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1 INFECrlON AND IMMUNrrY, May, 1973, p Copyright American Society for Microbiology Vol. 7, No. 5 Printed in U.SA. Enhanced Effect of Repeated Administration of Bacterial Vaccine Against Viral Respiratory Infection MIKLOS DEGRI AND HELEN DAHL Kapt. W. Wilhelmsen og Frues Bakteriologiske Institutt, Rikshospitalet, University of Oslo, Oslo, Norway Received for publication 19 December 1972 Administration of a standard bacterial vaccine (SBV) affords some protection against influenza infection in mice if given 4 to 5 h before inoculation of the virus. This effect was enhanced by repeated injections of SBV 7 and 14 days earlier, as measured by the length of survival, mortality rate, development of gross pneumonia, and virus multiplication in the lungs. Serum interferon levels were likewise enhanced by immunization with SBV, which may, at least in part, explain the increased preventive effect. Interferon (IF) production and protective effect against viral infection by various IF inducers may be influenced by earlier experiences of the host organism with the inducer. Viral agents may sensitize the host to increased production of IF when they are restimulated with the homologous agent (9, 18), provided that this happens well after the initial refractory period. This immune recognition mechanism is apparently in effect also when nonviral IF inducers are applied. Immunization with synthetic (11), bacterial (Hardegree and Singer, personal communication), and fungal (12) IF inducers resulted in an increased or prolonged IF response or increased protection against viral infections, or both, compared to that without previous immunization. Negative effect due to earlier experience with the inducer, specified by reduced IF production or reduced protection against viral challenge, has also been reported (6, 8). Bacterial vaccines commonly employed by some physicians in the treatment of bronchial asthma and recurrent or chronic respiratory infections induce or release an IF-like viral inhibitor in the serum of mice after a single intraperitoneal (i.p.) injection (5). A single i.p. injection of undiluted vaccine reduced the morbidity and mortality of mice due to vesicular stomatitis virus (VSV) (5), influenza A2 (2), Semliki Forest virus (15), and Sendai virus (Hardegree and Singer, personal communication) infection and slightly increased the survival time of Toxoplasma gondii-infected mice (4). The usual schedule of vaccine administra- 771 tion in clinical practice is by regularly repeated injections at 1- to 2-week intervals. Therefore, we decided to investigate the effect of vaccine on IF production and on resistance against viral respiratory infection mimicking the clinical administration. The previously investigated model of influenza A2 virus infection in mice was employed as viral challenge. MATERIALS AND METHODS Mice. Ham/ICR/CSE/Bom albino mice were originally obtained from the National Institute of Public Health, Oslo, Norway, and were randomly bred at our Institute. They were kept in plastic cages, fed mouse pellets, and given water ad lib. Young adults of either sex were used in all experiments. Bacterial vaccine. The standard bacterial vaccine (SBV) was purchased from the National Institute of Public Health, Oslo. The composition of the vaccine has been described elsewhere (5). Virus. Influenza AJSingapore 1/57 was kindly given to us by K. Herzberg, Frankfurt, Germany. In our laboratory it was passed two times in the allantoic cavity of embryonated hens eggs. Allantoic fluids were harvested 3 days after infection, and those with high hemagglutination titers were pooled and stored at - 70 C. Mouse infectious titer was estimated by inoculating mice intranasally (i.n.) with 0.1 ml of serial 10-fold dilutions of virus under light ether anesthesia, five mice per dilution. Mortality was recorded daily for 14 days. The mean lethal dose (LD50) was calculated by the method of Reed and Muench (13). Ten LD50 in 0.1 ml were used as challenge dose in the in vivo studies. Vesicular stomatitis virus (VSV) was used as challenge virus in all IF titrations. In our laboratory it was passed two times in the allantoic cavity of em-

