Human Infections with Sarcocystis Speciescmr.asm.org/content/cmr/28/2/295.full.pdfacquired from eating undercooked meat: Sarcocystis hominis, from beef, and Sarcocystis suihominis,

Human Infections with Sarcocystis Species

Ronald Fayera Douglas H Espositob Jitender P Dubeya

US Department of Agriculture Agricultural Research Service Beltsville Maryland USAa Division of Global Migration and Quarantine National Center for Emerging andZoonotic Infectious Diseases Centers for Disease Control and Prevention Atlanta Georgia USAb

SUMMARY 295INTRODUCTION 295

Life Cycle Stages 296Species Infecting Animals 297Species Infecting Humans 297Sources of Intestinal and Muscular Sarcocystosis 300

PREVALENCE SYMPTOMS AND DIAGNOSIS OF INFECTION IN HUMANS 301Intestinal Sarcocystosis Species and Symptoms 301Intestinal Sarcocystosis in Europe 301Intestinal Sarcocystosis in Asia 304Intestinal Sarcocystosis in Australia 305Intestinal Sarcocystosis in North and South America 305Diagnosis of Intestinal Sarcocystosis 305Extraintestinal Sarcocystosis 305Outbreaks and Case Descriptions 306Sarcocystosis and Cardiomyopathy 307Sarcocystosis and Glomerulonephritis 307Sarcocystosis and Malignancy 307

IMMUNITY PROPHYLAXIS AND TREATMENT 307Intestinal Sarcocystosis 307Muscular Sarcocystosis 308

PREVENTION 308CONCLUSIONS 309REFERENCES 309AUTHOR BIOS 311

SUMMARY

Recurrent outbreaks of muscular sarcocystosis among touristsvisiting islands in Malaysia have focused international atten-tion on sarcocystosis a disease once considered rare in hu-mans Sarcocystis species require two hosts definitive and inter-mediate to complete their life cycle Humans can serve asdefinitive hosts with intestinal sarcocystosis for two speciesacquired from eating undercooked meat Sarcocystis hominisfrom beef and Sarcocystis suihominis from pork Symptomssuch as nausea stomachache and diarrhea vary widely de-pending on the number of cysts ingested but appear more se-vere with pork than with beef Humans serve as intermediatehosts for Sarcocystis nesbitti a species with a reptilian definitivehost and possibly other unidentified species acquired by in-gesting sporocysts from feces-contaminated food or water andthe environment infections have an early phase of develop-ment in vascular endothelium with illness that is difficult todiagnose clinical signs include fever headache and myalgiaSubsequent development of intramuscular cysts is character-ized by myositis Presumptive diagnosis based on travel historyto tropical regions elevated serum enzyme levels and eosino-philia is confirmed by finding sarcocysts in muscle biopsy spec-imens There is no vaccine or confirmed effective antiparasiticdrug for muscular sarcocystosis but anti-inflammatory drugsmay reduce symptoms Prevention strategies are also dis-cussed

INTRODUCTION

Sarcocystis is classified in the phylum Apicomplexa along withspecies of Eimeria that cause coccidiosis in poultry and live-

stock Toxoplasma gondii which infects virtually all warm-bloodedvertebrates and species of Cystoisospora that infect humans and avariety of animals Sarcocystis species are ubiquitous in nature andare found worldwide Two hosts are required to maintain the lifecycle an intermediate or prey host in which cysts (sarcocysts)containing infectious zoites infect the muscles and a definitivefinal or predator host that ingests the cysts becomes infected withintestinal-stage parasites and excretes oocysts or sporocysts intothe environment For the 150 species of Sarcocystis most inter-mediate hosts include herbivorous mammals and humans and otherprimates but also some birds reptiles and possibly fish Definitivehosts include carnivores or omnivores including humans and somereptiles and raptorial birds (1) Although others may exist only Sar-cocystis nesbitti hasbeenidentifiedinhumansandnonhumanprimatesserving as intermediate hosts with a snake possibly serving as the defini-

Published 25 February 2015

Citation Fayer R Esposito DH Dubey JP 25 February 2015 Human infections withSarcocystis species Clin Microbiol Rev doi101128CMR00113-14

Address correspondence to Ronald Fayer ronaldfayerarsusdagov

Copyright copy 2015 American Society for Microbiology All Rights Reserved

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tive host However this identification is based on a comparison of avail-ablecongenersthatmostcloselymatchedthoseofspeciesinwhichsnakeswerethefinalhostsandhasyet tobeconfirmedTwospeciesSarcocystishominis and S suihominis have been identified in humans and non-human primates serving as definitive hosts (Fig 1)

Early knowledge of infections in humans is scant because therelationship between infection and symptoms was not under-stood tissue specimens were rare light microscopy (LM) had lim-itations the life cycle was unknown and other diagnostic toolswere not developed The first record of what would become rec-ognized as Sarcocystis was in 1843 by Meischer who observedlong thin white cysts in muscles of a deer mouse in Switzerland(1) For the following 2 decades this parasite with no scientificname was called Meischerrsquos tubules In 1865 a parasite with asimilar appearance in muscles of a pig was then described byKuhn who proposed the name Synchytrium miescherianum (1)However the name Synchytrium was already in use for anotherorganism Thus in 1899 Labbe changed the name to Sarcocystismeischeriana (1) and it became the type species of the genus Inthe following decades many species of Sarcocystis were namedbased on finding intramuscular cysts in various animals and thesewere referred to as sarcocysts In some references to Sarcocystis theterm sarcosporidium was used This possibly resulted from stud-ies in which sarcocysts in culture media appeared to develop hy-phae and mycelia resulting from contamination and Sarcocystistherefore was thought to be a type of fungal organism In 1967electron micrographs clearly demonstrated that the organismscontained within the sarcocysts were not fungal spores but werezoites morphologically similar to those of other apicomplexanprotozoa (2) removing any consideration that Sarcocystis was tax-onomically related to fungi Other life cycle stages remained un-known until the 1970s when zoites freed from sarcocysts in themuscles of grackles (Quiscalus quiscula) developed into sexual-stage parasites and oocysts in cultured mammalian cells (3 4)Additionally sarcocysts from cattle were fed to cats dogs andhumans establishing three distinct species with the proposednames Sarcocystis bovifelis S bovicanis and S bovihominis com-binations representing two hosts (5ndash7) Although these speciesnames were later changed the cumulative findings from this pe-

riod established the requisite relationship of the two-host prey-predator (intermediate host-definitive host) life cycle for all spe-cies of Sarcocystis

Life Cycle Stages

In intermediate hosts including humans only asexual-stage par-asites are found (Fig 2) The initial stages of asexual developmentare known from animal studies but have not been seen in humantissues The following descriptions are based on Sarcocystis cruzidevelopment in cattle Infection begins when oocysts or sporo-cysts in feces from a final host become ingested by a susceptibleintermediate host Exposure to trypsin and bile causes the platesthat form the sporocyst wall to disunite liberating four motilesporozoites contained within The sporozoites pass into orthrough the gut wall and are first found within endothelial cellsthat line small arteries in all parts of the body This is the first ofapproximately four cycles of asexual development called mer-ogony or schizogony the number and timing of which mayvary with the species During each of the first three cyclesnuclear division eventually gives rise to merozoites which aremotile crescent-shaped organisms with a structure similar tothat of sporozoites Subsequent generations are found down-stream in arterioles and then in capillaries and in veins in allparts of the body until the last generation develops in skeletalsmooth and cardiac muscles and sometimes in neural tissuewhere sarcocysts are formed

For S cruzi the first generation is found 2 weeks after inges-tion of sporocysts (Fig 3A) and the second generation is found assingles or pairs of merozoites within mononuclear cells in periph-eral blood nearly 4 weeks after ingestion of sporocysts (Fig 3C) Afew days to a week later the third generation is seen as immaturemultinucleate schizonts or mature schizonts containing merozo-ites in endothelial cells of capillaries throughout the body but theyare especially prominent in renal glomeruli (Fig 3B) Merozoitesfrom these schizonts enter muscle cells where they begin sarcocystformation first differentiating into a single round cell called ametrocyte or mother cell A series of divisions gives rise to numer-ous metrocytes as the sarcocyst grows while concurrently a walldevelops isolating the sarcocyst from the surrounding muscle

FIG 1 Humans as definitive (final) hosts for Sarcocystis species

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(Fig 3D) At the time when metrocytes develop into infectiousbradyzoites also referred to as cystozoites or just zoites the sar-cocyst is considered mature (Fig 3E and F) The maturation timeappears to differ among species and can take 2 months or more tocomplete but the sarcocyst can then persist for months or yearsDepending on the species sarcocysts differ in size and shape frommicroscopic to macroscopic They range from a few micrometersto several millimeters in length range from narrow to wide incircumference and have a great variety of wall structures thatdiffer in thickness and in patterns of peripheral protrusions calledcytophaneres Seven morphologically unique wall structures weredescribed in early reports of sarcocysts found in human muscles(8) (Table 1) but most subsequent reports of intramuscular sar-cocystosis in humans did not identify wall morphology (9ndash31)(Table 2) Some sarcocysts have internal septa that form compart-ments while in others no septa are apparent The septa and cyto-phaneres may be difficult to distinguish by light microscopy andare best seen by electron microscopy Sarcocysts can be found inthe muscles of limbs tongue esophagus diaphragm and heartbut also in neural tissue in the brain spinal cord and Purkinjefibers

Sexual stages occur in definitive hosts After a susceptible hosthas eaten meat containing mature sarcocysts the wall of the sar-cocyst becomes digested or broken Bradyzoites within the sarco-cysts are released and can soon be found intracellularly in villi ofthe small intestine Each bradyzoite transforms into either a mi-crogamont (male) or a macrogamont (female) stage (Fig 3G)Microgametocytes become multinucleate and a sperm-like mi-crogamete forms around each nucleus A single flagellated mi-crogamete finds and fuses with a macrogamont Their nuclei com-bine and the fertilized macrogamont develops into an oocyst thatsporulates in situ forming two sporocysts that each contain foursporozoites (Fig 3H) Although oocysts are immobile they reachthe lumen of the intestine and are excreted with feces sometimesintact with a barely visible wall appearing as a pair of sporocystsor more often the fragile wall breaks and individual sporocystsare released Sporocysts of virtually all species are indistinguish-able from one another measuring 10 by 15 m and containing

four sporozoites and a cluster of residual granules (Fig 3I) Sporo-cysts of S hominis and S suihominis have average sizes of 93 by147 and 105 by 135 m respectively and are immediately in-fectious when excreted (1)

