Prevalence of DNA of Mycoplasma haemofelis, ‘Candidatus Mycoplasma haemominutum,’ Anaplasma phagocytophilum, and species of Bartonella, Neorickettsia, and Ehrlichia in cats used as blood donors in the United States

Timothy B. Hackett Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523

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Wayne A. Jensen Heska Corp, 3760 Rocky Mountain Ave, Loveland, CO 80538

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Tracy L. Lehman Angell Memorial Animal Hospital, 350 S Huntington Ave, Boston, MA 02130

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Anne E. Hohenhaus Jaqua Transfusion Medicine Service, Animal Medical Center, 510 E 62nd St, New York, NY 10021

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P. Cynda Crawford Department of Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610

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Urs Giger Section of Medical Genetics and Penn Animal Blood Bank, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104

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Michael R. Lappin Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523

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Abstract

Objective—To identify the prevalence of DNA of Mycoplasma haemofelis; ‘Candidatus Mycoplasma haemominutum’; Anaplasma phagocytophilum; and species of Bartonella, Neorickettsia, and Ehrlichia in blood of cats used as blood donors in the United States. Design—Prospective study.

Animals—146 cats that were active blood donors.

Procedures—Environmental history was requested for each blood-donor cat from which a blood sample (mixed with EDTA) was available. Polymerase chain reaction assays capable of amplifying the DNA of the microorganisms of interest following DNA extraction from blood were performed.

Results—Overall, DNA of one or more of the infectious agents was detected in blood samples from 16 of 146 (11%) feline blood donors. Twenty-eight laboratory-reared cats housed in a teaching hospital had negative results for DNA of all organisms investigated. The DNA of at least 1 infectious agent was amplified from blood samples collected from 16 of 118 (13.6%) community-source cats; assay results were positive for ‘Candidatus M haemominutum,’ M haemofelis, or Bartonella henselae alone or in various combinations. Of the community-source cats allowed outdoors (n = 61) or with known flea exposure (44), DNA for a hemoplasma or B henselae was detected in 21.3% and 22.7%, respectively.

Conclusions and Clinical Relevance—When community-source cats, cats allowed outdoors, or cats exposed to fleas are to be used as blood donors, they should be regularly assessed for infection with M haemofelis,Candidatus M haemominutum,’ and Bartonella spp, and flea-control treatment should be regularly provided.

Abstract

Objective—To identify the prevalence of DNA of Mycoplasma haemofelis; ‘Candidatus Mycoplasma haemominutum’; Anaplasma phagocytophilum; and species of Bartonella, Neorickettsia, and Ehrlichia in blood of cats used as blood donors in the United States. Design—Prospective study.

Animals—146 cats that were active blood donors.

Procedures—Environmental history was requested for each blood-donor cat from which a blood sample (mixed with EDTA) was available. Polymerase chain reaction assays capable of amplifying the DNA of the microorganisms of interest following DNA extraction from blood were performed.

Results—Overall, DNA of one or more of the infectious agents was detected in blood samples from 16 of 146 (11%) feline blood donors. Twenty-eight laboratory-reared cats housed in a teaching hospital had negative results for DNA of all organisms investigated. The DNA of at least 1 infectious agent was amplified from blood samples collected from 16 of 118 (13.6%) community-source cats; assay results were positive for ‘Candidatus M haemominutum,’ M haemofelis, or Bartonella henselae alone or in various combinations. Of the community-source cats allowed outdoors (n = 61) or with known flea exposure (44), DNA for a hemoplasma or B henselae was detected in 21.3% and 22.7%, respectively.

Conclusions and Clinical Relevance—When community-source cats, cats allowed outdoors, or cats exposed to fleas are to be used as blood donors, they should be regularly assessed for infection with M haemofelis,Candidatus M haemominutum,’ and Bartonella spp, and flea-control treatment should be regularly provided.

