LEISHMANIASIS OF THE NEW WORLD: TAXONOMIC PROBLEMS R. Lainson&J. J. Shaw

LEISHMANIASIS OF THE NEW WORLD:TAXONOMIC PROBLEMS

R. LAINSON Ph.D. D.Sc.J. J. SHAW D.A.P.E. Ph.D.

The Wellcome Parasitology UnitBelim, Pard, Brazil

1 Visceral leishmaniasis2 Present classification3 Rodent leishmaniasis in Brazil and its relationship to the

disease in man4 Proposed re-classification of parasites5 The Leishmania mexicana complex6 The Leishmania braziliensis complex7 Conclusions

References

This paper concentrates on the taxonomic problems of NewWorld leishmaniasis, as we have recently extensively reviewedits epidemiology (Lainson & Shaw, 1971).

Because of past emphasis on clinical appearances, the NewWorld leishmaniae have been largely classified on this basisand a bewildering array of terms has resulted, often appliedto the same disease state and very often caused by the sameparasiteChiclero's ulcer, Bay sore, pian bois, bush yaws,"framboesiform" cutaneous leishmaniasis, uta, "simple" or"disseminated" cutaneous leishmaniasis, espundia, muco-cutaneous leishmaniasis, "verrucose", "vegetative" or"nodular" cutaneous leishmaniasis, and "diffuse" cutaneousleishmaniasis, to name but a few.

If leishmaniasis were restricted to man such a classificationmight be excused, but the various forms of the New Worlddisease are zoonoses, stemming from different wild or domesticanimals; man is normally to be regarded only as an incidentalhost and plays no important role in the maintenance of theparasites in nature. Finally, while a given Leishmania mayproduce an over-all similar clinical picture in man, individualsmay react differently to the same parasite and the appearanceof the disease may vary greatly at different stages of theinfection.

It has proved far from easy, however, to classify the leish-maniae on a sounder, zoological basis. In the vertebratehost they all assume the simplest form of the Trypanosom-atidae, the amastigote (Leishman-Donovan body), whichshows a strikingly similar morphology among all the leish-maniae infecting man and most of those infecting otherqnimak. In the invertebrate host, too, the morphology of thepromastigote (leptomonad) j s generally regarded as indistin-guishable among the different species of Leishmania. Ourlack of knowledge on many aspects of host-vector relation-ships and of a simple laboratory test to differentiate the leish-maniae has stood in the way of progress. These difficultiesmust be overcome, for information on the biology, morpho-logy, biochemistry, and immunology of Leishmania remainprerequisites to any sensible classification. Fortunately, inrecent years, there has been new interest in these aspects.

1. Visceral Leishmaniasis

The existence of visceral leishmaniasis in the Americas wasfirst noted by Migone (1913) in Paraguay and has since beenrecorded in Bolivia, Brazil, Colombia, Guatemala, ElSalvador and Mexico. In Brazil, where most of the pioneerepidemiological studies were made, the dog and wild foxeshave proved to be important reservoirs of infection (Deane &Deane, 1954). The major sandfly vector is generally consideredto beLutzomyia longipalpis, at least in the highly endemic areasof north-east Brazil. This insect is partially adapted to peri-domestic habitats and is prevalent in and around the houses,feeds readily on dogs, foxes and man, and has several timesbeen found infected in nature.

However, it was not in the arid areas that the first Braziliancases of visceral leishmaniasis were discovered, but at themouth of the Amazon, in the dense, humid forested areas ofPara (Chagas, Marques da Cunha, de Oliveira Castro, CastroFerreira & Romafia, 1937; Chagas, Marques da Cunha,Castro Ferreira, Deane, Deane, Guimaraes, von Paumgartten& Sa, 1938). Surprisingly enough, Lu. longipalpis was alsoidentified here as the local vector, found in the thatched hutsbuilt on the terra firma along the river and coastal marginsand in forest clearings. It was assumed that some wild animalreservoir must exist, but not until recently were infectionsfound in foxes caught near Belem (Lainson, Shaw & Lins,1969; Lainson & Shaw, 1971). There remains considerabledoubt as to the true epidemiology of this "sylvatic kala-azar" in north Brazil. Thus, recent searches for Lu. longipalpisin the endemic areas and where the infected foxes were caughthave produced no further evidence of this sandfly. Althoughreadily colonized in drier conditions, Lu. longipalpis does notdo well in laboratories with high temperature and humidity.Perhaps Chagas and his colleagues were dealing with another,closely related, species of sandfly.

