Enteric parasites and AIDS

INTRODUCTION

Since the first AIDS cases were described, a high prevalence o f gastro intestinal alteratio ns has been repo rted, especially diarrhea asso ciated with parasito sis.

This b e c a me mo re e vid e nt w he n the appearance o f a syndro me named “Slim Disease”, c ha ra c te riz e d b y a n inte nse w e ig ht lo ss accompanied by chronic diarrhea, prolonged fever and diffuse muscle weakness, was o bserved in Africa, especially in Uganda.1 ,2 ,3 Studies conducted in Zaire and Uganda have sho wn the presence o f so me patho genic agents respo nsible fo r the “ Slim Disease” , such as Iso spo ra, Crypto spo ridium, Salmo nella, Shigella and Campylo bacter species, amo unting to a prevalence o f 6 0 to 8 0 %.4 “ Slim Disease” has been o bserved in advanced stages o f HIV infe c tio n. The e xp re ssio n “ W a sting Syndro me” was ado pted in substitutio n by W HO in 1 9 8 8 o n the basis o f criteria laid do wn by the CDC.2

Thus, where as infections in the gastrointestinal tract play a critical ro le in AIDS patho genesis and dia rrhe ic dise a se s a ssume a pro mine nt ro le , re a c hing a ra te o f up to 5 0 % in de ve lo pe d co untries, in develo ping co untries there have been repo rts o f incidence o f up to 9 5 %, as in Haiti and

R eview A rticle

Ente ric parasite s and AIDS

Instituto de Infectologia Emílio Ribas and Univerisidade Federal de São Paulo/

Escola Paulista de Medicina, São Paulo, Brazil

ABSTRACT

O BJECTIVE: To repo rt o n the impo rtance o f intestinal parasites in patients with AIDS, sho wing relevant data in the medical literature, with special emphasis o n

epidemio lo g y, diag no sis and treatment o f entero parasito sis, especially crypto spo ridiasis, iso spo riasis, micro spo ridiasis and stro ng ylo idiasis.

DESIGN : N arrative review.

the African co ntinent.5

Amongst the causes of diarrhea in developing co untries, tho se o f a parasitic o rigin are pro minent in patients with AIDS.

O ppo rtunistic infectio ns caused by intestinal parasites also vary acco rding to the geo graphical area and the endemic levels in each lo catio n.

The progressive decline of immunological and muco us defense mechanisms predispo ses patients to early, intermediary and late g astro intestinal manifestatio ns o f HIV infectio n.6 At later stages o f the disease, the alteratio ns in no n-specific defense mechanisms in the pro ductio n o f Ig A and the reduc tio n in lo c a l immune c ell respo nse a lso pro g ress, thus increasing the susceptibility to a numb er o f intestina l o ppo rtunistic pa tho g ens, amo ng which Crypto spo ridium parvum, Iso spo ra belli and Micro spo ridia species are the mo st pro minent.7

After the emergence o f AIDS, these parasites, until then known solely in veterinary medicine, were no longer considered as commensal organisms and a re no w a d a ys re c o g niz e d a s o p p o rtunistic patho gens co mmo n to these patients. Infectio ns by these ag ents co nstitute a majo r seco ndary aggravating facto r o f the disease, o ften respo nsible fo r wo rsening the general health co nditio ns, due to manifestatio ns o f diarrhea which are difficult to co ntro l, so metimes resulting in the death o f the patient.

CRYPTOSPORIDIASIS

Crypto spo ridiasis, a disease caused by an intracellular protozoan named Cryptosporidium sp, was described fo r the first time in 1 9 0 7 by Tyzzer. This parasite was co nsidered a co mmensal up to 1 9 7 5 , when it was identified as the cause o f diarrhea in animals.8

The first manifestatio n o f crypto spo ridiasis was repo rted by N ine et al. in 1 9 7 6 , and the d ise a se b e c a me a ma jo r c o nc e rn w he n the no tificatio n o f the first 2 1 patients was given, 1 4 o f who m died o f chro nic diarrhea caused by Crypto spo ridium sp infectio n.9

It is worth noting that outbreaks of epidemic linked to c o nta mina ted wa ter a re o f extreme

importance for the dissemination of this parasite such as the 1 9 9 3 Milwaukee (USA) crypto spo ridiasis o utbreak, in which 4 0 3 ,0 0 0 human cases were reported, thereby becoming a relevant public health concern.10-12 After this outbreak, it was recommended tha t immuno c o mpro mise d pa tie nts sho uld b e extremely careful with water, foodstuffs and contact with animals.

