser extent, B.

anthracissynthesize lecithinases, forming opaque zones of precipitation around colonies on

egg yolk agar as the colonies grow (i.e., usually after overnight or perhaps 24 h of

incubation). Recognition of B. thuringiensis is largely dependent on observation of its cuboid

or diamond-shaped parasporal crystals in sporulated cultures (after 2 to 5 days) by phasecontrast

microscopy (Fig. 2c), or by staining with malachite green counterstained with carbol

fuchsin or safranin.

Toxin Detection

The enterotoxin complex responsible for the diarrheal type of B. cereus food poisoning has

been increasingly well characterized (128). Two commercial kits are available for its

detection in foods and feces, the Oxoid BCET-RPLA (Oxoid Ltd.) and the TECRA VIA (TECRA

Diagnostics, Roseville, New South Wales, Australia). However, these kits detect different

antigens, and there is some controversy about their reliabilities. Other assays, based on

tissue culture, have also been developed. The emetic toxin of B. cereus, cereulide, has been

identified as a dodecadepsipeptide, and it may be nonspecifically assayed in food extracts or

culture filtrates using HEp-2 cells (46), boar semen (4), and rat mitochondria (75). Specific

detection requires high-performance liquid chromatography-mass spectrometry (59), and the

synthetic apparatus may be detected by real-time PCR (49).



TYPING SYSTEMS Back to top

Genotyping of B. anthracis

B. anthracis is a genetically monomorphic species and has been shown to be clonal by

multilocus sequence typing (MLST). The first method described that could differentiate

strains with any useful resolution was a multiple-locus variable-number tandem-repeat

analysis (MLVA) assay targeting eight loci, MLVA-8 (76). This method was relied on during

the 2001 bioterrorism-associated outbreak in the United States, which implicated the Ames

strain, and continues to be useful today (76, 132). There are now multiple MLVA schemes

available for the genotyping of B. anthracis, including expanded versions of the original

MLVA-8. These include schemes which employ agarose electrophoresis, capillary

electrophoresis, or mass spectrometry for fragment analysis (76, 87, 89, 143). An online

database, MLVAbank, is also now available at http://minisatellites.u-psud.fr/MLVAnet/, which

can accept data entry for 25 variable-number tandem repeats. There are also several reports

on the analysis of single nucleotide repeats to differentiate very closely related isolates

(77, 78, 87,89, 131).

The sequencing of multiple B. anthracis genomes has also led to additional approaches to the

genotyping of B. anthracis, such as the use of single nucleotide polymorphisms and DNA

microarrays. Single nucleotide polymorphisms have been identified and used for the

differentiation of B. anthracis lineages and for detection of specific strains such as the Ames

strain (144, 145). This approach may continue to become more powerful as more genome

data become available and are analyzed. Microarrays have also been used for strain

characterization and comparisons (36, 153). However, they have not been widely used and

seem to be less attractive now that newer de novo sequencing technologies have become

more affordable and allow for the rapid generation of complete or almost complete genome

sequence data. As technologies continue to improve and the costs decrease, the complete

genomic sequence will increasingly be used for isolate characterization.

Genotyping of Other Species

The majority of work on molecular typing (i.e., genotyping) of Bacillus spp. has focused on

members of the B. cereus group due to their clinical importance and the value of genotyping

for molecular epidemiology. In the past, this group was differentiated into serovars based on

flagellar antigen variations; however, this is not commonly used today and has largely been

replaced by molecular methods. Numerous molecular methods have been attempted to some

degree for the differentiation of Bacillus isolates. Recently, MLST, which compares the partial

sequences of seven housekeeping genes to differentiate strains, has become the favored

approach due to decreasing costs, portability of data, and availability of public databases on

the World Wide Web. Several MLST schemes targeting different sets of genes have been

reported and generally show similar clusters of isolates into three distinct clades

