Cumitech 27: Laboratory Diagnosis of Zoonotic Infections

IN CLINICAL

MICROBIOLOGY

FEBRUARY

1996

Laboratory Diagnosis of Zoonotic Infections: Bacterial Infections Obtained from ~ Companion and Laboratory Animals _ EDWARD J. BOlTONE, BRUCE HANNA, TAO HONG, THOMAS J. INZANA, HASSAN NAMDARI, M. NASAR QURESHI, and ROBBIN S. WEYANT ,COORDINATING

THOMAS

_/

.P EDITOR‘

J. INZANA

-

-

-

, ‘, ,

*

A . ,aiii AMERICAN ; ,

. ”

SOCIETY -*

“*

FOR MICROBIOLOGY

“a--

“*

Cumitcch IA l Blood Cultures II l June 1982 Cumitcch 2A l Laboratory Diagnosis of Urinary Tract Infections l March 1987 Cumitcch 3A l Quality Control and Quality Assurance Practices in Clinical Microbiology l May 1990 Cumitech 4A l Laboratory Diagnosis of Gonorrhea l April 1993 Cumitech SA l Practical Anaerobic Bacteriology l December lYY I Cumitcch (,A l New Developments in Antimicrobial Agent Susceptibility Testing: a Practical Guide l February I99 I Cumttech 7A l Laboratory Diagnosis of Lower Respiratory Tract Infections l September 1987 Cumitcch 8 l Detection of Microbial Antigen\ by Counterimmunoelectrophoresis l December I978 Cumitech 9 l Collection and Processing of Bacteriological Specimens l August 1979 Cumitcch IO l Laboratory Diagnosis of Upper Respiratory Tract Infections l December I979 Cumttech I I l Practical Methods for Culture and Identification of Fungi in the Clinical Microbiology Laboratory l August 1980 Cumitech l2A l Laboratory Diagnosis of Bacterial Diarrhea l April 1992 Cumitech l3A l Laboratory Diagnosis of Ocular Infections l September 1994 Cumitcch l4A l Laboratory Diagnosis of Central Nervous System Infections l March 1993 Cumitech ISA l Laboratory Diagnosis of Viral Infections l August I994 Cumitech l6A l Laboratory Diagnosis of the Mycobacterioscs l October 1994 Cumitcch l7A l Laboratory Diagnosis of Female Genital Tract Infections l June 1993 Cumitcch IS l Laboratory Diagnosis of Hepatitis Viruses l January 1984 Cunutech I!, l Laboratory Diagnosis of Chlamydial and Mycoplasmal Infections l August 1984 Cumttcch 20 l Therapeutic Drug Monitoring: Antimicrobial Agents l October 1984 Cumttcch 21 l Laboratory Diagnosis of Viral Respiratory Disease l March I986 Cumitech 22 l Immunoscrology of Staphylococcal Disease l August I987 Cumitech 23 l Infections of the Skin and Subcutaneous Tissues l June 1988 Cumitcch 24 l Rapid Detection of Viruses by Immunofuorescence l August 1988 Cumttcch 25 l Current Concepts and Approaches to Antimicrobial Agent Susceptibility Testing l December 198X Cumitech 26 l Laboratory Diagnosis of Viral Infections Producing Enteritis l September 1989 Cumitech 27 l Laboratory Diagnosis of Zoonotic Infections: Bacterial Infections Obtained from Companion and Laboratory Animals l February l’s96 Cumitechs Qureshi. Obtarned Washington,

Editorial Janet Stephen

should

be cited

and R. S. Weyant. from Companion D.C.

Handler,

Board Thomas

for

ASM J

as follows,

e.g.:

Bottone,

1996. Cumitech 27, and Laboratory Animals.

Inzana,

Cumitechs: Brenda

Steven McCurdy,

E. J., B. Hanna,

Laboratory Coordinating

T. Hong,

T. J. Inzana,

H. Namdari,

M. N.

Diagnosis of Zoonotic Infections: Bacterial infections ed.. T. J. Inzana. American Society for Microbiology,

C Specter, Frederrck

Charman, S

Nolte,

John

Mary J R A Smtth,

GIlchrist, Altce S

Curt Gleaves, Wetssfeld, and

Young

The purpose of the Cumrtech series is to provide consensus recommendations by the authors as to appropriate state-of-the-art operating procedures for clinical microbiology laboratories which may lack the facilities for fully evaluating routine or new methods. The procedures given are not proposed as “standard” methods.

Copyright

0 1996 American Society for Mrcrobrology 1325 Massachusetts Ave , N W Washrngton, DC 20005

LABORATORY DIAGNOSIS OF ZOONOTIC INFECTIONS: BACTERIAL INFECTIONS OBTAINED FROM COMPANION AND LABORATORY ANIMALS EDWARD J. BO’ITONE, Division New York,

of Infectious

BRUCE HANNA, Division TAO HONG, Division

of Infectious

of Infectious

State University,

Blacksburg,

HASSAN NAMDARI, Clinical

Virginia

Mount

Mount

Regional 24061

Laboratories,

M. NASAR QURESHI, Department

Department

of Medicine,

The Mount

Sinai Medical

Center,

Sinai

of Medicine,

New York,

New York 10029

Sinai School

of Medicine,

College of Veterinary

Inc., Scranton,

of Pathology

School

Pennsylvania

and Laboratory

Medicine,

New York, New York

Medicine,

Virginia

10029

Polytechnic

Institute

and

I8503 Beth Israel Medical

Center,

New York,

10003

ROBBIN S. WEYANT, Emerging Georgia

Diseases,

Diseases,

THOMAS J. INZANA, Virginia-Maryland

New York

Diseases,

New York 10029

Bacterial

and Mycotic

Diseases

Branch,

Centers for Disease

Control,

Atlanta,

30333

COORDINATING THOMAS J. INZANA, Virginia-Maryland State University,

Blacksburg,

Virginia

Regional 24061

College

EDITOR

of Veterinary

Humanshave alwaysmaintaineda closeassociation with animals.From ancient times humans have dependedon animalsfor food, clothing, and companionship.Companionanimalshavebecome highly valued in this country. In 1992it was estimatedthat there were 52.4 million dogsand 54.6 million catskept aspetsin the United Statesalone (184). Domesticfarm animalshave been and will continue to be essentialsourcesof food and clothing materials.Horsesare also important for recreation and sport racing. Laboratory animalsare essentialin research,particularly in biomedical fields. Wild animalscontinue to be a source of sport and food for hunters.As a result of this close association,animalshave also served as a source of infectious diseasesto their human contacts. While someorganismsare frank pathogensfor both animalsand humans(i.e., Salmonella or Brucella spp.), many organismsthat are pathogenic for animalsor that colonize them do not cause infections in humans,unlessthey are immunocompromised.The advent of AIDS, moreeffective immunosuppressivedrugs for transplant recipients, and chemotherapyfor cancer patients have resulted in an increase in zoonotic infections. Somezoonotic agentsare encounteredonly rarely by clinical laboratoriesand thus may be difficult to identify or even isolate. Other agents,suchas Salmonella, enterohemorrhagicEscherichia coli, and Campylobacter jejuni, are commonly isolated 1

Medicine,

Virginia

Polytechnic

Institute

and

and have been reviewedin other Cumitechs.This Cumitech will not review diagnosisof infections caused by zoonotic agents that are commonly isolatedin clinical laboratories,but rather, it will focus on agents that are isolated occasionally or rarely and that may be unfamiliar to most laboratory personnel.Becauseof the large number of zoonotic agentsthat may be encountered, this Cumitechwill review the bacterial agentsthat may be transmitted to humans by companion and laboratory animals.Cumitech 28 is devoted to diagnosisof chlamydial, mycotic, viral, and parasitic agentsfrom companion and laboratory animals.Although they are bacteria, Chlamydia spp. will be reviewed in the companion to this Cumitech becausethey are usually diagnosedby methods more common to virology laboratories becauseof their obligate intracellular growth requirements. A later Cumitech will review the agentstransmittedto humansby farm animalsand wild animals.In casesin which a zoonotic agent could be reviewed in both Cumitechs(e.g., transmissionfrom farm animalsand from companion animals),the agentwill be reviewedon the basisof its most common mode of transmission.For instance,BruceZZa spp. are transmitted to humans more commonly from farm animals than from companionanimals,and rabies is most commonly transmitted by wild animals. These agents will therefore be reviewed in the later Cumitech.

2

BOTTONE

ET AL.

Diseases that are transmitted by insect vectors and animals that serve primarily as reservoirs (e.g., viral encephalitis) will also be covered in a later Cumitech. Isolation and identification of a zoonotic agent are aided when the mode of transmission is known. Therefore, description of these agents will be organized initially by transmission (e.g., animal bite), except in cases where the mode of transmission is usually not evident (e.g., systemic disease). A list of the zoonotic agents reviewed in this Cumitech, their most common animal reservoir(s), mode of transmission to humans, and the predominant associated disease(s) in humans are presented in Table 1. SPECIMEN COLLECTION, TRANSPORT, AND PROCESSING GUIDELINES FOR ANIMAL BITE WOUNDS Collection and Transport As with essentially all diagnostic microbiology tests, the probability of obtaining clinically relevant culture results from animal bite wound specimens is heavily dependent upon the quality of the specimen submitted to the laboratory. In general, specimens from open bite wounds may be collected following collection guidelines for wounds of skin and subcutaneous tissues (34, 121). Specimens from deeper bite wounds should be cultured following the guidelines for abscesses (121). Specimens collected after 12 h of the time of injury should not be cultured, as they usually do not contain detectable quantities of bacterial pathogens. Exceptions to this rule include bites to the face or hands and bite wounds that show obvious signs of infection. The preferred collection method involves aspirating purulent material with a syringe after decontaminating the surface of the wound to reduce the number of commensal species present. Excess air in the syringe should be expelled immediately. If it is not possible to use a syringe, then a sterile swab may be substituted. Two swabs should be inoculated, one for culture and the other for Gram stain analysis. The swabs should be suspended in a suitable medium, such as Stuart’s or Amies’, for transport to the laboratory. Specimens should be clearly identified as bite wounds and labeled with the date and time of collection, along with the collection site and, if known, the species (dog, cat, rat, human, etc.) responsible for the bite. Specimens should be delivered to the laboratory as soon as possible, although properly collected specimens may be held as long as 24 h at room temperature prior to processing. Dry swabs or specimens that arrive more than 24 h after collection should not be processed or a caveat should be issued about possible loss of viability in transit. If necessary, a repeat specimen should be requested.