2 772 DEGRI AND DAHL INFECT. IMMUNITY bryonated hens eggs and then several times in L-F, cells. Infectious titer was estimated by the end point titration method in microtrays as previously described (3). Newcastle disease virus (NDV) was received from L. A. Glasgow, University of Utah, Salt Lake City, Utah. It was passed two times in the allantoic cavity of embryonated hens eggs in our laboratory. Allantoic fluids with high hemagglutination titers were pooled and stored at - 20 C. Infectious titer was estimated by the end point titration method in Vero cell cultures. Cells. The L-F, strain of mouse fibroblasts was received from S. Haahr, Aarhus University, Denmark. It was grown in Eagle minimal essential medium (MEM) with Hanks salts (GIBCO) supplemented with 10% inactivated calf serum, 0.044% NaHCOs, and antibiotics, and maintained in the same medium but with 5 or 2% inactivated calf serum and 0.132% NaHCO,. The Vero line of African green monkey kidney cells was received from J. C. Ulstrup, UllevAl Hospital, Oslo. It was grown in medium 199 with Hanks salts supplemented with 5% inactivated calf serum, 0.044% NaHCOs, and antibiotics, and was maintained in the same medium, but with 2% inactivated calf serum and 0.132% NaHCO3. Tests for biological activities: hemagglutination. The presence of influenza virus in the lungs of inoculated mice was tested by the micro hemagglutination (HA) method in Meda microtrays with U bottoms (Orion OY, Finland). Serial twofold dilutions of lung suspensions were prepared in 0.05 ml of saline. To each cup 0.05 ml of a 0.5% suspension of threetimes-washed guinea pig erythrocytes was added. The tray was then carefully shaken to insure proper mixture of the red cells and antigen and read after 1 to 1.5 h of incubation at room temperature when the red cells had settled down. The highest dilution showing at least 50% hemagglutination was registered as HA titer. Interferon assay. Blood samples were obtained from the axillary vein at various time periods after administration of SBV as indicated in the results. Samples were allowed to clot at +4 C ovemight. Subsequently, serum was separated and diluted 1:5 in Eagle MEM adjusted to ph 1.0, which resulted in a final ph of approximately 2.0 for the serum dilutions. After 2 days at +4 C, the ph was readjusted to neutrality by addition of 1 N NaOH, and the samples were tested for presence of IF by the micro method described in detail elsewhere (3). In short, serial twofold dilutions of the samples were prepared in microtrays (Linbro IS-FB 96) in 0.05-ml volumes, three cups per dilution. To each cup was added 0.05 ml of medium and 40,000 L-F1 cells in 0.1 ml of medium. Control cups were seeded simultaneously with 40,000 L-F1 cells in 0.2 ml of medium without IF. The trays were sealed with cellophane tape and incubated overnight at 37 C. The next day the tape was removed and the test cups were challenged with approximately 10 mean tissue culture infective doses (TCID,o) of VSV in ml of medium. A back titration of the challenge virus was run in parallel in each test. After being sealed, the trays were incubated again at 37 C. Microscope reading was done after 3 days, when the end point titration of VSV was complete. The IF titer was estimated as the highest dilution which inhibited viral cytopathic effect in 50% of the cups, calculated by the method of Reed and Muench (13). The titers were calibrated to 10 doses of challenge virus by means of the standard slope of the regression line for mouse IF tested in the L-F/VSV system as described in detail elsewhere (3). Design of in vivo experiments. Mice were inoculated i.n. with 10 LD50 of influenza virus under light ether anesthesia. Those succumbing within one day after inoculation were excluded from the experiment because death was considered to be due to experimental manipulation. Mortality was recorded daily. After 14 days the survivors were killed and their lungs were inspected for macroscopic signs of pneumonia. The degree of pneumonia attack was graded using an arbitrary "- " to " +++" per lobe (maximal pneumonia score: 15+ per animal). Statistical methods. The results were subjected to statistical analysis employing the Student's t test and the x2 test. The Wilcoxon two-sample test was used to compare the length of survival. RESULTS Influence of SBV immunization on development of pneumonia and mortality of mice. Three groups of mice, 16 mice in each group, were immunized with SBV (0.2 ml of undiluted vaccine i.p.) at the time periods indicated in Table 1. Two of these immunized groups and one group of 16 unimmunized mice were given SBV (0.2 ml i.p.), and 5 h later all four groups were inoculated with influenza virus. A fifth group of 16 untreated mice was similarly inoculated with virus for control. Figure 1 illustrates graphically the cumulative mortality from two experiments. In Table 1, further results from these two experiments are summarized. Death of