Parasitic infections associated with HIV/AIDS in the Caribbean

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Parasitic Infections Associated with

HIV/AIDS

in the Caribbean

R. D.

ROBINSON~

444

This review article seeks to highlight the significance for the Caribbean of major parasitic infections associafed with AIDS, encourage awareness of these opportunistic parasites, and promote familiarity with appropriate diagnostic techniques and their clinica relevance. Spe- cific agents considered include Pneumocystis carinii; Toxoplasma gondii; the enferic coccidiuns Cryptosporidium spp., Isospora belIi, and Cyclospora cayetanensis; the hemoflagellates Leishmania spp. and Trypanosoma cruzi; the fungi Histoplasma capsulatum and Cryptococcus neoformans; the nematode Strongyloides stercoralis; and the mife Sarcoptes scabiei.

These disease agents can be divided into two groups, the immune-regulated ‘endogenous” parasites (the protozoans P. carinii and T. gondii, and possibly the roundworm S. ster- corak) and intracellular parasifes (including the enteric coccidia, hemoflagellates, and fungi). Both in the Caribbean and ezsewhere, the endogenous parasites (particularly P. carinii

and T. gondii) are the most troublesome for AIDS patients, partry because they are likely to be transmitted and establish a benign immunoregulated presence early in the subject’s life. Indeed, health management programs for AIDS patients often routinely include P. carinii prophylaxis, since nearly all such patients who survive long enough are expected to experience an episode of acute P. carinii infection. In contrast, there is no known epidemiologic association between AIDS and strongyloidiasis in the Caribbean, and the prevalence there of potenfiaZly opportunistic hemoflagellates such as Leishmania spp. and Trypano- soma cruzi is relafively low.

S

ince identification of the acquired immune deficiency syndrome (AIDS) as

cation, or immunocytotoxic events may contribute to cell death.

a novel disorder in 1981, HIV infections In addition to a wide range of consti- have claimed the lives of more than 3 000 tutional illnesses, AIDS predisposes indi- individuals in the Caribbean area (I). Im-

viduals

to several opportunistic parasitic paired cellular immunity, related to the infections, particularly pneumocystosis affinity of HIV for cells bearing the CD4 and cerebral toxoplasmosis. Other defi- antigen, is the immunologic hallmark of nite opportunists include human intes- AIDS. (The CD4 molecule is a surface tinal coccidia, and microsporidia have re- feature of all helper T (TH) lymphocytes cently been shown to exhibit significant but is also found on the surfaces of some enteric pathogenicity in immunode-

cells of the monocyte-macrophage series pressed individuals (2,3). In contrast, ex- (lo%-20%) and on a few B lymphocytes tracellular protozoan and helminthic in- (~5%) and glial cells.) Cellular destruc- fections are apparently not opportunistic tion may result directly from viral repli- in AIDS patients.

This review seeks to highlight the regional Caribbean significance of major parasitic infections implicated in AIDS. Our aim in providing this information is to encourage both laboratory diagnosti- ILecturer in Parasitology, Department of Zoology,

The University of the West Indies, Kingston 7,

Jamaica.

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cians and clinicians to become more aware of opportunistic parasites and the partic- ular problems they cause in immunocom- promised patients, and to familiarize themselves with appropriate diagnostic techniques and their clinical relevance.

SPECIFIC PARASITES

Pneumocystis carinii

Phylogenetically related to fungi but considered a protozoan because of its life- cycle and susceptibility to antiprotozoal drugs,

P. carinii

has a worldwide distribution in the lungs of humans and animals but usually causes no respiratory problems. Infection, through inhalation of cysts, apparently occurs early in life; some studies have shown serologic evidence of exposure by age four in more than 60% of the children tested (4). Al- veolar macrophages and TH cells are thought to be important in restricting the parasite to a dormant or controlled ex- istence in the body, and it is only when the host’s immune system is “compromised” that clinical infection ensues.

P. curinii

pneumonia is the opportunistic infection most commonly found in the United States’ AIDS patients, occurring at least once in up to 80% of the victims (5). The infection results in degeneration of alveolar cells, followed by infiltration of the spaces by a foamy ground substance containing trophozoites and cysts. Oxygen transport across the alveolar-capillary space is impaired, and the patient suffers pro- gressive dyspnea.

Diagnosis of P.

carinii

infection must be based on demonstration of organisms in lung material. The cysts measure 5-

12 Frn across and contain eight small sporozoites. Prior to the AIDS pandemic, the recommended diagnostic procedure was open-lung biopsy. However, less in- vasive procedures can be used when the presence of relatively large numbers of

cysts is expected. Specifically, a combination of transbronchial biopsy and bronchoalveolar lavage is considered 100% sensitive (6). Sputum specimens are not normally acceptable for recovery of organisms. The stain of choice is methenamine silver, which stains the cyst wall. Recent success has been reported using sensitive immunofluorescent techniques, but these are not yet available commercially.