Species Infecting Animals

Some species of Sarcocystis that infect agricultural and companionanimals such as cattle sheep and horses are of economic impor-tance because they cause illness that results in fever lethargy poorgrowth poor feed use reduced milk production lameness wooland hair loss abortion carcass condemnation at meat inspectionas well as death Information obtained from such infections hasbeen helpful in understanding aspects of clinical disease in hu-mans For example data on hematology serum enzyme levelchanges the inflammatory response histopathology the locationand timing of developmental stages the febrile response the neg-ative impact on growth abortion and other factors have been welldocumented from experimental and outbreak studies of sarcocys-tosis in livestock and have been reviewed (1 32)

Species Infecting Humans

Humans can be either final or intermediate hosts (Fig 1 and 2)Humans can become final hosts after eating undercooked porkand beef harboring mature sarcocysts of S suihominis and Shominis respectively Tissues of many species of domesticated an-imals wild mammals birds and reptiles that are eaten for meatthroughout the world contain sarcocysts capable of infecting un-identified final hosts possibly including humans and with un-known health consequences Therefore there may be additionalundocumented species for which humans can serve as a definitivehost Although sporocysts in the feces are diagnostic for Sarcocystisinfections of definitive hosts they are so morphologically similarthat species cannot be differentiated simply by the size and shapeof sporocysts

Within the Sarcocystis life cycle humans who are infected withmuscular sarcocystosis are considered aberrant intermediatehosts because they accidently substitute for the natural hosts thatroutinely serve as prey for a definitive predator host The num-

FIG 2 Humans as aberrant intermediate hosts for Sarcocystis species

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ber of species for which humans can serve as an intermediatehost is unknown but there may be seven or more species basedon differences in sarcocyst wall morphology observed in hu-man tissue specimens (8) Sarcocyst wall morphology has alsobeen used to differentiate species in animals (1) The use ofsarcocyst wall morphology to distinguish species has been con-troversial because morphology can be difficult to discern bylight microscopy can be affected during the processing of tis-sues and can change with the age of the sarcocysts Molecularmethods have been used but have been extremely limitedGreater use will extend and confirm species identity and im-prove diagnosis of infections

Humans have been identified as an intermediate host for Sar-

cocystis nesbitti (26ndash28) based on 18S ribosomal DNA (rDNA)sequence data Sarcocystis nesbitti described by Mandour in 1969was originally detected in muscles from a rhesus monkey based onLM but its taxonomic validity is questionable and there are nei-ther transmission electron microscopy (TEM) morphologicaldata nor LM photographic support for the original descriptionNevertheless the first report of Sarcocystis in nonhuman primates(Macaca fascicularis) in China which was supported by LM andTEM studies (33) was based on the perceived resemblance to Snesbitti so those authors named the organisms that they found inM fascicularis muscles S nesbitti Morphological similarities sug-gested that one species of Sarcocystis might infect Macaca fascicu-laris Macaca mulatta Papio papionis Cercocebus atys as well as

FIG 3 Sarcocystis stages in tissues of intermediate hosts (A to F) and definitive hosts (G to I) Panels A to G show hematoxylin-stained images All images are ofS cruzi except panel E which is an image of S hominis (A) Artery with a first-generation multinucleate schizont (arrow) in an endothelial cell (B) Kidneyglomerulus with immature (arrowhead) and mature (arrow) second-generation schizonts (C) Blood smear with a merozoite in a mononuclear cell (D) Heartwith an immature sarcocyst containing globular metrocytes (E) Skeletal muscle with a cross section of a mature sarcocyst with a thick striated wall surroundedby a mononuclear cell infiltrate (F) Skeletal muscle with longitudinal and cross sections of sarcocysts The was no inflammatory response (G) Lamina propriaof small intestine with a macrogametocyte (arrow) (H) Small intestine with sporulated sporocysts (arrow) (Whipfrsquos polychrome stain) (I) Phase-contrastmicroscopy of two sporocysts in a fecal float

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humans (34) Sarcocysts in muscles from M fascicularis identifiedas S nesbitti by Yang et al (33) were later examined by molecularmethods (34) and 18S rDNA sequence data from two sarcocystsplaced this species in a cluster with S atheridis and S singaporensisspecies with rodent intermediate hosts and snake definitive hostsThis suggested that a final host for S nesbitti might be a snakePCR evidence of Sarcocystis was found in feces from a cobra (26)the 18S rDNA sequence clustered with Sarcocystis sequences fromother snakes and with the two S nesbitti sequences obtained fromM fascicularis by Tian et al (34) Three reports from the PangkorIsland outbreak in Malaysia reported similar findings Muscle bi-opsy specimens from the swollen jaw of one patient and the leg ofanother showed intramuscular sarcocysts identified by LM and

TEM (26) The 18S rDNA sequences of Sarcocystis from thesepatients varied 1 from each other and a BLAST analysis foundthat they shared 99 homology with S nesbitti from the muscle ofM fascicularis (26) Another report also identified a patient withsarcocysts in the temporalis muscle and another with sarcocysts ina leg muscle for which DNA sequences matched 100 of those forS nesbitti in the clade with S atheridis (25) Still another study (27)reported the same 18S rDNA findings as those reported by Abu-Bakar et al (25) and Tian et al (34) The 18S rDNA sequence fromthe muscle biopsy specimen of a patient who had visited TiomanIsland in Malaysia also showed 100 homology with the S nesbittigene sequence reported under GenBank accession numberHF544323 (28)

TABLE 1 Summarization of early reports of humans with sarcocystsc

Country or regionPatient age (yr)gender Sarcocyst location(s) Biopsy or autopsy Sarcocyst typeb Original author(s) yra

Sudan 36 M Abdomen A 2 Kartuli 1893France Adult M Larynx A 1 Barbaran and St Remy 1894France Adult unknown Skeletal muscle A 1 Vuillemin 1902Malaysia 30 M Tongue A 4 Darling 1919UK Unknown Heart A 6 Manifold 1924India 55 M Chest B 2 Vasudevan 1927USA via West Indies 32 F Heart A 7 Lambert 1927Indonesia 20 M Cheek B 4 Bonne and Soewandi 1929China Adult M Leg B 1 Feng 1932UK Adult F Heart A 5 Hewett 1933Panama 11 F Heart A 7 Gilmore et al 1942Panama 48 F Heart A 7 Kean and Grocott 1943Brazil 32 F Heart A 7 DeFreitas 1946USA via Germany 31 M Heart A 7 Arai 1949USA via Puerto Rico 34 M Heart A 7 Arai 1949India 37 M Leg B 2 Dastur and Iyer 1955India 20 M Leg B Dastur and Iyer 1955Sudan 45 M Foot B 3 McKinnon and Abbott 1955UK via India 60 M Pectoral B 2 McGill and Goodbody 1957Brazil 40 F Heart A 6 Koberle 1958Italy 17 F Heart A 5 DrsquoArrigo and Squillaci 1962Indonesia 51 M Pectoral B 4 Van Thiel and Van den Berg 1964UK via Southeast Asia 51 M Leg B 4 Mandour 1965Angola 30 F Chest B 2 Liu and Roberts 1965India 22 F Leg arm B 2 Gupta et al 1973Southeast Asia 21 M Leg B 3 Jeffrey 1974UK via Malaysia 34 M Pectoral B 4 Jeffrey 1974Malaysia 34 M Larynx B 4 Kutty and Dissanaike 1975Malaysia 12 F Pharynx A 4 Kutty et al 1975India 56 M Arm B 3 Agarwal et al 1976India 54 F Leg B 3 Thomas 1976Malaysia 20 M Foot B 4 Prathap and Dissanaike 1976Malaysia 23 M Neck A 4 Prathap and Dissanaike 1978Unknown Unknown Skeletal muscle A 4 Frenkel 1976USA via Asia 40 M Arm B 4 McLeod et al 1979Uganda 50 M Leg B 1 Beaver 1979India 50 M Arm B 3 Beaver 1979Singapore Unknown Skeletal muscle B 4 Beaver 1979Singapore Unknown Skeletal muscle B 4 Beaver 1979Costa Rica 9 M Heart A 6 Beaver 1979a Original authors and years can be found in reference 8 and not all of these are included in the list of references in this studyb These types described by Beaver et al (8) differ from those described by Dubey et al (1) and are defined as follows type 1 thick radially striated wall large zoites often sparse inthe center and metrocytes type 2 generally large sarcocysts thin and smooth wall medium zoites and septa type 3 small and medium sarcocysts thin wall medium zoites andsepta type 4 long and medium sarcocysts thin wall small zoites and septa evident in center type 5 small sarcocysts thin wall medium zoites and in myocardium type 6 small tomedium sarcocysts thin wall large zoites and in myocardium type 7 small sarcocysts thin wall small zoites and in myocardiumc Data were compiled from reference 8 Abbreviations A autopsy B biopsy F female M male




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Sources of Intestinal and Muscular Sarcocystosis

The only source of intestinal sarcocystosis is ingestion of meatcontaining mature sarcocysts The range of meats and meat prod-ucts consumed by humans worldwide includes domestic and wild

animals of many species Although only two species are known toinfect humans as definitive hosts S hominis from beef and Ssuihominis from pork many others may exist throughout theworld but are as yet undefined

TABLE 2 Summary of reports of muscular sarcocystosis in humans not included in the review by Beaver et al and presented in chronological orderof publication

Country or regionDescription of human subject(s) orspecimen(s) Sarcocyst location Biopsy or autopsyc

Reference yr ofpublication

Malaysia 58-yr-old Ma Tongue B 9 1981

India 2 persons Leg B 10 1983Gluteus B

Denmark 4 of 112 specimensb Muscle A 11 1985

Malaysia 45-yr-old Ma Nasopharynx B 12 198753-yr-old Ma Nasopharynx B

Malaysia 1 person Skeletal muscle B 13 1988

Australia via Thailand 31-yr-old M Skeletal muscle B 14 1990

Egypt 1 person Skeletal muscle B 15 1990

Malaysia 45-yr-old Ma Tongue B 16 199267-yr-old Fa Tongue B32-yr-old Fa Pectoral muscle B

Malaysia 21 persons aged 16 to 57 yr Tongue A 17 1992

Belgium via Brazil Kenyaand Tanzania

31-yr-old M Thigh B 18 1995

India 40-yr-old M Thigh B 19 199614-yr-old F Arm B52-yr-old F Thigh B23-yr-old F Arm B

Malaysia 44-yr-old Fa Thigh B 20 199819-yr-old F Calf B

Malaysia 7 adults M 1 muscle B 21 1999

Thailand 66-yr-old Ma Larynx B 22 2011

India 20-yr-old M Arm B 23 2012

India 50-yr-old M Neck B

India 47-yr-old M Leg B 24 2013

Pangkor Island Malaysia 89 people Leg B 25 201326 201427 2014

Tioman Island Malaysia 39 F and 29 M subjects aged 4 to 72 yr Skeletal muscle from 15 patients 1PCR positive