As regards the parasite, most authorities have consideredit to be identical with Leishmania donovani (which causeskala-azar in India). This view arose largely from the clinicalpicture in man, and there has been little direct comparison ofthe actual parasites from the various parts of the two hemi-spheres in which they occur. Presumably, however, there is noreason why different leishmaniae might not cause a similarvisceral disease in man, in the same way that others causeskin disease.

Nicolle (1908) differentiated between Leishmania infantumand L. donovani, which cause Mediterranean and Indiankala-azar, respectively. This opinion was not unanimouslyaccepted, although Adler (1940) and Adler & Theodor (1957)gave it convincing epidemiological and experimental support.

If, as seems desirable, L. infantum is accepted as a validspecies, the taxonomy of the parasite causing New Worldvisceral leishmaniasis must be reconsidered. Many have sug-gested that the American disease was imported during theSpanish and Portuguese conquests and, if so, L. infantumwould be a more suitable name than L. donovani, on the basisof epidemiological evidence alone. Like Adler & Theodor(1957), however, we regard American visceral leishmaniasisas an indigenous disease, stemming from a wild animal source.

On grounds of geographical isolation alone, there wouldseem to be even more reason for separating off the parasite ofAmerican visceral leishmaniasis than there is for the distinc-tion between L. donovani and L. infantum. We thereforeintend to readopt the use of the two names L. infantum

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(Nicolle, 1908) and Leishmania chagasi (Marques da Cunha &Chagas, 1937) for the parasites of Mediterranean and NewWorld visceral leishmaniasis, respectively.

2. Present Classification

It is generally agreed that the leishmaniae causing cutaneousand mucocutaneous leishmaniasis in the Americas are indi-genous and do not represent strains or subspecies of importedLeishmania tropica (Noguchi, 1924; Adler, 1940; Adler &Theodor, 1957; Lainson & Shaw, 1971). The disease extendsfrom the Yucatan in the north to Argentina in the south and,early on, there was a tendency to regard all the differentclinical manifestations as due to a single parasite, Leishmaniabraziliensis (Vianna, 1911). As later stressed by Adler (1962),however, " . . . use of one name L. brasiliensis . . . has beenan important obstacle in the path of research."

The first attempt to clear the picture was made by Biagi(1953), who referred to the causative organism of Chiclero'sulcer in Mexico, Guatemala and British Honduras as L.tropica mexicana. This trinomial system was followed byFloch (1954), who added L. tropica brasiliensis for the parasiteof mucocutaneous leishmaniasis in Brazil and L. tropicaguyanensis for that causing uta in Peru, pian bois in theGuyanas and cutaneous leishmaniasis in Costa Rica andPanama. Pess6a (1961), on the other hand, considered allthese parasites as subspecies of L. braziliensis and differentiatedbetween L. braziliensis guyanensis andL. braziliensisperuviana.He included the name of L. braziliensis pifanoi, given to theparasite isolated from Venezuelan "diffuse" cutaneousleishmaniasis by Medina & Romero (1959). Finally, Garnham(1962) gave the parasite of "Chiclero's ulcer" specific rankas Leishmania mexicana.

Adler (1963, and personal communication in Lainson &Shaw, 1966) and Lainson & Shaw (1966) produced sero-logical and immunological evidence to differentiate L.tropica, L. mexicana, L. braziliensis (mucocutaneous case fromBrazil) and a strain of Leishmania (isolated from man inPanama); while Schneider & Hertig (1966) separated offPanamanian strains from both L. mexicana and L. braziliensisperuviana by immunodiffusion techniques.

mice. It produces large, tumour-like histiocytomata contain-ing enormous numbers of amastigotes, without any verymarked host cellular response; the parasite grows luxuriantlyand is easily maintained in most blood-agar media (e.g.NNN, the culture medium of Novy-Nicolle-McNeal).The "slow" parasite, on the other hand, grows very slowlyin the hamster skin, producing only a small fleshy swellingcharacterized by marked cellular response to scanty numbersof organisms.

