Pathologic Changes of Human Onchocerciasis: Implications for Future Research

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1 REVIEWS OF INFECTIOUS DISEASES VOL. 7, NO.6. NOVEMBER-DECEMBER 1985 Pathologic Changes of Human Onchocerciasis: Implications for Future Research Daniel H. Connor, Gladys H. George, and Dean W. Gibson From the Department of Infectious and Parasitic Disease Pathology and the World Health Organization Collaborating Centre for the Histopathology of Filarial Diseases in Man, Armed Forces Institute ofpathology, Washington, D.C. Onchocerciasis - infection by Onchocerca volvulus - has four cardinal manifestations: dermatitis, subcutaneous nodules, sclerosing lymphadenitis, and eyedisease. The first three are discussed here. The dermatitis begins when micro filariae degenerate in the dermis. This process is accompanied by inflammation, with degranulation ofeosinophils and deposition of the major basic protein of the eosinophil granules on the cuticle of the microfilariae. So far as is known, the chronic effects of onchocerciasis are all a consequence of the degeneration of microfilariae. Subcutaneous nodules contain coiled adult worms and have an outer layer of fibrous scar and a central inflammatory cell exudate, which may cavitate. Perfusion ofindiaink reveals arborization ofcapillaries around adult worms, which derive nutrition from these networks. Onchocercal lymphadenitis is characterized initially by histiocytic hyperplasia and follicular atrophy and later by fibrosis and obstruction of lymph flow, a condition causing adenolymphocele ("hanging groin") and elephantiasis of the genitalia. Some patients appear to have immune tolerance to degenerating microfilariae, perhaps as a result ofexposure in utero to microfilarial antigens in the maternal circulation. In contrast, other patients (Yemenites, for example) have a localized but intense response to a few micro filariae; these patients are hypersensitive - perhaps because they were not exposed to microfilarial antigens in utero. Autopsy data on infection of deep organs are limited. Onchocerciasis is the infection of humans by the filarial nematode Onchocerca volvulus. Three ofthe four cardinal manifestations of human onchocerciasis are discussed here: dermatitis, subcutaneous nodules, and sclerosing lymphadenitis. These and the fourth manifestation- ocular changes - have been reviewed previously [1-13]. Patients and Methods Findings from biopsy specimens from patients with onchocerciasis in Zaire, Cameroon, Liberia, Guatemala, and Yemen have been described previously [2, 5, 7-9, 11-13]. Most specimens discussed in this paper were obtained at various intervals after This work was supported in part by the World Health Organization (WHO), and the specimens and photographs are on file in the WHO Collaborating Centre for the Histopathology of Filarial Diseases in Man. The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the viewsof WHO, the Department of the Army, or the Department of Defense. Please address requests for reprints to Dr. Daniel H. Connor, Department of Infectious and Parasitic Disease Pathology, Armed Forces Institute of Pathology, Washington, D.C treatment with diethylcarbamazine (DEC) and/or suramin. These specimens include punches of skin 4- and 6-mm in diameter, subcutaneous nodules, and femoral and inguinal lymph nodes. Specimens were routinely fixed in buffered formaldehyde and processed at the Armed Forces Institute of Pathology (Washington, D.C.). Slides were stained with hematoxylin and eosin, Giemsa's reagent, and by the Russell-Movat technique and submitted to the World Health Organization Collaborating Centre for the Histopathology of Filarial Diseases in Man. Results and Discussion Dermatitis. Onchocercal dermatitis presents a broad spectrum of clinical and pathologic features. Itching precedes other early clinical changes, which include altered pigmentation of thighs, shins, buttocks, and trunk. Later changes include papular eruption, hypopigmentation, and scaling (figure 1); edema, depigmentation, and- in long-standing onchocerciasis - the development of a shiny, fragile, atrophic epidermis resembling tissue paper [2-4]. Microscopically the initial lesion comprises degenerated microfilariae. What triggers the natural death of microfilariae, with subsequent release of 809