Blood-borne infectious diseases are some of the most serious concerns among operators of human blood banks. By 1985, when the causative organism for acquired immunodeficiency syndrome was identified and tests were developed to screen donated blood, HIV had been transmitted to at least 50% of the 16,000 hemophiliacs in the United States along with 12,000 other recipients of blood transfusions.1 Currently, every unit of human blood in the United States undergoes 9 different tests for infectious disease before use. Donated blood is assessed for the presence of surface antigen of hepatitis B virus, antibodies against the hepatitis B virus core, antibodies against hepatitis C virus, antibodies against HIV (types 1 and 2), antibodies against human T-lymphotropic virus (types 1 and 2), and genetic material of viruses (via nucleic acid amplification testing) and for evidence of infection with Treponema pallidum (syphilis).2

With increasing frequency, blood transfusions are administered to anemic and bleeding cats.3,4 Worldwide, it is generally only healthy adult cats for which blood test results for FeLV antigen and anti-FIV antibody are negative that are selected as blood donors.4 However, depending on geographic location, cats can also be infected by multiple other blood-borne organisms, including Mycoplasma haemofelis, ‘Candidatus Mycoplasma haemominutum,' Bartonella spp, Ehrlichia spp, and Anaplasma phagocytophilum; the prevalence of these infections in cats used as blood donors in the United States is unknown. For each of these organisms, PCR-based DNA tests are now routinely available for use with blood product screening. In 2004, a consensus statement published by the American College of Veterinary Internal Medicine recommended screening blood collected from healthy feline blood donors not only for FeLV antigen and anti FIV antibody but also for hemoplasmas (infection by M haemofelis or ‘Candidatus M haemominutum'); some members of the panel responsible for formulation of that consensus statement suggested also screening for bartonellosis.5 The panelists also recommended evaluating blood-donor cats for infection with Cytauxzoon felis, Ehrlichia canis–like organisms, and A phagocytophilum in high-prevalence geographic areas.

Haemobartonella felis has been reclassified as a hemoplasma with 3 distinct species: M haemofelis, ‘Candidatus M haemominutum,' and ‘Candidatus Mycoplasma turicensis' (a new species initially identified in Switzerland).6–9 It is currently unknown whether ‘Candidatus M turicensis' infects cats in the United States. Hemoplasmas reside at least part of the time on the surface of RBCs and are proposed causes of feline infectious anemia.10 Hemoplasmas can be transmitted between cats with as little as 1 to 2 mL of blood administered IV. Fleas (Ctenocephalides felis) ingest DNA of M haemofelis and ‘Candidatus M haemominutum' when ingesting blood from infected cats, and DNA of each of these organisms has been amplified from fleas and flea feces.11–13 Mycoplasma haemofelis, but not ‘Candidatus M haemominutum,' was transmitted by C felis during feeding, but neither organism was transmitted to hemoplasma-naïve cats by allowing those cats to ingest infected C felis or their feces or eggs.11,12 In North America and Europe, isolates of M haemofelis and ‘Candidatus M haemominutum' are virtually identical, and M haemofelis DNA from a clinically ill cat in Australia has been amplified by use of a PCR protocol that detects M haemofelis in cats of North America and the United Kingdom.14–16 The M haemofelis isolates studied experimentally to date have induced severe clinical illness in most infected cats, whereas most cats that have been experimentally inoculated with ‘Candidatus M haemominutum' have developed minimal to no clinical abnormalities.17–20 However, most cats that require blood transfusions are extremely ill, and it is currently unknown what effects might be associated with inoculation of ‘Candidatus M haemominutum' into these cats. Hemoplasmas can be detected cytologically in blood smears prepared from infected cats during acute clinical illness; in addition, the organisms can also be detected cytologically in blood smears prepared from some apparently healthy cats.21 For detection of hemoplasma infections, PCR assays are considered superior to cytologic evaluations.10,22 In a recent study22 of healthy cats, the prevalence rates for infection by M haemofelis or ‘Candidatus M haemominutum' determined via cytologic evaluation or PCR assay were 0% and 15.2%, respectively.

Cats and humans can also be infected with Bartonella henselae, Bartonella clarridgeiae, and Bartonella koehlerae.23–26 These species of Bartonella have been associated with a number of human illnesses including cat-scratch disease, bacillary angiomatosis, and bacillary peliosis. The type I and II genetic variants of B henselae have been detected in infected cats and humans.27,28 Infections of cats with Bartonella spp are extremely common; as many as 93% of some groups of cats in some geographic areas of the United States are seropositive and thus were presumably infected at some time.29–31 Bartonella henselae has been cultured from blood samples collected from many cats following natural exposure to the organism; cats infected with the organism via ID, SC, IV, or IM inoculation; and cats infected via exposure to B henselae–infected fleas.32–37 Furthermore, inoculation of B henselae via IV, IM, or ID routes has resulted in development of fever, lethargy, lymphadenopathy, and neurologic diseases in some cats.34–37 In some naturally infected cats, uveitis and other clinical signs of disease, including gingivitis and lymphadenopathy, have been reported.38–40 Although Bartonella spp can be readily cultured from blood samples, PCR assays have recently been described41,42 that also can be used to distinguish Bartonella spp.

