1887

Abstract

An electron microscopic and cytochemical study of the Whipple bacillus in jejunal biopsies from three untreated patients was made using fixation procedures developed for the satisfactory preservation of bacterial ultrastructure. The envelopes of the normal- looking bacilli present free in the lamina propria consisted of the following layers. (i) A cytoplasmic membrane with a triple-layered profile and a mean thickness (peak-to- peak distance) of 6.08 nm. (ii) A thick (20 nm) cell wall containing peptidoglycan; the wall had a hitherto undescribed inner layer that contained polysaccharides, possibly teichoic acids. (iii) Surrounding the cell wall, a surface membrane with a symmetric profile and a mean peak-to-peak distance of 4.74 nm. The ultrastructural pattern of the Whipple bacillus wall corresponds to that of Gram- positive bacteria, but with an additional surface membrane. This membrane is different from the outer membrane of Gram- negative bacteria because it has a symmetric profile, is thinner and has no periodic acid-Schiff (PAS)-positive components.

Normal-looking bacilli were seen very rarely inside jejunal macrophages, but degenerating bacteria were abundant in these phagocytes. Electron microscopy and ultrastructural cytochemistry of Whipple bacilli inside jejunal macrophages of the three untreated patients showed that the degenerative process is a sequence that leads to the loss of bacillary forms and to the accumulation of bacterial remnants resistant to degradation by the macrophage. These remnants correspond to the innermost, polysaccharide-containing portion of the bacillus wall. The progressive accumulation of these PAS-positive wall remnants is the origin of the intramacrophagic inclusions that are important in the histological diagnosis of Whipple’s disease. The reported results indicate that in the three patients studied, the Whipple bacillus multiplies extracellularly, the bacteria that are phagocytosed by macrophages being degraded.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-131-5-1001
1985-05-01
2022-01-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/131/5/mic-131-5-1001.html?itemId=/content/journal/micro/10.1099/00221287-131-5-1001&mimeType=html&fmt=ahah