2 810 Connor, George, and Gibson Figure 1. Hypopigmentation and scaling of skin of a patient with onchocercal dermatitis (Armed Forces Institute of Pathology neg. no ). antigens, is unknown. Nor has anyone defined the antigen(s)-from micro filariae or adult wormsthat provokes or modulates the inflammation and immune response as that in the Mazzotti reaction to DEC [2-7, 12]. Microscopic changes in early onchocercaldermatitis consist of chronic inflammatory cells in the perivascular spaces of the upper dermis. The cells involvedare mainly lymphocytes, histiocytes, plasma cells, and eosinophils. Later in the infection hyper- keratosis, focal parakeratosis, and acanthosis are seen plus more advanced changes in the dermis, including pigmentary incontinence, dilation of lymphatics, development of tortuous dermal vessels, and an increase in the amount of mucopolysaccharide between the collagen fibers. Dermal fibroblasts increase in number as the infection becomes heavier. This increase leads to fibrosis, and the areolar connective tissue ofthe dermal papillae and the normal collagen and elastic fibers of the dermis are gradually replaced by hyalinized scar tissue, which has a striking pattern of concentric perivascular fibrosis [3]. An inconstant change is "fibrinoid degeneration" of dermal collagen. This development is characterized by the presence of amorphous eosinophilic "fibrinoid" material attached to some collagen fibers, which can be stained by the Russell-Movattechnique. This "fibrinoid" probably contains immune complexes and the major basic protein (MBP) ofeosinophil granules [7, 12]. Degenerating microfilariae go through a series of changes. First, they become more eosinophilic. Then "fibrinoid" material surrounds them and immunofluorescence staining demonstrates eosinophil granule MBP (figure 2). The eosinophil therefore has a special role in the inflammatory response to degenerating micro filariae. The nuclei of the degenerating micro filariae later become hyperchromatic, then fragmented, and finally indistinct. When degenera- Figure 2. Degenerating microfilaria in upper dermis of thigh of a Liberian patient two days after start of topical application of 20/0 diethylcarbamazine in Nivea lotion. A, section stained for eosinophil granule major basic protein (MBP). Note bright specific staining for MBP and an eosinophil (arrow) close to microfilarial cuticle. B, identical field, counterstained with hematoxylin and eosin. Reprinted with permission from Laboratory Investigation [12].

3 Pathologic Changes of Human Onchocerciasis 811 Figure 3. Numerous degranulating eosinophils in close proximity to cuticle of a degenerating microfilaria of Onchocerca volvulusin upper dermis of a Cameroonian patient 3.5 hr after oral diethylcarbamazine treatment (hematoxylin and eosin; x 2,000; Armed Forces Institute of Pathology neg. no ). tion of microfilariae is triggered by DEC, inflammatory cells rich in eosinophils are mobilized quickly and within minutes accumulate around the degenerating microfilariae. This process is followed by degranulation of eosinophils and the deposition of their MBP onto the cuticle of the microfilaria [12]. After patients are treated with DEC, the upper dermis becomes the "graveyard" for many degenerating microfilariae in a pool ofmbp (figure 3). Some Figure 4. Microfilaria (arrow) located partly in an intraepidermal eosinophil abscess in the thigh of a Liberian patient two days after topical applications of 20/0 diethylcarbamazine in Nivea lotion [5] (hematoxylin and eosin; Armed Forces Institute of Pathology neg. no ). microfilariae migrate into the epidermis and can be seen there in abscesses or in parakeratotic nests (socalled tombstones) up to seven days after the patient is treated with DEC (figures 4 and 5). The role of and interrelationships among eosinophil granule MBP, immune complexes, and mechanisms of microfilarial disintegration are not well understood. Nodules. Adult worms become encapsulated and form discrete nodules in the deep dermis and sub-

4 812 Connor, George, and Gibson Figure 5. "Tombstone" of degenerating microfilaria within focal parakeratotic nest in skin over knee of a Zairian patient six days after oral diethylcarbamazine treatment (hematoxylin and eosin; Armed Forces Institute of Pathology neg. no ). Figure 7. Cut surface of onchocercal nodule from a Cameroonian patient one week after treatment with suramin. Note cross-sections of worm. It is surrounded by matrix of granulation tissue (x 5.7; Armed Forces Institute of Pathology neg. no ). cutaneous tissue. Nodules form over bony prominences (e.g., skull, scapula, rib, iliac crest, trochanter, sacrum, and knee; figure 6) for unexplained reasons. The nodule has three essential components: an outer capsule of scar, an inflammatory cell exudate, and the enclosedadult worm, which can usuallybe identified in all layers of the nodule- including the outer layer ofscar tissue. The cutsurfaces ofnodules vary Figure 6. Three onchocercal nodules on forehead and skull of a Zairian boy. Nodules on forehead and scalp increase the risk of eye disease (Armed Forces Institute of Pathology neg. no ). Figure 8. Cut surface of onchocercal nodule from a Cameroonian patient one month after treatment with suramin. The central portion is rich in fibrin and is beginning to cavitate (x 4.5; Armed Forces Institute of Pathology neg. no ).

