Original Article
Improved Light-Microscopical Detection of Microsporidia Spores in Stool and Duodenal Aspirates
N Engl J Med 1992; 326:161-166January 16, 1992
- Abstract
- Abstract
Background.
The diagnosis of infection with Enterocytozoon bieneusi, a microsporidian organism that causes chronic diarrhea in patients infected with the human immunodeficiency virus (HIV), has depended on invasive procedures. We have developed a new method to detect microsporidia spores in feces and duodenal aspirates.
Methods.
Stool was obtained from four HIV-infected patients with biopsy-confirmed intestinal microsporidiosis. Slides prepared from unconcentrated, formalin-fixed stool specimens were stained with a new chromotrope-based technique and examined by light microscopy. Methods of stool concentration were also compared. The technique was then evaluated by examining 215 specimens from 134 HIV-infected persons with or without diarrhea. In addition, duodenal aspirates from 10 patients with unexplained chronic diarrhea were examined by light microscopy after staining according to the new and the traditional techniques.
Results.
E. bieneusi spores were found in all unconcentrated stool specimens from the four patients with microsporidiosis. The use of various methods of stool concentration did not improve the detection of microsporidia spores. In the prospective study, microsporidiosis was detected in samples from 6 of 27 patients with chronic diarrhea, but in none of those from 42 patients with acute diarrhea or 65 patients without diarrhea. The presence of microsporidia spores in stool specimens and duodenal aspirates allowed the successful prediction of the presence of microsporidia in small-bowel biopsy specimens from all four patients who subsequently underwent endoscopy.
Conclusions.
E. bieneusi is an important cause of chronic diarrhea in HIV-infected persons. This new diagnostic technique serves as a practical, noninvasive means to detect microsporidia spores in stool specimens and is also applicable to the examination of duodenal aspirates. (N Engl J Med 1992;326:161–6.)
Media in This Article
Figure 1
Transmission Electron Micrograph of an Individual Spore of E. bieneusi in an Endoscopic-Biopsy Specimen from an HIV-infected Man with Chronic Diarrhea and Wasting.Figure 2
Smear of Formalin-Fixed Stool Specimen, Showing Pinkish-Red—Stained Microsporidia Spores.Article Activity
- Article
MICROSPORIDIA are obligate intracellular spore-forming protozoa. Their range of hosts includes most major groups of animals,1 but they have been recognized infrequently as human pathogens.2 3 4 Eight cases of microsporidiosis have been reported among persons not infected with the human immunodeficiency virus (HIV).3 4 5 6 7 8 9 10 11 12 Since the first case reports of microsporidia infections as a complication of the acquired immunodeficiency syndrome (AIDS) in 1985,13 , 14 one microsporidia species, Enterocytozoon bieneusi, has gained increasing attention as an important cause of chronic diarrhea in patients with HIV infection.2 3 4 , 15 Different clinical syndromes attributed to other microsporidia species have also been described in patients with AIDS.16 17 18 19 20
The diagnosis of intestinal E. bieneusi microsporidiosis has depended on invasive procedures and identification of organisms in biopsy specimens of small intestine.14 , 21 22 23 24 25 Although other workers have recently reported a method for detecting spores in human fecal specimens with the use of Giemsa stain,26 this method is impractical for routine diagnostic use because it involves cumbersome processing and fails to differentiate spores clearly from other fecal elements.
To establish a practical method for diagnosing human intestinal microsporidiosis, we tested various stool-concentration techniques and staining procedures. We then developed simplified methods to detect microsporidia spores in fecal specimens and duodenal aspirates and evaluated these techniques by examining specimens from patients with HIV infection who were enrolled in a prospective study of enteric opportunistic infections. Our epidemiologic findings support those of earlier studies suggesting that E. bieneusi is an important cause of chronic diarrhea in patients with AIDS.