Ehrlichia canis–like DNA and A phagocytophilum DNA have been amplified from naturally exposed cats by use of PCR assays.43–46 In addition, Ehrlichia-like morula have been detected in mononuclear cells or neutrophils of some naturally exposed cats in the United States, Kenya, Brazil, France, Sweden, and Thailand, and some of those cats have also been seropositive for antibodies against E canis antigens.47,48 Although cats have been experimentally infected with Neorickettsia risticii, natural infections with that organism have not been detected in clinically ill cats.49 To date, most cats with ehrlichiosis or anaplasmosis have been clinically ill; anorexia, fever, inappetence, lethargy, weight loss, hyperesthesia or joint pain, pale mucous membranes, splenomegaly, dyspnea, lymphadenomegaly, nonregenerative anemia, leukopenia, leukocytosis, neutrophilia, lymphocytosis, monocytosis, pancytopenia, intermittent thrombocytopenia, and polyclonal gammopathy were reported43–47 for some affected cats. Prevalence rates for infections with Ehrlichia spp, Neorickettsia spp, or A phagocytophilum in otherwise healthy cats are unknown.

It is possible that some cats that are intended for use or that are being used as blood donors in clinical veterinary practices have been naturally exposed to hemoplasmas; A phagocytophilum; or species of Bartonella, Ehrlichia, or Neorickettsia and are chronic carriers. Cats in need of blood transfusions may be immunocompromised and more susceptible to infectious diseases than clinically normal cats. The purpose of the study reported here was to identify the prevalence of DNA of M haemofelis; ‘Candidatus M haemominutum'; A phagocytophilum; and species of Bartonella, Neorickettsia, and Ehrlichia in cats used as blood donors in the United States. In addition, the prevalence results were stratified with regard to source of the cat and selected historical findings.

Materials and Methods

Sample group—One hundred forty-six blood samples were collected from clinically normal feline blood donors from 3 academic institutionsa (n = 42 cats); 2 private referral veterinary clinicsb (78); and 6 private general practices in Mendota, Ill; Stillwater, Okla; Castle Rock, Colo; Baltimore, Md; Ontario, Ore; and Glendale, NY (26). Blood samples were collected into tubes containing EDTA and either packed on ice and transported overnight or stored at −20°C and sent in batches to Colorado State University, where the samples were frozen at −70°C until assayed.

Clinical information—Information about the cats including source (classified as laboratory-reared, universityhoused cats or community-source cats [from shelters or housed with private owners]), housing environment (resident indoors exclusively vs access to outdoors), and arthropod exposure history was requested for each blood sample submission. Serum samples from all cats were screened for FeLV antigen and FIV antibodies at the time of entry into the blood donor program and then at least annually; results were negative for all cats. For each cat, a blood smear was also cytologically examined for microorganisms, but blood samples had not been previously assessed via PCR assays.

Assays—Previously published PCR assays for amplification of the DNA of Bartonella spp,41 Ehrlichia spp,46 A phagocytophilum,46 Neorickettsia spp,46 M haemofelis,22 and ‘Candidatus M haemominutum' were performed on each blood sample.22 The results of the assays are presented descriptively.

Results

All blood samples from the 146 feline blood donors were evaluated for DNA of Bartonella spp, Ehrlichia spp, A phagocytophilum, Neorickettsia spp, M haemofelis, and ‘Candidatus M haemominutum' by use of PCR assays. Overall, the DNA of an infectious agent was detected in the blood of 16 of 146 (11%) cats. Results of all the PCR assays were negative for the 28 laboratoryreared cats that were group housed in a university colony. The DNA of at least 1 of the infectious agents of interest was amplified from 16 of 118 (13.6%) community-source cats (Table 1). Among these 16 cats, PCR assay results were positive for ‘Candidatus M haemominutum' alone in 9 cats, M haemofelis alone in 4 cats, ‘Candidatus M haemominutum' and M haemofelis in 1 cat, B henselae alone in 1 cat, and B henselae and ‘Candidatus M haemominutum' in 1 cat. Housing and flea exposure information was available for most of the 118 community-source cats (data regarding indoor residency vs outdoor access were available for 89 cats; data regarding arthropod exposure were available for 78 cats). The DNA of a hemoplasma or B henselae was amplified from blood samples obtained from 13 of 61 (21.3%) cats that were allowed outdoors and 1 of 28 cats (3.6%; DNA of ‘Candidatus M haemominutum' alone) reportedly housed totally indoors. The DNA of a hemoplasma or B henselae was amplified from blood samples obtained from 10 of 44 (22.7%) cats with known flea exposure and 1 of 32 (3.1%) cats (DNA of ‘Candidatus M haemominutum' alone) that were reportedly free of fleas.