CUMITECH

27

CUMI’IECH

27

DIAGNOSIS Processing

In general, bite wound specimensshould be processedfollowing guidelinesestablishedfor skin and subcutaneoustissuewoundsor, when appropriate, abscesses (34, 121). At a minimum, sheep blood agar, selectivemediafor gram-positiveand gram-negativespecies,enrichment broth, and an enrichedmedium,such aschocolate agar, should be inoculated. If cat scratch diseaseis suspected, heart infusion agar with 5% rabbit blood-should be inoculatedfor cultivation of Bationella species; although it has not been isolated from wound sites, if an AJipia speciesis suspected,buffered charcoal-yeastextract (BCYE) agar should be inoculated.Smearsfor Gram stainanalysisshould also be made. If the specimenis received on a swab,the swabshouldbe emulsifiedin enrichment broth and the resultingsuspension shouldbe used to inoculatethe primary growth media.If the specimenis receivedin a syringe,it may be inoculated directly onto the primary growth media. Specimens arriving in syringesshould also be inoculated onto anaerobicgrowth mediaand thioglycolate broth under anaerobicconditions. Aerobic cultures should be incubated in standard conditionsfor clinical bacteriology (elevated humidity, 35 to 37°C 3 to 7% CO,) and inspected daily for at least3 days.In caseswhere no growth is observed on the primary plate cultures, the enrichmentbroths shouldbe incubatedfor 7 days before the culture is finally determined to be negative. If the presenceof Bartonella speciesis suspected,an incubation period of as long as 4 weeksmay be required to yield a positive culture (198).If anAfipia speciesis suspected,BCYE agar plates should be incubated at 25 to 30°C for at least5 days. GRAM-NEGATIVE SPECIES ASSOCIATED WITH ANIMAL BITE OR SCRATCH INFECTIONS

It hasbeenestimatedthat one out of every two Americans will be bitten in his or her lifetime, usually by a dog. One to two million Americans suffer from animal bites every year, and these account for about 1% of emergencydepartment visits (47, 95). All of the bacteria describedin this section normally reside in the oral cavity and nasopharynxof dogs and cats (163). As a result, they are most commonly isolated from humans following bite wounds. Becauseof the frequent grooming nature of dogs and cats, however, the bacteria also may be recovered from wounds following scratches. Pasteurella

spp.

The taxonomy of speciesin the family Pasteurellaceae, which includes the genera Pasteurella, Haemophilus, andActinobacillus, is currentlv in a

OF ZOONOTIC

INFECTIONS

3

state of flux. Somespeciesin the genusPasteurella are closelyrelated to Actinobacillus spp.,asdetermined by DNA hybridization studies(124, 125). Speciesthat have been transferred to Actinobacillus include Pasteurella ureae, P. aerogenes, P. pneumotropica, and some isolates of P. haemolytica. For the purposesof this review, however, we will usethe traditional genusname. Description, natural habitat, and mode of transmission Pasteurella spp. are composedof a group of

small gram-negativecoccobacilliwith a tendency toward pleomorphism.Most of the speciesare parasitesof the respiratory or intestinal tract of a variety of householdpets,wild animals,and birds. Specifically, Pasteurella spp. have been found in cats, dogs, cattle, horses,swine, sheep,fowl, rodents, rabbits, monkeys, lions, panthers, lynxes, birds, buffaloes,and reindeer (78). Human infectionscausedby Pasteurella spp.are most frequently associatedwith animal contact, particularly bites and scratches.Pasteurella multocida is the speciesmostcommonlyrecoveredfrom human infections and is usually associatedwith more seriousinfectionsthan other Pasteurella spp. (89). P. multocida hasnow beendivided into three subspecies:subsp.multocida, subsp.septica, and subsp.gallicida (124).P. multocidk occupiesan ecological niche in the nasopharynxof cats, whereas in dogsthe tonsilsare commonly colonized. Pasteurella survivespoorly in water or soil. Transmissionof P. multocida to humansis usually through traumatic encounter with an animal host. Nontraumatic contact with catshasalsobeenreported to be associatedwith P. multocida pneumoniain a patient with AIDS (48). Human

infections

In humans,P. multocida causesvarious types of infections,mostof which follow somecontact with domesticanimals.Local infections in humansare usually associatedwith cat and dog bites and/or scratches inflicted by these animals (5). The wound infection is characterized by rapid development of pain, erythema, swelling,cellulitis, and purulent drainage. Osteomyelitis of underlying bonesmay developnear the site of initial infection asa consequenceof cellulitis spread. P. multocida has also been isolated from the human respiratory tract, especiallyin the setting of chronic respiratory disease.It may be a causeof pneumonia,empyema,bronchitis, sinusitis,tonsillitis, and otitis media. Casesof epiglottitis have also been reported (111, 161). A caseof P. multocida keratitis and cornea1laceration subsequent to a cat scratchhasbeen reported (84). P. multocida hasalsobeen identified asan etiologic agent of life-threatening systemicinfections (90, 194), including bacteremia followed bv endocarditis.

4

BOTTONE

ET AL.

purulent pericarditis, prosthetic valve infection, and central nervous systeminfections (e.g., meningitis, subduralempyema,or brain abscess). In at leastone case,in utero infection with P. multocida hasresulted in abortion of the fetus, resulting in or as a result of bacteremia(190). Most, but not all, patients with systemicP. multocida infections have had an underlying diseaseor been immune compromised.P. multocida peritonitis in patients undergoing ambulatory peritoneal dialysis has alsobeen describedand associatedwith a cat bite of the dialysistubing (113, 141).P. multocida has alsobeen isolatedfrom asymptomaticindividuals who haveprofessionalor recreationalcontact with animals(171, 174). Other Pasteurella

species

Although mosthumanPasteurella isolatesareP. muztocida, several other specieshave been isolated from human infections. In one study, P. canis, P. stomatis, and P. dagmatis were the most commonhuman isolatesafter P. muZtocida (89). Except for P. canis infections, which were associated with dog bites, infections were associated with cat bites or scratches.P. canis is a relatively new species,and isolateswere previously identified as canine P. muZtocida (124). There are two biotypes of P. canis; biotype 1 strainsoccur in the oral cavity of dogs and are indole positive, and biotype 2 isolatescomefrom cattle and are indole negative.P. canis is distinguishedfrom P. multocida by mannitol and sorbitol fermentation (Table 2). Isolatesof P. stomatis from companionanimal bites, scratches,or licking infections are also not uncommon. Most infections reported, however, have beenin woundsoriginating from catsor dogs (89) . ,. Pasteurella dagmatis and “P. pneumotropica” have been isolatedfrom the respiratory tracts of cats, dogs,rats, and mice. Isolatesof P. dagmatis were previously classified as Pasteurella “gas,” Pasteurella new species1, or P. pneumotropica Henriksen (124). Human infections with these agents may result from traumatic exposure to animals (61). P. pneumotropica and P. dagmatis are both indole and ureasepositive, but they can be differentiated by xylosefermentation (Table 2). “P. aerogenes ” is a commensalof swine,but it hasbeenisolatedfrom aborted swinefetuses.This specieshas been recovered from animal bites, urine, and peritoneal fluid from humans (146). Isolatesof “P. ureae” have beendocumentedonly from humans.This organismis thought to be a commensalof the humanrespiratory tract and has beenisolatedfrom humancasesof rhinitis, bronchitis, pneumonia, meningitis, endocarditis, and neonatal conjunctivitis (17, 21, 72, 115). Lack of indole production and presenceof ureaseactivity by “P. ureae” are the major biochemical differ-

CUMITECH

27

ences between it and P. muztocida. “P. aerogenes, ” “P. pneumotropica,” and “P. ureae” may not be true Pasteurella speciesand are likely to be transferred to another genus. P. haemolytica is primarily associatedwith infections in sheep,cattle, and deer. Strainscan be divided into two biotypes: biotype A (usually associatedwith cattle) and biotype T (usually associatedwith sheep). A rare case of human infection hasbeen reported (123). Isolation and identification Pasteurella spp. are small, nonmotile, coccoba-

cillary or rod-shapedgram-negativeorganisms0.3 to 1.0 pm by 1.0 to 2.0 pm in size. In smears preparedfrom infected tissues,they showbipolar stainingwith Giemsaor Wright’s stain.Pasteurella spp. are facultatively anaerobicand will grow on conventional laboratory media containing blood or hematin. On blood agar, P. muztocida is nonhemolytic, but it may produce a brownish discoloration of the medium in areas of confluent growth. A distinct odor, describedassmellinglike a wet mouseor “mousy,” is characteristic of P. muztocida. The optimum temperature for growth is 37°C.Growth may occur, however, between25 and 40°C.At optimum conditions,Pasteurella spp. grow rapidly, with colony size reaching1 to 3 mm after 24 h of incubation. Colonies are round, smooth,and gray, a feature sharedby most Pasteurella spp.Someisolatesof Pasteurella (particularly P. multocida type A) produce a large hyaluranic acid capsule that imparts a watery to mucoid character to the colonies.Other virulent strains produce smooth, encapsulated,iridescent colonies that may convert to rough, unencapsulated, noniridescentcoloniesupon subculture.P. multocida is catalase and oxidase positive and produces acid from glucose, mannitol, and sucrose.A key test is the production of indole only on media containing blood. Therefore, the spot indole test shouldbe done on suspectedP. multocida coloniesfrom blood agar. Five serotypesare known (A, B, D, E, and F) on the basisof capsular antigens.The differential propertiesof Pasteurella spp. are listed in Table 2. Antibiotic susceptibility P. multocida isolatesare generallysusceptibleto

a variety of antimicrobial agents(173), including penicillin,ampicillin,carbenicillin,ticarcillin, piperacillin, mezlocillin, expanded- and broad-spectrum cephalosporins,tetracycline, and chloramphenicol. However, isolatesresistantto multiple antibiotics have been encountered(37). P. multocida may be moderately resistantto erythromycin and the aminoglycosides and is resistantto vancomycin and clindamycin. In general,penicillin and broader-spectrumcephalosporinsare the drugsof

sp. A sp. B

-

+ +

+ +

-

V + V

+

+ -

+ V V -

NA NA

+ + -

-

-

NA NA -

+ -

+ -

V

NA NA NA NA NA

+ +

ONPG

+ + + + +

Urease

NA NA

NA NA NA + +

NA NA NA NA NA

Phosphatase

+

V -

V

V V +

+ + + +

ODC

+ +

+ + + + +

+ + + + +

+ + + + +

+ + + + +

Glucose

NA NA

V + + +

+ + + NA

+ NA + + +

NA

+ + + +

Sucrose

V -

V V -

+ + V V

V V -

V V V V

Lactose

V +

+ + -

+ V V

V V V V

V + + +

Xylose

species”

V -

V V +

+

+ + +

+ -

+ + + + -

Mannito1

+ +

+ V V +

+ + + +

+ + + V

V + +

Trehalose

+ -

+ + V -

-

-

V -

-

Arabinose

hydrolysis; ODC, ornithine decarboxylase.

V +

V V V V +

+

+ + + + -

+ +

Maltose

2. Biochemical characteristics for identification of Pasteurella

a +, positive; -, negative; V, variable; NA, not available; ONPG, orthonitrophenyl-P-D-galactopyranoside

Pasteurella Pasteurella

V V V V +

V + V + -

+ + +

-

-

-

bettii lymphangitidis main’ testudinis trehalosi

-

+ -

+ + + + +

P. P. P. P. P.

-

-

stomatis anatis langaa avium violantium

V -

P. P. P. P. P.

-

-

V

-

Lndole

TABLE

Hemolysis

-

Growth on MacConkey

V +

+ + + + +

”

+ + + + t’

P. haemolytica “P. aerogenes” P. dagmatis P. gallinarum P. canis

“P. ureae” ’ ‘P. pneumotropica

subsp. multocida subsp. septica subsp. gallicida

P. multocida

Species

Oxi- Catadase lase

-

V V V +

V

-

+ -

+ + + -

Sorbito1

NA NA

NA NA NA NA NA

NA NA NA NA NA

V NA NA NA

Dulcito1

NA NA

+ + V -

+ + + + NA

NA + + +

+

Galactose

6

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ET AL.

choice for treatment of infection caused by susceptible P. multocida.