B 28 2014

29 2014

Tioman Island Malaysia 3 F and 3 M subjects Febrile myositis syndrome NTE 30 2014

Tioman Island Malaysia 26 cases in Germany reported previously Symptomatic changes skeletal muscle B 31 2014a Cancer patientsb Tissues examined by trichinoscopyc NTE no tissue examined

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The source of muscular sarcocystosis is ingestion of sporocystsmost likely through contaminated water or fresh produce or pos-sibly through exposure to a contaminated environment It is dif-ficult to predict for unnamed species of Sarcocystis how specificeither the intermediate or the final host species must be but thereare some generalized patterns Dogs coyotes and foxes but nothumans or cats are final hosts for S cruzi with intermediate hostsbeing restricted to cattle and bison but not sheep monkeys pigsor rats Intermediate hosts of S odocoileocanis include white-taileddeer sheep and cattle There are other examples in which clustersof related host species serve as either intermediate or final hostsBased on the likelihood that one species of Sarcocystis can infectmultiple closely related host species some species of Sarcocystisthat infect nonhuman primates might also be expected to be ableto infect humans This is true for S nesbitti a species found inmuscles of macaques and recently in humans snakes and possiblyother reptiles may serve as definitive hosts (33 34) Because mostcases of human muscular sarcocystosis have been found in tropi-cal areas inhabited by many species of nonhuman primates andreptiles and because some locations could be subject to contam-ination from reptilian feces the combination of these factors ap-pears conducive to human infection

PREVALENCE SYMPTOMS AND DIAGNOSIS OF INFECTIONIN HUMANS

Intestinal Sarcocystosis Species and Symptoms

Humans with intestinal sarcocystosis (Fig 1) have been identifiedworldwide with the exception of Africa and the Middle East al-though such infections likely occur there given customs of eatingraw or undercooked meat in those areas Locations where cases ofintestinal sarcocystosis have been reported are listed in Table 3including infections that resulted after volunteers ingested natu-rally infected or experimentally infected meat (6 7 35ndash68) Earlyinvestigators with no knowledge of the Sarcocystis life cycle ob-served two parasites with characteristics of apicomplexan oocystsin stool samples of infected persons and named one Isospora belliwhich was excreted as a distinctive unsporulated (internally un-differentiated) oocyst unique in size and shape and unlike anyother apicomplexan parasite The other coccidian parasite ex-creted as a sporulated oocyst (containing sporocysts with sporo-zoites) or as individual sporocysts was named Isospora hominis(35 37 39 44) and represented what is now recognized as multi-ple species of Sarcocystis two of which are known to be S hominis(6 40 41 46ndash48 51 53 54 58 59) and S suihominis (6 40 50 5362) However other species may have been present because theoocysts and sporocysts of Sarcocystis species are morphologicallyindistinguishable Most reports cite infections in persons in Euro-pean countries including The Netherlands Germany PolandSlovakia France and Spain (Table 3) In Asia infections havebeen reported in China Tibet Laos and Thailand (Table 3)Other cases have been reported in Australia Argentina and Brazil(Table 3)

As definitive hosts humans can experience nausea vomitingacute and severe enteritis or chronic enteritis but many infec-tions appear to be mild or asymptomatic Differences depend onthe number and perhaps the species of sarcocysts ingested Fewaccurate data are available on the duration of infection or thenumbers of oocysts and sporocysts excreted Most case studiessuffer from not knowing the time of onset of infection the type or

quantity of meat consumed the species and number of sarcocystsconsumed and whether a patient ingested raw meat once or mul-tiple times The longest period of continuous sporocyst excretion(I hominis) was 21 months or more for a patient in The Nether-lands while other patients excreted sporocysts for at least 6months (35) A patient in Poland excreted sporocysts for at least12 months (36) However the most reliable information on theprepatent and patent periods is from human volunteer studies InGermany diaphragms from cattle and pigs were obtained from anabattoir ground in a meat grinder and found to contain zoites ofSarcocystis This ground meat was then fed to volunteers who werenot excreting oocysts or sporocysts in their stools (6) In the firstexperiment two volunteers ate 500 g of raw beef diaphragm withonions and spices and began excreting sporocysts 9 days latercontinuing for 40 days or longer In the second experiment fourvolunteers ate seasoned raw pork diaphragm and began excretingsporocysts 9 13 and 17 days later the fourth person remaineduninfected The patent period for the three volunteers was at least30 days For a volunteer in China who ingested S suihominis-infected pork the prepatent period was12 days and the patentperiod was 120 days (50) Another volunteer excreted sporo-cysts from days 8 to 40 after eating beef (51) Two other volunteersin China who ate beef and three who ate water buffalo had prepat-ent periods of 10 to 12 days and patent periods of 11 to 29 days(57) Another volunteer in China excreted sporocysts of Ssuihominis for an estimated 91 days beginning 10 days after eatingpork (62) Of seven volunteers in Brazil who ate raw kibbe (beef)six began to excrete S hominis oocystssporocysts 10 to 14 dayslater and excreted them for 5 to 12 days (58)

Intestinal Sarcocystosis in Europe

In The Netherlands oocysts and sporocysts were identified as Ihominis in stool samples of 17 of 72 persons some without illnessand others suspected of suffering from chronic amoebiasis addi-tionally in 5 of 17 subjects intestinal mucosa scrapings taken atautopsy contained sporocysts of I hominis (35) Also in TheNetherlands and in various other countries between 1960 and1970 several surveys were conducted in which stool samples fromhumans were examined (69) Ten percent to 50 of personsexcreting sporocysts were in countries where raw meat was usuallyconsumed In a subsequent survey in The Netherlands babiesborn to mothers who excreted sporocysts began excreting sporo-cysts at 9 to 10 months of age correlating with them being fed rawor partially cooked minced beef (69) In Poland a 29-year-oldwoman working in an orphanage had single and double sporo-cysts in her feces for 12 months (36) which could have resultedfrom repeated reinfection Neither her family nor her coworkerswere found to be positive but later 7 persons at the orphanagewere found to be infected and at other locations in Szczecin Prov-ince 92 additional persons were found to be infected

In Germany of 150 stool samples examined I hominis wasdetected in 12 persons who had eaten raw beef or pork (38) Six ofthe 12 persons had different gastric or intestinal symptoms and 6were asymptomatic Also in Germany a volunteer consumed 100to 200 g of raw beef naturally infected with S hominis or meatfrom cattle experimentally infected with S hominis for 1 to 3 dayson four separate occasions at intervals of several months (40) Thevolunteer had low-grade clinical symptoms of stomachache nau-sea and diarrhea beginning 3 to 6 h after meat consumptionsymptoms lasted 24 to 36 h Diarrhea and stomachache were again




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present when most sporocysts were excreted 14 to 18 days after themeat was consumed Again in Germany three volunteers whoconsumed 100 to 400 g of raw minced pork from pigs heavilyinfected with S suihominis became symptomatic beginning 6 to8 h later with diarrhea dyspnea vomiting bloat nausea stom-achache inappetence and rapid pulse (40) Symptoms continuedup to 48 h Well-cooked pork from the same pigs caused no clin-ical symptoms in nine other volunteers who ate the meat Based onthese observations S suihominis was considered either patho-genic or toxic for humans Others concluded that such patholog-ical effects were due to toxicity (69)

In eastern Slovakia a 12-year-old girl hospitalized for tubercu-losis was incidentally found to be excreting oocysts and sporocystsof I hominis in her stool (44) In central Slovakia of 1228 Viet-namese workers who immigrated over a period of 18 months 14excreted sporocysts of Sarcocystis for a mean of 49 days with nogastrointestinal symptoms (52)

Intestinal Sarcocystosis in Asia

In Thailand six patients 3 to 70 years of age with acute enteritisand leukocytosis underwent resection surgery of the ileum (48)The histopathological diagnosis indicated segmental eosinophilicenteritis or segmental necrotizing enteritis Sexual stages and de-veloping oocysts resembling those of Sarcocystis were observed inresected tissues from one patient and sporocysts and numerousGram-positive bacilli were observed in tissue samples from fiveothers Because sarcocysts were present in local market beef fromBos indicus cattle and the patients ate raw beef in chili dishes theauthors of that report concluded that the cattle-human parasite Shominis was responsible for the infections In northern ThailandSarcocystis was found in 232 of stool samples from 362 asymp-tomatic laborers 833 of whom were males (55) Of 253 stoolsamples from 140 female and 102 male villagers 2 to 80 years of agein Kaen Province northeastern Thailand 04 were positive forS hominis (66) Of 479 stool samples collected from rural UbonRatchathani Province and 1124 stool specimens from Khon Kaenin Thailand 46 and 8 were positive for Sarcocystis (63) Thesefindings and others (55 66) suggest that northern Thailand is anarea where enteric sarcocystosis is endemic In neighboring Laosstool samples from 1008 persons were examined and S hominiswas present in 10 of samples from persons 20 years of age(54)

In Tibet stool specimens from 926 persons from Linzhi Milinand Duilongdeqing counties were examined by the zinc sulfateflotation method and S hominis was detected in 205 to 229 ofthe specimens in the three counties (53) S suihominis was de-tected in 70 06 and 0 of the specimens respectively (53) Caseswere usually asymptomatic and most became negative after anundisclosed treatment

In China of stool specimens examined from 12 persons singleand double sporocysts were found in specimens from two men(49) No information was provided for one man but the other 48years of age had abdominal distention and pain with alternatingdiarrhea and constipation and with stomachache and dyspnea Hehad eaten raw pork between 13 and 65 days before his examina-tion and because he also had ova of Ascaris in his feces the sporo-cysts were assumed to be those of S suihominis However thepresence of Ascaris cannot be accepted as a valid reason for assum-ing that sporocysts were S suihominis without additional infor-mation In Yunnan Province China a volunteer developed diz-T

