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Study on the pathology of metagonimiasis in experimentally infected cat intestine
Jung Bin Lee,Je Geun Chi,Sang Kook Lee and Seung-Yull Cho
Department of Pathology, College of Medicine, Seoul National University, Korea.
Department of Parasitology, College of Medicine, Chung-Ang University, Korea.
Abstract
To study the basic pathological changes of small intestine in metagonimiasis, light- and electron microscopic studies were made, using a total of 21 cats which were experimentally infected with metacercariae of Metagonimus yokogawai. The metacercariae were obtained from naturally infected sweetfish (Plecoglossus altivelis) by digestion technique. The cats were divided in control, light-infection(10,000 metacercariae infected) and heavy-infection(50,000 metacercariae infected) groups. Cats were killed at the 5th, 10th, 15th day, and 4th, 8th and 10th week after the infection. And the small intestine was prepared for the study. Pathological studies comprised gross examination, worm distribution pattern, light microscopic examination and both transmission and scanning electron microscopic examinations.
The results obtained were summarized as follows.
1. Gross morphologic changes were the most marked during the first 2 weeks after infection. The gross abnormalities were severer in the heavily infected animals. The changes were dryness and listlessness of serosal surface due to dehydration, mushy and/or watery intestinal content, effacement of transverse nodes and enlargement of mesenteric lymph folds and Peyer's patches. After 4 weeks of infection, these changes became less marked showing a tendency to return to normal.
2. The sectioned flukes were distributed from duodenum to proximal ileum. However, individual variation was marked in distribution. In the heavy-infection group, the locality of parasitism tended to extend more distally.
3. The locality of M. yokogawai in the intervillous space was mostly in the lower-most portion of intervillous space, where they compressed and eroded epithelial cells probably due to mechanical damage to the structure. Very rarely the worms were found in lumen of Lierberkuehn's crypt, and reaching, in two occasions, into proprial lymphoid tissue.
4. Light-microscopically the lesion was restricted in mucosa: Early mucosal changes were shortening, blunting, fusion, and thickening of the villi, crypt hypertrophy with consequent decrease of villus/crypt ratio, as well as stromal changes of edema, capilliary ectasia and marked inflammatory cell infiltration of lymphocytes and plasma cells. Goblet cells were markedly reduced in number as with depletion of its cytoplasmic content. In the later stages of infection, mucosa restored its normal configuration in spite of persistent parasitism of the worms.
5. At the infection stage of 5-15 days, there was significant shortening of the microvillous height with varible destruction of glycocalyx in electron microscopic examination. With lapse of infection time, microvilli became to restore the normal pattern.
With these morphological changes, it appears that diarrhea in experimental metagonimiasis would be related to the decrease of absorptive surface of the small intestine particularly in the early phase of infection. The significant changes seen in villi and microvilli might be due to massive intrusion or invasion of Metagonimus worms into the crypts, causing direct mechanical and possible host-immune response to the small bowel mucosa.
Figures
Fig. 1 Distribution pattern and density rate of sectioned worms in light-infection group.
Fig. 2 Villous height-crypt length (V/C) ratios by duration of infection in light-infection group.
Fig. 3 Villous height-crypt length (V/C) ratios by duration of infection in heavy-infection group.
Figs. 4-7 Fig. 4. Serosal surface in a cat of 80,000 metacercarial infection at the 18th day of infection. Note marked enlargement of mesenteric lymph nodes and apparently dry serosal surface.
Fig. 5. Mucosal surface of control group in jejunum. Transverse folds are well preserved and surface is velvety.
Fig. 6. Mucosal surface of jejunum in preliminarily studied (80,000 metacercariae) group at the 5th day of infection. Transverse folds are markedly effaced. Note granular pattern presumably due to worm parasitism.
Fig. 7. Mucosal surface of jejunum in preliminarily studied group at the 18th day. Lumen contains foamy watery feces and there is moderate effacement of transverse folds.