CUMITECH

CDC Groups

27

EF-4a and EF-4b

Of the 97 EF-4a strainsstudied at CDC, 32% were isolatedfrom dogbite woundsand 11%were UNUSUAL BACTERIAL SPECIES ISOLATED isolatedfrom canineoral sources.Of the 34 EF-4b FROM ANIMAL BITES strains studied at CDC, 29% were isolated from dog bite woundsand 30% were isolatedfrom cat Description, Natural Habitat, and bite or scratchwounds.To the best of our knowlMode of Transmission edge, there have been no reports of human sysLess-commonbacterial speciesthat have been recoveredfrom companionanimalbite or scratch temic infections causedby these organisms,although systemicinfections have been reported in wound infections can be roughly divided into two categories.One category containsspeciesthat are cats and dogs(119, 199). generally limited to localized wound infections. Specieswithin this category include Neisseria ca- Identification and antibiotic susceptibility nis, Neisseria weaveri, Weeksella zoohelcum, CapCDC groupsEF-4a and EF-4b are gram-neganocytophaga cynodegmi, and Centers for Disease tive coccobacilli that characteristically produce Control and Prevention (CDC) groups EF-4a, smallyellow colonieswith a popcorn-like odor at EF-4b, and NO-l. The secondcategory contains 2 daysof incubationon sheepor rabbit blood agar. speciesof greater invasiveness that are more likely The biochemical characteristicsof these organto be cultured from systemic sources. Species ismsare presentedin Table 3. Key characteristics within this group include Capnocytophaga canifor identification include the production of acid morsus, Streptobacillus moniliformis, Spirillum mifrom glucose,but no other commonly tested carnus, and Bartonella spp. Biochemical profiles of bohydrate; positive oxidase,catalase,and nitrate thesespeciesare presentedin Tables3, 4, and 5. reduction tests;and negative testsfor indole and Recommended procedures for submissionof urease.Demonstration of a fermentative type of specimensto the laboratory may be followed (34, metabolism(moststrainswill acidify the butt of a 122). Unless otherwise indicated, the methods triple sugariron slant), arginine dihydrolaseactivusedto producethe data in thesetablesare those ity, and/or production of gas from nitrate differof the SpecialBacteriology ReferenceLaboratory entiates EF-4a from EF-4b. Antibiotic susceptiat CDC (40). bility studiespublished before group EF-4 was subdividedinto the -a and -b biovarsindicate that Weeksella zoohelcum theseorganismsare generally susceptibleto amiW zoohelcum is a medium-to-longgram-nega- noglycosidesand sulfamethoxazole-trimethoprim, tive rod that, prior to 1986,wasdesignatedCDC but susceptibilityto p-lactamsvariesfrom strainto group IIj (88). Surveysof canineoral flora indicate strain (7, 12). that this speciescommonlyoccursasan oral commensal (7, 163). Most human infections result Neisseria canis from bites or scratchesby cats or dogs. N. canis is a gram-negativediplococcusthat is a Of 41 W zoohelcum strainsstudiedat the CDC, commensalorganismof the canine pharynx and 20 were isolated from woundsassociatedwith a dog or cat bite or scratch. Most isolatesof this an infrequent causeof infection after dog or cat bites (13, 74, 85). Systemicinfections causedby specieshave been obtained from localized wound infections;however,onecaseof meningitiscaused N. canis have not been reported. by W zoohelcum following a dog bite in a S-yearold girl hasbeen reported (20). Identification and antibiotic susceptibility The biochemical characteristics of the type Identification and antibiotic susceptibility strain (ATCC 14687)are presented in Table 3. The biochemical characteristicsof W zoohelThis organismisvery similarto CDC group EF-4b cum are presentedin Table 3. Although colonies but canbe differentiated on the basisof its coccoid are usually nonpigmentedwhen grown on blood cellular morphology and weak, delayed acidificaagar, a tan to yellow diffusible pigment may be tion of glucose.Detection of glucoseacidification observed.Key identifying characteristicsinclude may be method dependent,assomeinvestigators lack of motility, failure to acidify carbohydrates have describedthis organismasasaccharolytic(85, or to grow on MacConkey agar, and positive 187).The literature on N. canis wound infections indole, oxidase,and ureasetests. Using the disk doesnot contain in vitro antibiotic susceptibility diffusion technique, Balie et al. (7) found 10 data, but Guibourdencheet al. reported that their strains of W zoohelcum to be susceptibleto a patient recovered from a mixed infection involvwide variety of antibiotics, including p-lactams, ing P. multocida, Eikenella cowodens, andN. canis aminoglycosides,and sulfamethoxazole-trimetho- after the administrationof amoxicillin at 3 g/day prim. for 1 week (74).

CUMITECH

27 TABLE

DIAGNOSIS

OF ZOONOTIC

INFECTIONS

7

3. Unusual gram-negative bacteria isolated from companion animal wound infections” EF-4a (n = 97)

Test performed

Sign

Motility Fermentative or oxidative Carbohydrate base Acid from: D-Glucose D-Xylose D-Man&o1 Lactose Sucrose Maltose Fructose Catalase Oxidase Growth on: MacConkey agar Salmonella-shigella agar Simmons citrate Urea, Christensen’s Nitrate reduction Gas from nitrate Indole TSI slant, acid TSI butt, acid H,S (TSI butt) H,S (Pb ac paper) Gelatin hydrolysis” Growth at: 25OC 35OC 42°C Esculin hydrolysis Lysine decarboxylase Arginine dihydrolase Ornithine decarboxylase Nutrient broth 0% NaCl 6% NaCl

% Positiveb

F FB + ND + +

EF-4b (n = 34) Sign 0

% Positiveb

OF 100 0 0 0 0 0 100 100 42 (8) 1 3 (1) 0 97” 62 0 3 73 0 95 (2) 60

V V +d V -

V + V V -

89 100 70 0 0 77 (2) 0

V + V --

Sign 0

Weeksella zoohelcum (n = 41)

Sign

% Positiveb

CTA

+ or (+) ND + +

V + V V + V

Neisseria canis (n = 1)

70 (26) 0 0 0 0 0 100 100 65 (6) 0 14 (6) 0 97 0 0 0 6 0 88 9 88 100 69 0 0 0 0

-

(+ 1 ND + +

ND + +

100 100

( +- 1 + + -

+ + V +

2 0 0 100 0 0 98 0 0 0 59 98

ND ND ND ND ND ND

V + + -

30 95 10 0 0 100 0

+ -

+ + or (+) V 15 94 (2) 89 (7) 0 0 6 (2) u +, 90% or more strains tested positive within 48 h of incubation; - , 10% or less strains tested positive; + or (+), positives and delayed positives together total 90% or more; V, variable reaction (11 to 89% of strains tested positive); ND, test not performed; 0, oxidative; F, fermentative; n-o, nonoxidizer; OF, King’s OF medium; FB, fermentation base broth with Andrade’s indicator; CTA, CTA carbohydrate medium (see reference 51 for formulations); TSI, tri le sugar iron; Pb ac, lead acetate. r Numbers in parentheses indicate percentage of strains that show a delayed reaction (positive test detected between 3 and 7 days of incubation). ’ Thirteen strains (13%) completely reduced nitrate and nitrite without gas formation. d Sixteen strains reduced nitrate and nitrite without gas formation. e Seven to 14 days of incubation. Neisseria weaveri

N weaveriisthe recently proposednamefor the gram-negative rods previously known as CDC group M5 (3, 87). N weaveti is the only species assignedto the genus Neisseriathat is not a diplococcus.Of the 132N. weaveristrainsstudied at the CDC, 65% were isolated from dog bite woundsor canineoral cavity specimens.An additional 32% of strainswere isolatedfrom unspecified wounds of the cheek, face, or extremities.

Systemicdiseaseassociatedwith this specieshas not been reported. Identification and antibiotic susceptibility Biochemical data for N weaveti are presented in Table 4. This speciesis negative for most commonly used biochemical tests. Key identifying characteristicsinclude failure to acidify carbohydrates and negative reactionsfor the indole, urease,and nitrate tests. Positive tests include cata-

8

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ET AL.

27

CUMITECH

4. Unusual gram-negative bacteria isolated from companion animal wound infections” S. moniliformis (n = 48)

Test performed

Sign Motility; flagella Fermentative or oxidative Carbohydrate base Acid from: D-Glucose D-Xylose D-Man&o1 Lactose Sucrose

Maltose Inulin Raffinose Catalase Oxidase Growth on: MacConkey agar Salmonella-shigella Simmons citrate Urea, Christensen’s Nitrate reduction Nitrite reduction Indole TSI slant, acid TSI butt, acid H2S

TSI butt Pb ac paper Gelatin hydrolysis” Growth at: 25°C 35°C 42°C Esculin hydrolysis Lysine decarboxylase Arginine dihydrolase Ornithine decarboxylase Nutrient broth 0% NaCl 6% NaCl

70

Positiveb

-

+ or (-t-) -

ND V V V V V V ND ND + ND -

Sign

C. cynodegmi (n = 13) 70

Positiveb

GL F FBd

F FB”

+ or (+) ND ND -

agar

C. canimorsus (n = 90)

79 (20) (4) 0 0 0 81(19)

V + or (+) + or (+)

2 3

+ +

0 0 0 0 0

-

0 29 (12) 26 (7)

V V V

Sign

N. weaveti (n = 132) %

Positiveb

0

0 100 100

+ or (+) + or (+) V + or (+) V V + +

%

Positiveb

-

GL F FBd 48 (32) 0 0 56 (39) 0 53 (39)

Sign

NO-1

Sign -

69 0 0 69 30 69 77 70 100 100

0 0 0 0 0

-

0 0 0 0 0

40 0 11 12

V -

67 0 8 8

(31)

(31) (46) (31) (11)

(10)

ND ND + +

0 0 0 0 0 0

-0 -0 -0 -0 -0 -0

100 100

ND ND + -

V V -

27 (18) 0 0 0 0 72 0 0 0

100

50

-

0

-

0

-

23 0

V -

33 0

V -

0 86 0

-0 V -0

40 87 20

V + -

24 95 8

V -

V + -

24 (31) 0 95 0

+ or (+) + -

10 70 0 77 (23) 0 100 0

+ + V -

94 100 41 0 0 0 0

V + V -0 -0 -0 -0

-

w

--

8 0

V V

85 18

V -

1

100 5

V -0 -0 -5 + ND -0 -0 -0

V -

7 4

70

Positiveb

n-o OF

7 50 0

100f

(n = 22)

5 (15)

20 100 15

10 (5) 0

a +, 90% or more strains tested positive within 48 h of incubation; -, 10% or less strains tested positive; + or (+), positives and delayed positives together total 90% or more; V, variable reaction (11 to 89% of strains tested positive); ND, test not performed; GL, gliding motility, not observed in motility medium (flagella are not detected); 0, oxidative; F, fermentative; n-o, nonoxidizer; OF, King’s OF medium; FB, fermentation base broth with Andrade’s indicator; CIA, CI’A carbohydrate medium (see reference 51 for formulations); TSI, triple sugar iron; Pb ac, lead acetate. b Numbers in parentheses indicate percentage of strains that show a delayed reaction (positive test detected between 3 and 7 days of incubation). ’ Usually requires 20% serum or ascitic fluid. d One to two drops of rabbit serum per 3 ml of medium may be required. e 7-14 days of incubation. f Fewer than 10 strains tested.

lase, oxidase, and, for some strains, growth on CDC Group NO-1 MacConkey agar and/or nitrite reduction. Like CDC group NO-l is a recently describedfastidmost commensalNeisseria spp.,N. weaved is usu- iousgram-negativerod. All 22 of the NO-l strains ally susceptibleto penicillin, ampicillin, and re- studied at CDC were isolated from wound cullated antibiotics. tures, 85% of which were dog or cat bite related.

