Proceeding of the NAVC North American Veterinary Conference Jan. 8-12, 2005, Orlando, Florida
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1 Proceeding of the NAVC North American Veterinary Conference Jan. 8-12, 2005, Orlando, Florida Reprinted in the IVIS website with the permission of the NAVC
2 Small Animal - Immunology 453 IMMUNOLOGIC METHODS OF DISEASE DIAGNOSIS Leah A. Cohn, DVM, PhD, DACVIM University of Missouri, College of Veterinary Medicine Columbia, MO INTRODUCTION Specific immunologic reactivity is often used for diagnostic purposes. Serologic testing for infectious agents or for an antibody response demonstrating exposure to an infectious agent is one of the most common ways immunologically based tests are used in clinical medicine. Immunologic testing is also used to evaluate the immune system itself in cases of suspected hypersensitivity or autoimmunity, to estimate resistance to a particular disease, or to document an immunodeficiency state. Immunologic principles are used in diagnostic tests not intended to evaluate either infection or immunity. For instance, many tests for drug or toxin concentrations are based on immunologic principles where the drug / toxin serves as an antigen (e.g., opiates, amphetamines, aflatoxin, ergot alkaloids). Other tests take advantage of the specificity of immunologic reactions to look for the presence of endogenous substances in bodily fluids (e.g., commercial tests for microalbuminuria, hormone assays). This review will describe the principles behind immunologically based diagnostic techniques, with an emphasis on principles for the use of serologic tests in infectious disease diagnosis and common tests of immune function. CONCEPTS OF SEROLOGIC TESTING FOR INFECTIOUS DISEASE Serology is the measurement of antigen-antibody interactions for diagnostic purposes. Although serology is used in the detection of drugs, hormones, and proteins, perhaps its most prevalent use by practicing veterinarians is in the diagnosis of infectious disease. In the most basic sense, measurement of antigen-antibody interactions can be done in either of two ways. First, detection of specific antibody in the fluids or tissues of an animal can provide evidence that the animal has been exposed to a given antigen. When the antigen to which the antibody is directed is a pathogen, this is used as circumstantial evidence of infectious disease. Second, a particular antigen can be detected within the animal s fluids or tissues via reaction with specific antibody provided in the assay system. When the antigen in question is a pathogen, detection of antigen can be used as direct evidence of infection. It is important to remember that direct or circumstantial evidence of infection is not necessarily proof that any particular disease process is a result of that infection. For instance, an ill cat may be found to have antibody directed against Bartonella spp, but this is not proof that the clinical illness is due to Bartonella infection since up to half of all healthy cats carry Bartonella without any clinical illness. Serologic tests can be classified as tests of primary antigen-antibody interaction, secondary tests of interaction, or tertiary tests of interaction. In primary binding tests, antigen and antibody are allowed to interact and form complexes. The resulting complexes are quantified using reagents labeled with radioisotopes, fluorescent dyes, or enzymes. Common examples of these sensitive diagnostic techniques include direct or indirect fluorescent antibody tests (IFA) and enzyme-linked immunosorbent assay (ELISA). These tests may be carried out on tissues, cells, serum, or a variety of other test substrates depending on the tests specifics. Secondary binding tests measure the results of antigen-antibody interaction (agglutination, hemagglutination, precipitation, neutralization, or complement fixation) in vitro. Examples include direct antiglobulin test (Coomb s test), gel immunodiffusion (e.g., Coggin s test) and immunoelectrophoresis. Tertiary binding assays are not commonly used for clinical disease diagnosis, but measure the actual protective effect of antibody in an animal. Results of serologic immunoassays may be provided in either of two formats. Binomial results are reported as either positive or negative, whereas the highest dilution of a sample that results in a positive end point (fluorescence, color change, agglutination, etc) provides a titer. In either case, someone must choose an end point to be called positive in the case of binomial tests like most of the point of care assay kits, the manufacturer sets the positive end point. In the case of titers like those for leptospirosis or corona virus, the practitioner decides what end point is considered positive. In many antibody detection assays, there will be significant overlap between infected and uninfected animals in terms of titer. Practitioners employ serology to evaluate the likelihood that a given animal has a particular infectious disease. Although quite useful, there are limitations to serologic testing. The first deals with the meaning of a positive antibody test. The presence of antibody indicates exposure to an antigen, but does not necessarily indicate active infection or disease. In some cases, the antigen may be cleared from the animal