Crypto spo ridia sis is distrib ute d o ve r a ll continents. In Haiti and the African continent the prevalence is 50%,13 while in the USA it ranges from 3 to 4%.14

In Brazil, due to the co ntinental size o f the country, the rates of incidence vary with the location. In the city o f São Paulo , fo r instance, repo rts have referred to levels aro und 1 2 .1 to 2 4 .4 4 %.1 5 -1 7 Ho wever, the latest epidemio lo g ical repo rt o n Bra z il, d a te d Fe b rua ry 1 9 9 8 , sho w s a crypto spo ridiasis rate o f o nly 3 .5 %.1 8

Crypto spo ridiasis in AIDS patients usually causes chronic, bulky and intermittent diarrhea, with liquid non-bloody stools, accompanied by pain and abdo minal co lic, and a no ticeable lo ss o f weight can be o bserved.8

Asympto matic cases are rarely described, o ccurring mo stly in develo ping co untries with patients sho wing milder immuno deficiency.1 9 ,2 0

Extra intestina l ma nifesta tio ns ha ve b een clearly described in the literature, especially in the gall bladder, biliary ducts and pancreas, leading to co nditio ns such as papillary steno sis, sclero sing c ho la ng itis a nd a c a lc ulo us c ho le c ystitis. The re sp ira to ry tra c t c a n a lso b e a ffe c te d w ith manifestatio ns o f chro nic bro nchitis.2 1 ,2 2

The intensity and duratio n o f diarrhea in crypto spo ridio sis cases is clo sely asso ciated with the CD4 + T cell co unts. This is well demo nstrated in a classic study on HIV-infected patients with CD4+ cell co unts higher than 1 8 0 / mm3 who displayed clinical healing o ver a perio d o f fo ur weeks, while 8 7 % o f the pa tie nts pre se nting mo re se ve re immuno suppressio n, with CD4 + co unts lo wer than 1 4 0 / mm3, presented persistent and hard-to -co ntro l diarrhea.2 3

Neelsen) and auramine-rho damine metho ds, via the detectio n o f reddish-stained Crypto spo ridium oocysts.2 4 More sophisticated diagnostic techniques using monoclonal antibodies are already available, such as ELISA and immuno fluo rescence, with high sensitivity and specificity.2 5 -2 7 The treatment is co ntro versial, with rehydratio n via an appro priate liquid balance and the maintenance o f the patient’s nutritio nal co nditio n being reco mmended. There sho uld be careful mo nito ring and administratio n o f antidiarrheic drug s when needed.2 8 Several treatments are available but they have no t sho wn significant clinical efficiency. Studies have been co nducted with hyperimmune bo vine co lo strum, letrazuril and diclazuril (veterinary medicine drugs), spira mic yn a nd mo re re c e ntly a z ithro mic yn, paro mo mycin, o ctreo tide and ro xithro mycin.2 9 -3 1

ISOSPORIASIS

Iso spo ra belli is a co ccidium described fo r the first time in 1 9 1 5 by W o o dco ck and later by W enyo n in 1 9 2 3 .3 2 It is fo und in tro pical and subtropical areas and is endemic in South America, Africa and in So uthern Asia,3 3 with an o ccurrence rate o f 1 5 % in Haiti,3 3 0 .2 % in the USA3 4 and 1 .8 % in Brazil.1 8

Higher rates o f iso spo riasis in Brazil have been repo rted in AIDS patients living in Santo s and in São Paulo , with a prevalence o f 9 .9 % and 6 .6 7 %, respectively.1 7 ,3 5 The lo wer prevalence o f Iso spo riasis may be ascribed to the seco ndary p ro p hyla xis fo r p ne umo c ysto sis thro ug h administratio n o f sulfametho xazo le-trimetho prim during the co urse o f AIDS, since Iso spo ra belli is sensitive to this therapy.3 6