CUMITECH

27

DIAGNOSIS

OF ZOONOTIC

INFECTIONS

9

Systemicdiseaseassociatedwith NO-l infection hasnot been described.

associatedwith bite wounds(7). However, unlike C. cynodegrni and the other speciesdescribed above, C. canimorsus may causea severesepticeIdentification and antibiotic susceptibility mia with complicationsthat include purpura fulThe biochemicalprofile of CDC group NO-1 is minans, arthritis, meningitis, and endocarditis similar to that of the asaccharolyticAcinetobacter (101, 129, 164, 193). Of the 90 strainsstudied at spp. (86) and is presentedin Table 4. Key identi- CDC, 89% were cultured from blood or cerebrofication characteristicsinclude negative tests for spinal fluid. In most cases,individuals who deoxidaseand urease,along.with positive tests for velop systemicC. canimorsus infections have a nitrate reduction and catalase.The nitrate reduc- predisposingcondition, most commonly a history tion test and bacillary cellularmorphologyare use- of splenectomy,alcohol abuse,or neoplasia(62, ful characteristicsfor differentiating NO-l from 129, 137). In splenectomizedpersons,the infecasaccharolyticAcinetobacter spp. However, cellu- tion is characterized by shock, disseminatedpurlar fatty acid analysisor transformation studies puric lesions,and disseminatedintravascular comay be required for a definitive identification agulation. Renal failure, gangreneof the bite, and (86). In their original description,Hollis et al. (86) wound and pulmonary infiltrates may also occur found that NO-l strains were susceptibleto a (66, 82). However, fatal caseshave alsooccurred variety of antibiotics, including aminoglycosides, in individualswith no known predisposingfactors P-lactams,tetracyclines, quinolones, and sulfon- (31, 101). amides. Capnocytophaga cynodegmi C. cynodegmi is the nameproposedfor a group

Identification

and antibiotic

susceptibility

The biochemical profile of C. canimorsus is presented in Table 4. Characteristicsuseful in of fastidious gram-negativerods formerly desig- differentiating C. canimorsus from C. cynodegmi nated CDC group DF-2-like (23). Of the 13 C. include the failure of C. canimorsus to ferment cynodegmi strains studied at CDC, 4 were ob- sucrose,inulin, and raffinose. Publishedin vitro tained from dog bite wound specimens,3 were antibiotic susceptibilitydata showthis organismto obtained from dog oral cavity specimens,and 1 be susceptibleto p-lactams,tetracycline, clindastrain was obtained from a systemic source mycin, and vancomycin. Susceptibilityto sulfame(blood). Although the number of known C. cynothoxazole-trimethoprim varies from strain to degmi strains is small, it appearsthat systemic strain, and resistanceto the aminoglycosideshas diseasecausedby this speciesis uncommon.As been reported (31, 101). Penicillin is considered indicated by its name, growth of Capnocytophaga the drug of choice for the treatment of C. canispp.is enhancedby CO,. morsus infection, as well as for prophylaxis for asplenicpatients following a dog bite (31, 101). Identification

and antibiotic

susceptibility

Gram-stainedsmearsof theseorganismsshow medium-to-long,thin rods with tapered ends.Although these organismsdemonstrate a gliding type of motility when studiedin wet preparations, they do not produce detectableflagella and give negative results with standard semisolid agarbasedmotility testing methods.Many of the isolates studied at CDC produce beta-hemolysisof rabbit blood that may be enhancedby microaerophilic conditions. The biochemical profile of C. cynodegmi is presentedin Table 4. Key identifying characteristicsfor this speciesinclude positive tests for oxidase and fermentation of glucose, lactose,maltose,and usually inulin and raffinose. Fermentation reactions may be enhanced by heavily inoculating small volumes of medium. Antibiotic susceptibility is similar to that describedbelow for C. canimorsus. Capnocytophaga canimorsus C. canimorsus (formerly CDC group DF-2)

sharesmany morphologic and biochemical features with C. cynodegrni (23). It has been recovered from canine oral and nasal fluids and is

Rat Bite Fever

The term “rat bite fever” (RBF) describestwo similar clinical syndromesassociatedwith infections due to Spirillum minus and Streptobacillus moniliformis following rat bites. Although rat bite is the most common mode of transmission,rare caseshave occurred following bites or scratches by other rodents or direct contact with other rodentsandrodent-ingestinganimals(147). Ingestion of foodscontaminatedwith the organismshas causedepidemicsof Haverhill fever (erythema arthriticurn epidemicurn),which clinically resembles RBF (52, 75). Most casesof RBF have resulted from exposure to wild rats; however, domesticrats have alsobeenimplicated (6,14). Both syndromesof RBF are characterized by a relapsing fever with sudden onset, chills, headache, vomiting, and a skin rash. Spirillum minus Description, natural habitat, and mode of transmission. The form of RBF known assodoku is causedby S. minus, a motile gram-negative

spiralbacterium3 to 5 pm in length and 0.2 to 0.5

10

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ET AL.

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27

pm wide. S. minus in actuality does not reside Streptobacillus moniliformis within the genusSpirillum. According to Bergey’s Description, natural habitat, and mode of Manual of Systematic Bacteriology, it is a “species transmission, The streptobacillaryform of RBF is incertae sedis” (99). Sincethis microorganismhas caused by Streptobacillus moniliformis, a highly yet to be cultivated on artificial media, a type pleomorphic, nonmotile, facultative, gram-negaspecieshasnot been designated. tive rod that frequently occurs in chains and The bacteriumappearsto resideon the teeth of tangled filamentswith bulbous or “monilia”-like rats and other rodents or rodent-ingesting ani- swellings.While morphology varies with the age mals.While it is most commonly transmitted by and conditions of the culture, the organism is the bite of a colonized animal,it isnot unusualfor usually 1 to 5 km long by 0.3 to 0.7 )-Lmwide. severalpersonsto be bitten consecutivelyby a rat Often, filamentsof up to 150 pm with elongated yet for only the first victim to developdisease(77). bulbousswellingsnot unlike a string of beadsmay Blood from injured gums, mouth lesions, and appear (78). The propensity of thesemicroorganconjunctival or pulmonary exudatescontaining S. ismsto produce L forms is well described(78). minus may also contaminate the rodents’ teeth As with S. minus, S. moniliformis resideson the (77). While the bite of an infected rodent is the teeth, middle ear, and upper respiratory tract of usual mode of transmission,caseshave been rats and other rodents (both feral and domestic) known to occur following the bitesof cats,ferrets, or rodent-ingestinganimalsand is part of their and weasels(77). normal flora (6). While the majority of casesresult Human infections. The incubation period for from the bite of rats and other rodents,caseshave sodokuis generally two weeks.This form is char- been reported to occur in the absenceof a bite in acterized by localized swellingand inflammation personswho have had close contact with dogs,. of the inoculation site accompaniedby lymphangi- cats, pigs, or rats (78). Consumptionof contamitis and regional lymphadenitis,in addition to the nated water, milk, or food also has been implisystemicsymptomsdescribed above (147). The cated as a source of infection (78). In a large site of the bite wound usually will be found to outbreak of streptobacillary fever affecting 304 of contain a variety of microorganisms.In the ab- 700 residents (43%) of a boarding school, the senceof a mixed infection, however, the wound etiology of the illnesswasconfirmed by the isolawill heal quickly, but after a week or two the site tion of S. moniliformis from blood culture. An will swelland becomepainful and discolored.An epidemiologicalinvestigation showedan associaindurated, encrusted ulcer of up to 10 cm may tion with the consumptionof water from a source developat the site. By this time the evolving lesion that waslikely contaminatedby rats (116). is accompaniedby lymphatic spreadwith enlargeHuman infections. The incubation period for ment of adjacent lymph nodes, general malaise, streptobacillary RBF is usually shorter (lessthan and fever. Subsequently,a relapsing fever cycle 10 days) than that for sodoku, and local inflambeginswith abrupt elevationsin temperaturefor 1 mation is lesspronouncedaround the wound site. to 2 days, separatedby 3 to 9 daysduring which This form is also characterized by the developthe patient is afebrile, and a purplish maculopap- ment of migratory polyarthritis. S. moniliformis ular rash appearson the armsi legs, trunk, and may be isolated from blood or joint Auid of occasionallythe face, which waxesandwaneswith symptomaticindividuals.Of the 48 S.moniliformis the febrile episodes(77). Some patients may de- strainsstudied at the CDC, 64% were obtained velop septic arthritis or subacutebacterial endo- from blood and 18% were obtained from joint or carditis (159). synovial fluid. While S. moniliformis usually proIsolation and identification. Sincethe organism ducesa mild, protracted illnessthat either has a doesnot grow on artificial media, evidencefor its favorable responseto antibiotic therapy or reetiologic role stemsfrom intraperitoneal inocula- solvesspontaneously,a fatal outcome occurred in tion of blood or exudate from the patient into a two-month-old infant bitten by a wild rat. At guinea pigs or mice. S. minus may be demon- autopsy, the child had an interstitial pneumonia, strated by dark-field examination of peritoneal endocarditis,meningitis,hepatosplenomegaly and fluid or blood from these animals for several lymphadenopathy,aswell aserythrophagocytosis, weeksfollowing inoculation. and sinusoidalmononuclearcell infiltrates in reIdentification of the organismis accomplished gional lymph nodesand the liver (166). by observing exudates of wounds, lymph node Isolation and identification. Primary blood culspecimens,or cutaneousspecimensfor the char- tures shouldbe performed in media that do not acteristicspiral forms by dark-field microscopyor contain sodium polyanethol sulfonate (SPS), as by examiningsmearswith Giemsaor Wright stain. this hasbeen reported to inhibit the growth of S, The organismmay alsobe identified infrequently moniliformis (102). Cultivation in the laboratory from blood. If animal inoculation is attempted, requiresuseof mediaenrichedwith 20% horseor spirillum-free animals, which may be assessed calf serum, 15% blood, or 5% ascitic fluid and serologically,shouldbe used. incubation in a humid environment of 7 to 8%