In the Caribbean,

P. carinii

pneumonitis has been encountered among AZDS patients in both Jamaica (J. F. Lindo, personal communication) and Trinidad (C. Whyte-Alleng, personal communication). Given the high recognition rate of this infection among persons with AIDS worldwide, more cases are expected in the region.

Toxoplasma gondii

Exposure to the coccidian I’.

gondii

also occurs early in life.

T. gondii

infections are zoonotic. The infections have a cos- mopolitan distribution; and while they can be transmitted transplacentally when a woman has a primary infection, they are typically transmitted to people by ingestion of oocysts in food, water, or dust contaminated with cat feces, or through ingestion of tissue cysts con- tained in raw or undercooked meat. Sero- logic testing indicates a high prevalence of infection (25%-90%) among farm animals and pets in the Caribbean (7). Simi- larly, a high level of exposure appears to exist among humans, with up to 57% seropositivity reported from Jamaica (8, 9), Cuba (IO), the Leeward Islands, and Suriname (7). Human congenital infections in the Caribbean are associated with severe pathology (8, 12, 22) most often resulting in chorioretinitis.

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inactive bradyzoites, which apparently persist indefinitely in these tissues. A role for Tn lymphocytes in the containment of latent T.

gondii

infections has been demonstrated in a mouse model (5).

Cerebral toxoplasmosis resulting from reactivation of latent infections is the most common opportunistic infection of the central nervous system in AIDS patients. HIV invasion of CD4+ glial cells is likely to result in release of viable zoites, which in turn reinvade nervous tissues. In the Caribbean, only one case of AIDS-related cranial toxoplasmosis (from Trinidad) had been reported up to 1995 (23); but ap- proximately 30% of the AIDS cases pos- sessing

T. gondii

antibodies may be expected to develop encephalitis in endemic zones (5).

The prognosis associated with

Toxo-

plasma encephalitis is poor. One study of 67 patients (24) found a median survival period of 4 months following chemother- apy, while half of those discharged from the hospital suffered clinical relapse.

For diagnosis, serologic techniques are recommended. In an immunodeficient patient, a presumptive diagnosis of toxoplasmosis may be made if there is an elevated antibody (IgM) titer in the presence of neurologic symptoms. The indirect fluorescent antibody (IFA) technique is the most common serodiagnostic procedure currently in use, although ELISA will supersede it in the near future.

Cyptosporidium

spp.

This coccidian, long known to cause diarrhea in calves and other animals, has emerged as an important diarrhea1 agent in AIDS cases and in malnourished children of developing countries (15). Gyp-

tosporidium

is widely distributed, with a prevalence of about 2% in persons with normal immune capabilities (16). Infec- tions are endemic in the Caribbean (17, 18), usually being found in otherwise

healthy children with moderately severe diarrhea.

Cryptosporidium

is typically located

within a parasitophorous vacuole close to the microvillus surface of intestinal cells. Impairment of T cell function results in loss of ability to eradicate the normally self-limiting infection (19). The cholera- like symptoms manifested in immunodeficient patients are extremely difficult to treat and impossible to cure. In addition, respiratory complications associated with cryptosporidiosis have been reported in AIDS patients (20). AIDS-related cryptosporidiosis has been reported among patients in Jamaica (J. F. Lindo, personal communication) and also in Trinidad and Tobago (27).

Cryptosporidium

infections are most

safely detected in formalin-fixed stool or sputum following concentration. Oocysts are 4-6 km in diameter and contain four sporozoites. Use of monoclonal antibodies (immunofluorescence) for the di- rect detection of cysts in fecal specimens has proven more sensitive than routine acid-fast methods that occasionally do not stain all the oocysts (21).

Isospora belli

Infections with I.

belli

are widespread in Africa, but well-defined endemic foci have also been identified in South Amer- ica. Like

Cyptosporidium,

this coccidian develops within the epithelial cells of the small intestine. Infections normally result in a transient diarrhea. However, profuse diarrhea and anorexia have been de- scribed in AIDS patients (22); in such cases it is thought that impairment of T cell- mediated immunity results in reduced ability to eradicate parasite stages from the intestine.

I.

belli

displays a high prevalence among AIDS patients in Haiti (23) and has also been recorded in a Jamaican patient suf- fering from a tropical spastic paraparesis

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syndrome related to presence of the human T cell lymphotropic virus type I (HTLV-I) (author’s unpublished data).

Because only small numbers of oocysts are commonly present in stools, concentration techniques are recommended for diagnosing the infection, even in AIDS patients. The oocyst of I.

belli

is large, about 30 pm x 12 pm, and contains a single spherical zygote. Maturation con- tinues outside the host until the oocyst develops two sporocysts, each containing four sporozoites. It is then infective through ingestion.

