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Serum Immunoglobulins and Coproantibody Formation in Infants After Artificial Intestinal Colonization with Escherichia Coli 083 and Oral Lysozyme Administration

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Serum Immunoglobulins and Coproantibody Formation in Infants After Artificial Intestinal Colonization with Escherichia Coli 083 and Oral Lysozyme Administration Pediat. Res. 7: 659-669 (1973) Colonization, intestinal lysozyme coproantibody newborn immunoglobulin Serum Immunoglobulins and Coproantibody Formation in Infants after Artificial Intestinal Colonization with Escherichia coli 083 and Oral Lysozyme Administration R. LODINOVA1401, V. JOUJA, AND V. WAGNER Institute for the Care of Mother and Child, Prague-Podoli, Czechoslovakia Extract In infants colonized with a nonenteropathogenic strain, Escherichia coli 083, the strain was detected in the stool from the 2nd day after oral administration and remained in predominance during 16 weeks. The serum antibody against E. coli 083 increased rapidly during the 4th week in breast-fed and in formula-fed, colonized infants and remained significantly higher for 16 weeks when compared with control subjects. Lysozyme did not influence the serum immunoglobulin levels. The production of hemagglutinating coproantibody against E. coli 083 started in the 2nd week and remained statistically significant up to the 6th week in breast-fed infants. In bottle-fed, colonized infants the increase of the antibody level is signifi- cantly higher between the 4th and 16th week when compared with control subjects. Immunoglobulin M (IgM) was detected in bottle-fed infants only. In breast-fed, colonized infants and in control subjects, a high level of secretory immunoglobulin A (IgA) was found between the 1st and 8th week. In bottle-fed, colonized infants the increase of secretory IgA started from the 4th week and stayed significantly higher in the 6th, 12th, and 16th week. No immunoglobulin G (IgG) at all was found in stool filtrates. Lysozyme did not influence the production of serum immunoglobulins, copro- antibody, and secretory IgA. The artificial oral colonization induced a higher formation of secretory IgA in the intestinal mucosa. This effect can be detected in bottle-fed infants only, as the infants own production of IgA is masked by IgA passively transferred from maternal milk during breast feeding. Speculation Oral colonization of neonates with a nonenteropathogenic E. coli may provide a better state of immunity for artificially fed infants. The unusual ability of the E. coli 083 strain to predominate in the stool for prolonged periods could be used as a therapeutic ap- proach for enteric infections caused by antibiotic-resistant bacteria and for individuals with altered stool flora due to prolonged antimicrobial therapy. Colonization experiments such as these confirm that the immune responses of human neonates are a useful model for the study of this important developmental phenomenon. 659 660 LODINOVA, JOUJA, AND WAGNER Introduction Fluorescent antibody studies show that most Ig-con- taining cells of the intestinal submucosa contain IgA, a After intrauterine life in a sterile environment, the lesser number of cells contain IgM and a very low newborn infant comes into contact with a variety of number of cells contain IgG [4]. Secretory IgA con- microorganisms. As shown by experiments in germ-free tains one more polypeptide chain (secretory compo- animals, this contact with organisms exerts a profound nent), synthesized by the intestinal epithelial cell, than effect upon the development of immune reactivity [35]. serum IgA [13, 38]. Secretory IgA also differs from Even though the human fetus produces a small serum IgA in its greater resistance to the degradative amount of immunoglobulins, the main protection dur- effect of proteolytic enzymes [33]. ing the first weeks of life is provided by maternal anti- There are unique factors in the neonate which may bodies. affect the local intestinal response. In the neonate, the The levels of all immunoglobulins are compara- number of Ig-producing cells in the submucosa and tively low [34], and the infants are very sensitive to the concentration of secretory immunoglobulins is very enteral and parenteral infections, especially those low [5]. caused by gram-negative bacteria. Human colostrum In our previous papers [21, 22], we demonstrated that and milk contain high amounts of IgA and less IgG after artificial oral colonization with a nonentero- and IgM [32]. Breast-fed infants obtain from colos- pathogenic strain, E. coli 083, this strain remained pre- trum, and later from milk, IgA-containing antibodies dominant for several weeks when compared with E. against all infections which the mother has met pre- coli strains acquired spontaneously from the environ- viously. Milk IgA could be detected in effective ment. E. coli 083 evoked an earlier and higher serum amounts in the stool of breast-fed infants, although it antibody response in full term as well as in premature could not be found in feces of bottle-fed infants [16, infants than the other E. coli strains [23]. 