CUMITECH

27

CO, at 35°C (148). The use of brain heart infusion-cysteinebroth supplementedwith 2.5% Panmede (a papain digest of ox liver) has alsobeen reported to support the recovery of five S. moniliformis strainsfrom simulatedblood cultures(168). Other mediatestedincluded brain heart infusioncysteine broth without Panmede and Brewer’s thioglycolate broth, which were found to be unreliable. The use of sedimentedblood cells as the inoculum for blood culture media has also been reported (158). At the CDC, heart infusion agar, heart infusionbroth, and thioglycolate broth, each supplementedwith rabbit serumto a final concentration of 20%, have been used successfullyto cultivate S. moniliformis. In liquid medium, after severaldaysof incubation, typical puff balls can be seen,while on solid media, l- to 2-mm,grey, smooth,glisteningcoloniesappear. Sincethe organismreadily produces L forms, typical fried egg colonies may also be present. Rapid subculture is recommendedto prevent lossof viability due to changesin pH of the medium (147). Biochemically,the organismis relatively inert, yielding negative reactionsfor indole production, gelatin hydrolysis,nitrate reduction, oxidase,catalase,urease,phenylalaninedeaminase,and digestion of caseinand serum.Carbohydrate reactions are performed in media containing 20% rabbit serum. Alternatively, cysteine tryptic agar base media may be used. In suitable media, acid is producedfrom the fermentation of glucose,maltose, fructose, galactose,glycogen, mannose,and starch but not from rhamnose,raffinose, mannitol, inositol, sorbitol, or glycerol (147). Other biochemicalreactionshave been reported to vary (158). The biochemicalcharacteristicsof S. monilifonnis are listed in Table 4. For microscopicstudies,specimensshould be mixed with an equal volume of 2.5% sodium citrate to prevent clotting (158).The distinctivecellular morphology of S. moniliformis is extremely usefulin the identification of the organism,especially if the patient’s clinical history is consistent with RBF. Serologic diagnosis. Serum agglutininsappear within 10 days after infection and reach a maximumtiter in 3 to 4 weeks.While any titer greater than 80 or a fourfold changein titer is considered to suggestinfection, a definitive titer indicative of infection hasnot been established.

DIAGNOSIS

OF ZOONOTIC

INFECTIONS

11

fication of S. moniliformis by gas-liquidchromatography has been reported but is not widely available (160). In this samestudy, penicillin was the most active of the antibiotics tested in vitro and is the drug of choice, while streptomycin, tetracycline, chloramphenicol, and erythromycin have alsobeen reported to be successful. CAT SCRATCH DISEASE AND BACILLARYEPITHELIOID ANGIOMATOSIS Description

It has been estimated that there are 22,000 casesof cat scratchdisease(CSD) per year in the United States,more than 2,000of which require hospitalizations,with an estimatedannual health care costof more than $12million (91). Numerous linesof evidenceindicate that bacillary-epithelioid angiomatosis(BEA) is a manifestationof CSD in immunosuppresed patients and that both diseases may be causedby Bartonella spp., especiallyBartonella (formerly Rochalimaea) henselae, a recently describedfastidious Rickettsia-like bacterium (154, 155, 197, 201). A closely related species,Bartonella quintana, isthe etiologicagentof trench fever and can alsocauseisolatedlymphadenopathy (153) and bacillary angiomatosisin human immunodeficiencyvirus (HIV)-positive individuals (98). Along with B. henselae and B. quintana, the genusBartonella includesthe following species:B. vinsonii, an organismthat is not associatedwith human diseaseand that was isolated from a Canadian vole; B. elizabethae, an organismassociatedwith endocarditis(42); andB. bacillifomzis, the type speciesand an organism associatedwith a febrile diseaselimited to the Peruvian Andes. Until recently, B. henseZae, B. quintana, B. vinsonii, and B. elizabethae were included in the genusRochalimaea, but they have been reclassifiedon the basisof their phenotypic similarity and close genetic relationship with B. bacilliformis (25). In addition, Bartonella (Rochalimaea) spp. are also responsiblefor bacillary peliosis hepatis (a vasoproliferative diseaseof the liver of HIV-infected patients), relapsing fever, and bacteremia(165). Prior to the identification of B. henselae, similaritiesin histopathologicfindings and a documentedexposureof the patient to cats were noted in patientswith BEA and CSD (93,97, 107, 108, 201). Data suggestingthat the agent of BEA was closely related to B. quintana were Suitability of rapid commercial methods and obtained from the analysisof 16s rRNA gene antibiotic susceptibility. The characteristics of fragmentsamplified in situ from tissuesectionsof seven strains of S. moniliformis, including four BEA lesions(157). Analysis of fastidious gramfrom an outbreak of Haverhill fever, were deter- negative organismsisolatedfrom blood and from mined by the API ZYM system (bioMerieux, cutaneous osseouslesions from BEA patients Plainview, N.Y.) and gas-liquidchromatography showedthem to be Bartonella spp., with both B. (52). Among thesestrains, the enzyme and fatty quintana and B. henselae identified (98). Further acidprofileswere generallyconsistentand may be evidence for the associationof B. henselae with of value in rapid identification. The rapid identi- CSD includes the finding of elevated titers of

12

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ET AL.

antibody to this organism in patients with CSD (68, 156,204), the detection of Bartonella DNA in the CSD skin test reagent by PCR assay (145), and the isolation of B. henselae from lymph node samples of two individuals with CSD (46). These findings suggest that B. henselae may be responsible for the majority of CSD cases. A second organism, Afipia fdis, has also been implicated asan etiologic agent of CSD (24) but hasnot been implicated in BEA. A. felis hasbeen isolated from lesionsof patients with CSD (15, 24). However& felis DNA wasnot found in CSD skin test antigenby PCR, asB. henselaeDNA was (145). Thus, a single etiology for CSD has not been definitively proven. Natural

Habitat

and Mode of Transmission

There is little information availableestablishing the natural habitat of these organisms.CSD has been associatedonly with cat scratchesor bites, and most CSD and BEA infections have been associatedwith immature cats (96). Recently Koehler et al. (96) have indicated that domestic and feral catsare the reservoir for B. henselaeand that this organismcan be cultured from the blood of asymptomaticpet cats of BEA patients. B. henselae hasalsobeen isolatedfrom the blood of a seropositivecat on two occasionsthree weeks apart and identified by PCR-restriction fragment length polymorphismanalysis(156). The authors concludedthat catsmay have active subclinicalB. henseZae infectionsover a long period of time and that cat ownershipwasa risk factor for CSD and BEA. Both B. henselae andA. felis are membersof the alpha-2 group of Proteobacteria,which includesseveralsoil and saprophytic rickettsia-like organisms(15). Thus, catsmay harbor the organismsastransientcommensals on their clawsand in their oral cavity from grooming,thereby transmitting the agent(s)from the soil. Alternatively, cats may transmitthe agent(s)from their salivato their clawsthrough grooming.Catswith fleashave also been reported to be more likely to transmit CSD than catswithout fleas(204).Therefore, fleasmay eventually be found to be the initial vector of B. henselae and/or A. felis. Cats and other animals tested have not appeared to be susceptibleto clinical diseasewith theseagents.Cats associated with CSD have been healthy, have been negative in the skin test, and did not develop diseasewhen inoculated with pus from lymph nodes of CSD patients (192). Development of CSD is almost alwaysassociated with cat contact, either a scratchor bite. The inoculation site may often be missedand sometimes requires thorough examination, including the scalp, within the earlobe, and between the fingers(33). Cat scratchor bite wasthe only analyzedvariableassociated with BEA in 5 HIV-negative immunocompetentpatients, 1 HIV-negative

CUMITECH

27

immunodeficientpatient, and 42 HIV-positive patients when compared with controls. However, one-third of patients had no documentedexposureto cats,indicating that other factors (etiology or reservoir) are also involved in BEA (179). CSD Clinical

disease

Typical CSD is usually a self-limited condition characterizedby the formation of a papule at the site of a cat bite or scratch, which is followed by enlargementof a distal axillary or cervical lymph node 7 to 50 dayslater. Lymphadenopathydue to neoplasiais easilydifferentiated by histopathology of the lymph node aspirate. Complications, although rare, include splenomegaly,encephalitis, thrombocytopenia, pneumonia, and focal demineralizing bone lesions. CSD has traditionally been considereda diseaseof children, but recent epidemiologicalevidence indicates that a significant proportion of casesalso occur in adults (91, 204). Atypical CSD constitutes 11% of casesand is most commonly manifestedby Parinaud’soculoglandular syndrome.Other atypical presentations include tonsillitis, encephalitis,cerebral arteritis, transversemyelitis,radiculitis,granulomatoushepatitis, splenitis,osteolysis,atypical pneumonia,hilar adenopathy,pleural effusion,erythema nodosum, and erythema annulare(112). In one patient with meningoencephalitis,a serologicalresponseto A. felis could be detected in the absenceof a responseto B. henselae and other organisms(49). Isolation

and identification

Until recently, the diagnosisof CSD wasmade on the basisof the following: history of cat contact or the presenceof a scratch or papular lesion at the inoculation site,’ a positive CSD skin test, a characteristic histopathologic analysisof biopsy material, and negative studiesfor other causesof lymphadenopathy (19). Satisfying these criteria cansometimesbe problematic.Numerouscasesof CSD have been reported with a history of cat contact but no evidence of a scratchor bite (68, 204). The CSD skin test.,which utilizes a reagent consisting of sterilized exudate obtained from known cases,is positive in over 90% of clinical cases,but it is also positive in 5% of normal individuals and in greater than 10% of veterinarianshaving no history of disease(188). Additional problemsencounteredwith the skin test include its lack of generalavailability and the fact that a positive test can result from either a recent or previous infection (68). Detection of a humoral immune responseto B. henselae (156) or A. felis (49) could be useful in diagnosis,particularly when acute- and convalescent-phasesera are available.The indirect fluorescent-antibodytest is

CUMITECH

27

DIAGNOSIS

currently beingusedat CDC for detection of antibodiesto speciesof the genusBartonella (Rochalimaea). Enzyme immunoassaysand immunoblotting assaysthat may be more sensitivethan indirect fluorescent-antibodyassaysfor detection of antibodiesto B. henselae have also been described(8, 196). The Infectious DiseaseLaboratory at the University of Georgia offers a serologic test and blood culture to practicing veterinarians to determinewhether cats have been exposedto or are infected with B. henselae. A PCR assayhas been usedto detect B. henselae DNA in patients with CSD (4). The isolation and identification of Bartonella species is describedbelowunder“BEA.” The most common sourcefrom which A. felis hasbeen isolatedis lymph node tissue.No blood or cerebrospinalfluid isolations have been reported. Further epidemiologic and pathogenic studieswith A. felis will be necessaryto further elucidateits role in CSD. Primary isolation of A. felis from lymph node tissuehasbeen difficult to perform, with most of the known isolatesarising from tissueculture infections using lymph node tissuefrom CSD patients (15, 24). Once primary culture is obtained, however, the organismgrows well in either BCYE or nutrient broth under aerobic conditions at 30°C. In fact, one should consider including a 30°C BCYE plate in the primary culture protocol for tissuesfrom suspected CSD patients. Since BCYE will also support the growth of Francisella tularensis, any positive cultures should be treated under biosafety level 3 conditions until the identification of F. tularensis hasbeen ruled out. The biochemicalprofile of A. felis is presented in Table 5. A. felis is a gram-negativerod that is motile with a single polar flagellum. Nitrate is reduced to nitrite, ureaseand oxidase are produced, and weak, delayed acid production from xylose is observed.The organismis negative for most other commonbiochemicaltests, including acid production from glucose.The catalasereaction is variable, with some strains producing a weak reaction. BEA Clinical

disease

In 1983,two independentgroupsreported cases of unusualvasculargrowthson the skin of patients with underlying AIDS (176, 189). Although cultures of biopsy specimensfrom these lesions yielded no growth, bacillary forms were observed by electron microscopyand Warthin-Starry staining. The term epithelioid angiomatosis wascoined for this disorderby Cockrell et al. in 1987andwas later revised to bacillary angiomatosisby LeBoit et al. (41, 107). The diseaseis characterized by proliferation of vascular endothelium and may occur in the skin and solid organs,particularly the