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ziness abdominal pain anemia and diarrhea 3 days afterconsuming 60 g of raw beef from a calf experimentally infectedwith S hominis (51) Also in China three volunteers consumed1500 sarcocysts in skeletal muscles from naturally infected cat-tle and two other volunteers ingested 14000 sarcocysts in waterbuffalo meat (57) Beginning a week after ingestion and endingspontaneously 3 weeks later symptoms included abdominal painand swelling diarrhea and eosinophilia In Guangxi China avolunteer who ate fresh pork containing sarcocysts of S suihomi-nis had abdominal distension beginning 5 h later and from 8 to 36h he had watery diarrhea followed by fever chills dizziness head-ache muscle joint and upper abdominal pain as well as loss ofappetite (62) Another volunteer in China who ingested raw beefdeveloped abdominal distention on the day that he consumed iton the following day he had stomach pain and diarrhea that lastedfor 28 days (65) Sarcocystis hominis sporocysts were found in stoolsamples 11 to 29 days after consumption of beef (65) In twocountryside villages in Guangxi 22 men and 5 women out of 501persons examined were excreting oocysts identified as Sarcocystissuihominis based on the finding that all persons had a history ofeating raw pork (60) Of 247 men and 254 women in that study 26persons with positive specimens were 30 years of age 8 haddiarrhea and abdominal pain 1 had only abdominal pain and theothers had no symptoms It is not clear if those authors revisitedone of the same villages but similar results were reported inwhich 32 of 489 fecal specimens from the Zhuang ethnic popula-tion were found to be positive for S suihominis (61)

In India the prevalence of S suihominis in pigs and humans washigh in an economically deprived sect (70 71) probably linked toslaughter practices A selected group of 20 children between 3 and12 years of age belonged to families who reared pigs and slaugh-tered them in their backyard for selling pork for human consump-tion (71) The children of these families consumed the offal in-cluding parts of the tail which they ate raw with salt The stools ofthese children were examined daily for 2 weeks and 14 childrenall of whom complained of abdominal pain and diarrhea excretedsporocysts of Sarcocystis (71)

Intestinal Sarcocystosis in Australia

At a local hospital servicing five aboriginal communities in West-ern Australia a 4-year parasitological survey was conducted inwhich fecal specimens from 385 children and adults were exam-ined (56) Sarcocystis detected in 2 specimens was attributed toadverse living conditions and inadequate hygiene

Intestinal Sarcocystosis in North and South America

In each of two studies a human volunteer and two dogs ate beefproducts from a retail grocery store in Maryland and feces wereexamined daily for 3 weeks thereafter (45) In the first study 227g of undercooked roast beef was eaten daily for 5 days and in thesecond study 227 g of raw ground beef was eaten daily for 3 daysBecause both dogs in both studies became infected whereas thehuman volunteer did not the findings suggested that S cruzi waspresent and infectious in both types of beef Neither the dogs northe volunteer exhibited any clinical symptoms of infection

Sarcocystosis was detected in stool and in duodenal and liverbiopsy specimens from a 31-year-old AIDS patient in Argentinawho had chronic diarrhea hepatitis and muscle pain (64) Sexualstages were seen in the lamina propria sporulated oocysts werefound in the stools and schizont-stage parasites were seen in the

liver However the illustrated objects do not appear to be schi-zonts and other findings are inconsistent with what is known ofthe life cycle Because those authors provide no explanation forthese differences the conclusion that these stages represent Sarco-cystis is considered doubtful A second unrelated infection withanother protist might explain this inconsistency In 25 Arabianrestaurants in Brazil Sarcocystis was found in 50 samplings ofkibbe (58) During a second period of collection of four men andthree women volunteers who ate between 128 and 260 g of kibbesix excreted S hominis oocystssporocysts in stools Two volun-teers had clinical symptoms one had abdominal pain 1 day laterand diarrhea for the first 3 days after eating the kibbe and theother had diarrhea 11 days after eating the kibbe

Diagnosis of Intestinal Sarcocystosis

The basis for a presumptive diagnosis of intestinal sarcocystosisincludes enteritis and a history of having consumed undercookedmeat although infected persons can be asymptomatic Confirma-tion requires identification of oocysts and or sporocysts in thestool Sporocysts with sizes of 10 by 15 m are easily seen by LMin a wet preparation just below the coverslip in a droplet of aspi-rated fluid from the surface of a fecal float and will autofluorescewhen viewed by fluorescence microscopy Flotation is performedby mixing feces with concentrated solutions of zinc sulfate su-crose sodium or cesium chloride Percoll or similar high-densitysolutions followed by centrifugation at 500 g to sediment fecaldebris while concentrating the parasites at the surface (1) Speciescannot be distinguished from one another by this method becausethey are so similar morphologically The presence of asexual stagesand sporulated oocysts in the intestine is more applicable for post-mortem diagnosis but biopsy or postsurgical specimens can re-veal the presence of infection when stool specimens appear nega-tive

Extraintestinal Sarcocystosis

Humans can become infected with unknown numbers of Sarco-cystis species acquired by ingesting contaminated food or watercontaining sporocysts excreted by infected carnivores (Fig 2) Insuch cases humans serve as an accidental and aberrant interme-diate host replacing the intermediate host found in nature Basedon studies of animal intermediate hosts multiple generations ofasexual reproduction develop in the vascular endothelium and incirculating monocytes followed by the development of sarcocystsin myocytes of skeletal cardiac and smooth muscle Based onanimal studies sarcocysts are the end stage in intermediate hostsSarcocysts may rupture from time to time but the released brady-zoites die and are not known to initiate new infection

Until recently 100 humans had been diagnosed with muscu-lar sarcocystosis (32) Most cases were diagnosed by use of inci-dental biopsy specimens with no associated clinical symptoms orat autopsies in tropical countries of which nearly 50 worldwidewere in Malaysia (8 16 17 22 24 72) Of the 40 infections re-viewed by Beaver et al (8) 13 8 5 4 4 3 and 1 were probablyacquired in Southeast Asia India Central or South America Af-rica Europe the United States and China respectively Reportsfrom Africa the Middle East and Central and South Americacontinue to be rare or lacking Examination of tongue muscleobtained at autopsy was extrapolated to suggest a sarcocystosisprevalence rate of 21 among Malaysians (17) although noneof the 1500 muscle biopsy specimens from limbs of patients




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with various muscle diseases acquired over a 20-year period at theMedical Centre of the University of Malaya are reported to haveyielded sarcocyst-positive tissues (25) Until the 21st century only10 cases were reported to be symptomatic with acute muscularsarcocystosis (18 19 21 73) All infections in humans until 2013were reported as intramuscular sarcocysts of unknown speciesSince then studies of two separate outbreaks in Malaysia haveidentified S nesbitti as the causative species and one capable ofinfecting humans (25ndash28)

Diagnosis during the early period leading to muscular infectionis difficult because symptoms are nonspecific Based on observa-tions from outbreaks and experimental animal studies muscularsarcocystosis might be suspected when a patient presents with ahistory of travel or residence in a tropical country especially inSoutheast Asia and with various combinations of fever myalgiaheadache cough episodic weakness or fatigue and arthralgia (2127 28) This early phase of disease also might not present withobjective laboratory abnormalities Nonspecific and slightly ele-vated levels of hepatic enzymes (aspartate aminotransferase [AST]and alanine aminotransferase [ALT]) inflammatory markers (C-reactive protein and erythrocyte sedimentation rate [ESR]) ormarkers of general cell damage (lactic dehydrogenase [LDH])might be encountered Later with the onset of myositis muscletenderness upon physical examination and possibly elevated se-rum creatinine phosphokinase (CK) levels and blood eosinophiliamight be found With negative test results for Toxoplasma andTrichinella a presumptive diagnosis of sarcocystosis should beentertained The detection of sarcocysts in a muscle biopsy speci-men would confirm the diagnosis although parasites might bediffusely distributed and difficult to find Magnetic resonance im-aging (MRI) has been suggested to be of benefit in guiding thechoice of muscle biopsy site (27) although there is no evidenceshowing this method to be superior to guidance using physicalexamination findings such as palpation to locate a point of max-imal tenderness visual observation to identify regions with swell-ing or touch to identify areas of increased warmth LM examina-tion of stained histological sections and those with a positiveperiodic acid-Schiff reaction of the sarcocyst wall facilitate identi-fication Although eosinophilic myositis muscle inflammationand necrosis and interstitial and perivascular inflammation canbe seen in some cases inflammatory cells are not often observed inclose proximity to sarcocysts (21 27 28 74)

An accurate and sensitive diagnostic test is needed to improvediagnosis Enzyme-linked immunosorbent assays (ELISAs) im-munofluorescence assays (IFAs) and other serologic tests forantibody to Sarcocystis using bradyzoite antigen have been limitedto specialized laboratories have not been standardized are notwidely available and have other inherent problems (75) Most ofthese tests no longer exist because there has been little or no con-tinued demand for their use In addition the specificity of sero-logic assays for muscular versus intestinal sarcocystosis has notbeen proven and cross-reactivity with other apicomplexans couldbe problematic Development of a molecular method to detectSarcocystis DNA in human blood or muscles could facilitate earlydiagnosis by expeditiously confirming the cause of the infectionand identifying the species involved all in one test PCR has beenapplied for diagnostic blood testing in animals and might have thecapability of detecting low numbers of circulating parasites at anearly stage of infection during merogony at a point before entryof the organism into muscles (76)

Outbreaks and Case Descriptions

Much can be learned of the clinical signs of intramuscular sarco-cystosis the potential routes of infection and the sources of infec-tion from outbreaks A series of outbreaks in Malaysia have beenrecorded (21 25ndash30)

During a civic project in 1993 in Malaysia seven members of aUS Air Force team were deployed for 1 week 80 km northeastof Kuala Lumpur in or near a jungle village (21) The seven per-sons had extensive opportunity for potential exposure to sporo-cysts in the environment from working shirtless and shoeless dur-ing heavy monsoon rains by exposing themselves to possiblycontaminated swimming and drinking water and soil and by eat-ing fresh vegetables that might not have been well cooked Within3 weeks after returning from deployment two members of thejungle cohort presented with acute fever myositis and broncho-spasm with elevated liver enzyme levels and eosinophilia Sevenmembers of the jungle cohort one of whom was asymptomaticwere tested for eosinophilia sedimentation rate and serum en-zyme levels including ALT CK LDH and AST levels and virtu-ally all subjects had at least some levels elevated above normal Thetiming of these laboratory determinations with respect to symp-tom onset or time beyond departure from the jungle area was notreported Four subjects developed bronchospasm myalgia skinlesions and swollen lymph nodes within 2 months after leavingMalaysia which waxed and waned over the following 6 monthsbut two were much more symptomatic with intermittent feversmyalgias arthralgia muscle wasting weight loss of 6 to 9 kg fa-tigue headache and rashes One of these two subjects remainedsymptomatic for several years with a waxing-waning course thispatient underwent a muscle biopsy 3 months after illness onsetand sarcocysts were observed histologically About a year laterpossible Sarcocystis-related myocarditis was diagnosed based onborderline left atrial enlargement with electrocardiogram (ECG)abnormalities These cardiac abnormalities subsided over the fol-lowing year but 5 years from the onset of illness he still reportedoccasional episodes of pruritus abdominal tenderness and sub-cutaneous nodularity

