Abstract
Extract: A model of embryonic mumps virus infection was developed in the chicken, which allows direct study of the interaction between developing tissues and virus in the aplacental host. White leghorn and Rhode Island red embryos were inoculated with 104 to 105 plaque-forming units (PFU) of mumps virus between the 12th and 16th hr of incubation.
Of the total virus recovery from the organs of 11 chickens at hatch, 54% of the sum was isolated from the heart. The lung, kidney, and brain yielded 20%, 12.5%, and 11%, respectively, of the total virus isolated. Lesser amounts of virus were recovered from the liver, spleen, bursa of Fabricius, and skeletal muscle. Viremia was detected in about half of the chickens. The population of virus-producing cells in tissues ranged from 0.002 to 4.0%, with the heart containing 10-fold more infected cells than the lung, and 100-fold more infected cells than the liver and brain. Virus disappeared from the organs during the 1st week after hatch. Low levels of interferon, 20 to 40 units/g, were detected in the tissues of 20-day-old infected embryos.
Intraperitoneal, intravenous, and intranasal inoculation of normal hatchling 1-, 2-, 3-, and 4-month-old chickens with mumps virus failed to promote multiplication of virus or antibody production.
Infected embryos were often significantly stunted at hatch. In one experiment infected embryos at hatch weighed 37.5 g (SD ± 5.9) versus 43.3 g (SD ± 2.4) for control birds, P < 0.025. The growth of infected hatchlings was reduced during the early weeks of life, but catch-up occurred by 1 month of age. Although spleen weights were similar to control birds, the weights of the liver (P < 0.025), heart (P < 0.025), and brain (P < 0.005) of infected chickens were significantly decreased at the completion of incubation.
Although capable of producing specific mumps virus-neutralizing antibody by 1 month of age, infected chickens experienced a delay in the maturation of immunoglobulin M (IgM) and immunoglobulin G (IgG) synthesis. Serum specimens were obtained from 10 experimental and control chickens during the 1st year of life. The mean level of IgM (expressed as a percentage of normal adult serum pool) at 1 month was 31.7 (SEM ± 2.6) for experimental chickens, significantly less (P < 0.005) than the level for control birds of 47.8 (SEM ± 5.5). At 2 months, the levels of IgM for both groups were the same. The mean titers of 19 S natural rabbit erythrocytic agglutinins were also lower (P < 0.005) in experimental chickens, 4.86 (SEM ± 0.75), than in control chickens, 7.80 (SEM ± 1.07), at 1 month of age but rose to equivalent titers by 2 months. The mean concentration of IgG was similar in both groups at 1 month, but fell significantly (P < 0.005) at 2 months when the level in experimental birds was 151 mg/100 ml (SEM ± 20) and in control birds was 415 mg/100 ml (SEM ± 64). IgG levels remained low (P < 0.005) at 5 months, 384 mg/100 ml (±46) versus 550 mg/100 ml ( ± 73). At 11 months, the IgG concentrations were equivalent. In contrast, infection did not alter the normal transition from embryonic to adult hemoglobin synthesis.
Speculation: This experimental model obviates consideration of placental dysfunction as a cause of diminished embryonic growth and immunoglobulin production. Thus, virus may either directly reduce the size of cells or their rate of division in embryonic organs or alter cardiac output with consequent peripheral hypoperfusion. A more subtle disturbance of bursal cell function must occur in the absence of abundant viral replication to explain the appearance of transient dysgammaglobulinemia.
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Geme, J., Davis, C., Peralta, H. et al. The Biologic Perturbations of Persistent Embryonic Mumps Virus Infection. Pediatr Res 7, 541–552 (1973). https://doi.org/10.1203/00006450-197306000-00001
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DOI: https://doi.org/10.1203/00006450-197306000-00001