OF ZOONOTIC

INFECTIONS

13

spleenand liver. BEA is grosslyindistinguishable from Kaposi’ssarcoma.If not treated, BEA can be fatal. In two of the five casesdescribedby Cockrell et al., BEA was considered to be the primary causeof death (41). B. henselae is considered the etiologic agent of BEA. Bacillary peliosishepatishasbeenseenin HIVpositive patients who may or may not have clinically visible bacillary angiomas.This liver disease is characterized by proliferation of cystic bloodfilled spacessurrounded by fibromyxoid stroma. Bacteria can be seenin these spaces.Symptoms include fever, weight loss,abdominalpain or fullness,and organomegaly;alkaline phosphataseand y-glutamyl-transferaselevels are elevated (165). B. henselae is alsoconsideredthe causeof bacillary peliosishepatis. B. henselae may alsobe a causeof bacteremia and fever in HIV-infected and non-HIV-infected adults and children (165, 196). Most, if not all, casesof B. henselae infections are associatedwith exposureto or ownershipof cats.However, not all casesare associatedwith cat scratchor bite. Isolation

and identification

The BEA specimenfrom which Bartonella has been mostcommonlyisolatedis blood. Successful isolationshave been performed usingthe Isolator lysiscentrifugation systemand the BACTEC NR 660 systemwith high volume aerobic PLUS 26 bottles (103,114).In a recent report of isolationof B. quintana using the BACTEC system,positive cultures did not produce enough CO, to exceed the positive threshold value; instead, they were detected by staining negative cultures with acridine orangeand/or an enhancedGram stain(103). These organismsusually will grow on chocolate agaror heart infusion-5% rabbit blood agarin 5% CO, at 35°C but they require an extended incubation period (at least 5 days) and produce very small,closely associatedcolonies.In caseswhere the inoculumis dilute, it may be helpful to placea drop of inoculum on the surface of the medium and incubate the plate without streakingfor isolation (unpublisheddata). Biochemicalcharacteristics of B. henselae and B. quintana are listed in Table 5. All strainsstudiedat the CDC required the presenceof rabbit blood to supportgrowth on heart infusion agar. Supplementationwith X factor (hemin) alone supportedthe growth of some but not all strains. Since growth generally does not occur in standard biochemical differential media,the mostuseful differential testsare those designedto detect the presence of preformed enzymes.The RapID ANA11 System(Innovative Diagnostic Systems,Atlanta, Ga.), MicroScan Rapid Anaerobe panel (Baxter Diagnostics,Deerfield, Ill.), Neisseria/HaemophilusIdentification Card (Vitek Systems-bioMerieuxVitek, Hazelwood, MO.), AnIDENT System (Analytab Prod-

14

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CUMITECH

TABLE Test

Motility; flagella Fermentative or oxidative Carbohydrate base D-Glucose D-Xylose D-Mann&o1 Lactose Sucrose Maltose Catalase Oxidase Growth on HIA with: X factor V factor Rabbit blood Growth on MacConkey agar Simmons citrate Urea, Christensen’s Nitrate reduction Indole Tryptone broth Spot test Optimal growth temperature Hydrolysis of d: p-Nitrophenyl-P-D-disaccharide p-Nitrophenyl-cll-L-arabinoside ONPG p-Nitrophenyl-a-D-glucoside p-Nitrophenyl-P-D-glucoside p-Nitrophenyl-cr-D-galactoside p-Nitrophenyl-cr-L-fucoside p-Nitrophenyl-Wacetylglucosamide p-Nitrophenyl-phosphate Leucyl-glycine+-naphthylamide Glycine+naphthylamide Proline+naphthylamide Phenylalanine-P-naphthylamide Arginine-p-naphthylamide Serine-P-naphthylamide Pyrrolidonyl+naphthylamide

27

5. Bacterial species associated with CSD” B. henselae

Sign

(n = 14)

% Positive

B. quintana

Sign

-

-

I& ND -

&T ND +ti

V + ND ND ND ND

0

64 0 100

ND 35-37°C + + + + + + -

0 0 0 0 0 0 0 0 0 0 100 100 92 100 100 100 0

V + ND ND ND ND ND 35-37°C + + + + + + -

(n = 2)

A$pia

% Positive

Sign

felis

(n = 16)

% Positiveb

+; l-2 pol ar 0 0 0 0 0 0

0 OF (+ > -

V

50 0 100

ND ND ND V

-

- or (+)

o/2

ND 30°C

0 0 0 0 0 0 0 0 0

ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND

100 100 100 100 100 100 0

0 (93) 0 0 0 0

37 100

(44) 0 88 (12) 100 0

a +, 90% or more strains tested positive within 48 h of incubation; -, 10% or less strains tested positive; + or (+), positives and negatives together total 90% or more; V, variable reaction (11 to 89% of strains tested positive); ND, test not performed; 0, oxidative; F, fermentative; n-o, nonoxidizer; OF, King’s OF medium; RST, rapid sugar test (see reference 51 for formulations); HIA, heart infusion agar; ONPG, orthonitrophenyl+-D-galactopyranoside. b Numbers in parentheses indicate percentage of strains showing a delayed reaction (positive test detected between 3 and 7 days of incubation). ’ Kovacs’ modification weakly positive, routine method negative. d Hydrolysis results were obtained with the RapID ANA11 system (Innovative Diagnostic systems,Atlanta, Ga.) using growth from 3- to 4-day rabbit blood agar cultures.

ucts, Plainview, N.Y.), and MicroScan HNID Panel (Baxter Diagnostics)are commercialassays that canbe usedto obtain enzymeprofiles andwill identify B. henselae, B. quintana, and other Bartonella spp. (197). However, of these commercial tests,only the MicroScan Rapid Anaerobe panel was capable of differentiating B. henselae from B. quintana and the other Bartonella spp. (197). Welch et al. (197) reported that bis-p-nitrophenyl

phosphateand L-lysine$-naphthylamidewere the mostuseful enzyme hydrolysistestsfor differentiating B. henselae (positive for both enzymes)from B. quintana. However, testsdone at CDC with the RapID ANA11 System indicated that the bis-pnitrophenyl phosphate test was negative for B. henselae (Table 5). Additional testsfor genus-level identification of Bartonella spp. are shown in Table 5. Confirmatory species-levelidentification

CUMITECH

27

DIAGNOSIS

can alsobe obtained by either DNA-DNA hybridization studies or restriction analysis of PCRamplified genefragments(42, 155). Antibiotic

susceptibility

and treatment

Standardizedsusceptibilitytesting hasnot been establishedfor A. felis or B. henselae.Antibiotic treatment of CSD has had varied success,but overall it doesnot seemto shorten the courseof CSD or prevent suppuration of lymph nodes.In order, the most clinically effective antibiotics have been reported to be rifampin, ciprofloxacin, gentamicin, and trimethoprim-sulfamethoxazole. Erythromycin, doxycycline, penicillin, and several cephalosporinshave not been beneficial in treating CSD. Lymphadenitisusually resolvesspontaneouslyin lessthan 2 to 4 monthswithout treatment (165). Aspiration of suppurativematerial is recommended,however (33). In contrast, BEA has respondedto antimicrobial therapy with rifampin, erythromycin, and doxycycline (165). INFECTIONS NONTRAUMATIC Bordetelk

ASSOCIATED WITH ANIMAL CONTACT bronchiseptica

The genus Bordetella comprisesfour species, B. pertussis,B. parapetiussis,B. bronchiseptica, and B. avium (22, 94). A recently proposed species,B. holnzesii,is associatedwith human septicemia and has previously been known as CDC nonoxidizer group 2 (NO-2) (200). Whereas B. pertussisand B. parapertussisare well-established human pathogens,B. bronchisepticais largely a commensaland opportunistic upper respiratory pathogenof animals,particularly dogs,swine,and rabbits. Only rarely has B. bronchisepticabeen reported to be pathogenic in humans.B. avium causesan upper respiratory infection in poultry referred to as turkey coryza. Human infections caused by B. avium have not been reported. However, B. avium may be misidentifiedasAlcaligenesfaecalis. natural

habitat,

and mode of

Ferry (55) in 1910 recovered a small gramnegativecoccobacillus,consistentwith B. bronchiseptica,from respiratory tract specimensof laboratory dogswith canine distemperand named it Bacillusbronchisepticus. Following a seriesof nomenclaturalchanges,the organismwasascribedto the genusBordetella (11). This designationwas basedon sharedbiological attributes, DNA homology, and residencein upper respiratory tracts of mammals (202),includingmonkeys,foxes,horses, rats, raccoons,swine,rabbits, dogs,and cats (69, 202). It is readily recovered from the respiratory tracts of animalswith bordetelliosis.Infections of

INFECTIONS

15

swine, dogs, and laboratory animalsare of great economicimportance. Despite the widespreadprevalenceof B. bronchiseptica,it is not commonly isolated from humans.Isolation of B. bronchisepticafrom nasopharyngeal cultures of animal caretakers has been describedpreviously (117, 202). McGowan (117) and Winsser (202) reported isolation of B. bronchisepticafrom 1 of 13 and 1 of 24 animal caretakers, respectively. However, Switzer et al. (178) studied nasopharyngealcultures from 80 swine farmers and did not recover B. bronchiseptica. Pedersonet al. (142), in a retrospective study of 565 gram-negativenonfermentative bacilli recovered from clinical specimens,reported 16 isolates designatedasB. bronchisepticafrom sputum (10 cases),respiratory equipment(1 case),lung biopsy (1 case),and undesignatedsources(4 cases).In a prospectivestudy, Gardner et al. (62) reported 18 B. bronchisepticaisolates from 194 consecutive isolationsof gram-negativeasaccharolyticorganismsfrom clinical sources.All of theseB. bronchiseptica isolateswere consideredto be clinically insignificant, except for two: one was from a patient with nosocomialsepticemiaand the other wasassociatedwith a nosocomialtracheobronchitis (62). These studies do not conclusively reflect the mode of transmissionof B. bronchisepticato humans.It is generally presumedthat the organism is acquiredthrough contact with infected animals, resulting in transient or chronic colonization. In an appropriate clinical setting, either alone or in combinationwith other organisms,it may acquire a pathogenicrole. Few well-documentedcasesof ex!posureto infected animals with subsequent diseaseproduction have been described (152), whereasin other casesof B. bronchiseptica-associated disease,the route of acquisition may have been nosocomial,concomitant with an immunocompromisedstate. In somecasesof documented infection with B. bronchiseptica,animal contact could not be identified (202). Human

