Vascular abnormalities in experimental and human lymphatic filariasis

T. Case, B. Leis, Marlys H Witte, D. Way, Michael J Bernas, P. Borgs, C. Crandall, R. Crandall, Raymond B Nagle, S. Jamal, J. Nayar, C. Witte

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Whereas clinical descriptions of grotesque lymphedema and standard light microscopy in human filariasis have elucidated the natural progression of this disease, the link between the nematode and vascular abnormalities including elephantiasis remains poorly understood. Accordingly, we examined the nature and distribution of lymphatic and blood vascular derangements in a variety of tissues and organs from 37 ferrets acutely and chronically infected with Brugia malayi and in 15 patients with Wuchereria bancrofti or Brugia malayi infestation (resected skin, subcutaneous tissue, and lymph nodes) using light and transmission electron microscopy, immunohistochemistry, and in vivo microscopy. In ferrets, eosinophilic abscesses and epithelioid and giant cell granulomas with fragmented worms in various stages of disintegration were found in multiple organs. Blood microvasculopathy consisted of endothelial hyperplasia, focal thickening and stenosis, vessel obliteration with marked perivascular infiltration of lymphocytes, plasma cells, eosinophils, and numerous large macrophages laden with a coarse golden-brown pigment. Endothelial ballooning and swelling, pavementing, denuding, scarring, and sludge formation were seen along with high endothelium in atypical locations. Dilated lymphatics were most prominent near adult worms and showed plump endothelium, thickened walls and valves, thrombus formation, and often perilymphangitis and adjacent tissue fibrosis. In vivo microscopy showed wriggling live adult worms in dilated incompetent sludge-filled groin lymphatics even when microfilaremia and peripheral edema were absent. In human tissues, in addition to 'pachyderm' skin changes (keratosis, papillomatosis, acanthosis and collagen deposition), there was blood vessel and lymphatic vasculopathy similar to ferrets (angiocentric inflammation, congestion, vasculitis, thrombosis, thickened vessel walls, dilated lymphatics, lymphangitis, reactive lymph nodal hyperplasia and nodal fibrosis). These changes reflect generalized endothelial damage due to worm products, physical injury to valves and vessel walls from lymphatic-dwelling live worms, and host immune reactivity. Whereas adult worms target the lymphatic apparatus, their offspring and the host immune response primarily affects the blood microvasculature.

Original languageEnglish (US)
Pages (from-to)174-183
Number of pages10
JournalLymphology
Volume24
Issue number4
StatePublished - 1991

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Filarial Elephantiasis
Ferrets
Brugia malayi
Blood Vessels
Sewage
Endothelium
Hyperplasia
Thrombosis
Fibrosis
Lymphangitis
Elephantiasis
Giant Cell Granuloma
Wuchereria bancrofti
Keratosis
Light
Filariasis
Epithelioid Cells
Skin
Lymphatic Vessels
Lymphedema

ASJC Scopus subject areas

  • Immunology

Cite this

Case, T., Leis, B., Witte, M. H., Way, D., Bernas, M. J., Borgs, P., ... Witte, C. (1991). Vascular abnormalities in experimental and human lymphatic filariasis. Lymphology, 24(4), 174-183.

Vascular abnormalities in experimental and human lymphatic filariasis. / Case, T.; Leis, B.; Witte, Marlys H; Way, D.; Bernas, Michael J; Borgs, P.; Crandall, C.; Crandall, R.; Nagle, Raymond B; Jamal, S.; Nayar, J.; Witte, C.

In: Lymphology, Vol. 24, No. 4, 1991, p. 174-183.

Research output: Contribution to journalArticle

Case, T, Leis, B, Witte, MH, Way, D, Bernas, MJ, Borgs, P, Crandall, C, Crandall, R, Nagle, RB, Jamal, S, Nayar, J & Witte, C 1991, 'Vascular abnormalities in experimental and human lymphatic filariasis', Lymphology, vol. 24, no. 4, pp. 174-183.
Case, T. ; Leis, B. ; Witte, Marlys H ; Way, D. ; Bernas, Michael J ; Borgs, P. ; Crandall, C. ; Crandall, R. ; Nagle, Raymond B ; Jamal, S. ; Nayar, J. ; Witte, C. / Vascular abnormalities in experimental and human lymphatic filariasis. In: Lymphology. 1991 ; Vol. 24, No. 4. pp. 174-183.
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abstract = "Whereas clinical descriptions of grotesque lymphedema and standard light microscopy in human filariasis have elucidated the natural progression of this disease, the link between the nematode and vascular abnormalities including elephantiasis remains poorly understood. Accordingly, we examined the nature and distribution of lymphatic and blood vascular derangements in a variety of tissues and organs from 37 ferrets acutely and chronically infected with Brugia malayi and in 15 patients with Wuchereria bancrofti or Brugia malayi infestation (resected skin, subcutaneous tissue, and lymph nodes) using light and transmission electron microscopy, immunohistochemistry, and in vivo microscopy. In ferrets, eosinophilic abscesses and epithelioid and giant cell granulomas with fragmented worms in various stages of disintegration were found in multiple organs. Blood microvasculopathy consisted of endothelial hyperplasia, focal thickening and stenosis, vessel obliteration with marked perivascular infiltration of lymphocytes, plasma cells, eosinophils, and numerous large macrophages laden with a coarse golden-brown pigment. Endothelial ballooning and swelling, pavementing, denuding, scarring, and sludge formation were seen along with high endothelium in atypical locations. Dilated lymphatics were most prominent near adult worms and showed plump endothelium, thickened walls and valves, thrombus formation, and often perilymphangitis and adjacent tissue fibrosis. In vivo microscopy showed wriggling live adult worms in dilated incompetent sludge-filled groin lymphatics even when microfilaremia and peripheral edema were absent. In human tissues, in addition to 'pachyderm' skin changes (keratosis, papillomatosis, acanthosis and collagen deposition), there was blood vessel and lymphatic vasculopathy similar to ferrets (angiocentric inflammation, congestion, vasculitis, thrombosis, thickened vessel walls, dilated lymphatics, lymphangitis, reactive lymph nodal hyperplasia and nodal fibrosis). These changes reflect generalized endothelial damage due to worm products, physical injury to valves and vessel walls from lymphatic-dwelling live worms, and host immune reactivity. Whereas adult worms target the lymphatic apparatus, their offspring and the host immune response primarily affects the blood microvasculature.",
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AU - Borgs, P.

AU - Crandall, C.

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AU - Jamal, S.

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AU - Witte, C.

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