Another outbreak of muscular sarcocystosis included collegestudents and teachers who visited Pangkor Island in the MalaccaStrait of Malaysia (25ndash27) Of 92 persons who attended a retreaton the island 89 became symptomatic within 26 days after leavingthe island Symptoms included fever (94 57 relapsing) myal-gia (91) headache (87) and cough (40) Eight persons withfacial swelling for 4 to 6 weeks showed changes in their muscles ofmastication by whole-body MRI consistent with inflammatoryedema (27) Similar findings were observed for the back musclesof four persons and the calf muscles of two others Four symptom-atic patients underwent muscle biopsy Of these patients at leastone sarcocyst was observed in the biopsy sections of three patientsa fourth specimen was definitively determined to be positive byPCR Of the four patients with confirmed muscular sarcocystosistwo had elevated serum CK levels and three had eosinophiliahowever the timing of these laboratory investigations was not welldescribed (27) Sequences of 18S rRNA extracted from groundtemporalis muscle tissue excised from one patient and from legmuscle of another matched 100 with sequences reported forSarcocystis nesbitti (34) suggesting that sporocysts in snake feceswere the probable source of infection Although snake feces werecollected from several sites in Malaysia including Pangkor Island

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Sarcocystis sporocysts were not recovered but PCR evidence of Snesbitti was found in feces of a cobra (Naja naja) collected inpeninsular Malaysia (26)

Two waves of infection in 2011 and 2012 involved 99 touristswho vacationed on Tioman Island in the South China Sea off theMalaysian coast all subjects were Europeans except for two resi-dents of Canada and a British resident of Singapore (28) Sixty-eight patients met the case definition with myositis eosinophiliaand negative trichinellosis serology Diagnosis of myositis re-quired at least one of the following signs a complaint of musclepain with a serum CK level of 200 IU per liter muscle tendernessdocumented upon physical examination or histological evidenceof myositis in a muscle confirmed by biopsy Sixty-two patientswere considered probable cases and six cases were confirmed byhistological observation of intramuscular cysts compatible withsarcocysts Symptoms that clustered during the second week andthe sixth week after returning from the island included fever(82) myalgia (100) and headache (59) similar to thesymptoms of visitors to Pangkor Island as well as fatigue (91)and arthralgia (29) Blood eosinophilia and elevated serum CKlevels were first observed during the fifth week postdepartureDNA recovered from sarcocysts in one biopsy sample identifiedthe infecting species as Sarcocystis nesbitti These first two waves ofinfection in 2011 and 2012 were associated with travel during thesummer No patients meeting the case definition were reported in2013 but a series of infections in travelers returning to Germanyfrom the same island was diagnosed beginning in the early springof 2014 (30)

Additional data collected from 39 German patients with a his-tory of travel to Tioman Island during 2011 to 2014 some ofwhom were included in the first report (28) were examined lon-gitudinally (31) These patients had periods of illness from rang-ing from 0 to 23 months (median duration 22 months) with17 having symptoms lasting 6 months Two patients had un-resolved but diminished symptoms at 13 and 23 months Themedian severity of pain on a scale of 0 to 10 was 6 (range 0 to 10)This was the first study of the duration of muscular sarcocystosisin multiple patients

Sarcocystosis and Cardiomyopathy

In 11 of the 40 cases cited by Beaver et al (8) sarcocysts werefound in heart muscle at autopsy Sarcocysts appeared to be ofthree morphological types suggesting three possible speciesSeven persons were from the Caribbean and Central and SouthAmerica In one case an 8-year-old boy in a hospital in Costa Ricawas diagnosed with cardiac insufficiency and died 13 days later(8) One year earlier he had been diagnosed with rheumatic feverThe autopsy revealed bilateral pulmonary thrombosis with infarc-tion and chronic cardiopathology Histopathology revealed nu-merous sarcocysts in cardiac muscle with no associated inflam-matory reaction The morphology of the sarcocysts resembled thatof sarcocysts found in myocardium in two other autopsy casesone of whom had sarcocysts in Purkinje fibers

Of the 68 confirmed cases associated with the outbreak on Tio-man Island Malaysia 10 patients had a mildly elevated CK MBfraction (ie the bound combination of isoenzymes creatininephosphokinase M and creatinine phosphokinase B) and 8 pa-tients had a normal electrocardiogram echocardiogram or tro-ponin level but none were considered to have cardiac pathology(28) One patient had an echocardiogram showing mild dilatation

of right ventricular outflow and was thought to have mild myo-carditis which ultimately resolved

Sarcocystosis and Glomerulonephritis

Although glomerulonephritis associated with acute sarcocystosiswith schizonts in the glomeruli is characteristic of S cruzi infec-tion in cattle there is only one human case in which a 47-year-oldIndian man with intramuscular sarcocysts and glomerulonephri-tis was described (24) Whether the two were related or coinciden-tal could not be established

Sarcocystosis and Malignancy

Several cases of sarcocystosis have been detected in patients withvarious types of cancer

At this time insufficient data are available to clearly link sarco-cystosis as an underlying cause or consequence of malignancy

In Malaysia when a patient with a malignant brain melanomawas examined to find the primary tumor site sarcocysts were dis-covered in the nasopharynx and oropharynx (77) Subsequentlyin Malaysia 8 of 11 muscular sarcocystosis cases were personswith malignancies mostly those of the nasopharynx and tongue(16) In Malaysia and other parts of Southeast Asia many resi-dents chew betel leaves in combination with other ingredientssuch as tobacco In Sri Lanka for example a high prevalence ofpotential oral malignancies was associated with betel-quid chew-ing (78) so factors other than sarcocystosis that might contributeto malignancy cannot be ignored Another case of malignancywith intramuscular sarcocysts that was reported in Malaysia in-volved a 44-year-old woman with progressive swelling pain andweakness of the midthigh this was diagnosed as a malignant his-tiocytoma with sarcocysts in muscle fibers deep within the lesion(20) Of 1063 laryngeal biopsy specimens examined in Thailandonly a single case of sarcocystosis concomitant with squamous cellcarcinoma of the larynx was found (23) These contrasting find-ings provoke several hypotheses (i) immunosuppression associ-ated with malignancy might facilitate opportunistic parasitismwith Sarcocystis (ii) sarcocystosis might cause malignancy or (iii)sarcocystosis in cancer patients might be coincidental in locationswhere there is a high prevalence of sarcocystosis Ultimately Shek-har et al (20) concluded that there was no evidence of tissue reac-tion at the site of the parasite to induce neoplastic changes Thoseauthors did not consider the possible effect of earlier developmen-tal stages or of other environmental or cultural factors For exam-ple areca nut sometimes mixed with tobacco slaked lime andvarious spices is chewed by millions of Indo-Asians and isstrongly associated with cancer risk (79)

IMMUNITY PROPHYLAXIS AND TREATMENT

Intestinal Sarcocystosis

Although intestinal infections do not involve multiplication de-velopment in the intestine consists of either a male or female stagefrom each bradyzoite within a sarcocyst Therefore such infec-tions are self-limiting Although some infections appear to persistfor long periods others might actually be the result of reinfectionand the lack of protective immunity A report of a volunteer whorepeatedly infected himself by consuming sarcocysts in pork andbeef suggests that there is little or no protective immunity to re-peated intestinal infection (40) Neither prophylaxis nor thera-




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peutic treatment for intestinal sarcocystosis of either animals orhumans has been developed

A patient with enteritis was diagnosed with Strongyloides sterco-ralis and I hominis (Sarcocystis) infection and was treated withdithiazanine but Sarcocystis persisted (35) Pyrimethamine pre-scribed at 37 mg daily for 5 days and then at 25 mg daily for 10 daysin combination with sulfisoxazole at 3 g per day for 14 days wasalso not successful (44) A volunteer who ingested S suihominissarcocysts was treated with acetylspiramycin for 15 days at a doseof 02 g four times a day but excretion did not stop until 30 dayslater (62)

Muscular Sarcocystosis

There are no vaccines to provide protection against muscular sar-cocystosis but protective immunity following an initial infectionhas been demonstrated in animals Prophylaxis for muscular sar-cocystosis was successful when the anticoccidial drugs ampro-lium salinomycin and halofuginone designed to prevent Eimeriainfections in poultry and livestock were administered at the timeof experimental infection in animal studies (80ndash83) Activityagainst the early development of asexual stages has been foundbut efficacy for therapeutic treatment once intramuscular cyst for-mation has begun has not been investigated under experimentallycontrolled conditions When salinomycin was administered tolambs for 29 days beginning 1 day before 100000 or 1 million Stenella sporocysts were fed clinical sarcocystosis was reduced butcompletion of the life cycle by some of the parasites was not pre-vented At 63 days after the initial infection lambs given salino-mycin were challenged with 1 million S tenella sporocysts andwere found to have developed protective immunity (82) Thismight explain at least in part why foreign tourists to TiomanIsland and not the local indigenous population became ill if it isassumed that the local indigenous population was infected sometime earlier (28 84) and why native Malaysian students did notappear to become as ill as the foreign students during the PangkorIsland outbreak (27)

Severe Sarcocystis myositis in two dogs with fever lymphopeniathrombocytopenia and elevated ALT and CK levels was con-firmed by muscle biopsy (85) Treatment with anti-inflammatorydrugs and clindamycin was unsuccessful One dog recovered aftertreatment with decoquinate (an anticoccidial drug) The otherdog died Consequently it is not clear if any antiparasitic drugsused for treatment after sarcocysts form are effective or if waningsymptoms are the natural course of the infection

Treatment of a patient involved in the outbreak among US AirForce personnel in rural peninsular Malaysia began with 400 mgalbendazole twice daily for 15 days 18 months after symptomsbegan (21) Treatment elicited intense pruritus but chronicsymptoms gradually waned and therapy was then discontinuedAfter several weeks discomfort returned therapy was initiated at600 mg twice daily for 20 days and symptoms abated Those au-thors note that it was unclear if improvement was related to theuse of albendazole or reflected the natural history of the infectionPatients returning from Tioman Island Malaysia received treat-ment with various antiparasitic agents including albendazole andsome received treatment with oral steroids (28) Some cliniciansreported relatively rapid symptom improvement resulting fromoral steroids including a patient with mild myocarditis who re-sponded favorably to such treatment

The antiprotozoal drug co-trimoxazole (trimethoprim at 160

mg and sulfamethoxazole at 800 mg) given as a dose of 3 tabletsper day for 12 days was used to treat a 31-year-old male patient3 months after muscular pain began (18) He was already feelingslightly better when diagnosis was made and before medicationwas prescribed but greatly improved except for some localizedpain