Methods
The method for detecting microsporidia spores in fecal material by light microscopy was developed with suspensions containing formalin and stool from four HIV-infected persons in whom electron microscopy had confirmed the presence of intestinal E. bieneusi microsporidiosis (Fig. 1Figure 1
Transmission Electron Micrograph of an Individual Spore of E. bieneusi in an Endoscopic-Biopsy Specimen from an HIV-infected Man with Chronic Diarrhea and Wasting.). The stool specimens were compared in a nonblinded fashion with specimens from 12 HIV-negative volunteers.Slides for light-microscopical examination of stool were prepared from 10-μl aliquots of a suspension of unconcentrated liquid stool in 10 percent formalin (1:3 ratio) thinly spread over an area 45 by 25 mm. Smears were fixed in methanol for 5 minutes and stained for 90 minutes with our new chromotrope-based stain. The staining solution, a modification of the trichrome stain,27 was prepared by mixing 6.0 g of chromotrope 2R (Harleco, Gibbstown, N.J.) (a concentration 10 times higher than that used in trichrome stain), 0.15 g of fast green (Allied Chemical and Dye, New York), and 0.7 g of phosphotungstic acid. After these ingredients had stood for 30 minutes in 3 ml of glacial acetic acid, they were mixed with 100 ml of distilled water. After staining, slides were rinsed in acid alcohol (4.5 ml of acetic acid; 995.5 ml of 90 percent ethyl alcohol) for 10 seconds and then rinsed briefly in 95 percent alcohol. Smears were then successively dehydrated in 95 percent alcohol for 5 minutes, 100 percent alcohol for 10 minutes, and Hemo-De (a xylene substitute; Fisher Scientific, Pittsburgh) for 10 minutes. One hundred light-microscopical oil-immersion fields (magnification, × 1000) per slide were scanned; each slide required an average reading time of approximately 10 minutes.
Smears prepared with use of the modified Ritchie formalin—ethyl acetate stool-concentration method,28 , 29 Sheather's sugar-flotation method,30 a sodium chloride—flotation method,26 or a simplified centrifugation-based spore-concentration procedure that appeared promising in pilot studies were evaluated and compared with unconcentrated fecal smears. Two additional centrifugation methods using sucrose and Percoll gradients were also evaluated.31
Stool specimens for electron microscopy were fixed in 10 percent formalin, and excess fecal debris was removed by sequential washing in deionized water followed by modified sugar flotation and high-speed centrifugation. Specimens were then transferred to Microfuge tubes, washed in 0.1 M phosphate buffer (pH 7.4) and secondarily fixed in 2 percent osmium tetroxide for two hours, resuspended in fixative, and centrifuged at 9000×g for five minutes in a Beckman microcentrifuge (Beckman Instruments, Palo Alto, Calif). After being washed and dehydrated in graded ethanol solutions, the pellets were embedded in Eponate 12 resin (Ted Pella, Redding, Calif), sectioned, stained with 2 percent uranyl acetate in water and with Reynolds lead citrate, and examined with a transmission electron microscope (Zeiss EM 10C, Zeiss, Thornwood, N.Y.).
Epidemiologic Evaluation
The spore-detection procedure was evaluated by examining 215 specimens from 134 outpatients with HIV infection who were enrolled in a prospective study of enteric opportunistic infections at the affiliated clinics (Grady Memorial Hospital, Veterans Affairs Medical Center, and Crawford Long Hospital) of the Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine (Atlanta). Patients were categorized as having chronic diarrhea (diarrhea lasting one month or longer), acute diarrhea (lasting less than one month), or no diarrhea (Table 1Table 1
Microsporidia-Positive Stool Specimens from HIV-Infected Subjects Enrolled in a Prospective Study.). Chronic diarrhea was defined as "unexplained" if no bacterial pathogens were identified and three consecutive stool examinations identified no parasitic pathogens other than microsporidia. Diarrhea was defined as the passage of three or more loose or watery bowel movements in one 24-hour period.Stool specimens were collected by the patients and placed in three vials — one with 10 percent formalin, one with polyvinyl alcohol (Para-Paks, Meridian Diagnostics, Cincinnati), and one without preservative. Because all stool specimens were evaluated with the microsporidia spore-detection procedure before any endoscopies were performed, the microscopists were blinded to the status of any given patient with respect to microsporidia infection. In patients with diarrhea, stool specimens concentrated with formalin—ethyl acetate were examined for ova and parasites with direct wet preparations, modified acid-fast staining,27 and cryptosporidium immunofluorescence (Merifluor Cryptosporidium, Meridian Diagnostics). Unconcentrated specimens preserved in polyvinyl alcohol were examined with trichrome staining.27 Stool specimens were cultured for routine bacterial pathogens, and the Clostridium difficile toxin assay was performed on the samples from the patients with chronic diarrhea.