In classifying our isolations of Leishmania into these twogroups, it soon became apparent that the slow-growingparasite was that responsible for the great majority ofinfections in man; this included all of 14 cases of muco-cutaneous leishmaniasis studied, and 50 out of 57 cases ofuncomplicated skin lesions. Only seven persons providedthe fast-growing parasite. Of these, four were cases ofanergid1 "diffuse" cutaneous leishmaniasis and three hadsingle ulcerative lesions.

Among the wild animals, isolations were almost exclusivelyof the fast-growing parasite. Thus, rodents and opossumshave yielded 39 infections with this Leishmania and only asingle example of the slow-growing organism; a slow-growing,Leishmania-Mk& parasite has been isolated from the viscera ofsloths (Choeloepus didactylus) in Para State, Brazil, but hasyet to be identified (R. Lainson and J. J. Shaw, unpublishedobservations).

There is little doubt that we can classify the slow-growingLeishmania, here in Brazil, with the species L. braziliensis.In man it gives rise to relatively severe, long-lasting lesions,frequently associated with later involvement and destructionof the nasopharyngeal tissues. The resemblance of the fast-growing parasite to L. mexicana has been mentioned (Lainson& Shaw, 1968), and at first we were inclined to refer to itsimply by this name. We were deterred from doing this,however, when considering the wide geographical separation,different hosts, different vectors (Lu. flaviscutellata andLutzomyia olmeca), and the absence of any entity comparablewith Chiclero's ear in Brazil. These, and some other dif-ferences in the behaviour of the parasites in laboratorynnimnk1 suggested to us that complete synonymy would be anover-simplification.

3. Rodent Leishmaniasis in Brazil and its Relationship to theDisease in Man

In recent publications we have discussed the prevalence ofrodent leishmaniasis in Brazil and its transmission by thesandfly Lutzomyia flaviscutellata (Lainson & Shaw, 1968;Shaw & Lainson, 1968). At first it was tempting to regardthis vast reservoir of infection as the major source of cutaneousand mucocutaneous leishmaniasis found so abundantly inthe same regions (Nery-Guimaraes, Azevedo & Damascene1966). Observations over the last five years, however, haveproduced two important facts: firstly that Lu. flaviscutellataonly rarely bites man, and secondly that the parasites isolatedfrom the rodents are in most cases vastly different from thoseisolated from man. From their behaviour in hamsters and inblood-agar media we concluded that we were dealing withtwo distinct leishmaniae which were provisionally referredto as the "fast-growing" and "slow-growing" parasites(Lainson & Shaw, 1969, 1970).

The "fast" parasite, from man or rodents, behaves likeL. mexicana when inoculated into the skin of hamsters and

4. Proposed Re-Classification of Parasites

Clearly, there is emerging more and more evidence of anevolving complex of leishmaniae in the New World for whichour present system of taxonomy is inadequate. As well as theexisting parasites known to infect man, we now have to dealwith such "oddities" as Leishmania enriettii, the leishmaniaeof rodents, sloths, porcupines and other forest animals,and the Leishmania or Leishmania-Uke parasites isolated fromwild-caught sandflies. Finally, workers in Panama havedemonstrated different serotypes among the Leishmaniaisolated from man in that country (Schneider & Hertig, 1966),and that a Leishmania isolated from the skin of porcupines isunrelated to any known human strain (Schneider, 1968).

An extension of the trinomial system as used by Pessfia(1961) would do much to ease the situation, and enable a moreready naming of Leishmania parasites which would otherwisesink into obscurity under such descriptions as "Leishmaniasp.", "fast-growing Leishmania of rodents" or "Leishmania

1 Not qohe mneigk.ED.

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brazilicnsis sensu lato". We have accordingly utilized twomajor groups, which we will refer to as the L. mexicana andL. braziliensis complexes, containing what we believe to besubspecies and related species of these organisms. Broadlyspeaking, these two groups coincide respectively with whatwe have previously referred to as the "fast-growing" and"slow-growing" parasites.

However, some leishmaniae either deserve separate specificrank or do not fit clearly into the present grouping. Thus,the morphology and host specificity of L. enriettii clearlymarks this peculiar organism off from all other known leish-maniae, although its behaviour in the guinea-pig and inNNN culture suggests links with the L. mexicana complex,with which we now place it.

Uta, in Peru, is the only form of New World cutaneousleishmaniasis unassociated with forest and which has appar-ently no wild animal reservoir. It is isolated on the dry,barren slopes of the Peruvian Andes, where the only knownreservoir is the domestic dog. From the little available infor-mation on its behaviour in hamsters and NNN culture, itseems best to include the parasite, as Leishmania peruviana,in the L. braziliensis complex.