Of three patients who sought medical attention within 6 days ofonset of fever and were treated with co-trimoxazole (a 960-mgdose twice each day) all improved clinically without an elevationof CK levels (30) Two other patients in a later phase of illness withelevated CK levels were also treated with co-trimoxazole but onehad to be re-treated with prednisone because of increasingly se-vere myalgia A sixth patient who had the longest interval fromthe onset of symptoms was treated with prednisone Both patientstreated with prednisone improved rapidly

Sulfathiazole sulfamethazine sulfamethoxazole sulfadimethox-ine sulfadiazine sulfachloropyridazine trimethoprim and pyri-methamine were tested at different concentrations in cell culturesagainst developing S neurona merozoites (86) Pyrimethamineand trimethoprim were each cidal but none of the sulfonamideshad activity when used alone Combinations of sulfonamidesdemonstrated improved activity

What is lacking is a protocol that has been tested found to beeffective and confirmed by replication Because it is impracticaland undesirable to use humans or primates for testing it would behelpful as new patients are identified to report successful and un-successful treatment regimens However because symptoms usu-ally wane with time the efficacy of long-term medication mightnot be discerned from the natural course of the disease process

PREVENTION

To prevent intestinal sarcocystosis meat must be thoroughlycooked or frozen to kill the bradyzoites in the sarcocysts Thor-ough cooking rendered bradyzoites noninfectious as demon-strated in a volunteer study involving S suihominis (40) If there isa toxic factor associated with the ingestion of sarcocysts possiblyas with S suihominis (40) cooking also appears to destroy theeffects Sarcocystis meischeriana in pork was rendered noninfec-tious for dogs after meat was cooked at 60degC for 20 min 70degC for15 min and 100degC for 5 min or frozen at 4degC for 48 h or at20degC for 24 h (87) Likewise whereas dogs fed uncooked chuckroast round steak hamburger and rare roast beef became in-fected other dogs fed cooked meat such as beef bologna and beeffrankfurters or frozen meat such as hamburger or sandwich steaksdid not become infected (45) Meat inspection might reduce someinfections but it would be costly and time-consuming requiringthe identification of organisms in meat Unless heavily infectedsarcocysts would be difficult to detect by microscopic or antibodymethods and these tests would not determine the species andtherefore could be misleading if the species does not infect hu-mans Molecular tests may determine the species but obtaininginfected tissues where sarcocysts are sparse would be impracticalTo prevent infection of domesticated food animals human fecescontaining sporocysts must not be permitted to contaminate wa-ter bedding and feed Sanitation is the key with the use of toiletsand diligent hand washing contamination can be reduced oreliminated

To prevent humans from acquiring muscular sarcocystosis thepossible ingestion of sporocysts must be eliminated Clean drink-ing water can reduce exposure to sporocysts but recreational wa-

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httpcmrasm

orgD

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ter and contact with soil are potential risk factors Wherecontaminated drinking water is suspected boiling will providedisinfection Filters with pores small enough to remove bacteriafrom water can also remove sporocysts of Sarcocystis Chemicaldisinfection with chlorine or other agents used for water treat-ments is not effective in killing sporocysts of Sarcocystis (88)Where available drinking safe bottled water from sealed contain-ers is recommended Food can be contaminated at many placesalong the production distribution and preparation line Wherefresh produce is suspected to be contaminated with sporocysts inirrigation water or by food handlers food should be painstakinglywashed with clean water andor thoroughly cooked before beingeaten

CONCLUSIONS

Since the first report of sarcocysts in the muscles of mice 170years ago 150 valid species of Sarcocystis have been named and2000 reports have been published Great contributions to ourcomprehension of the diversity and transmission of Sarcocystisspecies have been made by identification of hosts with intramus-cular sarcocysts and others excreting sporocysts by LM and TEMdescriptions of sarcocyst and sporocyst morphology by feedingexperiments to determine the relationships among intermediateand final hosts by identification of the asexual stages in tissues ofintermediate or aberrant hosts and the sexual stages in the gut ofthe final host and by the use of molecular markers to identifyendogenous and exogenous stages Clinical signs and outcomes ofnatural experimental and aberrant infections have raised aware-ness of muscular sarcocystosis from a biological curiosity to aneconomically important disease in livestock and companion ani-mals and a debilitating disease in some wildlife to a serious diseasein humans in certain geographic areas Treatment strategiesadapted from experimental animal studies and from treatment ofrelated protists in humans can provide guidance for treatment ofmuscular sarcocystosis when diagnosis is made early in infectionbefore sarcocyst formation begins The use of safe drinking waterfiltered to remove particles larger than bacteria and thoroughcooking of meat should be effective to prevent most cases of sar-cocystosis as well as most other enteric protist infections The useof molecular methods has become essential for future progress onsarcocystosis for identification and source tracking for potentialdevelopment of treatment strategies based on metabolic path-ways for development of immunological treatment strategiesand for unforeseen applications that follow the discovery of basicscientific data

REFERENCES1 Dubey JP Speer CA Fayer R 1989 Sarcocystosis of animals and man

CRC Press Boca Raton FL2 Senaud J 1967 Contributuion a lrsquoetude des sarcosporidies et des toxo-

plasmes Toxoplasma Protistologica 3169 ndash2323 Fayer R 1970 Sarcocystis development in cultured avian and mamma-

lian cells Science 1681104 ndash1105 httpdxdoiorg101126science16839351104

4 Fayer R 1972 Gametogony of Sarcocystis sp in cell culture Science 17565ndash 67 httpdxdoiorg101126science175401765

5 Heydorn AO Rommel M 1972 Beitrage zum Lebenszyklus der Sarko-sporidien II Hund und Katze als Ubertrager ser Sarkosporidien desRindes Berl Munch Tierarztl Wochenschr 85121ndash123

6 Rommel M Heydorn AO 1972 Beitrage zum Lebenszyklus der Sarko-sporidien III Isospora hominis (Railiet und Lucet 1891) Wenyon 1923eine Dauerform des Sarkosporidien des Rindes und des Schweins BerlMunch Tierarztl Wochenschr 85143ndash145

7 Rommel M Heydorn AO Fischle B Gestrich R 1974 Beitrage zumLebenszylus der Sarkosporidien V Weitere Enwirte der Sarkosporidienvon Rind Schaf und Schwein und die Bedentung des Zwischenwirtes furdie Verbreitung dieser Parasitose Berl Munch Tierarztl Wochenschr 87392ndash396

8 Beaver PC Gadgil RK Morera P 1979 Sarcocystis in man a review andreport of five cases Am J Trop Med Hyg 28819 ndash 844

9 Pathmanathan R Kan SP 1981 Human Sarcocystis infection in MalaysiaSoutheast Asian J Trop Med Public Health 12247ndash250

10 Agarwal PK Srvastava AN 1983 Sarcocystis in man a report of twocases Histopathology 7783ndash787 httpdxdoiorg101111j1365-25591983tb02290x

11 Greve E 1985 Sarcosporidiosismdashan overlooked zoonosis Man as inter-mediate and final host Dan Med Bull 32228 ndash230

12 Pathmanathan R Kan SP 1987 Two cases of human Sarcocystis in EastMalaysia Med J Malaysia 42212ndash214

13 Pathmanathan R Jayalakshmi P Kan SP 1988 A case of human Sarco-cystis infection in Malaysia J Malays Soc Health 645ndash 47

14 Pamphlett R OrsquoDonoghue P 1990 Sarcocystis infection of human mus-cle Aust N Z J Med 20705ndash707 httpdxdoiorg101111j1445-59941990tb00403x

15 Abdel Mawla MM 1990 Ultrastructure of the cyst wall of S lindemanniwith pathological correlations J Egypt Soc Parasitol 20319 ndash325

16 Pathmanathan R Kan SP 1992 Three cases of human Sarcocystis infec-tion with a review of human muscular sarcocystosis in Malaysia TropGeogr Med 44102ndash108

17 Wong KT Pathmanathan R 1992 High prevalence of human musclesarcocystosis in south-east Asia Trans R Soc Trop Med Hyg 86631ndash 632httpdxdoiorg1010160035-9203(92)90161-5

18 Van den Enden E Prae M Joos R Van Gompel A Gigasse P 1995Eosinophilic myositis resulting from sarcocystosis J Trop Med Hyg 98273ndash276

19 Mehrotra R Bisht D Singh PA Gupta SC Gupta RK 1996 Diagnosisof human sarcocystis infection from biopsies of the skeletal muscle Pa-thology 28281ndash282 httpdxdoiorg10108000313029600169164

20 Shekhar KC Pathmanathan R Krishnan R 1998 Human muscularsarcocystosis associated with neoplasms Case report Trop Biomed 1561ndash 64

21 Arness MK Brown JD Dubey JP Neafie RC Granstrom DE 1999 Anoutbreak of acute eosinophilic myositis attributed to human Sarcocystisparasitism Am J Trop Med Hyg 61548 ndash553

22 Larbcharoensub N Cheewaruangroj W Nitiyanant P 2011 Laryngealsarcocystosis accompanying laryngeal squamous cell carcinoma case re-port and literature review Southeast Asian J Trop Med Public Health421072ndash1076

23 Makhija M 2012 Histological identification of muscular sarcocystis areport of two cases Indian J Pathol Microbiol 55552ndash554 httpdxdoiorg1041030377-4929107813

24 Balakrishna JP Chacko G Manipadam MT Ramyal 2013 Glomeru-lopathy in a patient with sarcocystis infestation Indian J Pathol Microbiol56285ndash287 httpdxdoiorg1041030377-4929120400

25 AbuBakar S Teoh BT Sam SS Chang LY Johari J Hooi PS Lakhbeer-Singh HK Italiano CM Omar SF Wong KT Ramli N Tan CT 2013Outbreak of human infection with Sarcocystis nesbitti Malaysia 2012 EmergInfect Dis 191989ndash1991 httpdxdoiorg103201eid1912120530

26 Lau YL Chang PY Tan CT Fong MY Mahmud R Wong KT 2014Sarcocystis nesbitti infection in human skeletal muscle possible transmis-sion from snakes Am J Trop Med Hyg 90361ndash364 httpdxdoiorg104269ajtmh12-0678

27 Italiano CM Wong KT AbuBakar S Lau YL Ramli N Syed Omar SFKahar Bador M Tan CT 2014 Sarcocystis nesbitti causes acute relapsingfebrile myositis with a high attack rate description of a large outbreak ofmuscular sarcocystosis in Pangkor Island Malaysia 2012 PLoS Negl TropDis 8e2876 httpdxdoiorg101371journalpntd0002876