5 Pathologic Changes of Human Onchocerciasis 813 Figure 9. Cut surface of mineralized nodule from a Cameroonian patient 14 months after treatment with suramin. Portions of degenerating worms are still visible microscopically (see figure 16; x 3.7; Armed Forces Institute of Pathology neg. no ). in appearance, manifestations reflecting different stages of scarring and degeneration of the worms. Some nodules have a solid matrix of granulation tissue that surrounds coiled worms (figure 7). Others have a soft central fibrin lake that surrounds por- Figure 11. Nodule from an untreated Cameroonian patient. A cavity occupies a large portion ofthe central nodule, and portions of worm "float" in the cavity. The residue is rich in fibrin (Russell-Movat; x 4.25; Armed Forces Institute of Pathology neg. no ). tions of worm (figure 8). The end stage of the nodule is mineralization (figure 9). Microscopically a variety of inflammatory components (granulomatous, suppurative, and chronic inflammation) may all be present (figure 10). The central cavity is rich in fibrin and invariably contains portions of adult worm (figure 11). The Russell Movat stain often reveals a thick layer of fibrinoid material (immune complex?) surrounding the cuticle of the adult worm (figure 12)and sometimes reveals mucopolysaccharide in the matrix (figure 13). Figure 10. Granulomatous reaction in nodule from a Cameroonian patient one month after treatment with suramin. A very long foreign body giant cell is applied to the cuticle of the degenerating female worm and follows intimately the contour of the worm's cuticle (Russell Movat; Armed Forces Institute of Pathology neg. no ). Figure 12. Thick layers of fibrin-rich material surrounding portions of adult worm in the same nodule as in figure 11 (Russell-Movat; Armed Forces Institute of Pathology neg. no )..

6 814 Connor, George, and Gibson Figure 13. Inflamed granulation tissue surrounding portions of an adult worm in the same nodule as in figure 10. The tissue is rich in acid mucopolysaccharides, which stain light blue with the Russell-Movat stain (Armed Forces Institute of Pathology neg. no ). Clusters ofneutrophils attack and remove this fibrinoid material from the worm's cuticle (figure 14). In later stages histiocytes and giant cells phagocytose the cuticle and other portions ofthe degenerating adult worms (figure 15). Even in mineralized nodules, fragments of cuticle can usually be identified (figure 16). Nodules also contain "free" micro filariae (outside the adult worms), some of which degenerate with degranulation ofeosinophils as in the dermis (figures 2 and 3); other "free" micro filariae in nodules are phagocytosed by giant cells(figure 17). Figure 15. Histiocytes and giant cells phagocytosing cuticle ofdegenerating worm in same nodule as in figure 8 (Russell-Movat; Armed Forces Institute of Pathology neg. no ). In the absence of treatment, worms survive for up to 18 years. How they do this while centered in an inflammatory "storm"- so to speak - is a mystery. They not only survive but appear to thrive in this environment. Attempts to understand this relationship may offer a key to how it may be interrupted. In pursuit of this, one of us (G. H. G.) inoculated India ink into vessels protruding from two nodules (figure 18). Sections ofthese nodules revealed an intimate relationship between the cuticle of the adult worms and the capillaries of the host. There is a proliferation ofcapillaries in granulation tissue surrounding the worms, with vesselsfrom the outer cap- Figure 14. Neutrophils attacking fibrinoid material surrounding cuticle of adult worm in nodule from an untreated Zairian patient [2] (Russell-Movat; Armed Forces Institute of Pathology neg. no ). Figure 16. Diffusely calcified nodule shown in figure 9. There are recognizable fragments of cuticle even at this advanced state of degeneration (Russell-Movat; Armed Forces Institute of Pathology neg. no ).