The diarrheic co nditio n is also no tewo rthy and is acco mpanied by fever, intestinal co lic, ano rexia, abdo minal pain, lo ss o f weig ht and peripheral eo sino philia.3 7

Iso spo riasis can also sho w extraintestinal disseminatio n features, affecting the mesenteric, periaortic, mediastinal and tracheobronchial lymph no des.3 8 ,3 9 It may also be related to biliary disease, causing manifestatio ns o f acalculo us cho lecystitis.3 7 Iso spo ra belli differs mo rpho lo gically fro m Crypto spo ridium sp no t o nly because o f its intrinsic

mo rpho lo gy (elliptical o o cyst measuring 2 2 x 1 5 µm in diameter, co ntaining two spo ro cysts with fo ur spo ro zo o ites), but also fo r the intracellular lo catio n in the abso rptive cell, while Crypto spo ridium is restricted to the brush bo rders, immediately under the apical membrane o f abso rptive cells.4 0

Labo rato ry diagno sis is carried o ut in the same way as fo r Crypto spo ridium parvum, using the Kinyoun and auramine-rhodamine techniques,4 1 altho ugh co mmo n pro cesses such as Faust’s are o fte n e no ug h fo r the dia g no sis. The spe c ia l c o lo ra tio n thus b ec o mes a further dia g no stic element fo r finding the parasite.

The the ra p e utic re c o mme nd a tio n fo r iso sp o ria sis is the a d ministra tio n o f sulfa me tho xa z o le -trime tho p rim fo r 1 0 d a ys, fo llo wed by pro phylaxis fo r a further three weeks. This le a d s to a re d uc tio n in the numb e r o f discharg es and the reco very o f bo dy weig ht.3 6 In re c urre nt situa tio ns o r in no n-re sp o nd ing patients it is necessary to administer o ther drug s suc h a s p yrime tha mine , in iso la tio n o r in asso ciatio n with sulfadiaz ine,4 2 ro xithro mycin4 3 and metro nidazo le.4 4 Drug s such as tetracycline, a mp ic illin, nitro fura nto in, q uina c rine a nd furazo lido ne have already been used but sho wed no therapeutic success.3 4

MICROSPORIDIASIS

The third majo r gro up o f intestinal patho gens to be repo rted are the micro spo ridia, which are strictly intracellular pro to zo a, spo re-pro ducing and with great variety of genera and species. They have widespread distributio n and o ver 4 0 0 cases o f patients with co -infectio n o f micro spo ridia and HIV have been repo rted. The majo r etio lo gic agent is Entero cyto zo o n bieneusi.4 5

The first d e sc rip tio n o f inte stina l mic ro sp o rid ia sis in a n HIV-p o sitive p a tie nt o ccurred in France.4 6 The first descriptio n o f this co nditio n in Braz il dates back to 1 9 9 3 , with cases having o ccurring in Rio de Janeiro , São Paulo and Ceará.4 7 -5 0

technique fo r detectio n o f micro spo ridian spo res in the sto o l samples o f 1 4 0 HIV-po sitive patients sho wed that the rate o f prevalence o f intestinal micro spo ridiasis was 1 7 .8 6 %.5 2 The fact that these c a se s ha ve o nly re c e ntly a p p e a re d c a n b e explained by the diagno stic difficulty, as electro nic micro sco py is required fo r co nfirmatio n o f the presence o f the parasite. In co ntrast, in the city o f São Paulo only 1.3% of microsporidian spores were sho wn up in pa tients with AIDS a nd c hro nic dia rrhe a via the mo difie d tric hro me sta ining metho d.5 2 A

O ptical micro sco py metho ds, such as the chromotrope method, were then proposed whereby spo res wo uld appear as o val-shaped and stained pink o r pa le re d.5 3 This te c hniq ue ha s b e e n impro ved and named G ram-chro mo tro pe. Fecal sample smears are stained in G ram’s stain, followed by a chro mo tro pe so lutio n.5 4

