Leishmania braziliensis: Development of primary and satellite lesions in the experimentally infected owl monkey, Aotus trivirgatus

Abstract

Twelve male and 8 female feral owl monkeys, Aotus trivirgatus, were inoculated intradermally at the dorsal base of the tail with 2 × 10 7 promastigotes (strains WR 128 or WR 539) or 5 × 10 5 amastigotes (strain WR 128) of Leishmania braziliensis panamensis, and the progression and regression of subsequent lesions were examined for up to 13 or 54 weeks after inoculation. Three of these monkeys had been infected previously with L. donovani, had been treated with meglumine antimoniate, and had recovered clinically from visceral leishmaniasis. All monkeys developed a cutaneous nodule at the inoculation site, but the size of the nodule varied (maximum 78 to 326 mm 2 between 4 and 16 weeks after inoculation.) The initial nodule became ulcerated after 4 to 8 weeks in 17 of the 20 monkeys, and the ulcers persisted for 4 to 16 weeks until covered by a crust. Primary lesions disappeared by 17 to 52 weeks after inoculation, but satellite lesions, of similar morphology to the primary lesions but smaller, developed after 4 to 21 weeks in 14 of the monkeys. The primary nodule was excised in 4 monkeys at 6 weeks and did not recur nor did satellite lesions subsequently develop. The satellite lesions (median total number of 4, range 1 to 25) were adjacent to or at a maximum distance of 6 cm from the primary lesion, varied in size from 3 to 117 mm 2, and persisted for 10 to 37 weeks. At 6 and 8 weeks after inoculation, tissue from the cutaneous leishmanial lesions from five monkeys was excised and examined. The granulomatous leishmanial lesions, located primarily in the dermis and subcutis, consisted of macrophages containing parasites, lymphocytes, plasma cells, and occasionally eosinophils. Satellite lesions at 14 weeks after inoculation were similar grossly and microscopically to the initial nodule. No significant differences were observed between promastigote or amastigote derived infections, between the two strains of L. b. panamensis, or between the course of infection based on the sex, age, karyotype, or country of origin of the owl monkeys. Cutaneous lesions developed when 5 × 10 5 amastigotes of L. b. panamensis (strain WR 128) were inoculated intradermally into the dorsal base of the tail, the upper eyelid, and the thorax of three monkeys. Leishmanial nodules which developed on the thorax regressed rapidly (after 2 to 5 weeks) whereas those on the upper eyelid and at the dorsal base of the tail persisted for 5 to 45 weeks after inoculation. The three monkeys inoculated previously with L. donovani had no cross protection when inoculated subsequently with L. b. panamensis, and they developed cutaneous leishmanial lesions similar to those observed in monkeys with no history of previous infection. These studies confirm that the owl monkey is a susceptible host for L. b. panamensis and indicate that the dorsal base of the tail is a useful site for the induction of a cutaneous lesion. Lesions produced by L. b. panamensis on the owl monkey are similar to those of human localized cutaneous leishmaniasis, except that multiple satellite lesions are more common on the owl monkey. Our results indicate that the owl monkey is a satisfactory model for the study of the pathogenesis of the skin lesion and the chemotherapeutic and immunologic responses to cutaneous leishmaniasis. Studies in this model confirm the lack of cross protection to L. braziliensis by previous exposure to L. donovani infections.