17]. In this study the effect of oral colonization with a Lysozyme is another component of breast milk that nonenteropathogenic E. coli, strain 083, and feeding is capable of altering the microbial flora as well as with lysozyme in breast-fed and bottle-fed infants upon mediating a beneficial effect upon enteric infection. the production of serum and secretory immunoglobu- Lysozyme is present in human milk and is absent in lins and antibodies was studied. cow's milk [6, 20]. The importance of the intestinal flora, which repre- Methods sent a strong antigenic stimulus for the whole orga- nism, has been confirmed by many experimental stud- All infants under long term investigation were deliv- ies. It influences the development of immune reactions ered in our institute and kept in the department for and preforms them, to some extent, for the rest of life healthy infants from birth until the age of 6 months. [35]. We started with 14 artificially fed infants. They In a study dating back to 1927, Besredka [2] devel- were colonized with E. coli type 083. A suspension oped a concept of local immunity on the surface of prepared from a 24-hr culture containing 5 X 10s orga- mucous membranes. However, he did not postulate an nisms/ml was administered during the first 24 hi- after immunity mediated by antibodies. In 1938 Torikata birth and again 3 times a week for 3 successive weeks. and Imaizumi [37] demonstrated opsonins in the intes- The suspension was prepared freshly every day and 10 tine after oral or parenteral vaccination. It was found colonies from each petri dish were tested for specificity. subsequently that many different external secretions The S phase was proved by boiling and with acriflavin. bathing mucous surface contained a predominance of The stool specimens were cultured and E. coli colonies IgA and smaller concentrations of IgM, IgG, and IgD were tested with E. coli antiserum to serotype 083 for [36]. specificity. Antibodies produced locally by the intestinal mu- Later, eight breast-fed and nine artificially fed in- cosa were named coproantibodies by Burrows et al. [3]. fants were colonized in the same way. Coproantibody formation was shown after experimen- Lysozyme, 10 mg/100 ml, was added to the milk tal immunization in laboratory animals [7, 18] and formula of 11 bottle-fed infants for a 2-month pe- natural infection and vaccination in man [27, 29]. Oral riod [40]. The control groups consisted of 11 breast- vaccination in adults and infants induced higher titers fed and 10 artificially fed infants. The bottle-fed in- of coproantibodies than did serum antibodies [10, 15]. fants were fed with humanized cow milk formula [41]. Immunoglobulins and coproantibodies in infants 661 Blood samples were drawn from the mothers and Table I. Serum-hemagglutinating antibody against Escherichia from each child before the colonization. Additional coli 0831 blood and stool samples were taken during the 1st and Group X SE P Group X SK P 2nd week after colonization, after which the samples 1 week 2 weeks were taken every 2 weeks for a 24-week period. Stool a 2.63 0.41 a 3.50 0.60 samples were collected under sterile conditions. Sera b 3.33 0.67 b 3.29 0.84 c 2.20 0.58 c 3.09 0.46 were stored at —15° and stool samples were stored on d 3.00 0.38 d 1.80 0.80 Dry Ice. Antibodies against E. coli 083 were deter- e 2.80 0.86 e 3.11 1.08 mined by a hemagglutination technique on microtitra- 4 weeks 6 weeks tor plates according to the method of Neter et al. [25]. a 5.88 0.76 a/e a 5.50 0.56 ale P < 0.05 P < 0.05 Concentrations of IgG, IgM, and IgA in the sera b 5.00 0.41 b 4.89 0.54 b/e were first determined quantitatively by double immu- P < 0.05 c 2.81 0.68 c 2.72 0.38 nodiffusion technique in a micromodification of the d 3.00 0.82 d 3.13 0.54 Ouchterlony method using monospecific antisera [42] e 3.27 0.80 e 2.45 0.62 in three dilutions and normal human serum Behring- 8 weeks 10 weeks werke. Where the immunoglobulins were present, the a 5.29 0.51 a/e a 4.57 1.16 P < 0.05 concentration was determined quantitatively by radial b 4.78 0.52 b/e b 4.63 0.68 immunodiffusion according to the method of Fahey P < 0.05 c 2.90 0.84 a/d c 3.40 0.87 and McKelvey [8]. The serum concentrations were ex- P < 0.05 pressed in milligrams per milliliter. Stool samples col- d 2.78 0.40 d 3.00 0.36 lected under sterile technique were mixed thoroughly e 2.81 0.53 e 2.54 0.65 and diluted to 10 volumes of sterile saline with a vor- 12 weeks 14 weeks a 5.00 0.26 ale a 5.29 0.41 tex for 3 min and centrifuged for 30 min at 5° at P < 0.05 10,000 rpm and the supernatant passed through Milli- b 4.11 0.66 b 4.63 0.53 c 3.00 0.73 c 2.80 0.71 pore filters (type HF, pore sizes 5 ^m and 22 pxa).
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