5. The Leishmania mexicana Complex

Leishmaniae of this complex are principally cutaneousparasites of small forest rodents, more rarely opossums,producing inconspicuous dermal nodules, plaques or ulcerson the cooler extremities, predominantly the tail, although theymay be isolated from apparently normal skin. Transmissionamong natural hosts apparently is limited to a few species ofthe intermedia group of sandflies (Theodor, 1965), in particularLu. olmeca and Lu. flaviscutellata. Prolific development ofpromastigotes occurs throughout the mid-gut and fore-gut,but excluding the hind-gut triangle. Parasites multiply rapidlyin hamster skin, producing histiocytomata which are packedwith amastigotes and show a poor host-cell response; meta-static spread to the extremities commonly occurs in thehamster.

Growth is luxuriant and maintenance easy in NNN andother blood-agar media. Cutaneous lesions in man areusually of a mild nature and there is no nasopharyngeal in-volvement.

Classificationi. L. mexicana mexicana (Biagi, 1953) = L. tropica mexicana(Biagi, 1953); L. braziliensis mexicana (Pessoa, 1961); L. mexicana(Garnham, 1962).Reservoir hosts: small forest rodentsHeteromys desmarestianus(Heteromyidae) Nyctomys sumichrasti, Ototylomys phyllotls, andSigmodon hispiaus (Cricetidae).Sandfly vector: Lu. olmeca.Geographical area: Mexico (Yucatan), Guatemala and BritishHonduras, possibly extending into other parts of Central America.Behaviour in hamster: rapid production of histiocytomata at point ofinoculation into any part of skin, with spread to extremities withina few months.Behaviour in NNN media: grows luxuriantly and is easily main-tained.Clinical features: causative agent of Chiclero's ear or Bay sore;in immunologically competent persons usually a relatively mildinfection with a single cutaneous lesion which is self-healing;ear lesions, however, form up to 40% of cases, arc persistently

chronic and cause extensive destruction of the pinna; no naso-pharyngeal involvement; has produced one recorded case of anergid

diffuse" cutaneous leishmaniasis from Mexico.

ii. L. mexicana amazonensis nov. s.sp. L. braziliensis (Nery-Guimaraes & da Costa, 1966).Reservoir hosts: small forest rodents, more rarely opossumsOryiomys capito, Oryzomys macconnelli, Oryzomys laticeps,Nectomys squamipes, Neacomys spinosus (Cricetidae); Proechimysguyannensis (Echimyidae); Marmosa murina, Marmosa fuscata andMarmosa mills (MarsupiaJia: Didelphidae).Sandfly vector: Lu. flaviscutellata.Geographical area: Amazon basin, into Mato Grosso State,Brazil, and Trinidad, probably extends into other South Americancountries where the vector occurs.Behaviour in hamster: rapid production of histiocytomata in skin ofextremities (but grows less readily in hamster flank or other furredparts than does L. mexicana mexicana); metastasizes to extremitiesafter a few months.Behaviour in NNN media: grows luxuriantly and is easily main-tained.Clinical features: rarely infects man, owing to disinclination ofvector to bite him; single or limited cutaneous lesions, usuallywith abundant parasites; no predeliction for ear tissue as in L.mexicana mexicana, and no nasopharyngeal involvement; respon-sible for occasional cases of anergid "diffuse" cutaneous leish-maniasis (in Par& State, Brazil); recorded in rodents in Trinidad,but the disease is unknown in man there.

iii. L. mexicana pifanoi L. brasiliensispifanoi (Medina & Romero,1959); L. diffusa (Adler, 1962); L. pifanoi (Medina & Romero,1962).Reservoir hosts: probably small forest rodentsZygodontomysmicrotinus (Cricetidae) and Proechimys guyannensis found withtail lesions.Sandfly vector: unknown.Geographical area: Venezuela.Behaviour in hamster: rapidly produces large histiocytomata at siteof inoculation in skin, with metastases to other extremities after afew months.Behaviour in NNN media: grows luxuriantly and is maintainedeasily.Clinical features: so far only known from cases of anergid "diffuse"cutaneous leishmaniasis.

iv. L. enriettii (Muniz & Medina, 1948); the only species readilydistinguished from all others by the morphology of the amastigotes,which are unusually large.Natural host: unknown; discovered in laboratory guinea-pi^s(Cavia porcelhts); but will not infect the wild Brazilian guinea-pig(Cavla apered).Sandfly vector: unknown; has produced heavy experimental infec-tion in Lutzomyia gomezi, with no involvement of the hind-guttriangle.Geographical area: Curitiba, ParanA State, Brazil.Behaviour in hamster: not infective, or produces only a fleetinginfection.Behaviour in guinea-pig: produces marked nodules and ulcers inthe extremities with metastases; lesions contain abundant parasites.Behaviour in NNN media: grows well and easily maintained.