without causing disease, and yet result in a positive antibody titer. Such is often the case for fungal antibody titers to Histoplasmosis, for example. In other cases, the antibody detected may not be pathognomonic for a given infection. For example, antibody generated in response to feline infectious peritonitis (FIP) is indistinguishable from antibody generated against feline enteric corona virus. In yet other cases, the antibody may be found as a result vaccination or of passive transfer rather than as a result of the animal having a given infection. Such may be the case with kittens allowed to nurse feline immunodeficiency virus (FIV) infected queens. There may also be cross reactivity between antibodies, where the antibody detected is not really to the infection in question, but to something that appears quite similar; for example, Rickettsia risticii looks similar to non-pathogenic R. montana. On the other hand, antibody is not always detected in the presence of active infection. The most common reason for antibody tests to be negative despite infection is that insufficient time has elapsed between infection and measurement of an antibody response. For example, serologic testing for cytauxzoonosis would be relatively useless because the peracute nature of the illness means that illness precedes antibody production. Acute titers in dogs with Rocky Mountain spotted fever or leptospirosis are often negative on presentation, but become positive if tested again in a few weeks (seroconversion). Alternatively, immunocompromised animals may fail to produce detectable antibody despite longstanding infection. For example, this may be the case during the terminal stages of either FIV or FIP infection when an ill cat simply doesn t produce antibody to infection any longer.
3 The North American Veterinary Conference 2005 Proceedings Those tests that detect the presence of antigen instead of antibody have limitations as well. For instance, although detection of feline leukemia virus (FeLV) antigen does denote infection, the animal may be able to clear the infection before the virus becomes permanently incorporated. In this case, a serum ELISA test might be positive but the cat will not have a shortened lifespan due to FeLV induced-disease. On the other hand, antigen may be sequestered at a site that is not assayed by the test. Again using FeLV ELISA as our example, latent infection results in viral incorporation into marrow, but leaves tests of peripheral blood negative. Antigen tests generally assay for only one type of antigen, while in reality infection is not always associated with that one antigen. For example, antigen tests for heartworm disease test for antigen present on the female worm, leaving antigen test results negative in cats (or dogs with low worm burdens) with only male parasites. Although it is more common for antibody to be present in the absence of infection than for antigen to be present in the absence of infection, it is still possible. For instance, fecal parvoviral antigen tests may be positive for several days after vaccination with modified live parvoviral vaccine, or after exposure of a dog to feline parvovirus (panleukopenia). Immunoassays can be designed to reflect the presence of any or all antibodies to a given antigen, or they may specifically detect antibodies of a given isotype (i.e., IgM, IgG, IgA, and IgE). Because antibody isotype varies in relation to onset and duration of antigen exposure, it is often important to know what isotypes of antibody are being measured by a given test. Initial antibody response to infectious agents is predominantly IgM mediated, but the response later switches to IgG and/or IgA. For agents like Toxoplasma gondii, capable of causing chronic infection without illness, an IgG response may persist for years without illness. Vaccine titers, such as canine distemper virus titers, may also persist for years without disease. Titers may persist after elimination of disease either by medical therapy or through natural clearance. Ehrlichia canis titers, for instance, can persist for months or even years after treatment of infection and resolution of clinical illness. Therefore simple detection of a positive antibody titer, even a high titer, is not proof of active infection for these diseases. In such cases, documentation of active infection requires either a positive IgM titer or proof of an increase in IgG titer (2 doublings, or a 4-fold increase) over a period of several weeks. Because of variability inherent in immunoassay, titers should be run by the same laboratory using the same methodology, and samples should ideally be banked in order to run assays simultaneously. An additional set of limitations pertains to the likelihood that a given test accurately reflects disease presence or absence. Any test, no matter how good, is subject to both false positive and false negative results. These are reflected in the diagnostic sensitivity and specificity of the test. Diagnostic sensitivity refers to the proportion of tests run on infected animals that are positive, while diagnostic specificity refers to the proportion of tests run on uninfected animals that are negative. It is apparent then that to rule out a diagnosis, a test with a high sensitivity is desired, while to rule in or confirm a