Table 1—

Results of PCR assays for DNA of Mycoplasma haemofelis, ‘Candidatus Mycoplasma haemominutum,’ and Bartonella spp in blood samples collected from 118 community-source cats were used as blood donors in the United States.

DNA amplificationAll cats (n = 118)Subgroup of cats
Not allowed outdoors (28)Allowed outdoors (61)Absence of fleas (32)Presence of fleas (44)
Any of the infectious agents of interest16 (13.6)1 (3.6)13 (21.3)1 (3.1)10 (22.7)
Either of the hemoplasmas of interest15 (12.7)1 (3.6)12 (19.7)1 (3.1)10 (22.7)
Bartonella henselae2 (1.7)0 (0)2 (3.3)0 (0)1 (2.3)
Subgroups
 ‘Candidatus Mycoplasma haemominutum’ alone9 (7.6)1 (3.6)7 (11.5)1 (3.1)6 (13.6)
 Mycoplasma haemofelis alone4 (3.4)0 (0)4 (6.6)0 (0)3 (6.8)
 M haemofelis and ‘Candidatus M haemominutum’1 (0.8)0 (0)0 (0)0 (0)0 (0)
 ‘Candidatus M haemominutum’ and B henselae1 (0.8)0 (0)1 (1.6)0 (0)1 (2.3)
 B henselae alone1 (0.8)0 (0)1 (1.6)0 (0)0 (0)

Data are presented as the number (%) of cats for which microbial DNA was amplified from blood samples via PCR assay in each characteristic category; information was not available for each cat in each category, and so denominators vary among categories.

Discussion

Results of the present study indicated that some cats used as blood donors in the United States are currently infected with M haemofelis, ‘Candidatus M haemominutum,' or B henselae. The PCR assay used for detection of DNA of Bartonella spp can amplify DNA of multiple species; however, with the exception of DNA of B henselae, no DNA of the other Bartonella spp known to infect cats was amplified.41 Hemoplasmas and Bartonella spp can be transmitted via IV inoculation of blood and are sometimes associated with clinical illness in experimentally inoculated or naturally exposed cats. Thus, we believe that veterinarians should consider screening for these infectious agents in cats that are intended for use as blood donors.

Currently, cytologic evaluation of blood smears and amplification of microbial DNA in blood samples are the only commercially available diagnostic methods for detection of M haemofelis or ‘Candidatus M haemominutum.' Although serum antibodies against those organisms have been detected in some experimentally inoculated cats, serologic assays are not currently available commercially.18 Because PCR assays are more sensitive than cytologic evaluations for the diagnosis of hemoplasmas in healthy cats, the former should be used to screen cats that are likely to be used as blood donors.5,22 False-positive results should be unlikely if the laboratory is applying appropriate procedural controls. False-negative results can occur if low levels of bacteremia are present at the time of testing or the cat has recently been treated with antimicrobials, particularly fluoroquinolones or tetracyclines.18,50

In the United States, there are several laboratories that commercially perform PCR assays to detect hemoplasmal DNA, but there is no standardization for those procedures among laboratories at present. Thus, veterinarians should consult with their laboratory to determine that the assay to be used is sensitive and capable of amplifying both M haemofelis and ‘Candidatus M haemominutum' and that quality control is maintained. Because M haemofelis appears to be more pathogenic than ‘Candidatus M haemominutum,' identification of the species that is infecting an individual cat may be important. Prior to submission of the sample, the laboratory should be contacted to determine optimal sample handling. Further information is needed to determine whether ‘Candidatus M turicensis' infects cats in the United States.

