Structure and function of the small intestine in some

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					Structure                       and function    of the small                                                              intestine
in some                        parasite  diseases1
Lloyd        Leon        Brandborg,2              A.B.,        M.D.,       F.A.C.P.

     Diarrheal           illnesses           and malabsorption                     syn-      often      not been          studied.          The mucosal                  mor-
 dromes          are common                   and often             epidemic            in   phology         has frequently               been        related         to the
 the tropics           (1 , 2). Because                 of the ubiquitous-                   appearance           of the “normal”                 small bowel             mu-
ness of multiple                  intestinal           parasites          found         in   cosa in North            Americans               and in Europeans.
 persons         residing         in these          areas,       it is tempting              Many        reports        describe          histological             findings
 to incriminate               them         as etiologic            in these         dis-     but do not contain                photomicrographs                      for ex-
eases.        To date,           however,             malabsorption                 has      amination           by the          reader.          Frequently,               the
 been      caused,           in some            patients,          only by Gi-               critical      necessity         for careful              orientation             of
ardia lamblia               (3-7),         Strongyloides               stercoralis           the small        biopsy       specimen             and careful             serial

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(8,     9), Capillaria                  philippinensis                 (10),        and      sectioning          of the entire                specimen             (exactly
Coccidia            (Isospora)              (1 1-13).           Although              re-    perpendicular            to the mucosa                   with examina-
ports of malabsorption                           associated          with hook-              tion of the central                  core       for diagnosis)                has
worm         are recorded,                it seems         likely that these                 not      been        appreciated               (15).         Pathological
helminths             are not a cause                        of steatorrhea.                 changes         have     been       implied           that can be ac-
Many          parasites,            including             the above,               may       counted        for solely        on the basis              of artifactual
cause diarrhea                 without          significant          malabsorp-              sectioning         or inadequate               sampling.             Further-
tion.                                                                                        more,       many       of the studies                 have        originated
     Diverse           pathological                changes            have       been        from      areas      where       tropical          sprue        is endemic
described           to occur           in the small intestine                      mu-       and this diagnosis                has not always                    been       cx-
cosa in patients                   harboring             parasites           studied         cluded.       Celiac      sprue       also occurs             in the trop-
by suction             biopsy         techniques.              These         reports         ics; this disease          has not always                been excluded
are extremely                 difficult         to evaluate.              Many         of    by a strict        gluten-free           diet.
the patients              studied           had multiple                 parasites.               This review         will attempt             to survey           some of
The site of biopsy                    is often          not stated.            A dif-        the reports         regarding          structural          alterations           in
fering       morphology,                even with adequate                      spec-        the presence            of parasitic             infections            and at-
imens,         occurs         as one samples                   the entire            gut     tempt      to place        these       infections           in some          sort
at different           levels.       As an example,                    branched,             of perspective.
fused,        and broad                villi are common                       in the
duodenum              in healthy            North        Americans.              Pen-        Giardia            lamblia
etrating        Brunner’s             glands         may have an over-                           Various          protozoological            surveys          have
lying        flat      mucosa              and        appear           abnormal.             shown       that    Giardia       lamblia     infection        has a
Adjacent           lymphoid              nodules,           which        are com-            prevalence         of from         2 to 25%           in subjects
mon       in the proximal                     small        gut in children,                  studied      (16-18).       This is certainly           an under-
result      in a flat artifact.               The criteria             of normal             estimate        as some        studies    relied       only     on a
and abnormal                  are rarely            given.       Examination                 single      stool     examination.          The       parasite        is
of coded            slides        by multiple                observers            with
suitable         control         slides        included           has virtually
                                                                                                  ‘Supported              in     part         by      the     Medical          Research
never        been       done.         Many           apparently             healthy          Service           and     the       Anatomical                  Pathology           Service,
persons         native        to the same               areas       have a mu-               Veterans           Administration                   Hospital,          San      Francisco.
cosal      appearance               that is as abnormal                      as that              2   Chief,      Gastroenterology                     Section,          Veterans         Ad-
in patients            with disease                (14).       Control          biop-        ministration            Hospital,                4150      Clement            Street,        San
                                                                                             Francisco,          California             94121,         and    Clinical        Professor
sies from            populations                of the same               age and            of Medicine,     University                         of    California            School         of
socioeconomic                   strata         as the patients                   have        Medicine,    San Francisco.
                            The     American         Journal      of (ii,zical Nutritio,z 24: JANUARY                        1971,      pp.      124-132.       Printed       in USA.
                                                  PARASITE       DISEASES         AND       THE      SMALL       INTESTINE                                                 125