diagnosis, a test with a high specificity is desired. In generally, any time an assay is made more sensitive, some degree of specificity is lost, and vice versa. Perhaps even more important to the clinician than a given test s sensitivity and specificity are the test s positive and negative predictive values. The positive predictive value is the probability that an animal that tests positive actually has the disease in question, while the negative predictive value is the probability that an animal that tests negative is free of disease. While predictive value certainly is related to the sensitivity and specificity of the diagnostic assay, it is also related to the prevalence of disease in the population of animals tested. This means that a positive test result in a population with a low incidence of disease, even when the test is very sensitive and specific, has a much greater chance of being a false-positive than when the same test is applied to a population with a high disease prevalence (figure 1). Remember that no test is perfectly accurate all the time. Every immunodiagnostic test result must be interpreted in light of signalment, history, physical exam, and supportive or refuting imaging and laboratory studies. Serologic test results should be viewed as one piece of the puzzle, not as the entire picture! Infected Non infected Positive test 4, Negative test 250 4,500 A. area with 50% prevalence of infection Infected Non infected Positive test Negative test 25 8,550 B. area with 5% prevalence of infection Figure 1. A serologic test with 90% and 95% sensitivity is applied to 10,000 dogs in each of regions A and B, where disease prevalence in A is 50% while disease prevalence in B is 5%. For region A, the positive predictive value can be calculated as: PPV = 4,750/(4, ) = 90%. This realistically means that one out of 10 positive tests is a false positive. For region B, the positive predictive value of the same test can be calculated as PPV = 475/( ) = 33%. This means that two out of three positive tests are false positives. TESTS OF AUTOIMMUNITY Autoimmunity is a form of hypersensitivity. The effector functions of immunity act normally, but regulation and direction of those effector functions has gone awry. Autoimmunity may be primary or secondary, organ specific (e.g., IMTP) or non-organ specific (e.g., SLE), predominantly cell mediated (e.g., diabetes mellitus) or humoral (e.g., rheumatoid arthritis). Tests of autoimmunity are often quite specific to the disease process. A few of the most commonly used tests in small animal practice are described. The direct antiglobulin test (Coomb s test) is the most commonly performed test for autoimmunity in veterinary medicine. It identifies that patient RBC are coated with antibodies or complement and is therefore used as supportive evidence of immune mediated hemolytic anemia (IMHA). The test can not distinguish between primary and secondary causes of IMHA. There are multiple potential causes of false positive (e.g., transfusion) and false negative (e.g., steroids) test results. Because the test evaluates only for autoantibody directed at RBC, a positive result does not imply that any other type of autoantibodies (e.g., ANA, antiplatelet antibodies) are present. The test itself involves washing the patient s RBC, and then incubating these cells with species specific antiserum. Most 454
4 Small Animal - Immunology commercial antiserum uses a combination of antiglobulin reactive with IgG, IgM, and complement. After reaction with the antiserum, the patient s cells are again washed. If antibody was originally attached to the RBC, the antiglobulin will cause a positive agglutination reaction. Because agglutination is the endpoint of this test, it is redundant and unnecessary in animals presenting with persistent autoagglutination. Often, the test is conducted at both body temperature and at 4 o C. The lower temperature tests are done to look for cold acting hemagglutinin, but most cases of IMHA resulting in clinical anemia will be positive at body temperature. Antinuclear antibody tests (ANA) are just what the name implies, tests that evaluate for the presence of antibody in the serum of a given patient directed against nuclear antigens. Classically, the presence of these antibodies would suggest systemic autoimmune disease such as systemic lupus erythematosus (SLE). It is important to understand that a positive result does not cinch a diagnosis of SLE, but is only one single piece of supportive evidence that must be combined with multiple other findings to make a diagnosis of SLE. Any inflammatory process, including many types of infection, may result in a positive test. Likewise, autoimmunity can be present without a positive ANA test. In fact, the most common types of autoimmune disease of the dog and cat including IMHA, IMTP, pemphigoid skin conditions, and polyarthropathies are accompanied by negative ANA. There are more than 25 types of ANA tests used in human medicine with each suggesting a slightly different interpretation. In veterinary medicine only non-specific immunofluorescent ANA testing is used commonly. Either cultured cells or slices of rodent liver are used as a source of nuclear antigen (DNA, RNA, histones). Patient sera is reacted with the antigen source, and then washed away. Next, species