(64, 81, 110, 126, 136). Pathogenic isolates are distributed throughout clades 1 and 2, while

no clinical isolates have been identified as belonging in clade 3 (34, 68). With the exception

of B. anthracis and emetic isolates of B. cereus, which are largely clonal, B. cereusgroup

isolates are represented by a large number of distinct sequence types, and clustering does

not correlate with classic microbiological species identification. Simpson’s index of diversity

(measure of the likelihood of two isolates from epidemiologically distinct events having the

same sequence type) was calculated to be 0.989 (1.0 is absolute discrimination) in one study

of clinical isolates, which suggests that in addition to being a powerful phylogenetic tool, it

may be useful for molecular epidemiology (68). The most powerful aspect of MLST is the

availability of online databases for several of the MLST schemes, which allows for worldwide

access to view and deposit isolate data. The Priest scheme is available

athttp://pubmlst.org/bcereus/, and an optimized version of the Tourasse scheme, including a

multischeme database (SuperCAT), is available at mlstoslo.uio.no/ (110, 136, 137).

SEROLOGIC TESTS Back to top

Serologic assays for the detection of antibody response against the anthrax toxin protein, PA,

have been used in combination with PCR or IHC assay results to confirm anthrax cases when

culture failed. A quantitative human anti-PA immunoglobulin G (IgG) enzyme-linked

immunosorbent assay was performed at the CDC during the 2001 outbreak and was positive

only with sera from individuals with anthrax or vaccinated with anthrax vaccine adsorbed

(AVA; see “Vaccines” below) (112). An FDA-approved, qualitative kit (QuickELISA Anthrax-

PA kit) from Immunetics (Boston, MA) is not currently available, but production could be

initiated if needed for the detection of anti-PA IgG and IgM antibodies in human serum.

Serologic assays aided in the effort to confirm cases in the 2001 attack, particularly

cutaneous ones; however, the time to seroconversion after infection limits the usefulness of

this approach, given the rapid diagnosis necessary for treatment and public health response.

The three protein components of anthrax toxin (PA, LF, and edema factor [EF]), and

antibodies to them, can be used in enzyme immunoassay systems. For routine confirmation

of anthrax infection or for monitoring response to anthrax vaccines, antibodies against PA

alone appear to be satisfactory; they have proved useful for epidemiological investigations

with humans and animals. In human anthrax, however, early treatment sometimes prevents

development of a detectable rise in antibody titer (113). PA, LF, and EF are available

commercially from List Biological Laboratories, Inc., Campbell, CA (http://www.listlabs.com).

In countries of the former USSR, a skin test utilizing anthraxin, a heat-stable extract from a

noncapsulate strain of B. anthracis that has been licensed for human and animal use since

1962, is widely acclaimed for retrospective diagnosis (123). The delayed-type

hypersensitivity is interpreted as indicating cell-mediated immunity to anthrax and can be

used to evaluate the vaccine-induced immune status after periods of several years, as well

as to diagnose anthrax retrospectively. Anthraxin does not contain highly specific anthrax

antigens and relies on the fact that the only Bacillus species likely to proliferate within and

throughout an animal is B. anthracis. This is also true of the Ascoli test, which, dating from

1911, must be one of the oldest antigen detection tests in microbiology. It is a precipitin test

using hyperimmune serum raised to B. anthraciswhole-cell antigen to provide rapid

retrospective evidence of anthrax infection in an animal from which the material being tested

was derived. The test is still in use in Eastern Europe and central Asia.