7 Pathologic Changes ofhuman Onchocerciasis 815 Figure 17. Giant cell that has phagocytosed a microfilaria in the same nodule as in figures 10and 13(Russell Movat; Armed Forces Institute of Pathology neg. no ). sule arborizing into capillary beds that form a "jacket" or "sleeve" around adult worms. There is also a space around the worm that is continuous with blood vessels and the central fibrin lake of the nodule (figure 19). Immunoperoxidasestaining for factor VIII antigen (von Willebrand's factor) helps identify the proliferation of endothelium of host vessels around theworms [13]. The iron stain (Prussian-blue reaction) reveals that hemosiderin is concentrated in the worm's intestinal epithelium. Thus the worm seems to subvert the vascular reaction by causing controlled hemorrhage within the nodule that serves the worm's nutritional needs. Thus the nodule is an Figure 19. Fibrin lake containing coiled adult worms in nodule from a Cameroonian patient (Russell-Movat; Armed Forces Institute of Pathology neg. no ). enclave that protects the worm and nourishes it for years with little or no damage to the host. What prompts the vascular leak and what controls it are important questions for future research. Lymphadenitis and associated adenolymphocele andelephantiasis. Onchocercal lymphadenitis is of special concern because it may lead to the development ofa hanging scrotum, "hanging groin" (adeno- Figure 18. Carbon in fibrin lake of nodule from a Guatemalan patient after perfusion of India ink through vessels [13] (x 4; Armed Forces Institute of Pathology neg. no ). Figure 20. Bilateral inguinal and femoral adenolymphoceles (hanging groins) in a Cameroonian patient. Inguinal and femoral lymph nodes beneath hanging groins are fibrotic and contain microfilariae of Onchocerca volvulus (Armed Forces Institute of Pathology neg. no ; contributed by Dr. John Anderson, Helminthiasis Research Unit, Kumba, Cameroon).

8 816 Connor, George, and Gibson Figure 21. Cut surfaceof scarredfemoral lymphnode from a patient in Zaire. Note extensive fibrous replacement of lymphoid tissue(armed ForcesInstitute of Pathology neg. no ). lymphocele), and elephantiasis [2-6,9, 10]. Furthermore, onchocercal lymphadenitis and especially the alterations in lymphoid tissue probably playa key role in the inflammatory and immunologic responses seen in onchocerciasis. Many Africans with onchocerciasis have a progression of changes in their lymph nodes. At first the femoral and/or inguinal lymph nodes are enlarged, and then they become fibrotic. This change is followed by lymphatic obstruction and the development of overlying "hanging groin" (figure 20). The nodules show various degrees of scarring of the capsule, the pericapsular tissues, and the interior of the nodes, with fibrous replacement of up to of the cross-sectional area of a node (figures 21 and 22). Nodes in the "early stage" show only slight fibrosis but have follicular hyperplasia and sinus histiocytosis, with dilated subcapsular sinusoids that also contain plasmacells, eosinophils, and neutrophils. Nodes in the "intermediate stage" show moderate fibrous replacement but less pronounced dilation of sinusoids and sinus histiocytosis. Nodes in the "late stage" show lymphoid atrophy, with fibrous replacement of almost all of the lymphoid tissue (figures 21 and 22) and obliteration of the subcapsular sinusoids. There is a circumferential perivascular pattern to the fibrosis, a finding suggesting that antibody diffuses from vessels and forms immune complexes that may "seed" the fibrosis (figure 23). The Russell-Movat connective tissue stain reveals "fibrinoid material" that may in part be immune complex [9, 10]. Immunofluorescence staining is being performed to determine if this "fibrinoid material" in lymph nodes contains eosinophil granule MBP such as has been shown previously in specimens of skin [12]. The perivascular fibrosis in lymph nodes with onchocercal lymphadenitis resembles the "onion-ring" pattern of periarterial fibrosis in the spleen of patients with systemic lupus erythematosus [14]. There were microfilariae of O. volvulus in lymph nodes of 24 (75%) of the 32 African patients studied [9]. The microfilariae were mostly in the fibrous Figure 22. Microscopic appearance of femoral lymphnode beneathhanging groin from a Zairian patient [2]. There is fibrous replacement of 1'\)75070 of the lymphoid tissue. The small amount of remaininglymphoid tissue is atrophic; no follicular or histiocytic hyperplasia isevident (Giernsa; x 4.5; Armed Forces Institute of Pathology neg. no ).