Description, transmission

OF ZOONOTIC

infections

Approximately 30 casesof infection with B, bronchisepticahave been describedin the literature (62, 117, 120, 130, 142, 152, 178, 202, 203), most in associationwith a compromised host immunestatus(9, 10,27,32,38, 65, 120,130,138, 152, 177). Thesecasesinclude pneumoniaand/or bacteremia associatedwith alcoholismand malnourishment(65), Hodgkin’s disease(177), heart transplant (38), chronic lymphocytic leukemia(27, 138, 142),bone marrow transplantation (lo), and hemodialysis(9), aswell as peritonitis associated with continuousambulatorydialysis(32) and sinus infection in a patient with chronic lymphocytic leukemia(50). Readersare referred to a previous review of B. bronchisepticainfections in humans

16

BOTTONE

ET AL.

for additional details (202). In non-immune compromised hosts, a causative role cannot be clearly determined and recovery of B. bronchiseptica may have been an incidental cultural finding (55). Most B. bronchiseptica infections in children have been described as resembling whooping cough. Kristensen and Lautrop (100) reported whooping cough-like symptoms in three children of a Danish farm family. Cultures from these children grew B. bronchiseptica; three older siblings became asymptomatic carriers. Their pet rabbits, and subsequently their cats, died of B. bronchiseptica infection. Brown (26) and Chang (36) have also reported B. bronchiseptica-associated parapertussis in children, and in 1960, Lautrop and Lacey (106) estimated that 1 in 1,000 cases of whooping cough in England was caused by B. bronchiseptica. Whooping cough due to B. bronchiseptica in children is not surprising, since this organism produces an endotoxin (dermonecrotoxin), tracheal cytotoxin, and adenylate cyclase similar to those produced by B, pertussis. However, pertussis toxin is not known to be produced, although silent copies of the gene are present (81). Furthermore, Chang et al. (35) reported the recovery of B. bronchiseptica from the cerebrospinal fluid of a child with meningitis subsequent to a closed fracture of the skull after being kicked by a horse. B. bronchiseptica infections have also been stated to occur in children with cystic fibrosis (202). B. bronchiseptica infection in association with AIDS has recently been reported (120, 130, 152). Ng et al. (130) reported that five of seven isolates of B. bronchiseptica received in a five-year period were from AIDS patients. In addition, several other cases of pneumonia possibly associated with B. bronchiseptica have been reported (2, 44, 120). The clinical significance of these isolates was complicated by coinfection with other organisms such as Pneumocystis carinii, Pseudomonas and Haemophilus spp., and cytomegalovirus. Treatment for the coinfecting organisms may have resolved the B. bronchiseptica infection in some of these cases, while in others B. bronchiseptica clearly seemed to be the offending organism. In addition to respiratory infections, Qureshi et al. (152) have reported a case of recurrent bacteremia in a patient with an indwelling broviac catheter, which cleared only after removal of the catheter, suggesting colonization of the catheter by B. bronchiseptica . Isolation

and identification

Stringent criteria for differentiating B. bronchisepticafrom other phenotypically similargramnegativeasaccharolyticorganisms,includingAcinetobacter,Achromobacter,Alcaligenes,and Pseudomonasspp., have been detailed by Johnson and Sneath (92) and Bemis and coworkers (11). B. bronchisepticais a gram-negative,non-spore-

CUMITECH

27

forming, pleomorphic coccobacillary bacterium, which is motile by peritrichous flagella. It is an obligate aerobeand growswell even on selective nutritive media (such as MacConkey agar) as small circular glistening (pearlescent) or rough colonies.Dependingon the sourceof blood, some isolates will be hemolytic on blood agar. The organismgrowsoptimally at 35 to 37”C, and after 48 h of incubationin air, the coloniesreach 0.5 to 1.0 mm in diameter. Biochemical characteristics aiding identification include positive reactionsfor catalase and oxidase, citrate utilization, nitrate reduction (without gas), tetrazolium reduction, growth on salmonella-shigella agar, and a strong and rapid ureasereaction. The organismdoesnot grow on tellurite agar and is negativewhen tested for indole production, hydrogen sulfide, and tyrosinehydrolysis.Simplesugarsare not fermented or oxidized. Growth on a Kligler’s or a triple sugar iron agar slantresultsin an alkalinereaction both in the butt and on the slant. An alkaline (blue) reaction alsooccursat the top of a tube of aerobic oxidation-fermentation medium. Motility is best demonstratedin semisolidagar at 30°C;however, nonmotile isolateshave been described(69, 202). Suitability

of rapid

or commercial

methods

Commercially available identification systems such asRapid NFT (API SystemSA, MontalieuVercieu, France), the API-Zym and API-20E (Analytab Products), the Corning N/F system (Corning Medical Products, Roslyn, N.Y.) (202), and Microscan Gram-Negative Panel (Baxter Healthcare, Sacramento, Calif.) (2, 152) have been reported to provide adequateidentification of B. bronchiseptica. Antibiotic

susceptibility

Antibiotic susceptibility of B. bronchisepticais similar to that of Pseudomonas aeruginosa.The aminoglycosidesamikacin,gentamicin,and tobramycin, but not streptomycin,are highly effective in vitro. The antipseudomonalpenicillins(azlocillin, mezlocillin, piperacillin, and ticarcillin) and the antipseudomonalbroad-spectrumcephalosporins (cefoperazone and ceftazidime) are also highly effective; other broad-spectrum cephalosporins vary widely in efficacy. Tetracyclines, chloramphenicol, and imipenemalsoshow good efficacy. The MICs of quinolonesare near the susceptibility breakpoint, but effective serumconcentrations may be achievedwhen administeredintravenously or in high doses.Susceptibility reports for trimethoprim-sulfamethoxazoleand rifampin vary widely. The primary penicillins(such aspenicillin G and ampicillin), expanded- and narrow-spectrum cephalosporins,and the macrolidesclindamycin and erythromycin can be consideredineffective (202). Becauseof the rapid growth of B. bronchisepticain Mueller-Hinton broth and on

CUMITECH

DIAGNOSIS

27

agar, disk diffusion, agar dilution, and broth dilution should all produce acceptableresults when recommendationsof the National Committee for Clinical Laboratory Standardsfor gram-negative, aerobic bacteria are used (127, 128). As recommendedby the manufacturer,susceptibilityresults determined with the Vitek AMS System (Vitek Systems,Hazelwood, MO.) should be confirmed by another method (202). ZOONOTIC CAMPIZOBACTER AND HELICOBACTER SPECIES Campylobacter upsaliensis Description, natural habitat, and mode of transmissign C. upsaliensis is a memberof group I, subgroup

IA, of the true thermotolerant, enteropathogenic campylobacters,which also includesC. jejuni, C. coli, and C. laridis. In 1983,a Campylobacter-like organismwasoriginally isolatedfrom the fecesof healthy and diarrheic dogs (162) and was subsequently named Campylobacter upsaliensis (132, 143). This organismhassincebeen isolatedfrom asymptomaticcats as well as from humanswith enterocolitis (28, 59, 71, 83, 180). Humans may acquire the microorganismby direct contact with infected healthy or diseasedpets,especiallyyoung dogs and cats (16). Children may be infected through contactwith animalfecesby the fecal-oral route. Human infections C. upsaziensis is a potential human pathogen

that hasbeenrecoveredfrom adultsand pediatric patientswith gastroenteritisand septicemia(1,71, 104,140, 180,181, 191).Furthermore, it hasbeen associatedwith diarrhea1infections on a worldwide basis(83,136,180).Extraintestinal infections include bacteremiain normal hostswith chronic illnessesand in immunocompromisedindividuals (104, 140), a breastabscess in a normal host (63), and abortion following contact with a household cat (76). Isolation and identification C. upsaliensis is the most likely enteropathogenie Campylobacter to be missedin the clinical

laboratory becauseof wide strain variation in susceptibility to antibiotics in the isolation medium (144).As a rule, this speciesis susceptibleto cephalothin,and therefore a cephalothin-containing selectivemediumroutinely usedfor recovery of C. jejuni is not appropriate for isolation of this organismfrom stool specimens(18,29,53). Membrane filtration of stool specimensfollowed by direct cultivation of the membraneon an antibiotic-free agar mediumis considereda preferred techniaue for isolation of C. wsaliensis (18, 67,

OF ZOONOTIC

INFECTIONS

17

172). Semisolid selective motility medium and charcoal-basedselective medium containing cefoperazone,vancomycin, and cycloheximidehave also been successfullyused for isolation (29, 53, 191). The feature of C. upsaliensis that most easily distinguishesit from other Campylobacter species is that it is either catalasenegative or weakly positive. C. upsaliensis demonstratespyraxinamidase activity and lacks arylsulfataseproduction, which are additional phenotypic characteristics usedfor its identification and differentiation from other Campylobacter-like organisms(30). Biochemically,it reducesnitrate to nitrite and hydrolyzes indoxyl acetate but not hippurate (59, 70, 148). It is urease and H,S negative (144). The organism grows at 42”C, but not at 25OC.In addition to being susceptibleto cephalothin, isolates are susceptibleto nalidixic acid and polymyxin B (59). Rapid identification of C. upsaliensis in epidemiological surveys is accomplishedby DNA-DNA hybridization and dot-enzyme-linked immunosorbentassays(29, 59, 73, 140, 180). In addition, hippurate-negativethermophilic campylobacters,including C. upsaliensis, can be characterized by polyacrylamide gel electrophoresisof their cellular proteins (70, 137). Although tested on a limited number of isolates, a commerciallyavailablelatex agglutination test (Meritec-campy; Meridian Diagnostic, Cincinnati, Ohio) appearsto be helpful in detecting a C. upsaliensis-specific antigen in colonies after growth (126). Plasmid profiling and restriction endonucleaseanalysis of genomic DNA of C. upsaliensis have been shown to be useful for epidemiologicaltyping of dog and humanisolates from various geographiclocales(135, 136). Antibiotic susceptibility C. upsaliensis isolatesare susceptiblein vitro to

fluoroquinolones, chloramphenicol, tetracycline, gentamicin, and p-lactam antibiotics. They are resistantto cefoperazone,trimethoprim, and vancomycin (70, 140, 150, 191). Campylobacter jejuni and Campylobacter coli C. jejuni is commonly isolated in clinical labo-

ratories from human fecal specimensand is usually obtained by exposureto or consumptionof infected food animals.It is mentioned here becausedogsand catsmay becomeinfected with C. jejuni and be a source of human infection (56). Pets obtained from commercialkennels,shelters, or “pet mills” may be more likely to carry C. jejuni than petsfrom private breeders(167). In addition, animalswith diarrhea shed significantly higher levels of C. jejuni than clinically normal animals (60). Besidespets, a wide variety of laboratory animalsmay serveas reservoirsfor C. jejuni (58) and mav be a source of infection for laboratorv

18

BOTI’ONE

ET AL.

technicians, animal handlers, and exotic pet owners (167). Readers are referred to Cumitech 12A (67) for diagnosis of C. jejuni infections. C. coZi may also causehuman gastroenteritis, although not as frequently asC. jejuni. Clinicians at the Virginia-Maryland Regional College of Veterinary Medicine have found a strong association between neonatal mortality in puppiesand isolation of high numbersof C. coli from these puppies (unpublished data). It remains to be establishedwhether C. coli is a commoncommensal of dogs, but if so these animals may be a reservoir of this sometimeshuman pathogen.