ANTIMICROBIAL SUSCEPTIBILITIES Back to top

Bacillus anthracis

Most strains of B. anthracis remain susceptible to penicillin (30, 102, 141). Of 25 genetically

diverse isolates from around the world, three strains were resistant to penicillin but were

negative for β-lactamase production. Most strains give variable susceptibility results for

cephalosporins; in vitro results, even if susceptible, may not predict clinical efficacy,

particularly for expanded- and broad-spectrum cephalosporins (30). In a study of 50

historical isolates from humans and animals and 15 clinical isolates from the 2001

bioterrorism attack in the United States, the majority of strains could be regarded as not

susceptible to the broad-spectrum cephalosporin ceftriaxone, and 3 were resistant to

penicillin (102). Tetracyclines, fluoroquino lones, and chloramphenicol are suitable for the

treatment of patients allergic to penicillin; most strains in the previously mentioned study

showed only intermediate susceptibility to erythromycin (102). Ciprofloxacin and the newer

quinolone gatifloxacin had good in vitro activities against 40 Turkish isolates, but for another

new quinolone, levofloxacin, it was observed that MICs were high for 10 strains (43). Other

in vitro studies have shown novel fluoroquinolones and a ketolide to be of potential

therapeutic value (37, 48). Standards for antimicrobial susceptibility testing of B.

anthracis have been recently adopted (28), and a DNA microarray for detecting antimicrobial

resistance determinants in B. anthracis and B. cereus has been developed (7).

Postexposure prophylaxis (PEP) is needed for the prevention of inhalation anthrax following

exposure to aerosols containing B. anthracis spores; the recommended regimen is 60 days of

antimicrobial therapy and three doses of AVA (17), and recommended antimicrobial agents

include ciprofloxacin, doxycycline, and levofloxacin. PEP was, for example, recommended for

four persons who had been in the unventilated work space during procedures that generated

aerosols from untreated animal hides used for making drums. Amoxicillin is recommended as

an option in cases where the B. anthracis strain has been demonstrated to be susceptible to

penicillins, and when other antimicrobial agents are not considered safe, as in the treatment

of children and pregnant or lactating women (20, 21). The use of penicillins for PEP or for

treatment of inhalation anthrax following the use of B. anthracis as a bioweapon gives cause

for concern, owing to the presence of β- lactamases in B. anthracis isolates and the poor

penetration of β-lactams into macrophages, the site of spore germination (9). Combination

intravenous antimicrobial therapy with two or more antimicrobial agents, begun early, such

as with ciprofloxacin and one or more other antimicrobial agents to which the organism is

sensitive, appeared to improve survival rates during treatment of cases in the 2001 event in

the United States (71). Following that event, the recommendation for initial treatment of

inhalation anthrax is intravenous ciprofloxacin or doxycycline along with one or more agents

to which the organism is normally susceptible (19); ciprofloxacin is favored over doxycycline

as the primary antimicrobial agent due to its bactericidal action and central nervous system

penetration in the event of meningeal involvement (129). A mouse aerosol challenge model

has been developed for determining antimicrobial agent efficacy in the treatment of

inhalation anthrax (62). In a case of inhalation anthrax that was naturally acquired when

processing untreated animal hides for drum construction, the patient’s therapy included

adjunctive use of human anthrax immunoglobulin (147); however, the use of anthrax

immunoglobulin in the treatment of a subsequent inhalation anthrax case in 2008 did not

prevent a fatal outcome (3).

Bacillus cereus

There have been rather few studies of the antimicrobial susceptibility of Bacillus cereus, and

most information has to be gleaned from reports of individual cases or outbreaks. Bacillus

cereus and B. thuringiensis produce a broad-spectrum β-lactamase and are thus resistant to

aminopenicillins and cephalosporins; they are also resistant to trimethoprim. An in vitro

study of 54 isolates from blood cultures by disk diffusion assay found that all strains were

susceptible to imipenem and vancomycin and that most were sensitive to chloramphenicol,

ciprofloxacin, erythromycin, and gentamicin (but a small number of strains showed moderate

or intermediate susceptibility), while 22 and 37% of strains showed only moderate or

intermediate susceptibilities to clindamycin and tetracycline, respectively (148). Although

strains are almost always susceptible to clindamycin, erythromycin, chloramphenicol,

vancomycin, and the aminoglycosides, and are usually sensitive to tetracycline and

sulfonamides, there have been several reports of treatment failures with some of these

drugs: a fulminant meningitis which did not respond to chloramphenicol (96); a fulminant