9 Pathologic Changes ojhuman Onchocerciasis 817 Figure 23. Circumferential fibrosis around small vessel of inguinal lymph node in a Nigerian patient [9]. Reticulum fibers are intermingled with collagen fibers and fibrinoid material in a symmetrical pattern around vessels (reticulum stain; Armed Forces Institute of Pathology neg. no ). Figure 24. Entangled mass of degenerating micro filariae in inguinal lymph node from a Cameroonian patient 71 hr after treatment with oral diethylcarbamazine [9]. Abscess in subcapsular lymphoid tissue also contains inflammatory cells that include neutrophils, histiocytes, and lymphocytes (Giemsa; Armed Forces Institute of Pathology neg. no ). Figure 25. An ll-year-old Zairian boy with severe onchocercal dermatitis and scrotal and penile elephantiasis that has developed over several years [9]. His scrotum hangs about 20 cm from the pubis, his penis is 15-cm long, and his inguinal lymph nodes are firm and slightly enlarged (Armed Forces Institute of Pathology neg. no ). capsule or in interstitial connective tissue but were sometimes also in the medullary and corticallymphoid tissues. Afterpatients weretreated with DEC, lymph nodes contained degenerating microfilariae surrounded by degranulating eosinophils (as seen also in the skin). An inguinal node from one patient, 71 hr after DEC treatment, revealed an abscess that contained hundreds of entangled degenerating microfilariae (figure 24). In contrast to the atrophic and fibrotic nodes from Africans, the inguinal and femoral lymph nodes of two Yemeniteswith sowda were much more enlarged and microscopically showed follicular hyperplasia rather than atrophy [9]. No micro filariae were present in either node ofthese two patients with sowda, just as there has been found to be a paucity of microfilariae in the skin of patients with sowda, in general [11].

10 818 Connor, George, and Gibson The histopathologic patterns of lymphadenitis in Africans vs. those in Yemenites (with generalized and localized onchocerciasis, respectively) show a parallel to the clinicopathologic spectrum in leprosyfrom anergic, lepromatous leprosy (with numerous acid-fast bacilli) to hyperergic, tuberculoid leprosy (with granulomatous response and few acid-fast bacilli). There likewise appears to be a spectrum in onchocerciasis - a generalized, anergic, and varying form with many microfilariae in the skin and lymph nodes (endemic onchocerciasis in Africans) vs. a localized, hyperergic form with few micro filariae in the skin and lymph nodes (sowda in Yemenites and onchocerciasis in Europeans acquiring the disease in Africa). Patients with anergic onchocerciasis in endemic regions may have "immune tolerance," or unresponsiveness, to microfilariaeas a result of exposure in utero to microfilarial antigens from the maternalcirculation [15]. In such individuals the surface antigens of micro filariae may be recognized as "host" and the millions of micro filariae thus "tolerated." Patients with hyperergic, localized onchocerciasis apparently lack this immune tolerance, presumably because they were not exposed in utero to microfilariae of O. volvulus. On the death of the microfilariae, these patients have a severe, localized reaction (e.g., severe lymphedema of the affected limb). Adenolymphocele (hanging groin) is a feature of onchocerciasis in Zaire, Central African Republic, Chad, Cameroon, and Nigeria and perhaps in other African countries (figure 20; [9]). We have not seen any patients with hanging groins in Guatemala or Yemen. Elephantiasis ofthe genitalia likewise was seen in patients in Zaire, Cameroon, and Ethiopia (figure 25; [9]) but not in Guatemalans or Yemenites. The reasons for these geographic differences are not clear, but they may be related in part to infection with other filariae as well (e.g., Wuchereria bancrofti and/or Loa loa). But the elephantiasislimited to the genitalia ofafricans with onchocercal lymphadenitis contrasts with the variable elephantiasis, often affecting an entire leg, that is commonly seen in patients with bancroftian filariasis. Additional research on multiple filarial infections may help provide an explanation of these observations. Further research is needed on the mechanisms involvedin the development of onchocercallymphadenitis, hanging groin, and elephantiasis. For example, what roles do immune complexes and eosinophil granule MBP playas "seeds" for the perivascular fibrosis? What antigens are involved in the immune complexes (e.g., microfilarial cuticular antigens, antigens from adult worms, or host antigens)? Which types oflymphocytes are involvedin cellular immune responses (e.g., suppressor T cells or helper T cells)? Are some of the immunologic responses suitable bases for the development of a vaccine? Infections ofdeep organs (including limited autopsy results). Information on infections of deep organs by O. volvulus is very limited because few autopsies have been performed on patients in hyperendemic regions [4, 5, 8]. One autopsy revealed microfilariae ofo. volvulus in the kidney, liver, pancreas, and lung, and another autopsy revealed adult O. volvulus in the thoracic aorta [8]. Additional autopsies are needed to provide information on the extent of involvementand the kinds oflesions provoked in other deep organs. Such studies should provide other basic information- which can be obtained in no other way- on the pathology and pathogenesis of onchocerciasis. References 1. Taylor HR. Onchocerciasis. In: Costello JH, Dawson C, Pizzarello LD, Sommer A, Sperduto RD, Taylor HR. Research priorities for the prevention of blindness in developing countries. Proceedings of meeting of Helen Keller International, Inc. (HKI) Expert Committee. New York: Helen Keller International, 1983:15-19, Connor DH, Morrison NE, Kerdel-Vegas F, Berkoff HA, Johnson F, Tunnicliffe R, Failing FC, Hale LN, Lindquist K. Onchocerciasis: onchocercal dermatitis, lymphadenitis, and elephantiasis in the Ubangi Territory. Hum Pathol 1970;1: Buck AA, ed. Onchocerciasis: symptomatology, pathology, diagnosis. Geneva: World Health Organization, 1974: Connor DH, Neafie RC. Onchocerciasis. In: Binford CH, Connor DH, eds. Pathology oftropical and extraordinary diseases. Vol.2. Washington, DC: Armed Forces Institute of Pathology, 1976: Gibson DW, Heggie C, Connor DH. Clinical and pathologic aspects of onchocerciasis. Pathol Annu 1980;15(Part 2): Connor DH, Gibson DW,Taylor HR, Mackenzie CD, Meyers WM, Neafie RC. Onchocerciasis. In: Strickland GT, ed. Hunter's tropical medicine.6th ed. Philadelphia: WB Saunders, 1984: Gibson DW, Connor DH, Brown HL, Fuglsang H, Anderson J, Duke BOL, Buck AA. Onchocercal dermatitis: ultrastructural studies of microfilariae and host tissues, before and after treatment with diethylcarbamazine (Hetrazan). Am J Trop Med Hyg 1976;25: Meyers WM, Neafie RC, Connor DH. Onchocerciasis: inva-