influenza-inoculated mice was delayed and reduced by administration of SBV, if given 5 h prior to virus challenge. Repeated treatment prior to challenge further increased this effect. However, early treatment alone was without significant effect. The incidence of morphological signs of pneumonia among the survivors was reduced by repeated vaccine treatment as compared to those given only one dose of SBV. The number of survivors in the virus control group was too low for meaningful comparison. Influence of immunization with SBV on virus replication in the lungs. Two groups of mice, nine mice in each group, were injected with 0.2 ml of SBV i.p. Fourteen days later one of these groups and another group of nine unimmunized mice were given 0.2 ml of SBV, and 4 h later all three groups were inoculated with 10 LD,0 of influenza virus in a 0.1-ml

3 VOL. 7, 1973 VACCINE AGAINST VIRAL RESPIRATORY INFECTION 773 TABLE 1. Influence of single and multiple injections of a standard bacterial vaccine on the development of pneumonia and mortality due to intranasal inocalation of influenza virusa Mortality 50% Mortality Time of vaccine No. of No No Pneumonia treatment prior to Total no. survivors difference difference score (in virus inoculation in p at 14 days % from After days from survivors) controls controls (P) 14 days, 7 days, 5 h < < days, 5 h < < days > < h < < None = 8a 2 60 a Combined results of two experiments. _40 p,e. -& k,*-t.~..5viruds 2 X,.. control.5 hours e014 days & 5 hours. hours.,14&7days & i./o Days after Infection FIG. 1. Influence of single and multiple injections of the standard bacterial vaccine on mortality of mice due to influenza virus. Vaccine was injected at the indicated times prior to virus inoculation. Combined results of two experiments. volume. A fourth group of nine untreated mice was similarly inoculated with virus for control. After 5 days all mice were sacrificed, their lungs were inspected for macroscopic signs of pneumonia, and the pneumonia score was registered for each mouse. The lungs were then washed in Hanks basal salt solution and homogenized. The suspensions were tested for the presence of influenza virus. The results of this experiment are tabulated in Table 2. Immunization 14 days prior to challenge was without effect on the virus titer in the lungs and on the development of pneumonia. One injection 4 h before challenge had little if any effect. In contrast, SBV given both 14 days and 4 h before challenge reduced both pneumonia score (P < 0.005) and HA titer (P < 0.005) compared to the control group. The differences from the groups given one dose of SBV are also significant (pneumonia score, P < 0.05; HA, P < 0.005). Influence of immunization on the level of circulating interferon. One group of mice was immunized by two i.p. injections of 0.2 ml of (P) TABLE 2. Influence of single and multiple injections of a standard bacterial vaccine on multiplication of influenza virus in the mouse lungs Time of vaccine Log1. HA titer Pneumonia score treatment prior to in the lungs (mean) virus inoculation (mean) 14 days, 4 h 0.825a 3.6b 14 days h None a Probability of no difference from controls < Probability of no difference from 4-h group <0.05. b Probability of no difference from control and 4-h group < SBV at weekly intervals. Seven days after the last injection, both the immunized and an untreated group of mice were given 0.2 ml of SBV i.p. Samples of blood for determination of IF levels were obtained 2, 4, 6, 8, 24, and 48 h later. Blood from two mice was pooled for each determination. The combined results of two experiments are summarized in Fig. 2. IF appeared earlier, reached higher peak titer, and remained longer in the serum of immunized mice compared to those given only a single injection. To test the effect of immunization on IF production by viral induction, 10 mice were immunized as in the previous experiment. One week later half of the immunized mice and a group of untreated mice were inoculated i.p. with 0.2 ml of NDV containing approximately 2 x 108 TCID50. Six hours later all three groups of mice were bled from the axillary vein, and sera from each group were pooled and assayed for presence of IF. The results of this experiment are shown in Table 3. A moderate increase of IF titer was demonstrated in the serum of mice immunized with SBV prior to inoculation