6. The Leishmania braziliensis Complex

Wild animal hosts are poorly known. Infections arcoccasionally found in forest rodents (Panama and Brazil)and in procyonids and marmosets (Panama): Leishmania-

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like organisms in the skin and viscera of sloths (Panama andBrazil) are of a more doubtful nature.

Parasites are limited to discrete but inconspicuous skinlesions, or to apparently normal skin. The parasites aretransmitted among wild animals and to man by a variety ofsandflies of the intermedia and Psychodopygus groups;parasites develop throughout mid-gut, fore-gut, and in thehind-gut triangle. They grow slowly in the skin of hamsternose or foot, producing a small fleshy swelling which usuallydoes not ulcerate. The numbers of amastigotes are scantyto moderate and the host cellular response is marked. There isno metastatic spread. Growth in blood-agar media is poorto moderate and often impossible to maintain. With the excep-tion of L. braziliensis guyanensis, serological differentiationhas been made between the different members of the L.braziliensis complex, and between these and parasites of theL. mexicana complex. In man, single or multiple skin lesionsare often very extensive and disfiguring. Nasopharyngealinvolvement has occurred with at least one subspecies.

Classification

i. L. braziliensis braziliensis (Vianna, 1911)-Z. wrightii (Pedroso &da Silva, 1910); L. tropica var. americana (Laveran & Nattan-Larrier, 1912); L. americana var. flagellata (Escomel, 1913); L.tropica var. brasiliensis (Pifano C , 1940); L. tropica brasiliensis(Floch, 1954).Reservoir hosts: poorly known; based on isolation and behaviourin hamster and NNN media, a single infection is recorded in therodent Oryzomys concolor from Mato Grosso State, Brazil;reports also exist of infections in the paca (Cuniculus paca), anagouti (Dasyprocta azarae) and another rodent, Kannabateomysamblyonynx, but with no observations on the parasites' behaviourin hamsters or NNN culture.Sandfly vectors: (a) based on infections in hamsters, and behaviourin NNN culture, of promastigotes found in sandflies from endemicareas of north Brazil: Lutzomyia paraensis; and two different,hitherto undescribed species of the Psychodopygus group (J. J.Shaw and R. Lainson, unpublished observations); (b) based onmicroscopic evidence, only, of promastigotes in dissected sandfliesin south Brazil and Venezuela: Lutzomyia migonei; Lutzomyiawhitman!; Lutzomyia anduzei.Geographical area: typically Brazil; also in adjacent forested areas,east of the Andesin Peru, Ecuador, Bolivia, Venezuela, Paraguayand Colombia.Behaviour in hamster: small, slowly growing swelling at point ofinoculation in nose or foot; usually non-ulcerative, with markedhost cellular response and containing scanty numbers of parasites;no metastatic spread in skin.Behaviour in NNN media: moderate to poor growth; often difficultto maintain.Clinical features: most destructive form of cutaneous leishmaniasis;lesions single or few in number, but frequently very large, persistentand disfiguring; violent tissue reaction, usually with very few para-sites; metastases to nasopharyngeal tissues a common sequel(espundia).