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      FIG.   1. Several    Giardia      lamb/ia       in the    submucosa.          They          are residing      in loose    connective       tissue    near    fibers of
the     muscularis      mucosa.       Modified         Masson      stain.     X    1,000.

more        common          in children            than adults,            more             have      reported          the mucosal                morphology                to
prevalent          in underdeveloped                     areas,       and un-               vary from normal                  to mild nonspecific                   abnor-
der      unhygienic             conditions.            Although             most            malities       (22, 23).
individuals           harboring             Giardia          are probably                        We have examined                      103 proximal              mucosal
asymptomatic,               the parasite             has been          respon-              biopsies       from 26 patients                  with Giardia             infec-
sible for epidemic                 diarrhea        in which          apparent               tion.     Using       Bouin’s          fixation        and a modified
steatorrhea           was a prominent                      symptom            and           Masson          trichrome           stain       (2 1) we have               been
documented              in one patient               (19).      Steatorrhea                 able     to identify            invasion          of the mucosa                  in
seems        to be more              common            in children            and            16 patients          with diarrhea               (Fig.      1). Unfortu-
may mimic             celiac        sprue      (6). Steatorrhea                oc-          nately,      when        we were investigating                      these      in-
curs      less often          in adults          but has been                well           dividuals          we could           not perform              reliable        fat
documented              (3-5,        7, 19, 20, 25). There                    is a          balance        studies;        d-xylose          had been           removed
striking        association           of Giardia            infection        with           from the market                 except        as an investigational
dysgammaglobulinemia                          (20).                                         drug,       and      our      clinical         laboratory            was      not
     A       spectrum             of      pathological                mucosal               doing      the serum           carotene.          In 10 of 1 8 symp-
changes         has been associated                    with Giardia             in-         tomatic        patients        Sudan         III stain of the stool
fection.        These       have        ranged        from        a flat mu-                was estimated             at “2+           to 4+”         for qualitative
cosa       (7) that        was reversible                  on quinacrine                    fat. Two symptomatic                        patients        did not have
therapy          to mild           nonspecific             changes          to a            invading         organisms.          Both were studied                   within
structurally           normal          mucosa         on light micros-                      a week          of a course               of quinacrine               therapy
copy (21). Yardley                   et al. (4) described                a focal            that had failed              to cure their              diarrhea.          They
acute       inflammatory               response          in five of their                   had scanty           numbers          of organisms             in the lum-
six patients.            Bacterial          cultures          were      not re-             inal aspects          of the specimens.                 Four       asympto-
ported.         Two       of their          patients          with      remote              matic      patients       with only cysts in the stool did
gastrectomy              may        have       had      bacterial          over-            not have           Giardia         trophozoites              even        within
growth         syndromes.             This was most conspicu-                               the luminal             aspects          of the biopsies.                   Four
ous in the crypts                  and was associated                    with a             other     asymptomatic                carriers        had small            num-
variable         amount          of epithelial            damage.          Some             bers of organisms                  present         without         invasion.
shortening           of the villi and an increase                         in the            All of our patients                 had a structurally                 normal
epithelial         mitotic        index       were       also present             in        mucosa         or, at most,             only a mild nonspecific
five of their           six patients.            Other        investigators                 abnormality             by light            microscopy             (Fig.       2).
126                                                                               BRANDBORG

    FIG.    2.       Normal      small   bowel     mucosa       from     a patient          with    symptomatic          giardiasis     with    tissue   invasion.      Modified
Masson           stain.       x 40.