specific antisera attached to a fluorescent substrate is added, again followed by a wash step. The fixed antigens are then examined under a fluorescent microscope. If initial evaluation is positive for fluorescence, patient sera is serially diluted and retested to provide an eventual titer. The pattern of fluorescence is often noted, but no firm correlations exist in veterinary medicine between the pattern and any given disease process. Rheumatoid factors (RF) are autoantibodies directed against other antibodies, and which bind only after the target antibody has itself bound an antigen. Although RF are often produced by the synovium and found in joint fluid in animals / people with rheumatoid arthritis, their exact role in disease pathophysiology is poorly understood. Both serum and joint fluid may be tested for RF by either of two methods. The older method is the Rose-Waller test. In this test sheep RBC (SRBC) are reacted with a subagglutinating dose of speciesspecific antiserum sensitized to SRBC. Next, the serum or joint fluid from the patient is serially diluted and added to a standardized number of sensitized SRBC. If the serum contains RF, they bind the antibody on the SRBC and cause agglutination. The highest dilution of serum causing agglutination provides the titer. Newer methodology uses an ELISA type test. Like with the ANA, testing is neither sensitive nor specific for rheumatoid arthritis. Titers wax and wane, and may be negative in up to 30% of patients with arthritis, or may be positive in animals that don t have immune mediated arthritis. TESTS FOR IMMUNE COMPETENCE Tests of immune competence are used for two main purposes. One is to check if an animal will be protected from a particular infectious disease, and the other is to see if an animal has a congenital (or acquired) immunodeficiency state. Because of concerns about adverse vaccine reactions, veterinarians are interested in evaluating individual animals for adequacy of protection rather than simply administering booster vaccines. This is often done through the measurement of serum antibody titers. Although such titers may provide a rough correlate with protective immunity for certain viral infections, this is merely a correlation. Vaccine induced protection often relies on cell mediated or other aspects of immunity in addition to humoral immunity. Antibody titers don t provide information relative to cellular immunity. Animals with negative titers may well be protected from disease, and conversely, animals with positive titers may be susceptible to disease. These titers are best used only for disease in which titer has been demonstrated to at least roughly correlate with resistance to disease challenge (feline and canine parvo, distemper, feline viral respiratory). Additionally, since prevalence of protection by vaccination should be high, negative predictive value of even sensitive and specific testing is low, meaning that many animals with negative titers are false negatives and are truly protected from disease. Tests of immune function applied to animals with suspected immunodeficiency are as diverse as the immune response itself. Before choosing what tests are appropriate for any animal with a suspected immunodeficiency, it is important to have some idea what aspect of immune function may be lacking. Often, simple observation of the prevalent type of infections provides the needed clues (e.g., phagocytic defects predispose to fungal and bacterial infection, defects in CMI predispose to viral and intracellular pathogens). Repeated or persistent infections in a single body system often signal defects in physical barriers to infection (e.g., ciliary dyskinesia leads to respiratory infection) rather than immunodeficiency. Tests of immunity include evaluation of cell number and morphology, evaluation of cell proliferation, evaluation of specific cellular functions (e.g., phagocytosis, killing), and evaluation of secreted molecules (e.g., antibodies, cytokines, complement). Tests as simple as a CBC can provide great clues to the presence of some immunodeficiency states (e.g., persistent or cyclic neutropenia, severe leukocytosis with leukocyte adhesion deficiency, or granule alterations in Chediak-Higashi). Other tests require more sophisticated assays (e.g., lymphocyte proliferation in response to mitogens, secretion of cytokines, assay of antibody concentration) to confirm the presence or absence of immunodeficiency. In general, if primary immunodeficiency is suspected, consultation should be sought. Previously presented at the 22 nd Annual ACVIM Forum, Minneapolis, MN, June REFERENCES 1. Tyler JW. Cullor JS. Titers, tests, and truisms: rational interpretation of diagnostic serologic testing. JAVMA : Schultz RD, Adams LS. Immunologic methods for the detection of humoral and cellular immunity. Vet Clin N Am :
5 The North American Veterinary Conference 2005 Proceedings 3. Compton SR, Riley LK. Detection of infectious agents in laboratory rodents: traditional and molecular techniques. Comp Med. 2001; 51: Gorman NT, Werner LL. Immune-mediated diseases of the dog and cat. IV. Therapy and immunodiagnosis. Br Vet J : Moore GE, LT Glickman. A perspective on vaccine guidelines and titer tests for dogs. JAVMA. 2004; 224:
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