Behaviour in NNN media: very difficult to culture; initial growthweak, usually lost on subsequent passage.Clinical features: causative agent of pian bois; may occur as singlelesion but very commonly spreads to give many crater-like ulcersall over body; metastases often seen as nodules along lymphatics;scanty numbers of parasites; the rare cases of nasopharyngealinvolvement recorded are almost certainly due to geographicaloverlap of L. braziliensis braziliensis.

iii. L. braziliensis panamensis nov. s.sp. = L. brasiliensis guyanensis(Floch, 1954).Reservoir hosts: forest rodentsProechimys semispinosus andHoplomysgymnurusCEchimyidae;); the marmoset, Saguinusgeoffroyi;the kinkajou, Potosflavus; the olingo, Bassaricyongabbii; the sloths,Choeloepus hoffmanni and Brady pus infuscatus; uncertain if allrepresent infection with the same parasite, although the parasiteof Proechimys has produced typical lesions in volunteers.Sandfly vectors: based on infection of hamsters with promastigotesfrom dissected sandflies: Lutzomyia trapidoi; Lutzomyia ylephiletrix;Lu. gomezi; Lutzomyia panamensis.Geographical area: Panama, possibly extending into CentralAmerica in the north, or Colombia in the south.Behaviour in hamster: slow development of small fleshy swelling atpoint of inoculation (nose or foot); moderate numbers of amasti-gotes in lesions, and considerable tissue response; no metastaticspread in skin.Behaviour in NNN media: grows reasonably well and relativelyeasy to maintain.Clinical features: single or limited number of shallow, crater-likelesions with tendency to spread as nodules along lymphatics;nasopharyngeal involvement rarely described and possibly due to abite on the nose rather than to metastatic spread. Immunodiffusiontests indicate serologjcally different strains within the subspecies.

iv. L. peruviana (Velez, 1913) L. brasiliensis guyanensis (Floch,1954); L. braziliensis peruviana (Pessfla, 1961).Reservoir host: the domestic dog; small nodules or ulcers of skin,in particular of the nose and lips; often no apparent lesions andparasites scattered through areas of apparently normal skin.Sandfly vectors: uncertain; Lutzomyia verrucarum and Lutzomyiaperuensis strongly suspected.Geographical area: Peru; on western slopes of the Andes, up to analtitude of nearly 3000 metres; the only known form of New Worldcutaneous leishmaniasis unassociated with forested areas.Behaviour in hamster: surprisingly little information; but pre-sumably infections are of mild nature or difficult to maintain,judging from the non-availability of this parasite in the laboratory;the few existing NNN cultures appear to have lost their infectivityfor hamsters.Behaviour in NNN media: presumably growth and maintenanceoffer few problems as this parasite has been used to produceantibody for serological tests and is maintained in culture in someLeishmania reference centres.Clinical features: causative agent of uta; in immunologicallycompetent individuals produces single or limited lesions whichare self-healing; no nasopharyngeal involvement.

ii. L. braziliensis guyanensis (Floch, 1954) - L. brasiliensis (Floch &Sureau, 1953); L. tropica guyanensis (Floch, 1954).Reservoir host: unknown.Sandfly vector: based on demonstration of promastigotes in dis-sected sandflies in endemic areas: Lu. anduzei in Surinam.Geographical area: Guyana, French Guyana, Surinam; certainlyextending into north Brazil in the Territories of Amapa and Roraima,and the States of Para and Amazonas; probably into east Venezuela.Behaviour in hamster: slow development of small, fleshy swellingat site of inoculation in nose or foot: scanty numbers of parasitesand marked host cellular response; no metastatic spread in skin.

7. Conclusions

Garnham (1966), in discussing problems in the taxonomyof the malaria parasites, wrote:

A large body of opinion, although recognizing the need for re-classification, has advised delay in order to collect more data.It seems . . . that this attitude can be maintained too long . . . itis probably better to possess a list of names which can be sunkwhen proof of synonymy is forthcoming than to struggle withcircumlocutions like the "long-term relapse form of P. vhax"or make do with the non-committal "Plasmodium sp."

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These sentiments apply equally well in considering theleishmaniae, which have suffered too long from such terms as"the New World variety of L. donovani", "kala-azar of theMediterranean type" and "L. braziliensis sensu lato".During a lifetime devoted to the study of these parasites,Adler (1947) consistently stressed the great need for " . . . somesystem of nomenclature because the differences between themare real, constant and of the greatest importance."

ADDENDUMSince this paper was written, we have noted that workers

in Panama have discovered another Leishmania, "similarto L. mexicana", in the rodents of that country (Herrer,1970). Whether or not this parasite is the same as L. mexicanaamazonensis of Brazilian rodents remains to be seen but, fromthe brief description given, it is clearly a member of the L.mexicana complex.

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L., Deane, G., Guimaraes, F. N., Paumgartten, M. J. von &Sa, B. (1938) Mems Inst. Oswaldo Cruz, 33, 89

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