References

  1. Bhagavan B. S., Hofkin G. A., Cochran B. A. 1981; Whipple’s disease: morphologic and immunofluorescence characterization of bacterial antigens. Human Pathology 12:930–936
    [Google Scholar]
  2. Chears W. C., Asworth C. T. 1961; Electron microscopic study of the intestinal mucosa in Whipple’s disease. Gastroenterology 41:129–137
    [Google Scholar]
  3. Dobbins W. O. III 1981; Is there an immune deficit in Whipple’s disease?. Digestive Disease Science 26:247–252
    [Google Scholar]
  4. Dobbins W. O. III, Kawanishi H. 1981; Bacillary characteristics in Whipple’s disease: an electron microscopy study. Gastroenterology 80:1468–1475
    [Google Scholar]
  5. Dobbins W. O. III, Ruffin J. M. 1967; A light and electron microscope study of bacterial invasion in Whipple’s disease. American Journal of Pathology 51:225–242
    [Google Scholar]
  6. Fainstein V., Boliram R., Mavligit G., Rios A., Luna M. 1982; Disseminated infection due to Mycobacterium avium-intracellulare in a homosexual man with Kaposi’s sarcoma. Journal of Infectious Diseases 145:586
    [Google Scholar]
  7. Ghuysen J. M. 1977; Biosynthesis and assembly of bacterial cell walls. In The Synthesis, Assembly and Turnover of Cell Surface Components463–595 Poste G., Nicolson G. Amsterdam & New York; North-Holland Publishing Co:
    [Google Scholar]
  8. Gillin J. S., Urmacher C., West R., Shuke M. 1983; Disseminated Mycobacterium avium–intracellulare infection in acquired immunodeficiency syndrome mimicking Whipple’s disease. Gastroenterology 85:1187–1191
    [Google Scholar]
  9. Glauert A. M., Thornley M. J. 1969; The topography of the bacterial cell wall. Annual Review of Microbiology 23:159–198
    [Google Scholar]
  10. Hayat M. A. 1970 Principles and Techniques of Electron Microscopy I New York: Van Nos-trand Rheinhold Co;
    [Google Scholar]
  11. Keren D. F. 1981; Whipple’s disease: a review emphasizing immunology and microbiology. CRC Critical Reviews in Clinical and Laboratory Science 14:75–108
    [Google Scholar]
  12. Keren D. F., Weisburger W. R., Yardley J. H., Salyer W. R., Arthur R. R., Charade P. 1976; Whipple’s disease: demonstration by im-munofluorescence of similar bacterial antigens in macrophages from three cases. Johns Hopkins Medical Journal 139:51–59
    [Google Scholar]
  13. Luft J. H. 1961; Improvements in epoxy resin embedding methods. Journal of Biophysical and Biochemical Cytology 9:409–414
    [Google Scholar]
  14. Macedo P. M., Silva M. T. 1983; Morphogenesis of the PAS-positive inclusions of macrophages in Whipple’s disease. XVIII Reuniào Anual, Sociedade Portuguesa Microscopia Electrónica abstract 70
    [Google Scholar]
  15. Maizel H., Ruffin J. M., Dobbins W. O. III 1970; Whipple’s disease: a review of 19 patients from one hospital and a review of the literature since 1950. Medicine 49:175–205
    [Google Scholar]
  16. Miksche L. W., Blumke S., Fritsche D., Kuche-Mann K., Schuler H. W., Grozinger K. H. 1974; Whipple’s disease: ethiopathogenesis, treatment, diagnosis and clinical course. Case report and review of the world literature. Acta hepato-gastroen-terologica 21:307
    [Google Scholar]
  17. Palade G. E. 1952; A study of fixation for electron microscopy. Journal of Experimental Medicine 95:285–298
    [Google Scholar]
  18. Petitprez A., Derieux J. C. 1970; Mise en évidence des polysaccharides sur quelques types de bactéries. Journal de microscopie 9:263–272
    [Google Scholar]
  19. Rambourg A. 1971; Morphological and histochemical aspects of glycoproteins of the surface of animal cells. International Review of Cytology 31:57–114
    [Google Scholar]
  20. Rosseau M., Hermier J. 1975; Localization en microscopie électronique des polysaccharides de la paroi chez les bactéries en sporulation. Journal de microscopie 23:237–248
    [Google Scholar]
  21. Roth R. I., Owen R. L., Keren D. F. 1983 Letter to New England Journal of Medicine 309:1324
    [Google Scholar]
  22. Ryter A., Kellenberger E. 1958; Étude au microscope électronique de plasmas contenant de 1’acide désoxyribonucléique. I. Les nucléoides des bactéries en croissance active. Zeitschrift für Naturforschung 13b:597–605
    [Google Scholar]
  23. Silva M. T. 1971; Changes induced in the ultrastruc-ture of the cytoplasmic and intracytoplasmic mem-branes of several Gram-positive bacteria by variations in OsO4 fixation. Journal of Microscopy 93:227–232
    [Google Scholar]
  24. Silva M. T. 1975; Ultrastructure of the membranes of Gram-positive bacteria as influenced by fixatives and membrane-damaging treatments. In Biomem-branes-Lipids, Proteins and Receptors255–289 Burton R. M., Packer L. Webster Groves, Mo., USA: BI-Science Publication Division;
    [Google Scholar]
  25. Silva M. T. 1984; The use of transmission electron microscopy of ultrathin sections for the characterization of the ultrastructure of normal and damaged bacterial membranes. In Biomembranes: Dynamics and Biology1–36 Guerra F. C., Burton R. M. New York: Plenum Press;
    [Google Scholar]
  26. Silva M. T., Macedo P. M. 1982; Ultrastructure of Mycobacterium leprae and other acid-fast bacteria as influenced by fixation conditions. Annales de microbiologie 133B:59–73
    [Google Scholar]
  27. Silva M. T., Macedo P. M. 1983a; A comparative ultrastructural study of the membranes of Mycobacterium leprae and of cultivable mycobacteria. Biology of the Cell 47:383–386
    [Google Scholar]
  28. Silva M. T., Macedo P. M. 1983b; Electron microscopic study of Mycobacterium leprae membrane. International Journal of Leprosy 51:219–224
    [Google Scholar]
  29. Silva M. T., Macedo P. M. 1983c; The interpretation of the ultrastructure of Mycobacterium cells in transmission electron microscopy of ultrathin sections. International Journal of Leprosy 51:225–234
    [Google Scholar]
  30. Silva M. T., Macedo P. M. 1983d; Ultrastructural and cytochemical study of Whipple bacillus. XVIII Reunião Anual, Sociedade Portuguesa Microscopia Electrónica abstract 69
    [Google Scholar]
  31. Silva M. T., Sousa J. C. F. 1973; Ultrastructure of the cell wall and cytoplasmic membrane of Gram-negative bacteria with different fixation techniques. Journal of Bacteriology 113:953–962
    [Google Scholar]
  32. Silva M. T., Macedo P. M., Salema R., Santos I. 1982; Improvement in the Thiéry reaction by the use of silver vitelinate. XVII Reunião Anual, Sociedade Portuguesa Microscopia Electrónica abstract 30
    [Google Scholar]
  33. Sleytr V. O., Silva M. T., Kocur M., Lewis N. F. 1976; The fine structure of Micrococcus radiophilus and M.radioproteolyticus . Archiv für Mikrobiologie 107:313–320
    [Google Scholar]
  34. Strom R. L., Grunninger R. P. 1983 Letter to New England Journal of Medicine 309:1323–1324
    [Google Scholar]
  35. Thiéry J. P. 1967; Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. Journal de microscopie 6:987–1019
    [Google Scholar]
  36. Thiéry J. P., Rambourg A. 1974; Citochimie des polysaccharides. Journal de microscopie 21:225–232
    [Google Scholar]
  37. Trier J. S., Phelps P. C., Eidelman S., Rubin C. E. 1965; Whipple’s disease: light and electron microscope correlation of jejunal mucosa histology with antibiotic treatment and clinical status. Gas-troenterology 48:684–707
    [Google Scholar]
  38. Venable J. H., Coggeshall R. 1965; A simplified lead citrate stain for use in electron microscopy. Journal of Cell Biology 25:407–408
    [Google Scholar]
  39. Watson J. H. L., Haubrich S. 1969; Bacilli bodies in the lumen and epithelium of the jejunum in Whipple’s disease. Laboratory Investigation 21:347–357
    [Google Scholar]
  40. Wicken A. J., Knox K. W. 1980; Bacterial cell surface amphiphiles. Biochimica et biophysica acta 604:1–26
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-131-5-1001
Loading
/content/journal/micro/10.1099/00221287-131-5-1001
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error