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Despite            a careful          search        we did not observe                                 In the few autopsy                reports        available         (3,
any acute               inflammatory               response            or epithe-                  6), the small          bowel       is described           as having
hal cell damage                   in the crypts.               Rarely,         at the              small superficial,         sharply       demarcated            ulcera-
site      of     epithelial           invasion          one or two cells                           tions    with      some       focal     constriction           of the
were         undergoing                necrosis.         On a review                   of          bowel,    particularly         in the ileum.
coded          slides these cells tended                       to be near the                           The significance           of mucosal         and epithelial
tips of villi and may                            be merely              senescent                  invasion      remains        obscure.        Insufficient         dam-
cells.       In some           there       was a slight              increase          in          age is apparent,          by light microscopy,                  to ac-
lymphocytes                   within         the      epithelium.               None               count    for either      steatorrhea          or diarrhea.          The
had        a mucosa               that      was flat or resembled                                  number          of    invading           organisms            is    small       in
celiac          sprue.        There         was no morphological                                   comparison         to the multitudes         in the luminal
evidence             of a reaction             to the parasite                on the               aspects      of the biopsies.     Consistent      ultrastruc-
part        of the host.                The       epithelial          cells      were              tural    damage      to the epithelium         has not been
generally             somewhat             enlarged.          Brush         borders                described.       The mechanisms          by which      Giardia
were          prominent.                Although             reminiscent               of          cause      symptoms      is still unknown.
the large epithelial                    cells occurring               in vitamin
                                                                                                   Strongyloides              siercoralis
B12 or folic acid deficiency,                              these       large      cells
may have                resulted         from       a more          rapid        turn-                  Strongyloidiasis              occasionally              has been          as-
over.         Vitamin            B12 or folate                deficiency            has            sociated         with malabsorption                     (8, 9, 26, 27).
not been associated                       with giardiasis.                                         The clinical           histories        in some           are almost           in-
       On        electron           microscopy,                 some         reports               distinguishable             from      the patient            with tropical
have described                   a shortening             of the microvilli                        sprue       (8). The          history         differs       in that        most
 (7, 24), whereas                    others        have        found        the mi-                individuals          infested        with Strongyloides                    often
 crovilli         (25)      to be normal              even when              the or-               have       a history         of an irritating                 rash     and of
ganism             was closely              adherent            to them.            Ta-            pulmonary             symptoms             (8,     28). The           steator-
 kano         and Yardley                 (24) describe                ultrastruc-                 rhea      may be gross                and substances                  such       as
 tural changes                in the crypt             cells suggestive                of          d-xylose         and folic acid may be malabsorbed
 cell damage.                These       changes         were more prom-                           (8). Although             most patients               harboring          Stron-
 inent        in areas          where         an acute           inflammatory                      gyloides         are apparently                 asymptomatic,                 this
 response            was      observed.            Morecki           and Parker                    parasite        should        always         be treated.           Its endo-
 (25)       observed            Giardia          within        epithelial          cells            autoinfectivity            may       result        in chronic            infec-
 without            damage          to the organdIes                   of the cell                  tion     of up to 40 or more                           years’       duration
 or any apparent                    site of entry.             In their study,                      (28).      The      administration                of corticosteroids
 epithelial            damage           was not present.                                            to patients          harboring           Strongyloides               may re-
                                                PARASITE       DISEASES        AND   THE        SMALL           INTESTINE                                                        127

suit    in a fatal dissemination                      of the organism                ill    patients,          therapy          with      tetracycline          and
(29,      30).                                                                       folic      acid       resulted         in no improvement,                    cx-
     Although           the helminth             has been observed                   cluding          tropical          sprue      as a diagnosis.              The
in mucosal           suction        biopsies,          the diagnosis            is   control          patients          generally        had      lower      caro-
best made            by examination                  of the duodenal                 tenes,       d-xylose           absorption,          and higher          fecal
contents         for rhabditiform                 larvae.        The orga-           fats than          North        Americans           and Europeans.
nism       in various           stages        of development               has             When        coded        slides     of the small bowel              mu-
been found            in large numbers                   throughout          th      cosal       biopsies           were       submitted          to an mdc-
entire       intestinal         tract       in patients            dying       of    pendent           referee        for interpretation,              no differ-
 strongyloidiasis              (29,        30).       Adult         females,         ence      between           the Capillaria-mnfected                 patients
rhabditiform              larvae,        filariform           larvae,      and       and         the        normal            controls            was     observed.           Both
ova may           be found            within        the mucosa            (26,       the        patients               and
                                                                                                                 the controls          had a flat mu-
 27, 3 1). The filariform                    larvae        are the infec-            cosa;    the only       difference        in the patients            was
 tive stage.        The larva,           when         present       in small         the presence          of worms           within       the mucosa.
bowel        mucosal           biopsies,         is   diagnostic,            but     The    mode        of transmission              of this parasite
biopsy         cannot        be relied          on for diagnosis.                    has not been          determined,           but the fulminant
Dc Figueiredo              and his colleagues                (32) found              nature     suggests       autoinfection           once      acquired.
larvae       in only          2 of 108 cases                 studied        by       Treatment         with thiabendazole                in dosages          of