Cyclospora cayetanensis

Similar to

Cyptosporidium

and Zsospora, this enteric coccidian causes a self-limiting diarrhea1 syndrome in immunologically competent patients worldwide. The organism was first reported in 1986 as a “new intestinal pathogen” in four otherwise healthy visitors to Haiti and Mexico (24). However, four years later

Cyclospom

was given a potentially opportunistic sta- tus, having been detected in eight patients with diarrhea, four of whom had AIDS (25).

Infections are likely to be acquired through accidental ingestion of oocysts, possibly in water (26), or through con- sumption of tissue cysts in raw or undercooked meat (25).

Cyclosporidiosis may be detected mic- roscopically in fecal smears or duodenal aspirates. The spherical, unsporulated oocysts are 8-10 km in diameter (roughly twice the diameter of

Cryptosporidium

oocysts but only half that of

Zsospora

oocysts). Most stain acid-fast with Ziehl- Neelson’s stain, but some remain un- stained as wrinkled spheres (27). Mature oocysts have two sporocysts, each containing two sporozoites.

Our understanding of C. cayetanensis infections is still incomplete, but increased awareness coupled with careful

microscopic diagnosis should provide additional information about their epidemiologic and clinical aspects.

Histoplasma

capsulatum

H. capsulafum

is a fungus with mod-

erate levels of endemicity in the Carib- bean and other parts of the Americas (28, 29). Spores are typically found in soil containing the composted manure of birds (including fowl) and bats, which are among its wide array of natural animal hosts. Humans are usually infected by inhaling the spores. Benign pulmonary infections are sometimes seen among speleologists (28, 30), hence the common name “cave disease.” However, disseminated histoplasmosis (which in some re- spects resembles visceral leishmaniasis) is known to be associated with host immune defense deficiency. Cutaneous infections have been reported in 11 of 18 AIDS patients attending the General Hospital in Port of Spain, Trinidad and Tobago (32).

Diagnosis of disseminated

HisfopIasma

infection may be made by examining a patient’s sputum, excised lymph glands, ulcer base, bone marrow, or peripheral blood. Fungal cells appear within large mononuclear cells (occasionally poly- morphs) in the buffy coat as oval masses measuring 2-3 x 3-4 Frn.

Cyptococcus

neoformans

Cryptococcosis is also a fungal infection. It involves a primary focus in the lung with a characteristic spread to the meninges and viscera that is greatly ac- celerated in immunodeficient hosts. Its distribution is worldwide, with many animal reservoirs.

C. neofurmans

grows quickly in accu-

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mally seek medical care as a result of blurred vision or mental disturbances, Disseminated infection was first reported in an AIDS patient in Trinidad and To- bago (23), but additional AIDS-related infections have emerged in Puerto Rico (32). A diagnosis of cryptococcosis is strongly suggested by a finding of yeast cells in a preparation of sputum, pus, or cerebro- spinal fluid stained with India ink. The cells range from 15 q to 45 pm in diameter and contain a single mass of centrally located protoplasm 5-15 Frn across. Culture on glucose agar or Sabouraud’s medium will distinguish nonpathogenic forms.

Strongyloides

stercoralis

S. stercoraEis

is a small nematode that produces a chronic, usually subclinical, enteric infection in humans. Although disseminated strongyloidiasis was origi- nally included in the U. S. Centers for Disease Control and Prevention’s classi- fication of AIDS-related infections in 1986, such infection is no longer listed as an index diagnosis for AIDS.

Difficulties associated with detection of strongyloidiasis, even in compromised hosts, have resulted in confusion re- garding the disease’s relevance in HIV- infected patients. Several independent studies have indicated that agar plate culture detects S.

stercoralis

infections with significantly higher sensitivity (87% -100%) than other parasitologic methods (33). The most convenient and widely used im- munodiagnostic technique for detecting strongyloidiasis in non-AIDS patients is ELISA (34). A modification involving preincubation of sera with filarial antigen recently produced a sensitivity of 85%- 100% and a specificity of 97% in a Ja- maican population (35).

Only a few well-documented cases of AIDS with disseminated strongyloidiasis have been reported, and there is an ap- parent lack of epidemiologic association

between the two diseases (36,37). Among other things, work on Martinique found no association between S.

stercoralis in-

fections and AIDS (38). In contrast, a strong epidemiologic association has been reported for severe strongyloidiasis and potentially immunosuppressive HTLV-I infections in Jamaica (39).

Eosinophils and IgE antibodies appear to be important in the regulation of strongyloidiasis (39, 40), but their activity is in turn regulated by lymphokines produced by T cells that are presumably vulnerable to HIV. Even so, it appears that disseminated S. stercoralis infection is unlikely to feature prominently in AIDS.