Chro nic diarrhea and/ o r biliary disease manifestatio ns in HIV-infected individuals with CD4 + T cells o f between 5 0 and 1 0 0 / mm3 may suggest micro spo ridio sis. Transmissio n is unkno wn to date, but there have been repo rts o f co ngenital tra nsmissio n a nd via inha la tio n o f a irb o rne spo res.5 1

Regarding treatment, albendazo le has been the mo st pro mising drug fo r handling intestinal micro spo ridiasis. 5 5 -5 7

GIARDIASIS AND AMEBIASIS

The p ro to z o a ns G ia rd ia la mb lia a nd Entamoeba histolytica are important causes of acute diarrhea in ho mo sexual males, even fo r tho se that are no t HIV-po sitive. To gether with Campylo bacter, Salmo nella, Shiguella and Yersinia they cause high frequencies o f enteritis, co litis and pro ctitis.5 8

Statistical data fo und in the literature are ra the r d ive rg e nt, b ut the inc id e nc e o f the se pro to zo ans amo ngst the ho mo sexual po pulatio ns o f large cities, such as New Yo rk, Lo s Angeles, San Francisco and To ro nto is quite high.5 9

The prevalence o f Entamo eba histo lytica in HIV-neg ative ho mo sexual patients in the USA ranges between 2 1 and 3 2 %, and is aro und 1 2 % in the United Kingdo m.6 0

A study perfo rmed in Lo s Angeles with 1 0 0 HIV-po sitive patients, mo stly ho mo sexuals, sho wed a prevalence rate o f 5 5 % fo r giardiasis and 3 % fo r amo ebiasis.6 1

In Fra nc e , stud ie s fo c use d up o n the prevalence o f intestinal parasito sis sho wed a high frequency o f pro to zo an species in AIDS patients, and the rates o f G iardia lamblia and Entamo eba histo lytica were 5 .8 % and 2 %, respectively 6 2.

Previo us studies demo nstrated that giardiasis incidence do es no t differ amo ngst HIV-po sitive and negative patient po pulatio ns.6 3

Infec tio n with G ia rdia la mb lia a nd HIV amo ng st ho mo sexual males is co rrelated with enteritis o r entero co litis, but no histo lo gical study o f the co lo nic muco sa has yet been carried o ut.6 4 In Brazil, examinatio n o f 7 7 1 fecal samples fro m AIDS patients living in São Paulo , perfo rmed under the pro gram fo r the co ntro l and preventio n o f AIDS, have sho wn rates o f 5 .1 8 % and 8 .4 9 % o f amebiasis and giardiasis, respectively.1 5 In a recent study in the city o f São Paulo analyzing patients with mo re severe immuno deficiency, E. histo lytica was no t o bserved but G . lamblia cysts were seen in about 2 7 % of the examined patients.1 7 De sp ite this hig h p re va le nc e , c la ssic a l pro to zo a such as G iardia Lamblia and Entamo eba histo lytica are less frequent as causes o f severe illnesses in HIV-infected patients, when co mpared w ith M ic ro sp o rid ia , Iso sp o ra b e lli a nd C ryp to sp o rid ium p a rvum a nd the y a re no t co nsidered as o ppo rtunistic infectio ns in AIDS.

A me b ia sis ma y p re se nt w ith inva sive characteristics, but this has rarely been repo rted in the literature.6 5

Mo re re c e ntly, in Re c ife , a stud y w a s co nducted to evaluate invasive amebiasis in AIDS patients. Seventy fo ur patients were examined, o ut of which 54 had diarrhea but Entamoeba histolytica was found in only one patient (1,3%) and practically an absence o f invasive amo ebiasis.6 6

STRONGYLOIDIASIS

first described in 1 8 7 6 by Normand, after necropsy o f patients with diarrhea in fro m Co chin-China, then an auto no mo us regio n o f China.6 7

This geo helminth presents its majo r effects in immuno d e p re sse d p a tie nts, le a d ing to the dissemina tio n o f the infec tio n. This o c c urs in tra nspla nte d pa tie nts, individua ls pre se nting malnutritio n and patients submitted to pro lo nged use o f co rtico stero ids, suffering fro m leukemia, lympho mas o r AIDS.6 8 ,6 9