CUMITECH

27

mia and meningitis in a neonate whose mother cared for pet hamsters during her pregnancy (131). Isolation

and identification

Specimensshould be submitted to the clinical laboratory under conditionsappropriatefor Campylobacter spp.Fecal specimens may be submitted in an appropriate transport medium (e.g., CaryBlair). Noncontaminatedspecimenssubmittedfor the isolation of H. cinaedi should be inoculated onto trypticase soy agar and Mueller-Hinton agar supplementedwith 5% sheep blood. ContamiHelicobacter (Campylobacter) cinaedi nated specimensshouldbe inoculated onto selective brucella base agar supplementedwith 10% Description, natural habitat, and mode of sheepblood, 10 mg of vancomycin per liter, 2,500 transmission IU of polymyxin B per liter, 5 mg of trimethoprim H. cinaedi wasoriginally describedasa Campylobacter-like gram-negative organism associated per liter, and2 mg of amphotericinB per liter (54, with proctocolitisin homosexualand bisexualmen 106, 176). Stool filtered through a nitrocellulose (54, 105, 151). The organismwas later character- filter (pore size, 0.65 pm) is inoculatedonto these media and incubated in a microaerophilic enviized and differentiated from other Campylobacter spp. on the basisof phenotypic characteristics, ronment at 37°C for 7 days. Such an atmosphere G+C ratios, 16s rRNA sequences,and DNA- can be generatedby usingan anaerobicgasgenrRNA hybridization studies(54, 183, 186). DNA erating kit (Oxoid, Columbia, Md.) with the removal of the catalyst or by using the current probeshave been usedto showthat strainsof H. commercialCampyZobacter gasgeneratingkit (Oxcinaedi may fall into one of two groups: CLO-lA, which consistsof strainsisolated from symptom- oid), which has its own catalyst. Unlike many of the Campylobacter spp.,H. cinaedi fails to grow at atic and asymptomaticindividuals, and CLO-lB, which consistsof strainsisolated from symptom- temperaturesof 25 or 42°C (133, 183), and its atic patients. Phenotypic tests can be used to growth at 37°C is not supportedin either aerobic differentiate thesetwo groups(144). or anaerobicatmospheres(54, 133). Zoonotic H. cinaedi isolateshave been recovH. cinaedi is a faintly staining, gram-negative, ered from fecal and ileal specimensfrom healthy, spiral-shapedmicroorganismthat is motile by a immunocompetentSyrian hamsters(64, 182). To singlepolar flagellum and producescatalaseand date, hamstersare the only known animal reser- oxidase(175).Occasionallythe bacteriamay occur voir for H. cinaedi. The primary mode of trans- as straight rods; older cultures may contain cocmissionof H. cinaedi to humansis through direct coid forms (144). H. cinaedi developsnonhemoor indirect contact with the fecesof hamsters(64). lytic, pinpoint, watery colonies(usually within 72 Human infectionswith H. cinaedi, like thosewith h) on brucella base agar containing 10% sheep other enteropathogeniccampylobacters,may be blood (54). Biochemical characteristicsof H. cilinked to the consumptionof contaminatedfood naedi aiding identification include reduction of or water or both (16). Sexual transmissionof H. nitrate and lack of hippurate hydrolyase, urease, cinaedi among homosexualsand bisexuals,espe- and indoxyl acetate hydrolyase. Glucose is not cially through oral-anal contact, has been sug- fermented (64, 122, 148, 175). H. cinaedi grows gested(105,151). In HIV-infected individuals,the in 0.04% triphenyltetrazolium chloride and 1% gastrointestinal tract is usually considered the glycine but not in 2% sodium chloride. It is sourceof endogenousH. cinaedi bacteremia(43). susceptibleto nalidixic acid and is intermediate in susceptibility to cephalothin. In addition to phenotypiccharacteristics,protein electrophoresis Human infections Many workers have associatedH. cinaedi with ‘and immunotyping procedurescan also be used proctitis and/or proctocolitis, diarrhea1infections, for proper identification of H. cinaedi isolates and bacteremia, especially in homosexual and (183). bisexualmen (39, 43, 122, 133, 139, 182). However, human infections due to H. cinaedi are not restricted to thesepatient populationsalone.This Antibiotic susceptibility Helicobacter speciesalsohasbeen describedasan H. cinaedi is susceptibleto ampicillin, chloramagentof diarrhea and bacteremiain adult females phenicol, gentamicin, and ciprofloxacin (57, 60, and in children (185) and asthe causeof septice- 142, 149) but resistantto trimethoprim (64, 184).

CUMITECH

27

DIAGNOSIS

OF ZOONOTIC

INFECTIONS

19

Miscellaneous Species Campylobacter-like organismsresemblingHelicobacter fennelliae have beenisolatedfrom healthy

identified by electron microscopy,a feature thus far associatedonly with H. felis (195). Although LLH. heilmanni” is difficult to isolate,a ureaseassay and diarrheic dogs(28, 170)by usingnonselective similar to one usedfor H. pylon’ can be used to culture proceduresdescribedfor isolation of C. detect the presenceof the organisms(144). Huupsaliensis (70). An identical organismwas iso- man infections with animal helicobacters have lated from a young boy with gastroenteritis(185). thus far been uncommon,but cats should noneThe organismsappearphenotypically identical to thelessbe consideredto be a potential reservoir spp. H. fennelliae, except they lack catalaseand aryl- for zoonotic infections with Helicobacter (134). sulfataseactivity. Helicobacter pylori

Since its discovery in 1983,it has been established that H. pylori is the etiologic agent of chronic gastritisand duodenalulcer diseaseand a possiblecofactor in gastric adenocarcinomain humans.However, the natural reservoir andmode of transmissionof this agent have not been confirmed. Recently, H. pylori (identified by morphologic and biochemicalparameters,fatty acid analysis, and 16s rRNA sequence analysis) was cultured from six catsobtainedfrom a commercial vendor (79). In addition, H. pylori-like bacteria were identified in 15 additional cats by histologic examination. Cats infected with H. pylon’ had typical gastritison histopathologicexamination.In addition to being a potential model for H. pylori disease,cats may be a source of transmissionof this organismto humans. HeZicobmter-Like

Spiral Bacteria

The genusHelicobacter containsseveralspecies that colonize the gastricmucosaof mammals.In particular, a high percentageof catsare colonized with large, spiral, gastric helicobacter-likeorganisms.Thus far, however,only one species(Helicobatter felis) hasbeencultivated on artificial media (110). In a recent study, gastric helicobacter-like organismswere associatedwith 70% of juvenile and 97% of adult catswith chronic gastritis.Once established,the infection appearsto persistfor life (134). Two morphologic types of spiral bacteria have been identified in cats and dogs: H. felis, which has been characterizedby the presenceof periplasmicfibrils (1lo), and “H. (Gastrospirillum hominis) heilmanni,” which lackssuchperiplasmic fibrils and has not been cultured on artificial media (45). G. hominis hasbeen reclassifiedinto the genusHelicobacter as“H. heilmanni” basedon MS rRNA sequenceanalysis (169). “H. heilmanni” or gastrospirillum-likeorganismscolonize most dogs and cats and a small subsetof the human population, Human infection with these organismshasbeen proposedto be zoonotic (80, 109, 118). According to one set of casereports, two patientswith infectionsdue to “H. heilmanni” or similar organismshad closecontact with pets (51). In another caseof human infection, a helicobacter-likeorganismwith periplasmicfibrils was

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13:771-772.

3. Andersen, B. M., A. G. Steigerwalt, S. P. O’Connor, D. G. Hollis, R. S. Weyant, R. E. Weaver, and D. J. Brenner. 1993. Neisseria weaveri sp. nov., formerly CDC group M-5, a gram-negative bacterium associated with dog bite wounds. J. Clin. Microbial. 31:2456 -2466. 4. Anderson, B., K. Sims, R. Regnery, L. Robinson, M. J. Schmidt, S. Goral, C. Hager, and K. Edwards. 1994. Detection of Rochalimaea henselae DNA in specimens from cat scratch disease patients by PCR. J. Clin. Microbial. 32:942-948. 5 Arons, M. S., L. Fernando, and I. M. Polayes. 1982. Pasteurella multocida: the major cause of hand infection following domestic animal bites. J. Hand Surg. 7:47-52. 6 Azimi, P. 1990. Pets can be dangerous. Pediatr. Infect. Dis. J. 9670-684. 7. Balie, W. E., E. C. Stowe, and A. M. Schmitt. 1978. Aerobic bacterial flora of oral and nasal fluids of canines with reference to bacteria associated with bites. J. Clin. Microbiol.

7~223-23

1.

8. Barka, N. E., T. Hadfield, M. Patnaik, W. A. Schwartzman, and J. B. Peter. 1993. EIA for detection of Rochalimaea henselae-reactive IgG, IgM, and IgA antibodies in patients with suspected cat-scratch disease. J. Infect. Dis. 167:15031504. 9 Barras Sans, M., J. Bonal, J. Bonet, J. Arnal, F. Rota, and C. Caralps. 1991. Bordetella bronchiseptica septicemia in a hemodialysis patient. Nephron 59:976. 10 Bauwens, J. E., D. H. Spach, T. W. Schacker, M. M. Mustafa, and R. W. Bowden. 1992. Bordetella bronchiseptica pneumonia and bacteremia following bone marrow transplantation. J. Clin. Microbial. 30:2474-2475. 11 Bemis, D. A., H. A. Greisen, and M. J. G. Appel. 1977. Bacteriological variation among Bordetella bronchiseptica isolates from dogs and other species. J. Clin. Microbial. 5:471-480. 12. Bercovier, H., F. Escande, R. Chatelain, and R E. Weaver. 1982. Group EF-4 bacteria: a newly recognized pathogen. Adv. Pathol. 1:27-30. 13. Berger, U. 1962. Ueber das Vorkommen von Neisserien bei einigen. Tieren. 2’. Hyg. 148:445-457. 14. Bhatt, K. M., and N. B. Mirza. 1992. Rat bite fever: a case report of a Kenyan. East Afk Med. J. 69~5542-5543. 15. Birkness, K. A., V. G. George, E. H. White, D. S. Stephens, and F. D. Quinn. 1992. Intracellular growth of Afipia felis, a putative agent of cat scratch disease. Infect. Immun. 60:2281-2287. 16. Blaser, M. J. 1990. Campylobacter species, p. 1649-1657. In G. L. Mandell, R. G. Douglas, and J. E. Bennett (ed.), Principles and Practice of Infectious Diseases, 3rd ed. Churchill Livinestone Inc.. New York.

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19 Boyer, K. M., and J. D. Cherry. 1992. Cat scratch disease, p. 1084-1089. In R. D. Feigin and J. D. Cherry (ed.), Textbook of Pediatric Infectious Diseases, 3rd ed. W. B. Saunders Company, Philadelphia. 20 Bra&, R., K. Siebers, and R. M. Julien. 1979. Meningitis caused by group IIj following a dog bite. West. J Med. 131~438-440. E. P. , L. M. Wary, and T. McDuff. 1983. Pasteurella ureae meningitis associated with endocarditis. Eur. Neurol.

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