The first description of the microfilariae of Onchocerca volvulus was probably made by O'Neill (1875) from samples taken from the skin of six West African natives with papular skin rashes. He described the microfilaria as:
. . . easily detectable ... by its violent contortions. Thread-like in form, at one time undulating, and now twisted as if into an inexplicable knot, then, having rapidly untwined itself, it curls and coils into many loops.
This evocative description is readily recognised by those who have examined microfilariae emerging from skin fragments under a microscope. O'Neill also described the pointed tail and reported the microfilariae to be about 250 ^ x 12 ^ in size. There can be little doubt that O'Neill was describing O. volvulus micro-filariae.
Leuckart (1893) described and named worms from specimens sent by missionaries from the Gold Coast. Prout (1901) later described worms from a subcutaneous nodule removed from a Sierra Leone frontier policeman with vague rheumatic pains. He described the adult male and female worms and microfilariae (unsheathed, with a sharp tail, central granular appearance and a size of 250 ^ x 5^), which he tentatively called Filaria volvulus after Leuckart. Parsons (1908) also gave a description of nodules and commented that he suspected that the disease was more common than generally recognised and probably spread by a blood-sucking insect.
Robles (1917) working in Guatemala, demonstrated an association between nodules and clinical features of onchocerciasis—the skin lesions and anterior ocular disease—and suggested that blackflies could transmit the infection. However, it was
Principles and Practice of Clinical Parasitology
Edited by Stephen Gillespie and Richard D. Pearson © 2001 John Wiley & Sons Ltd
Fig. 18b.1 The global distribution of onchocerciasis. Cross-hatched area—main endemic area; black-shaded areas—isolated endemic foci
Blacklock (1926a, b), working in Sierra Leone, who provided definite evidence of transmission of onchocerciasis by Simulium damnosum. He showed that onchocercal larvae developed in the gut, then thorax, of simuliids and subsequently that the head of the blackfly is invaded by developing worms, which can escape from the proboscis through the membranous labrum.
The use of skin snips to make the diagnosis was first recorded by Macfie and Corson (1922), who used a needle and scissors to remove a 0.25 cc piece of skin from the lower back. The recognition of ocular onchocerciasis in Africa occurred in the 1930s with the work of Hissette (1932) in the Congo, who described punctate keratitis, sclerosing keratitis, iritis, retrobulbar neuritis and retinal lesions, while Bryant (1935) noted diffuse retino-choroiditis associated with optic atrophy in the Sudan. The definitive description of ocular onchocerciasis by Ridley (1945), working in Ghana, was published as a monograph.
The species Onchocerca volvulus (Phylum Nematoda, Superfamily Filarioidea, Family Dipetalonematidae) is a vector-borne filarial nematode transmitted by blackflies of the genus
Simulium. All filarial genera of medical importance belong to the Dipetalonematidae. The adult female Onchocerca volvulus is exceptionally long for a member of the Filarioidea, as adult filariae usually measure only 2-10 cm in length. Adult O. volvulus are normally found in characteristic fibrous nodules, which allows them to be distinguished from Dracunculus medinensis (Superfamily Dracunculoidea), another long (about 100 cm) filarial human parasite found in subcutaneous tissues.
A diagram of the life-cycle is shown in Figure 18b.2. Infective third stage (L3) larvae are introduced into the human host by biting female Simulium damnosum or other blackfly vectors. There is no significant zoonotic cycle. Larvae undergo two moults before developing into adult worms. The first moult occurs close to the point of entry after 3-10 days (Strote, 1987; Bianco et al., 1989; Duke, 1991) and the second moult about 1-2 months later (Lok et al., 1984; Duke, 1991).
Adult worms are long and thin, tapering at both ends, with a rounded anterior end. They are
typically found in subcutaneous nodules and in lymph spaces in the tissues of humans. Both sexes exhibit sluggish movement. Microscopically, the cuticle is seen to be raised in prominent transverse ridges and annular and oblique thickenings, which are more distinct posteriorly. The annulations on males are more closely spaced and inconspicuous compared with those on females. The presence of two striae in the inner layer of the cuticle is a helpful diagnostic feature of Onchocerca in tissue sections. Adult worms are long-lived; the average lifespan of female worms is estimated to be about 8 years but can be as long as 15 years (Roberts et al., 1967). The prominence of the cuticular ridges and the cuticular coat diminish with age. As worms become older they become discoloured, changing from transparent white to yellowish to brown. They also exhibit more inclusions and patches of calcification as they age.