Despite the po ssibility o f disseminatio n o f this helminth in HIV-po sitive patients, o nly 1 4 cases had b e e n re po rte d b y 1 9 9 4 in the inte rna tio na l literature.7 0

A case o f massive infectio n by Stro ngylo ides sterco ralis in AIDS patients in São Paulo was recently repo rted, presenting the nemato de even in sputum samples.7 1

The c linic a l synd ro me o f d isse mina te d stro ngylo idiasis is characterized by gastro intestinal signs and sympto ms, such as nausea, vo miting, meteo rism, ano rexia and diarrhea, alternating with perio ds o f intestinal co nstipatio n and seco ndary infectio ns. Respirato ry sympto ms such as dyspnea, hemo ptysis, co ughing, o r manifestatio ns o f asthma and even extensive pneumo nia, may be o bserved. At the same time, the patient can present fever, cachexia and lo ss o f weight.7 2 , 7 3

In immuno suppressed patients, self-infestatio n is speeded up and a large number o f larvae are re le a se d , c a using the d isse mina tio n o f the infectio n.7 4

In Brazil, the prevalence o f stro ngylo idiasis in HIV-po sitive patients is aro und 4 to 1 5 %, in c o mp a riso n w ith 1 . 4 % in the g e ne ra l po pulatio n.1 5 ,1 7 ,6 9

Labo rato ry diag no sis is based upo n the Baerman-Mo raes o r Rugai-Matto s-Briso la metho ds, presenting as their basic principle the thermo and hydro tro pism o f Stro ngylo ides sterco ralis larvae seen in sto o l samples.6 7

Stro ngylo ides sterco ralis larvae may also be detected in aspirated duo denal material, sputum, bro ncho -alveo lar lavage, cervico vaginal cyto lo gy, cerebro spinal fluid and gastric cyto lo gy.7 4

G e ne ra lly, the se a rc h fo r Stro ng ylo ide s sterco ralis, even in iso lated samples, sho ws a

p o sitivity o f 3 0 % in immuno c o mp ro mise d individuals with AIDS. W hen three or more samples are taken, this po sitivity reaches levels as high as 8 0 %.6 7

Thia b enda z o le is c o nsidered the drug o f c ho ic e fo r tre a ting stro ng y lo id ia sis, in immuno sup p re sse d ind ivid ua ls. The ra te s o f eradicatio n by this anti-helminth drug can reach le ve ls a s hig h a s 9 0 % .6 7 , 6 8 , 7 2 O the r c hemo thera py a g ents tha t ma y b e used inc lude a lb enda z o le a nd c a mb enda z o le.

In Stro ng ylo ides sterco ralis hyperinfectio n cases, treatment with thiabendazo le may be used fo r pro lo nged perio ds, fo llo wed by maintenance do ses. O ften, eradicatio n is difficult.7 0 ,7 1 Ano ther o ptio n in these cases is the administratio n o f ivermectin, a drug used fo r o ncho cerciasis, with healing rates aro und 9 4 %.7 0 ,7 5 ,7 6 This drug is no t yet available in Brazil.

OTHER PARASITES

O ther helminths such as Ascaris lumbricoides (3.52%), Trichiuris trichiura (4.14%), Ancylostomidae (2 . 6 9 % ), Ente ro b ius ve rmic ula ris (0 . 2 1 % ), Schistosoma mansoni (1 .6 6 %), Taenia sp (0 .2 1 %) and Hymenolepis nana (10.41%) have shown lesser frequency and importance in AIDS patients.1 5

Several o ther intestinal parasito ses may lead to aggravatio n and/ o r disseminatio n o f the co urse o f AIDS. Pro to zo a such as Cyclo spo ra sp and Blasto cystis ho minis have arisen, which may also cause majo r diarrhea manifestatio ns.