4 DEGRg AND DAHL 774 INFECT. IMMUNITY with NDV, compared to the group treated only with NDV. The IF activity found in the serum of animals receiving only SBV treatment should be considered with caution. At the time of this experiment our mouse colony was hampered by epidemic diarrhea of unknown etiology and log 1 to 1.2 unit IF was demonstrated in the mice sera several times. Dose dependence of the SBV protection against influenza. Six groups of mice, 17 mice per group, were immunized with SBV according to the schedules shown in Table 4. Four hours after the last injection all groups were challenged with influenza virus as described. The H LO24 GO (16i 2.2 0* Z 2.0 I '- 1.4 od*--, HOURS FIG. 2. Comparison of interferon production in immunized (open circles) and nonimmunized (closed circles) mice after injection of 0.2 ml of vaccine. TABLE 3. Influence of immunization with a standard bacterial vaccine on interferon production following induction with Newcastle disease virus Vaccine treatment Induction with Interferon titer at days prior to NDVa in pooled sera viral induction 14, 7 ± 2.55b 14, 7 _ 1.17 None a +, NDV induction; -, no NDV induction. b Log,0 units of interferon per 0.1 ml of serum. TABLE 4. Group no.... mice were inspected daily for 14 days, and mortality was recorded. The mortality was clearly dependent on the dose of SBV (Table 4). Death of mice was delayed in all groups treated with SBV 4 h before challenge; however, only the largest doses reduced the mortality rate significantly. Again in this experiment previous immunization increased the protective effect. DISCUSSION This study confirms our previous results (2) that the combined bacterial vaccine gives some protection against influenza infection in mice provided it is administered shortly before inoculation with the virus. Furthermore, the results indicate that immunization with the vaccine enhances this effect. Death was delayed and the mortality rate was reduced in immunized mice compared to those given only one dose of vaccine shortly before virus challenge. Also, virus multiplication in the lungs and development of gross pneumonia were further reduced by the immunization with SBV. Comparable results were obtained with a vaccine similar to ours and with house dust extracts by Hardegree and Singer (personal communication) against Sendai virus, but not against influenza A2 PR 8 virus. However, repeated doses of another interferon inducer, statolon, afforded higher protection against influenza A2 PR 8 infection in mice than a single dose (12). The mechanism of the preventive effect is not clear. It is well documented that a number of IF inducers, especially the nonviral ones, induce a complex response in the host organism. One part of this reaction is production of IF. As a working hypothesis we assumed that IF production is at least partly responsible for the protection afforded by the bacterial vaccine against different viruses. The present findings support this hypothesis; thus, the increased protection produced by immunization was followed by an increased production of IF. Of course, this is not Dependence of the protective effect against influenza infection of mice on the dose of the standard bacterial vaccine Vaccine treatment prior to challenge Total no. Survival 50% Survival 5 atrday 14 days 7 days 4h mice (%) atday Undiluted Undiluted Undiluted a i " Undiluted Ob a Probability of no difference from controls < a Probability of no difference from controls <0.01.

5 VOL. 7, 1973 VACCINE AGAINST VIRAL RESPIRATORY INFECTION 775 necessarily the whole explanation of the enhanced effect. The role of humoral and cellular immunity, both stimulated by different IF inducers (1, 14, 17), still remains to be determined. In fact the relatively marked protection is not proportional to the low levels of IF, which could indicate that other mechanisms must be involved. Numerous studies suggested that immune recognition mechanism may function as enhancer of IF production. Glasgow (9) has shown that cultures of peritoneal leukocytes from Chikungunya virus-immunized mice produced more IF than cells from normal mice, stimulated with the same agent. Similar results were reported by Yamada et al. (18) employing NDV. Repeated administration of nonviral IF inducers initiates probably a more complex response of the host as indicated by varied results reported after examination of different models. BCG-immunized mice produced more IF than normal mice when stimulated with protein derivative of tuberculin (PPD) (16). Nonviral antigens, such as PPD, tetanus toxoid, and diphtheria toxoid may induce IF production in lymphocyte cultures from sensitized human donors but not in cells from nonimmune donors (10). Our present findings agree with these results. On the other hand, rabbits immunized with