Subcutaneous nodules (onchocercomata) are usually less than 2 cm in diameter, firm, mobile and well-defined, and neither tender nor painful. Adult worms in nodules are generally no more than a minor cosmetic problem, as they do not directly cause the pathological features of onchocerciasis. In an average nodule, one or two male and one or two female worms are found coiled in a mass within a rim composed of vascularised and hyalinised scar tissue derived from the host. Interspersed in the worm bundle are evidence of chronic inflammation: macrophages, fibrin, plasma cells, neutrophilic and eosinophilic granulocytes, lymphocytes, giant cells and Russell bodies. These nodules may rarely contain 10 or more adult worms and are usually found in association with bony prominences lying subcutaneously, sometimes attached to the skin, or occasionally more deeply. Some nodules contain liquefied or calcified necrotic worms. It is recognised that not all nodules are palpable and that not all adult worms are found within such nodules (Albiez, 1983).
Adult male worms lengthen throughout life but are usually found to measure 2-4 cm in length x about 0.15-0.20 cm in breadth. In nodules, males are usually found on the outside of the worm bundle, coiled around the anterior end of a female. The nerve ring is 140 ^ from the anterior end. The alimentary canal is straight, ending close to the tip of the tail. The tail ends in a spiral and has a bulbous tip. There are two pairs of preanal and two postanal papillae, an intermediate large papilla and two unequal copulatory spicules, which can protrude from the cloaca. The reproductive tract consists of a testis, a vas deferens and an ejaculatory duct leading to the cloaca.
Adult female worms measure 35-70 cm in length x about 400 ^ in breadth. The nerve ring is 170 ^ from the anterior end, and the anus is about 210 ^ from the posterior end of the worm. The female reproductive tract runs from the posterior to anterior end of the worm and consists of paired ovaries, oviducts, seminal receptacles and uteri, and a single vagina and vulva found close to the anterior extremity. O. volvulus are ovoviviparous and the eggs (30-50 ^ in diameter) have a striated shell with a pointed process at each end.
The sessile female worms have a cyclical reproductive pattern, requiring fertilization by males for each successive brood of larvae (Schulz-Key and Karam, 1986). From the evidence that nodules normally contain more female worms than males (ratio 1:1.1 or 1.2) and that some nodules contain fertilized females but no male worms, it is thought that the much shorter male worms are migratory, moving from nodule to nodule (Schulz-Key and Albiez, 1977). Primary oocytes mature as they pass down the length of the ovary and are released as individual cells into the oviduct and seminal receptacles, where they are fertilised and begin dividing. Multicellular stages develop along the length of the uteri until, finally, they escape from the vulva as stretched microfilariae. Unfertilised oocytes degenerate within the uterus and are not released. The prepatent period, from infection with infective larvae to production of detectable microfilariae, is usually 12-15 months, with a range of 7-34 months (Prost, 1980).
The unsheathed, non-periodic microfilariae occur mainly in the skin (90%) and are also found in nodules. They are occasionally found in blood specimens, probably by dislodgement from the skin. They are also found in the tissues and chambers of the eye in heavy infections and have been reported in urine, sputum, cerebrospinal fluid and ascitic fluid, particularly after treatment with diethylcarbamazine.
Microfilariae are produced in large numbers from female worms, possibly up to 10 000 per female daily (Eberhard and Orihel, 1986) and migrate to the skin and eyes of infected subjects. Microfilariae are usually 200-360 ^ long and 59 ^ broad. They have a cephalic space 7-13 ^ long. The anterior nuclei are found in rows. The caudal space is 9-15 ^ long and the terminal nuclei are elongated. The tail is tapered to a fine point. These features distinguish microfilariae of O. volvulus from those of Mansonella perstans (under 200 ^ long and no caudal space), Mansonella streptocerca (180-240 p.m long, a curved tail and no caudal space) and Mansonella ozzardi (200-230 ^ long and a fine attenuated tail), which are all unsheathed microfilariae that are possible sources of misdiagnosis of onchocerciasis in endemic zones (Figure 18b.3). Skin microfilariae are characteristically found in the upper dermis, usually without any surrounding host reaction. It has been suggested that normally they reside in the lymph vessels of dermal papillae, at which site they cause no host reaction, and that it is only extralymphatic microfilariae, particularly those that are dead or dying, which excite the host inflammatory response (Vuong et al., 1988). Normally, microfilariae live 1-2 years before dying (Eberhard, 1986) unless taken up by the vector.
If microfilariae are taken up with the blood meal by biting female Simuliids, some of them migrate from the gut of the blackfly into the thoracic muscles. There they undergo three moults and develop into infective larvae over a period of 6-8 days. Infective larvae migrate to the head of the blackfly, where they may be transmitted to humans in the process of the blackfly taking a blood meal by emerging through the membranous labrum of the mouthparts and
into the wound created by the vector. Infective larvae are 440-700 ^m in length x 19-28 ^m broad. The caudal extremity narrows behind the anus and ends in a rounded tip.
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