Bla sto c ystis ho minis is a p o te ntia lly patho genic parasite, mo re predo minant in male ho mo sexuals than in o ther po pulatio n gro ups, and its o ccurrence is no t higher in individuals suffering fro m digestive disturbances.7 7 It has been iso lated in human feces with a frequency ranging fro m 1 to 6 0 % in individuals fro m different parts o f the wo rld and expo sure to co ntaminated water co ntributes to the increase o f this parasito sis.7 8

were recently repo rted with parasite eradicatio n in the sto o l samples after specific treatment.8 1

Bla sto c ystis infe c tio n is c o mmo n in immunocompromised hosts and it may be diagnosed through conventional techniques such as the Lutz and Faust methods. There are reports in the literature that show trichrome stains and Ficol concentrations as alternatives for finding this parasite.8 2 ,8 3

The re is so me c o ntro ve rsy a b o ut the appro priateness o f treating this entero parasito sis. W hen treatment is chosen, metronidazole is used.8 4 Cyclo spo ra sp was initially iso lated in 1 8 7 0 by Eimer. The first repo rt o n its asso ciatio n with AIDS dates back to March 1 9 8 9 , in a male patient with chro nic diarrhea.8 5

Studies o n the prevalence o f cyclo spo riasis sho w very lo w ra tes, no t hig her tha n 1 % in develo ped co untries.8 6 ,8 7

O utb re a ks o f c yc lo spo ria sis due to the c o nsump tio n o f ra sp b e rrie s imp o rte d fro m G uatemala o ccurred recently: 1 4 6 5 cases were repo rted fro m 2 0 sta tes o f the USA.8 8 O ther o utbreaks were repo rted in Virginia (USA), due to contamination of fresh basil, causing gastrointestinal disease.8 9

The diag no sis o f infectio n by Cyclo spo ra cayatenensis is based upo n the detectio n o f o o cysts in fe c a l sa mp le s, via o p tic a l mic ro sc o p y. C yc lo sp o ra c a ya te ne nsis d iffe rs fro m Crypto spo ridium in its larg e size.9 0 Due to the mo rpho lo gical similarities and lack o f kno wledge o n ho w to differentiate between these two species, d ia g no sis o f c yc lo sp o rid io sis is se ld o m acco mplished.3 3 It is essential to determine the spo rulatio n o f Cyclo spo ra, which may be do ne using 2 .5 % po tassium dichro mate.

The low frequency of this protozoan may once again be explained by the use o f sulfametho xazo le-trimetho prim administratio n as a pro phylactic treatment ag ainst Pneumo cystis carinii in AIDS patients presenting CD4 + cell co unts lo wer than 2 0 0 / mm3.9 1 ,9 2

CONCLUSION

It can be no ted that parasito sis presents a very significant interface with AIDS, and this has b een the o b jec t o f studies b y ma ny a utho rs.

Investigatio ns o n the etio lo gy o f diarrhea in HIV-infected patients indicate parasito sis as the cause in up to 4 0 % o f patients.

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Sérgio Cimerma n - MD. Instituto de Infecto lo gia Emílio Ribas and Esco la Paulista de Medicina, Univerisidade Federal de São Paulo . São Paulo , Braz il.

Benja min Cimerma n - Parasito lo gy Department, University o f Mo gi das Cruzes. Mo g i das Cruz es, Braz il.

Da vid Sa lomã o Lew i- MD, PhD. Infectio us and Parasitic Diseases Unit, Universidade Federal de São Paulo / Esco la Paulista de Medicina. São Paulo , Braz il.

Sources of funding: No t declared

Conflict of interest: No t declared

La st received: 1 9 March 1 9 9 9

Accepted: 7 April 1 9 9 9

Address for correspondence:

Sérgio Cimerman

Alameda Jauaperí, 8 9 0 - Apto . 1 1 1 São Paulo / SP - Brasil - CEP 0 4 5 2 3 -0 1 4 E-mail: sc@ mandic.co m.br

RESUMO

O BJETIVO : Relatar a impo rtância das parasito ses intestinais em pacientes co m Aids, mo strando dado s relevantes na literatura médica, co m enfo que em especial, abo rdando a epidemio lo g ia, diag nó stico e tratamento das entero parasito ses, principalmente da cripto spo ridíase, iso spo ríase, micro spo ridíase e estro ng ilo idíase. TIPO DE ESTUDO : Revisão narrativa.