infection in a neonate which was refractory to treatment that included vancomycin,

gentamicin, imipenem, clindamycin, and ciprofloxacin (139); failure of vancomycin to

eliminate the organism from CSF in association with a fluid shunt infection (11); vancomycin

resistance in strains from respiratory specimens from pediatric intensive care patients (73);

and persistent bacteremias with strains showing resistance to vancomycin in two

hemodialysis patients (A. von Gottberg and W. van Nierop, personal communication). Oral

ciprofloxacin has been used successfully in the treatment of B. cereus wound infections,

bacteremia, and pulmonary infection, and in vitro activity has been shown for daptomycin

(27). Clindamycin with gentamicin, given early, appears to be the best treatment for

ophthalmic infections caused by B. cereus, and experiments with rabbits suggest that

intravitreal corticosteroids and antimicrobials may be effective in such cases. CLSI document

M45-A (29) tabulates antimicrobial breakpoints for aerobic, endospore-forming species.

Other Species

Information is sparse on treatment of infections with other species. Gentamicin was effective

in treating a case of B. licheniformis ophthalmitis, vancomycin was successful in cases of B.

licheniformis peritonitis in a CAPD patient (107) and a pacemaker wire infection, meropenem

succeeded in a case of brain abscess, and cephalozin was effective against B.

licheniformis prosthetic aortic valve endocarditis. Resistance to macrolides appears to occur

naturally in B. licheniformis. B. subtilis endocarditis in a drug abuser was successfully treated

with a cephalosporin, and gentamicin was successful against B. subtilis septicemia. A B.

pumilus central venous catheter infection treated with several drugs, including flucloxacillin,

clindamycin, and vancomycin, failed to clear, and the catheter had to be replaced with a new

one (10). Two cases of cutaneous infections with B. pumilus initially diagnosed as anthrax

were treated successfully with amoxicillin-clavulanate, while a third such case was treated

with ciprofloxacin (134). Daptomycin and ciprofloxacin show in vitro activity against strains

of B. pumilus, B. subtilis, and some other species (27). Penicillin, or its derivatives, or

cephalosporins probably have long been the first choices for treatment of infections

attributed to other Bacillusspecies. However, in a study by Weber et al. (148), over 95% of

isolates of B. megaterium, B. pumilus, B. subtilis, B. circulans, B. amyloliquefaciens, and B.

licheniformis, along with strains of B. (now Paenibacillus)polymyxa and three unidentified

strains from blood cultures, were susceptible to imipenem, ciprofloxacin, and vancomycin,

and only between 75 and 90% were susceptible to penicillins, cephalosporins, and

chloramphenicol. Isolates of “B. polymyxa” and B. circulans were more likely to be resistant

to the penicillins and cephalosporins than strains of the other species—it is probable that

some or all of the strains identified as B. circulans might now be accommodated

in Paenibacillus, along with “B. polymyxa.” An infection of a human bite wound with an

organism identified as B. circulans did not respond to treatment with amoxicillin and

flucloxacillin but was resolved with clindamycin, while peritonitis in a CAPD patient was

resolved with vancomycin. However, a strain identified as B. circulans and showing

vancomycin resistance has been isolated from an Italian clinical specimen (88). Vancomycin

resistance has been reported for P. popilliae, a biopesticide, and isolates of this species have

been shown to carry genes resembling those responsible for high-level vancomycin

resistance in enterococci (108). Of two South African vancomycin-resistant clinical isolates,

one was identified as Paenibacillus thiaminolyticus and the other was unidentified but

considered to be related toBacillus lentus. The latter was isolated from a case of neonatal

sepsis and has been shown to have inducible resistance to vancomycin and teicoplanin; this

is in contrast to the B. circulans and P. thiaminolyticus isolates mentioned above, in which

expression of resistance was found to be constitutive (von Gottberg and van Nierop, personal

communication).