For B henselae, results of serum antibody tests, bacterial culture of blood, or PCR assays can be used to assess the infection status of individual cats. However, similar to PCR assay procedures to detect hemoplasmal DNA, there is no standardization of PCR assays to detect DNA of Bartonella spp among commercial laboratories at present. Some B henselae–infected cats have been seronegative for antibodies against that organism when initially assessed.51 Thus, false-negative anti–Bartonella spp antibody test results can occur. Positive Bartonella-specific serologic test results generally represent exposure to a species of Bartonella, but because serum antibodies against Bartonella spp can be detected for months to years after bacteremia has resolved, positive test results do not prove that the cat is currently infected. The proportion of cats that are seropositive for antibodies against Bartonella spp vary by region but can be as high as 93% in states with high levels of flea infestations.29–31 Therefore, whether to assess cats that are to be used as blood donors for antibodies against Bartonella spp or whether to exclude cats with serum antibodies against Bartonella spp from a blood donor program is unclear at this time, largely because reports of clinical disease caused by transmission of blood-borne Bartonella spp to transfusion recipients are lacking in the literature.5

Positive results of bacterial culture of blood samples or amplification of microbial DNA from blood via PCR assay proves that a cat is currently infected with a species of Bartonella. If performed by qualified laboratory staff who are performing the assays with appropriate control procedures, false-positive results should be unlikely. However, it is possible that Bartonella spp–specific primers could amplify some other closely related bacteria.42 Bacterial culture of blood is the best method for determining whether a cat is currently infected with a Bartonella sp, but the technique requires 1 to 2 weeks for microbial growth to occur. It is possible for PCR assays to provide false-negative results if the designated primers fail to amplify the DNA of all Bartonella spp. In addition, levels of Bartonella spp bacteremia are variable, and so falsenegative results of PCR assay or bacterial culture of blood samples may occur in some infected cats.35 False-negative results can also occur if the cat has recently been treated with antimicrobials.33 Assessment of the results of tests for serum antibodies against Bartonella spp along with results of a Bartonella-specific PCR assay or bacterial culture of blood is the most sensitive way to define the infection status of an individual cat. It is likely that most cats that are seronegative for antibodies against Bartonella spp and for which results of bacterial culture of blood or Bartonella-specific PCR assay are negative are not infected with Bartonella spp. Thus, if the goal of testing is to prevent Bartonella spp–infected cats from being used as blood donors, a combination of serologic evaluation and appropriate PCR assay or bacterial culture procedures should be performed and any cat with a positive test result should be excluded as a donor.

Infections with Ehrlichia spp or A phagocytophilum among domestic cats of the United States have rarely been reported, but nationwide prevalence studies have not been performed. The vector associated with transmission of Ehrlichia spp to cats is unknown. In some cats infected with A phagocytophilum, ticks of the genus Ixodes have been implicated as the vector.43–46 Thus, infection of cats with A phagocytophilum may be limited to regions with Ixodes spp. In a recent study52 of feral cats in Florida, none of the 553 cats for which blood samples were evaluated with the PCR assays used in the present study were positive for DNA of Ehrlichia spp or A phagocytophilum. In addition, Ehrlichia spp DNA or A phagocytophilum DNA was not amplified from the blood of healthy cats that were used as a control group in a studyc of cats with fever of unknown origin. The results of the 2 aforementioned studies and the failure to amplify DNA of any Ehrlichia spp or A phagocytophilum in blood samples collected from cats used as blood donors in the present study suggest that infection of healthy cats with those organisms is uncommon in the United States. Thus, there is insufficient information available to suggest that blood samples should be collected from all cats used as blood donors for screening for E canis–like DNA or A phagocytophilum DNA. However, if there is a history of clinical illness that could be potentially associated with these infections or a history of tick exposure, evaluation of that particular cat via appropriate PCR assays is indicated.

Cats that have DNA of a hemoplasma, Bartonella spp, Ehrlichia spp, or A phagocytophilum detected in blood should not be used as blood donors. Antimicrobial treatment usually does not eliminate these infections; therefore, rather than attempt to treat and prove persistent resolution of infection in an affected cat for purposes of blood donation, it may be more cost effective to identify another cat to be used as a blood donor.18,20,33,35,46,48

On the basis of the results of our study and other investigations, a laboratory-reared cat or a clientowned cat that has been housed indoors without a history of flea or tick infestation is unlikely to have DNA of a hemoplasma, Bartonella spp, Ehrlichia spp, or A phagocytophilum detected in its blood and is likely a highly suitable candidate for participation in a blood donor program. Once suitable blood donors have been identified, keeping those cats housed indoors and maintaining control of arthropod vectors on the cats and in their environment are strategies that would contribute to the maintenance of an uninfected blood supply for transfusions in cats.

a.

University of Pennsylvania, Virginia-Maryland Regional College of Veterinary Medicine, and University of Florida.

b.

Angell Animal Medical Center, Boston, Mass, and The Animal Medical Center, New York, NY.

c.

Lappin MR. Infectious causes of fever in cats (abstr). J Vet Intern Med 2002;16:366.

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