polyinosinic polycytidylic (poly I: poly C) acid and with high antibody titers against this agent produce less IF in response to induction with poly I: poly C than nonimmunized rabbits (6, 8). Ho et al. (11) suggested that the late effect of one or repeated injections with endotoxin or poly I:poly C may represent unknown complex biological phenomena. The initial tolerant state in their experiments was followed by a hyper-reactive state in the mice. The late effect of immunization is not necessarily restricted to the immunizing agent. Serum IF titers induced by NDV, Chikungunya virus, and poly I: poly C were depressed, but if induced by endotoxin they were enhanced in mice immunized with viable or nonviable Corynebacterium acnes (7). In our model, immunization with SBV enhanced IF production induced by NDV. The data support the concept of the involvement of reticuloendothelial system in IF production; however, they do not explain the differences obtained with the various models. Undiluted SBV, shown to be protective against influenza and VSV infection in mice (2, 5), far exceeds the doses employed in clinical practice. The present findings suggest that, if given repeatedly, considerably smaller doses may offer some protection. Although the 1/1,000 dilution still contains a large amount of antigen for an animal the size of a mouse, the 10 LD50 challenge dose is also much higher than the dose one has to expect under natural conditions. On the basis of these considerations we suggest, with all reservations, that bacterial vaccines administered as regularly repeated injections may produce a protective effect against small doses of respiratory virus infections in mice. The value of the vaccine against human infections remains to be determined. LITERATURE CITED 1. Braun, W., and M. Nakano Antibody formation: stimulation by polyadenylic and polycytidylic acids. Science 157: Dahl, H., and M. Degre Preventive effect of a nonviral interferon inducer, a bacterial vaccine, on experimental influenza in mice. Acta Pathol. Microbiol. Scand. Sect. B. 80: Dahl, H., and M. Degre A microassay for mouse and human interferon. Acta Pathol. Microbiol. Scand. Sect. B. 80: Degr6, M Effect of a standard bacterial vaccine on infection with an obligate intracellular parasite (Toxoplasma gondii) in mice. Acta Pathol. Microbiol. Scand. Sect. B. 80: Degre, M., and H. Dahl Production of an interferon-like agent following inoculation with bacterial vaccine. Proc. Soc. Exp. Biol. Med. 137: Dianzani, F., G. Forni, A. Negro Ponzi, A. Pugliese, and G. Cavallo Decreased interferon response to polyinosinic polycytidylic acid in rabbits immunized against the inducer. Proc. Soc. Exp. Biol. Med. 139: Farber, P. A., and L. A. Glasgow Effect of Corynebacterium acnes on interferon production in mice. Infect. Immunity 6: Field, A. K., A. A. Tytell, G. P. Lampson, and M. R. Hilleman Antigenicity of double-stranded ribonucleic acids including poly I: C. Proc. Soc. Exp. Biol. Med. 139: Glasgow, L. W Leukocytes and interferon in the host response to viral infections. II. Enhanced interferon response of leukocytes from immune animals. J. Bacteriol. 91: Green, J. A., S. R. Cooperband, and S. Kibrick Immune specific induction of interferon production in cultures of human blood lymphocytes. Science 164: Ho, M., M. K. Breinig, B. Postic, and J. A. Armstrong The effect of pre-injections on the stimulation of interferon by a complexed polynucleotide, endotoxin and virus. Ann. N.Y. Acad. Sci. 173: Kleinschmidt, W. J., and F. Streightoff Inhibition of influenza virus and interferon response intranasally with statolon. Infect. Immunity 4: Reed, L. J., and H. Muench A simple method of estimating fifty per cent end points. Amer. J. Hyg. 27: Regelson, W., and A. E. Munson The reticuloendothelial effects of interferon inducers: polyanionic and non-polyanionic phylaxis against microorganisms. Ann. N.Y. Acad. Sci. 173:

6 776 DEGRA AND DAHL INFECT. IMMUNITY 15. Singer, S. H., and M. C. Hardegree Induction of interferon by bacterial vaccines and allergenic extracts. J. Allergy 47: Stinebring, W. R., and P. M. Absher Production of interferon following an immune response. Ann. N.Y. Acad. Sci. 173: Turner, W., S. P. Chan, and M. A. Chirigos Stimulation of humoral and cellular antibody formation in mice by poly-ir: Cr. Proc. Soc. Exp. Biol. Med. 133: Yamada, M., M. Azuma, R. Nishioka, and T. Togashi Relationship between immunity and interferon production in macrophages. I. Effect of immunity on interferon production. Jap. J. Microbiol. 14:

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