VACCINATION Back to top

AVA, the current human vaccine in the United States, is a cell-free filtrate (formalin treated),

in an aluminum hydroxide-adsorbed gel, from a noncapsulated, nonproteolytic derivative of

strain V770-NP1_R grown under microaerobic conditions. The FDA has approved a new route

and schedule for preexposure immunization with AVA, which calls for a series of five

intramuscular injections administered at 0 and 4 weeks and at 6, 12, and 18 months (95).

To maintain immunity, an annual booster injection is recommended. Anthrax vaccine

precipitated, the current human vaccine in the United Kingdom, is an alum-precipitated cellfree

filtrate of Sterne strain (34F2) cultured, under static batch conditions, with activated

charcoal to increase PA production. Both anthrax vaccine precipitated (150) and AVA contain

PA as well as trace amounts of LF, EF, and cell wall proteins. In October 2008 the ACIP voted

to accept provisional recommendations for the pre-event use of anthrax vaccine among

persons considered to be at risk for exposure to aerosolized B. anthracis spores; these

provisional recommendations included new language to address emergency responders, in

addition to the previously approved recommended occupational and laboratory populations.

The ACIP recommends routine preexposure vaccination with AVA for persons engaged in

work involving (i) production of high concentrations or pure cultures of B. anthracis spores,

(ii) activities with a high potential for production of aerosolized spores, (iii) handling of

environmental samples associated with anthrax investigations (especially powders) and

performance of confirmatory testing for B. anthracis in the U.S. LRN for bioterrorism level B

laboratories or above, (iv) making repeated entries into known B. anthracis sporecontaminated

areas or settings in which repeated exposure to aerosolized B. anthracis spores

might occur, and (v) engaging in environmental investigations or remediation efforts of

spore-contaminated areas or other settings with aerosol exposure. Immunization is not

routinely recommended for emergency and other responders but may be offered on a

voluntary basis as part of a comprehensive occupational health and safety program.

Laboratory workers using standard biosafety level 2 practices in the routine processing of

clinical or environmental specimens in general diagnostic laboratories are not at increased

risk for exposure to B. anthracis spores (22, 25). The development of anthrax vaccines,

including second- and third-generation products, and that of several human monoclonal and

polyclonal antibody products currently in their early development and testing phases are the

subjects of recent reviews (120, 138).

EVALUATION, INTERPRETATION, AND REPORTING OF

RESULTS Back to top

While, of course, the isolation of B. anthracis is always significant and requires urgent

reporting, the majority of other aerobic endospore-forming species are environmental

organisms, and so they are frequent laboratory contaminants. Therefore, isolation from a

single clinical specimen is generally not a sufficient basis for incriminating one of these

organisms as the etiological agent; however, any such organism should be considered of

potential clinical significance if it is isolated in pure culture or at least apparently dominating

the microbiota, or if it is isolated in large numbers or isolated more than once. Opportunistic

infections with Bacillusspecies other than B. anthracis have been reported since the late 19th

century, and in the last 30 years the clinical importance of aerobic endospore formers (most,

but not all, of them Bacillus species) has become widely accepted. It is most important to

assess any clinical isolation of such an organism in the light of any other species cultured and

the clinical context and to be wary of dismissing it as a mere contaminant. Moderate or

heavy growth of aerobic endospore formers from wounds is usually significant, and B.

cereusinfections of the eye are serious emergencies that should always be reported to the

physician immediately.

Low-level contamination of foodstuffs by aerobic endospore formers is commonplace, as is

asymptomatic transient fecal carriage. Therefore, in foodborne illness investigations,

qualitative isolation tests are insufficient. The ideal criteria for establishing that an aerobic

endospore former is the etiological agent are (i) isolation of significant numbers

(>105 CFU/g) of the organism from the epidemiologically incriminated food (and, in the case

of suspected B. cereus food poisoning, detection of emetic toxin and/or enterotoxin) and (ii)

recovery of the same strain (biovar, plasmid type, etc.) in significant numbers from acutephase
specimens (feces or vomitus) from the patients but not from healthy controls.

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