Figs. 8-13 Fig. 8. Jejunum of heavy-infection group in the 5th week. Because of marked shortening of villi, a worm is found in the full length of intervillous space. Goblet cells are markedly reduced in number, and depleted. H-E stain, ×40.
Fig. 9. Duodenum of heavy-infection group in the 10th day. Worms are observed in the mouth of Lieberkuehn's crypts. H-E stain, ×0.
Fig. 10. 4th week, light-infection group. A worm is tightly impacted in the mouth of crypt. Adjacent epithelium is compressed, and goblet cells are moderately depleted. PAS stain, ×100.
Fig. 11. At the 4th week of heavy-infection, one worm is seen in the mid region of Lieberkuehn's crypt, but within the lumen of gland. H-E stain, ×100.
Fig. 12. Proximal ileum of heavy-infection group in the 4th week. Two worms are seen. One is present in the gland directly contacted with lymphoid tissue, and the other, inside lymphoid tissue. H-E stain, ×100.
Fig. 13. Higher magnification of Fig. 12. In the lower portion glandular structure is entirely destructive. H-E stain, ×400.
Figs. 14-19 Fig. 14. The epithelial cells around the oral sucker of a worm show a marked attenuation and obscured basement membrane, asssociated with stromal inflammatory reaction. H-E stain, ×360.
Fig. 15. Duodenal mucosa of heavy-infection group in the 5th day. There are marked fusion and shortening of villi together with flattening of their tips. H-E stain, ×40.
Fig. 16. Higher magnification of Fig. 15, showing marked capillary ectasia, edema and inflammatory reaction in lamina propria. H-E stain, ×100.
Fig. 17. Jejunal mucosa of heavy-infection group in the 5th day. Blunting of villi and adhesion are seen, together with stromal edema and inflammatory cells. H-E stain, ×360.
Fig. 18. Jejunal mucosa of heavy-infection group in the 4th week of infection. Villus/crypt ratio is relatively normal and goblet cells are slightly depleted. PAS stain, ×100.
Fig. 19. Jejunal mucosa of light-infection group in the 10th week. Three parasitic worms are seen impacted in the mouths of crypts. H-E stain, ×100.
Figs. 20-23 Fig. 20. Transmission electron micrograph of jejunal microvilli in the mid portion of a villus. Heavy-infection group after 10 days of infection. The microvilli are definitely reduced in height. There is also irregularity of surface plane of individual microvillus with destruction of glycocalyx. ×17,000.
Fig. 21. Jejunal microvilli at mid-villous region in heavy-infection group after 4 weeks of infection. Althoughless prominent than Fig. 20, there is still reduction of the height. ×17,000.
Fig. 22. Jejunal and mid-villous microvilli in a heavy-infection group after 8 weeks of infection. The height of microvilli is decreased. ×17,000.
Fig. 23. Mid-villous, jejunal microvilli in a light-infection group after 8 weeks of infection. The microvilli become almost completely restored to normal appearance. ×17,000.
Figs. 24-27 Fig. 24. Scanning electron micrograph, showing fusion of villi of jejunal mucosa in a heavy-infection group, 4 weeks after infection. ×360.
Fig. 25. Irregularity of the shape and erosive change at the tips of villi seen in a light-infection group after 4 weeks of infection. ×200.
Fig. 26. Depletion of goblet cells on the surface of the villus shown. Jejunum in a heavy-infection group after 4 weeks of infection. ×750. Inset; ×2,250.
Fig. 27. Leaf-like villous picture in a light-infection group, 8 weeks after infection. ×360. Inset (×1,080); Goblet cell depletion is no longer present.
Tables
Table 1 Distribution pattern and density rate of sectioned worms in small intestine by the duration of infection
Table 2 Summary of mucosal changes in light-infection group
Table 3 Summary of mucosal changes in heavy-infection group
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