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suction        biopsy.       It is not clear           in their report               25 mg/kg          per day for a month                    resulted        in
whether          any of their patients               had symptoms.                   a cure.      Inadequate           treatment         was heralded
We have            examined         seven       biopsies        from      two        by the appearance               of ova in the stools               prior
patients         with     asymptomatic              strongyloidiasis.                 to clinical                 relapse.
Their       mucosae           were      normal          without        para-
                                                                                      Coccidia                  (Isosporiasis)
sites    in any of the serial                 sections.
      The pathology             observed         in strongyloidiasis                         Three                     of
                                                                                                                  species      Coccidia,              Isospora
ranges       from a flat mucosa                to mild nonspecific                    belli,          hominis,  and natalensis            are thought             to
changes.          The epithelium,               generally,         appears            infect      man.      Zaman        (33)      holds        the opinion
to be well preserved.                 In the vicinity            of invad-            that Isospora           hominis       and belli are the same
ing worms,            extensive        destruction           of the mu-               organism          and that the different                 appearances
cosa,      with little or no tissue                   reaction        of the          of oocysts         in the stool         merely        represent          dif-
host is seen.            There      is usually          an increase          in       ferent      stages     of maturity.          Although           infection
eosinophiis            in the lamina              propria.        On suc-             with     this sporozoan             parasite        has been           con-
cessful       treatment         of the infection,             the worms               sidered       rare, Jarpa       Gana       ( 1 2) diagnosed             394
are no longer             observed        in the biopsy            and the            cases      in Santiago          during        an 8-year            period.
mucosa           reverts       toward         normal.         Treatment               He described             the clinical          course        in 57 pa-
with      thiabendazole              reverses        the steatorrhea                  tients    that he was able to manage                        personally.
in the patients              with malabsorption.                                      Steatorrhea          was a common                finding        although
                                                                                      formal         fat     balances         were         not       reported.
Capillaria          philippinensis                                                    Ninety-eight          percent      of the patients             had diar-
     Whalen          et al. (10) have recently                    described           rhea often         with undigested             food present,             and
a striking         malabsorption                syndrome          with pro-           there               was        only          one      asymptomatic                  patient
tein-losing           enteropathy              due to a newly                de-      who            had        lost     weight.            Clues         to the      diagnosis
scribed        intestinal         roundworm,             Capillaria        phi-       were            generally              an     acute        onset     with       fever     and
lippinensis.           More        than      1,000      cases with          100       a    peripheral                  eosinophilia.                Some       patients         had
deaths        have        been       recorded         in the northern                 an       illness          of several               weeks       to    months         Sugges-
Philippines.            They          carefully        studied        11 pa-          tive           of  “functional”        diarrhea.         The stools     in
tients      infected          with      Capillaria          and used          15      Jarpa            Gana’s       patients    contained         large  num-
relatives         who        did not harbor                the worm           as      bers           of Charcot-Leyden               crystals.      The orga-
controls.          The         striking         malabsorption               and       nism            was very difficult        to isolate       and identify
protein-losing              enteropathy            were documented                    by parasitological                           examination              of feces.         Even
by fat balance                 studies         and protein           loss by          in       the        presence            of severe             diarrhea          and     stea-
51Cr-albumin               techniques.           In the less severely                 torrhea               oocysts               were      often         scanty.       In     con-
128                                                                                  BRANDBORO

trast to the usual         techniques         of searching         for                                The pathology               in these         six patients            con-
parasites      in freshly       passed      stool,    the speci-                                 sisted     of a flat mucosa                in two, including                the
men       is best    allowed        to incubate          at room                                 ileal specimens.             Both       of these         patients        died.
temperature        for 2 days          before      concentrates                                  The mucosa             at postmortem               examination             was
are examined          by zinc sulfate-flotation                 tech-                            flat in the entire              length       of the small             bowel.
niques.      The various         species      of Coccidia          are                           The      other       fatal     case      had      tall but clubbed
identified      by the appearance               of the oocysts                                   viili, a markedly               thickened           basement            mem-
as    observed            in    stool.                                                           brane,       extensive        collagen         in the lamina              pro-
      Smitskamp                and       Oey-Muller                  (34)         diag-          pria,     and markedly               dilated        vascular         spaces.
nosed        8 1 cases in Rotterdam                          during        a 1 -year             One had elongated                  crypts       with stubby             resid-
period.          Their        population                consisted            of 685              ual villi. One had tall villi with focal                               fusion
individuals            who had               traveled           or resided               in      and flattening.            The least           severely         ill patient
the tropics.              Only        1 7 of their               patients           had          had a patchy            abnormality            with some biopsies
diarrhea.          In 10, Amoeba                     histolytica,           Giardia              representing           only a mild,            nonspecific            abnor-
lamblia,           Schistosoma,                   Taenia,           or Shigella                  mality      (Fig. 3A, B, C, D, E, F).
could       have explained                  the diarrhea.                They         did             The epithelium               was often           normal          except
not consider               the organism                 to be particularly                       in one of the patients                       with      a flat mucosa
pathogenic.             A minimum                   of 30 proved                  cases          where       it was cuboidal               without         visible       brush