28 Esposito DH Stich A Epelboin L Malvy D Han PV Bottieau E daSilva A Zanger P Slesak G van Genderen PJJ Rosenthal BM CamerJP Visser LG Munoz J Drew CP Goldsmith CS Steiner F Wagner NGrobusch MP Plier DA Tappe Sotir MJ Brown C Brunette GWFayer R von Sonnenburg F Freedman D Neumayr A Kozarsky PE2014 Acute muscular sarcocystosis an international investigation amongill travelers returning from Tioman Island Malaysia 2011 and 2012 ClinInfect Dis 591401ndash1410 httpdxdoiorg101093cidciu622

29 Slesak G Tappe D Keller C Cramer J Guthoff W Zanger P Frank M




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Ernestus K Rauthe S Stic A Schafer J 2014 Muscular sarcocystosisafter travel to Malaysia a case series from Germany Dtsch Med Wochen-schr 139990 ndash995 httpdxdoiorg101055s-0034-1370004

30 Tappe D Stich A Langeheinecke A von Sonnenburg F Muntau BSchafer J Slesak G 2014 Suspected new waves of muscular sarcocystosisin travelers returning from Tioman Island Malaysia May 2014 EuroSurveill 19(21)pii20816 httpwwweurosurveillanceorgViewArticleaspxArticleId20816

31 Slesak G Schafer J Langeheinecke A Tappe D 2015 Prolonged clinicalcourse of muscular sarcocystosis and effectiveness of cotrimoxazoleamong travelers to Tioman Island Malaysia 2011-2014 Clin Infect Dis60329 httpdxdoiorg101093cidciu791

32 Fayer R 2004 Sarcocystis spp in human infections Clin Microbiol Rev17894 ndash902 httpdxdoiorg101128CMR174894-9022004

33 Yang ZQ Wei CG Zen JS Song JL Zuo YX He YS Zhang HFAttwood SW Chen XW Yang GC Zhou X Quan X Li CY Han D LiuAW Lin P 2005 A taxonomic re-appraisal of Sarcocystis nesbitti (Proto-zoa Sarcocystidae) from the monkey Macaca fascicularis in Yunnan PRChina Parasitol Int 5475ndash 81 httpdxdoiorg101016jparint200412004

34 Tian M Chen Y Wu L Rosenthal BM Liu X He Y 2012 Phylogeneticanalysis of Sarcocystis nesbitti (Coccidia Sarcocystidae) suggests a snake asits probable definitive host Vet Parasitol 183373ndash376 httpdxdoiorg101016jvetpar201107034

35 Laarman JJ 1962 Isospora hominis (Railliet and Lucet 1891) in the Neth-erlands Acta Leiden 31111ndash116

36 Plotkowiak J Klasa IA 1973 Opis pierwszego przypadku inwazji Isosporahominis w Polsce Wiad Parazytol 19725ndash730

37 Plotkowiak J 1973 Inwazja Sarcocystis hominis nowy problem parazyto-logiczny w Polsce Ann Acad Med Stetin 1053ndash55

38 Janitschke K 1974 Coccidia infections in man in Germany p 116 InProceedings of the 3rd International Congress of Parasitology MunichAugust 25-31 1974 Facta Publication Munich Germany

39 Janitschke K 1975 Neue Erkenntnisse uber die Kokzidien-inkstensionendes Menshen II Isospora Infektion Bundesgesundheitsblatt 18419

40 Heydorn AO 1977 Sarkosporidieninfiziertes Fleisch als moglicheKrankheitsursache fur den Menschen Arch Lebensmittelhyg 2827ndash31

41 Tadros W Laarman JJ 1977 Studies on sarcosporidiosis and Sarocystis-induced coccidiosis in man monkeys and other animals abstr 137 Abstr5th Int Congr Protozool 26 June to 2 July 1977

42 Flentje B Jungmann R Hiepe T 1975 Vorkommen von Isospora-hominis Sporozysten beim Menschen Dtsch Gesundheitsw 30523ndash525

43 Plotkowiak J 1976 Wyniki dalsych badan nad wystepowaniem i epide-miologia inwazji Isospora hominis (Railliet and Lucet 1891) Wiad Para-zytol 22137ndash147

44 Giboda M Rakaacuter J 1978 First record of ldquoIsospora hominisrdquo in Czecho-slovakia Folia Parasitol (Praha) 2516

45 Leek RG Fayer R 1978 Infectivity of Sarcocystis in beef and beef productsfrom a retail food store Proc Helminthol Soc Wash 45135ndash136

46 Tadros W Hazelhoff W Laarman JJ 1979 The detection of circulatingantibodies against Sarcocystis in human and bovine sera by the enzyme-linked immunosorbent assay (ELISA) technique Acta Leiden 4753ndash 63

47 Deluol AM Mechali D Cenac J Savel J Coulaud JP 1980 Incidenceand clinical aspects of intestinal coccidiosis in a tropical medicine practiceBull Soc Pathol Exot Filiales 73259 ndash265

48 Bunyaratvej S Bunyawongwiro P Nityanant P 1982 Human intestinalsarcosporidiosis report of six cases Am J Trop Med Hyg 3136 ndash 41

49 Zuo Y-X Chen F-Q Li W-Y 1982 Two patients with Sarcocystis infec-tion p 52ndash53 In Jiang JB (ed) Malaria and other protozoal infectionsChinese Society of Protozoologists Zhongshan (Sun Yatsen) UniversityGuangzhou China

50 Li Y Lian Z 1986 Studies on man-pig cyclic infection of Sarcocystissuihominis found in Yunnan Province China Acta Zool Sin 32329 ndash334

51 Lian Z Ma J Wang Z Fu L Zhou Z Li W Wang X 1990 Studies onman-cattle-man infection cycle of Sarcocystis hominis in Yunnan Zhong-guo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 850 ndash53 (InChinese)

52 Straka S Skracikova J Konvit I Szilagyiova M Michal L 1991 Sarco-cystis species in Vietnamese workers Cesk Epidemiol Microbiol Imunol40204 ndash208 (In Slovak)

53 Yu S 1991 Field survey of Sarcocystis infection in the Tibet autonomousregion Zhongguo Yi Xue Ke Xue Yuan Xue Bao 1329 ndash32 (In Chinese)

54 Giboda M Ditrich O Scholz T Viengsay T Bouaphanh S 1991

Current status of food borne parasitic zoonoses in Laos Southeast Asian JTrop Med Public Health 22(Suppl)56 ndash 61

55 Wilairatana P Radomyos P Radomyos B Phraevanich R Plooksaw-asdi W Chanthavanich P Viravan C Looareesuwan S 1996 Intestinalsarcocystosis in Thai laborers Southeast Asian J Trop Med Public Health2743ndash 46

56 Meloni BP Thompson RC Hopkins RM Reynoldson JA Gracey M1993 The prevalence of Giardia and other intestinal parasites in childrendogs and cats from aboriginal communities in the Kimberley Med J Aust158157ndash159

57 Chen X Zuo Y Zuo W 1999 Observation on the clinical symptoms andsporocysts excretion in human volunteers experimentally infected withSarcocystis hominis Zhongguo Ji Sheng Chong Xue Yu Ji Sheng ChongBing Za Zhi 1725ndash27 (In Chinese)

58 Pena HFJ Ogassawara S Sinhorini IL 2001 Occurrence of cattle Sar-cocystis species in raw kibbe from Arabian food establishments in the cityof Sao Paulo Brazil and experimental transmission to humans J Parasitol871459 ndash1465 httpdxdoiorg1016450022-3395(2001)087[1459OOCSSI]20CO2

59 Clavel A Doiz O Varea M Morales S Castillo FJ Rubio MC Goacutemez-Lus R 2001 Abdominal discomfort and soft stools in a habitual consumerof rare beef Enferm Infecc Microbiol Clin 1929 ndash30 httpdxdoiorg101016S0213-005X(01)72545-1

60 Li JH Lin Z Tan YX Du JF 2004 Sarcocystis suihominis infectiondiscovered in Guangxi Zhongguo Ji Sheng Chong Xue Yu Ji Sheng ChongBing Za Zhi 2282 (In Chinese)

61 Tan YX Li JH Lin Z Du JF 2005 Investigation of the Sarcocystissuihominis infection status in the Zhuang ethnic population in part ofGuangxi Province Guangxi Med 11295ndash296 (In Chinese)

62 Li JH Lin Z Du JF Qin YX 2007 Experimental infection of Sarcocystissuihominis in pig and human volunteer in Guangxi Zhongguo Ji ShengChong Xue Yu Ji Sheng Chong Bing Za Zhi 25466 ndash 468 (In Chinese)

63 Tungtrongchitr A Chiworaporn C Praewanichm R Radomyos PBoitano JJ 2007 The potential usefulness of the modified Kato thicksmear technique in the detection of intestinal sarcocystosis during fieldsurveys Southeast Asian J Trop Med Public Health 38232ndash238

64 Velaacutesquez JN Di Risio C Etchart CB Chertcoff AV Mendez NCabrera MG Labbeacute JH Carnevale S 2008 Systemic sarcocystosis in apatient with acquired immune deficiency syndrome Hum Pathol 391263ndash1267 httpdxdoiorg101016jhumpath200801016

65 Chen X Zuo Y Rosenthal BM He Y Cui L Yang Z 2011 Sarcocystissinensis is an ultrastructurally distinct parasite of water buffalo that cancause foodborne illness but cannot complete its life-cycle in human be-ings Vet Parasitol 17835ndash39 httpdxdoiorg101016jvetpar201012026

66 Boonjaraspinyo S Boonmars T Kaewsamut B Ekobol N Laummaun-wai P Aukanimart R Wonkchalee N Juasook A Sriraj P 2013 QAcross-sectional study on intestinal parasitic infections in rural communi-ties northeast Thailand Korean J Parasitol 51727ndash734 httpdxdoiorg103347kjp2013516727

67 Nimri L 2014 Unusual case presentation of intestinal Sarcocystis hominisinfection in a healthy adult JMM Case Rep 11ndash3 httpdxdoiorg101099jmmcr0T00019

68 Lee SC Ngui R Tan TK Muhammad Aidil R Lim YA 2014 Neglectedtropical diseases among two indigenous subtribes in peninsular Malaysiahighlighting differences in co-infection of helminthiasis and sarcocystosisPLoS One 9e107980 httpdxdoiorg101371journalpone0107980

69 Laarman JJ Tadros W 1982 Sarcosporidiosis of farm animals p 81ndash 88In Walton JR White EG Hall SA (ed) Agriculture some diseases ofemerging importance to community trade Luxembourg Commission ofthe European Communities Luxembourg City Luxembourg