Sarcop tes sea biei

The itch mite,

S. scabiei,

has a cosmo- politan distribution with discrete strains parasitizing humans and domestic animals. Adult mites excavate serpiginous burrows in the upper epidermis, and a delayed (type IV) hypersensitivity reac- tion to dead mites and their feces causes intense itching. Scratching may result in bleeding and scab formation, and sec- ondary bacterial infection often follows. The disease is diagnosed by finding adult mites or their eggs, usually at the distal parts of fresh burrows in the skin. Epi- dermal scrapings may be cleared by add- ing a few drops of 20% aqueous potas- sium hydroxide prior to microscopic examination.

S.

scubiei

infections appear to be exac- erbated in persons whose immunity is compromised by any means, but a gen- eralized dermatitis, characterized by ex- tensive scaling and crusting, has been reported in patients with HTLV-I seropositivity and adult T cell leukemia (ATL) (41), and also in patients with AIDS (42, 43). Cases of severe scabies infection and HIV have been recognized in Jamaica (L. LaGrenade, personal communication). A strong association between infective der-

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matitis and HTLV-I has also been reported from Jamaica (44) in cases having increased CD4KD8 ratios with elevated total CD4 counts.

Leishmania spp.

Visceral leishmaniasis is endemic in Central and South America. The respon-

ible organisms live in mononuclear phagocytes of the host and are .detected through microscopic observation as Leishman-Donovan bodies (amastigotes) in affected tissues. ELISA provides sensitive immunodiagnosis, but problems with specificity still exist in areas where other hemoflagellate infections occur.

Elimination of the infection requires ac- tivation of T lymphocytes and macrophages. It is therefore not surprising that opportunistic leishmanial infections of this type have been recognized in HIV-positive patients in Europe and South America (45). In the Caribbean, however, only historical reports exist of symptoms associated with

“leishmaniose viscerale”

in non-AIDS patients from Guadeloupe and Martinique (45, 46).

Cutaneous leishmanial infections, be- sides being endemic in Central and South America, are also endemic in the Domin- ican Republic, French Antilles, and Trin- idad (45). A case of disseminated cutaneous leishmaniasis (probably caused by

L. braziliensis)

has been reported in a Bra- zilian AIDS patient (45), and it seems likely that the combination of T cell and macrophage dysfunction seen in HIV- associated visceral infections is also important in cutaneous infections. Due to their low level of endemicity in the Car- ibbean islands, however, leishmanial infections are unlikely to pose a major risk to AIDS patients in the region.

Typanosoma

cruzi

There is serologic evidence of exposure to T.

cruzi

in Jamaica, Curafao, and Trin-

idad, but this has not been clinically cor- related

(47).

On the other hand,

T. cruzi

is associated with significant morbidity and mortality in Central and South America, where infections have been associated with acute CNS symptoms in AIDS patients. Impairment of the primary role played by activated macrophages in stemming infection, particularly in the acute phase, is likely to be crucial here.

DISCUSSION

In the Caribbean, as elsewhere, AIDS- related opportunistic parasites are re- stricted to those species that can exploit the specific immune defect associated with AIDS and are thus able to proliferate and cause problems. Within this context, HIV- infected individuals are susceptible to parasites that fall roughly into two categories: immune-regulated “endogenous” parasites such as

P. carinii, T. gondii,

and possibly S.

stercoralis;

and intracellular species, particularly those that invade macrophages and whose elimination requires T cells or T cell-macrophage cooperation, such as enteric coccidia, some hemoflagellates, and fungi such as

Crypfococcus

neof0rmans

and

Histoplasma capsulatum.

There are comparatively few published reports of AIDS-related parasitic infections in the Caribbean, but with increased awareness of opportunistic organisms more cases are likely to be diagnosed in the future. It should also be noted that there is a comparatively low prevalence in the Car- ibbean islands of potentially opportunistic hemoflagellates such as

LRishmania

spp. and Trypanosoma cruzi.

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with depressed CD4 counts, health management programs often incorporate prophylaxis for Pneumocystis curinii pneumonia-since nearly all AIDS patients are expected to have an episode of it if they survive long enough. Chemopro- phylaxis involving pyrimethamine- sulfadoxine, trimethoprim-sulfamethox- azole, or inhaled pentamidine has been used with considerable success in the United States (48).

As the AIDS pandemic progresses without prospect for a vaccine in the fore- seeable future, much less a cure, the incidence of primarily endogenous opportunistic infections is likely to feature more prominently among AIDS patients in the Caribbean region.

Acknowledgments. I am grateful to Dr. E. S. Cooper and Dr. M. Hammond for reading the manuscript and offering helpfuI suggestions for improvement, and to Mr. W. Forbes for bibliographic as- sistance.

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