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of coccidiosis               are seen each year at the Uni-                                      borders        on light microscopy.                    There        was fo-
versity        of Chile in Santiago                       (Dr. 0. Brunser,                       cal marked             vacuolization             of the epithelium
personal            communication).                                                              in all of the patients.                Paneth        cells were pres-
      Although            the parasite                was first identified                       ent in the bases              of the crypts.            Although            mi-
within        epithelial         cells by Klebs                 (35)      in I 858,              totic counts           were not done,               they seemed              in-
little    information              is published                 regarding             the        creased.
morphology                of the mucosa                  or of the life cy-                           The lamina               propria          contained            abundant,
dc of this organism                       in the intestinal                   epithe-            and even increased,                     numbers            of plasma         cells
hum of man.                  Niedmann                (36) published                 one          and lymphocytes.                   Eosinophils             were increased
photograph                of a mucosal                     biopsy          showing               and       in two            patients           rather         substantially.
schizonts          in the epithelium                    from a patient                 in-       Scanty         histiocytes           were        usually        present       and
fected        with Coccidia                in 1963.                                              a few mast cells were present.                             The capillaries
      My colleague,                 Dr. Stanley                 B. Goldberg,                     in all of the patients                      were        more       prominent
and I have              had the opportunity                         to examine                   than those            usually         seen in sections.               No lym-
 17 mucosal               biopsies          from         six patients              with          phectasia           was seen.           The submucosal                   vessels
coccidiosis.            These         included             15 proximal                 bi-       and neurons              appeared            normal.
opsies          and       two       ileal         Specimens              procured                     We identified               schizonts          in all six patients.
through          an ileostomy              from an infant.                   Two of              By extrapolation                   from       observations             of Coc-
the patients            with severe diarrhea                       and steator-                  cidia      in other          species,        we feel that we have
rhea       died       as a result              of their          disease.          One           identified         most,       if not all, of the stages                   of the
who had malabsorption                             for 14 years              expired              endogenous               life cycle             in man           (Brandborg
from        a massive             pulmonary                 embolus            before            and Goldberg,                 unpublished              observations).            In
any therapy              could       be tried.            Although            the ill-           one patient              four       biopsies           procured          over      a
ness is self limited                     (12)         in the majority                   of       2-year        interval         all contained                Coccidia.         The
patients          with a duration                     of 6 weeks               to ap-            parasites          resided         within         or immediately               be-
proximately                6 months,                all of our patients                          neath        the       epithelium,              usually         in vacuoles
had been             chronically              ill. All had significant                           (Fig.       4). Rare            forms         were        present         in the
weight         loss and all had steatorrhea.                              Two        pa-         lamina         propria         or the submucosa.                     Although
tients       had       oocysts          of Isospora                belli       in the            they      destroy          the cells           that      are parasitized,
stool.      In two, schizonts                     were observed                 in the           adjacent          epithelium             often       appeared           normal.
proximal           intestinal         contents.            It is our opinion                     Except         for the least             severely         ill patient,        who
that      detection            of schizonts                by small             bowel            also     had a heavy                Giardia          infection        with tis-
mucosal            biopsy         may         be the most                  sensitive             sue      invasion,            the       mucosa            appears          to be
technique            for diagnosis                of coccidiosis                (37).            sufficiently          damaged             to account           for the diar-
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                                                                                                       -         .              -      . .‘.   -          :

                                                                                                  I:                                                                                        ‘1
                                                                                                                            ‘                                         #{149};:

      FIG.    3. Spectrum             ofmucosal           pathology         seen in coccidiosis.           A. Small bowel       mucosa                from       patient     with coccidio-
sis    (isospora        beii)of       2 years       duration.         Moderately         abnormal.         There   is marked         focal           vacuolization           of the   surface
epithelium.         A large     blood    clot overlies      the             section.      Modified     Masson           strain.   X 40. B. Small bowel     mucosa   illus-
trating     elongated       crypts    and stubby       residual                villi.   Hematoxylin       and        eosin.     X 40. C. Mild abnormality.      Some tall
villi and branched      and fused villi. This biopsy is from our least severely ill patient.    Hematoxylin         and eosin. X 40.
D. Flat mucosa.      Ileal biopsy from the infant who died from coccidiosis.        Hematoxylin       and eosin, Alcian blue. X
40. E. Flat mucosa.        Biopsy from near ligament     of Treitz in patient   who expired     from     the pulmonary       embolus.
Colophonium        Giemsa.      X 40. F. Tall but clubbed      villi with markedly   dilated    vascular     spaces    and excessive
collagen           in the    lamina      propria.         Destained         Gomori        trichrome,       counterstained           with           Colophonium             Giemsa.      X 40.
130                                                                                                    BRANDBORG

rhea           and  steatorrhea,    particularly       if these                                                    these       syndromes.           Banwell      and his                               colleagues
changes          are diffuse.    Most       of our     biopsies                                                    (39)      studied        patients      with hookworm                                        infec-
were      from      the proximal    gut. Organisms          were                                                   tion       and      patients        with     pancreatic                                   insuffi-
difficult      to see in the ileal specimens            because                                                    ciency         and      hookworm           infection                                 and      con-
of the        large      numbers   of goblet       cells.     The                                                  cluded         that      hookworm           did not                                 cause       the
distal     gut may be more          severely     damaged         as                                                steatorrhea.            Many        of the      studies                               of        hook-
in       many           species                of      animal           coccidiosis.                               worm            have            originated                   from  the      areas           of
    Although        there   is said to be no treatment                                                             world   in which      tropical       sprue    is endemic          and
for the infection,            one    of our  patients       re-                                                    this diagnosis       has     not      been     excluded         as a
covered      coincidentally        with a 1-week      course                                                       cause   of malabsorption                in the infected            pa-
of 300           mg      lid nitrofurantoin                            for     the        associated               tients.  The range         of mucosal           changes        illus-
Giardia               infection.                    French’s             patient              (11)      re-        trated  in the various         articles    is from a normal
covered              coincidentally                           with     administration                    of        mucosa      to mild        nonspecific          abnormalities.
nitrofurantoin.                       Although                       both          of      these       pa-         We have        examined           14 biopsies           from        six
tients          appeared                  to        benefit          from          therapy,            it is       asymptomatic                       persons               with            hookworm.                     All
more           likely          they        had         a self-limited                    illness       and         of      the    biopsies            were         normal              or     only       had         mild
were            recovering                     spontaneously                            despite         the        nonspecific                 abnormalities.                          In      most           studies,
chronicity                of      their             symptoms.                                                      control              patients             from              the          same         socioeco-

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                                                                                                                   nomic           levels            were         not       used            and        when          they
A ncylostomiasis                                                                                                   were          the mucosal                morphology                       of control              sub-
       Although                 hookworm                         has         been          described               jects         appears              to    be          similar.             Although                it     is
to       be         associated                      with        malabsorption                        (38),         possible             that         very        heavy             hookworm                   infesta-
most           investigators                         (39,       40)         have          concluded                tion          may        result          in     malabsorption,                         no         con-
that          the       worm              itself           is not            responsible                for        vincing             evidence             has         been         presented                to    date.

      FIG. 4. Several  stages of Coccidia                                      within     the epithelium.       Note   well preserved    brush    borders    in this section.
A,   B) Merozoites       (early developing                                      schizonts).     C) Early merozoites.         D) Young       macrogamete.       E) Schizont.
Coccidia     are often not this numerous.                                         Colophonium           Giemsa.      x 1,000. (Reproduced,       with permission       of the
publisher,     from:  Human     coccidiosis:                                     a possible   cause of malabsorption.           New   Engi. J. Med.       283: 1306, 1970.)
                                                      PARASITE            DISEASES       AND    THE       SMALL           INTESTINE                                                                       131
                                                                                                Harris,          Emmett                 Kehoe,             Telfer          Reynolds,                Harvey
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132                                                                                                   BRANDBORO

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