70 Solanki PK Shrivastava HOP Shah HL 1991 Prevalence of Sarcocystisin naturally infected pigs in Madhya Pradesh with an epidemiologicalexplanation for the higher prevalence of Sarcocystis suihominis Indian JAnim Sci 61820 ndash 821

71 Banerjee PS Bhatia BB Pandit BA 1994 Sarcosystis suihominis infectionin human beings in India J Vet Parasitol 857ndash58

72 Tappe D Abdullah S Heo CC Kannan Kutty M Latif B 2013 Humanand animal invasive sarcocystosis in Malaysiamdashrecent cases review andhypotheses Trop Biomed 30355ndash366

73 Jeffrey HC 1974 Sarcosporidiosis in man Trans R Soc Trop Med Hyg6817ndash29 httpdxdoiorg1010160035-9203(74)90247-8

74 McLeod R Hirabayashi RN Rothman W Remington JS 1980 Necrotizing

Fayer et al



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vasculitis and Sarcocystis a cause-and-effect relationship South Med J 731380 ndash1383 httpdxdoiorg10109700007611-198010000-00026

75 Poulson S Stensvold CR 2014 Current status of epidemiology anddiagnosis of human sarcocystosis J Clin Microbiol 523524 ndash3530 httpdxdoiorg101128JCM00955-14

76 Heckeroth AR Tenter AM 1999 Development and validation ofspecies-specific nested PCRs for diagnosis of acute sarcocystiosis insheep Int J Parasitol 291331ndash1349 httpdxdoiorg101016S0020-7519(99)00111-3

77 Kutty MK Dissanaike AS 1975 A case of human Sarcocystis infection inwest Malaysia Trans R Soc Trop Med Hyg 69503ndash504 httpdxdoiorg1010160035-9203(75)90108-X

78 Amarasinghe HK Usgodaarachchi US Johnson NW Lalloo R War-nakulasuriya S 2010 Betel-quid chewing with or without tobacco is amajor risk factor for oral potentially malignant disorders in Sri Lanka acase-control study Oral Oncol 46297ndash301 httpdxdoiorg101016joraloncology201001017

79 Warnakulasuriya S Trivedy C Peters TJ 2002 Areca nut use an inde-pendent risk factor for oral cancer BMJ 324799 ndash 800 httpdxdoiorg101136bmj3247341799

80 Fayer R Johnson AJ 1975 Effect of amprolium on acute sarcocystosis inexperimentally infected calves J Parasitol 61932ndash936 httpdxdoiorg1023073279240

81 Leek RG Fayer R 1980 Amprolium for prophylaxis of ovine SarcocystisJ Parasitol 66100 ndash106 httpdxdoiorg1023073280598

82 Leek RG Fayer R 1983 Experimental Sarcocystis ovicanis infection inlambs salinomycin chemoprophylaxis and protective immunity J Para-sitol 69271ndash276 httpdxdoiorg1023073281218

83 Voigt WP Heydorn AO 1981 Chemotherapy of sarcosporidiosis andtheileriosis in domestic animals Zentralbl Bakteriol Mikrobiol Hyg A 250256 ndash259

84 Husna Maizura AM Khebir V Chong CK Shah A Hakim L 2012Surveillance for sarcocystosis in Tioman Island Malaysia Malaysian JPublic Health Med 1239 ndash 44

85 Sykes JE Dubey JP Lindsay LL Prato P Lappin MR Guo LT MizisinAP Shelton GD 2011 Severe myositis associated with Sarcocystis sppinfection in 2 dogs J Vet Intern Med 251277ndash1283 httpdxdoiorg101111j1939-1676201100828x

86 Lindsay DS Dubey JP 1999 Determination of the activity of pyrimeth-amine trimethoprim sulfonamides and combinations of pyrimethamineand sulfonamides against Sarcocystis neurona in cell cultures Vet Parasi-tol 82205ndash210 httpdxdoiorg101016S0304-4017(99)00020-5

87 Saleque A Juyal PD Bhatia BB 1990 Effect of temperature on theinfectivity of Sarcocystis miescheriana cysts in pork Vet Parasitol 36343ndash346 httpdxdoiorg1010160304-4017(90)90047-F

88 Dubey JP Saville WJ Sreekumar C Shen SK Lindsay DS Pena HFVianna MC Gennari SM Reed SM 2002 Effects of high temperatureand disinfectants on the viability of Sarcocystis neurona sporocysts J Para-sitol 881252ndash1254 httpdxdoiorg1016450022-3395(2002)088[1252EOHTAD]20CO2

Ronald Fayer is a Senior Scientist in the Agricul-tural Research Service US Department of Agri-culture He received his BS from the Universityof Alaska Fairbanks and his MS and PhD fromUtah State University He has conducted researchon protist parasites of veterinary and public healthimportance including Sarcocystis Cryptospo-ridium Giardia microsporidia and Blastocys-tis and currently studies the molecular epide-miology of zoonotic protists He recently visitedTioman Island the site of outbreaks of muscu-lar sarcocystosis

Douglas H Esposito is a medical epidemiolo-gist and pediatrician in the Division of GlobalMigration and Quarantine Travelersrsquo HealthBranch CDC He received his bachelorrsquos degreefrom the University of Rochester in New Yorkand his MD and MPH from the University ofNorth Carolina at Chapel Hill and he thentrained in pediatrics at Childrenrsquos Hospital andMedical Center in Seattle WA He worked for13 years with the Indian Health Service in ruralArizona and Alaska He completed an EpidemicIntelligence Service Fellowship at the Centers for Disease Control and Pre-vention He is interested in the epidemiology of infectious diseases amonginternational travelers and has been working with travelers with acute mus-cular sarcocystosis after they returned from Tioman Island Malaysia Herecently visited the island

Jitender P Dubey is a senior scientist with theAnimal Parasitic Diseases Laboratory Agricul-tural Research Service US Department of Ag-riculture He received his veterinary degree in1960 in India and a PhD in 1966 from the Uni-versity of Sheffield England He has publishedextensively on cyst-forming zoonotic coccidianparasites including Sarcocystis Toxoplasmaand Neospora and continues his research withthese organisms In 2010 he was elected to theUS National Academy of Sciences Washing-ton DC




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tive host However this identification is based on a comparison of avail-ablecongenersthatmostcloselymatchedthoseofspeciesinwhichsnakeswerethefinalhostsandhasyet tobeconfirmedTwospeciesSarcocystishominis and S suihominis have been identified in humans and non-human primates serving as definitive hosts (Fig 1)

Early knowledge of infections in humans is scant because therelationship between infection and symptoms was not under-stood tissue specimens were rare light microscopy (LM) had lim-itations the life cycle was unknown and other diagnostic toolswere not developed The first record of what would become rec-ognized as Sarcocystis was in 1843 by Meischer who observedlong thin white cysts in muscles of a deer mouse in Switzerland(1) For the following 2 decades this parasite with no scientificname was called Meischerrsquos tubules In 1865 a parasite with asimilar appearance in muscles of a pig was then described byKuhn who proposed the name Synchytrium miescherianum (1)However the name Synchytrium was already in use for anotherorganism Thus in 1899 Labbe changed the name to Sarcocystismeischeriana (1) and it became the type species of the genus Inthe following decades many species of Sarcocystis were namedbased on finding intramuscular cysts in various animals and thesewere referred to as sarcocysts In some references to Sarcocystis theterm sarcosporidium was used This possibly resulted from stud-ies in which sarcocysts in culture media appeared to develop hy-phae and mycelia resulting from contamination and Sarcocystistherefore was thought to be a type of fungal organism In 1967electron micrographs clearly demonstrated that the organismscontained within the sarcocysts were not fungal spores but werezoites morphologically similar to those of other apicomplexanprotozoa (2) removing any consideration that Sarcocystis was tax-onomically related to fungi Other life cycle stages remained un-known until the 1970s when zoites freed from sarcocysts in themuscles of grackles (Quiscalus quiscula) developed into sexual-stage parasites and oocysts in cultured mammalian cells (3 4)Additionally sarcocysts from cattle were fed to cats dogs andhumans establishing three distinct species with the proposednames Sarcocystis bovifelis S bovicanis and S bovihominis com-binations representing two hosts (5ndash7) Although these speciesnames were later changed the cumulative findings from this pe-

riod established the requisite relationship of the two-host prey-predator (intermediate host-definitive host) life cycle for all spe-cies of Sarcocystis

Life Cycle Stages

In intermediate hosts including humans only asexual-stage par-asites are found (Fig 2) The initial stages of asexual developmentare known from animal studies but have not been seen in humantissues The following descriptions are based on Sarcocystis cruzidevelopment in cattle Infection begins when oocysts or sporo-cysts in feces from a final host become ingested by a susceptibleintermediate host Exposure to trypsin and bile causes the platesthat form the sporocyst wall to disunite liberating four motilesporozoites contained within The sporozoites pass into orthrough the gut wall and are first found within endothelial cellsthat line small arteries in all parts of the body This is the first ofapproximately four cycles of asexual development called mer-ogony or schizogony the number and timing of which mayvary with the species During each of the first three cyclesnuclear division eventually gives rise to merozoites which aremotile crescent-shaped organisms with a structure similar tothat of sporozoites Subsequent generations are found down-stream in arterioles and then in capillaries and in veins in allparts of the body until the last generation develops in skeletalsmooth and cardiac muscles and sometimes in neural tissuewhere sarcocysts are formed

For S cruzi the first generation is found 2 weeks after inges-tion of sporocysts (Fig 3A) and the second generation is found assingles or pairs of merozoites within mononuclear cells in periph-eral blood nearly 4 weeks after ingestion of sporocysts (Fig 3C) Afew days to a week later the third generation is seen as immaturemultinucleate schizonts or mature schizonts containing merozo-ites in endothelial cells of capillaries throughout the body but theyare especially prominent in renal glomeruli (Fig 3B) Merozoitesfrom these schizonts enter muscle cells where they begin sarcocystformation first differentiating into a single round cell called ametrocyte or mother cell A series of divisions gives rise to numer-ous metrocytes as the sarcocyst grows while concurrently a walldevelops isolating the sarcocyst from the surrounding muscle

FIG 1 Humans as definitive (final) hosts for Sarcocystis species

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PREVENTION



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PREVENTION



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PREVENTION



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CONCLUSIONS



































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Documents

Human Infections with Sarcocystis Speciescmr.asm.org/content/cmr/28/2/295.full.pdfacquired from eating undercooked meat: Sarcocystis hominis, from beef, and Sarcocystis suihominis,