11 Pathologic Changes of Human Onchocerciasis 819 sion ofdeep organs by Onchocerca volvulus. Autopsyfindings. Am J Trop Med Hyg 1977:26: Gibson OW, Connor DH. Onchocercal lymphadenitis: clinicopathologic study of 34 patients. Trans Roy Soc Trop Med Hyg 1978:72: Racz P, Tenner-Racz K, Luther B, Buttner OW, Albiez EJ. Immunopathologic aspects in human onchocercal lymphadenitis. Bull Soc Pathol Exot Filiales 1983;76: II. Connor DH, Gibson DW, Neafie RC, Merighi B, Buck AA. Sowda - onchocerciasis in North Yemen: a clinicopathologic study of 18 patients. Am J Trop Med Hyg 1983; 32: Kephart GM, Gleich GJ, Connor DH, Gibson OW, Ackerman SJ. Deposition of eosinophil granule major basic pro- tein onto micro filariae of Onchocerca volvulus in the skin of patients treated with diethylcarbamazine. Lab Invest 1984:50: George GH, Palmieri JR, Connor DH. The onchocercal nodule: interrelationships of adult worms and blood vessels. Am J Trop Med Hyg, 1985 (in press) 14. Cruickshank B. The basic pattern of tissue damage and pathology of systemic lupus erythematosus. In: Dubois EL, ed. Lupus erythematosus. 2nd ed. Los Angeles: University of Southern California Press, 1974: Brinkmann UK, Kraemer P, Presthus GT, Sawadogo B.Transmission in utero ofmicro filariae ofonchocerca volvulus. Bull WHO 1976:54:708-9

ONCHOCERCIASIS, A POSSIBLE ETIOLOGY IN SOUTH-WEST ETHIOPIA. Title. Wonde, Teferra; Tada, Isao; Iwamoto. Citation 日本熱帯医学会雑誌, vol.1(1), pp.

ONCHOCERCIASIS, A POSSIBLE ETIOLOGY IN SOUTH-WEST ETHIOPIA. Title. Wonde, Teferra; Tada, Isao; Iwamoto. Citation 日本熱帯医学会雑誌, vol.1(1), pp. NAOSITE: Nagasaki University's Ac Title Author(s) ONCHOCERCIASIS, A POSSIBLE ETIOLOGY IN SOUTH-WEST ETHIOPIA Wonde, Teferra; Tada, Isao; Iwamoto Citation 日本熱帯医学会雑誌, vol.1(1), pp.25-29; 1973 Issue Date

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