Eleven of 21 patients with chronic diarrhea of unexplained origin underwent esophagogastroduodenojejunoscopy and colonoscopy. Between 2 and 10 ml of duodenal fluid was aspirated; specimens of duodenal and jejunal tissue were obtained with a pediatric colonoscope (Olympus PCF-10, Olympus, Hyde Park, N.Y.).
Sections of paraffin-embedded, formalin-fixed tissues were stained with hematoxylin and eosin and Giemsa and Brown—Brenn stains. Glutaraldehyde-fixed tissues were postfixed in 1 percent osmium tetroxide, buffered in 0.2 M trimethylpyridine (sym-collidine), and embedded in Maraglas (an epoxy resin). Sections were stained with uranyl acetate and lead citrate and examined with an electron microscope (Phillips 410, Phillips, Mahwah, N.J.).
The study protocol was approved by the appropriate institutional review boards, and written informed consent was obtained from the study participants.
Detection of Spores in Duodenal Aspirates
Duodenal aspirates were fixed in 10 percent formalin and centrifuged at 1500×g for 20 minutes. Slides were prepared from 10-μl aliquots of the sediment spread over an area 10 by 10 mm, and stained with Gram's, Giemsa, toluidine blue O, Kinyoun carbolfuchsin, and trichrome stains and our new stain. The slides were scanned by light microscopy at magnifications of 400 and 1000. To confirm the findings of light microscopy, an aspirate from a patient with biopsy-confirmed microsporidiosis was fixed in 2 percent glutaraldehyde and then processed and examined by electron microscopy as the stool specimens had been.
Results
E. bieneusi spores were distinctly visualized by light microscopy of very thin direct smears from unconcentrated stool—formalin suspensions stained according to our technique. The spores were ovoid and refractile, and the spore wall stained bright pinkish red. Whereas the cellular content of some spores did not stain and appeared transparent, other spores showed a distinct pinkish-red—stained belt-like stripe that girded the spores diagonally or equatorially (Fig. 2Figure 2
Smear of Formalin-Fixed Stool Specimen, Showing Pinkish-Red—Stained Microsporidia Spores.). The size of each spore was approximately 1.5 by 0.9 μm. Most bacteria and background debris counterstained faint green. Although other fecal elements, such as yeast, sometimes stained reddish, they could be distinguished from microsporidia spores by their larger size and more intense staining. A few bacteria also stained reddish but were round or rod-shaped, more uniformly stained, and never transparent.Microsporidia spores were found by light microscopy in all stool specimens from 4 retrospectively examined patients with biopsy-confirmed intestinal microsporidiosis, but in none of the specimens from 12 HIV-negative volunteers. The presence of microsporidia spores in these stool specimens was verified by electron-microscopical examination of fecal material (Fig. 3Figure 3
Transmission Electron Micrograph of an Individual Spore of E. bieneusi from the Stool of an HIV-infected Man with Biopsy-Confirmed Intestinal Microsporidiosis.).Direct smears prepared from unconcentrated stool—formalin suspensions were superior to those obtained with any of the concentration procedures that we evaluated. Centrifugal sedimentation, flotation-based stool concentration, and centrifugation through discontinuous gradients all failed to concentrate microsporidia spores and did not adequately separate spores from bacteria. Use of the formalin—ethyl acetate technique and the flotation methods led to a considerable loss of microsporidia spores and false negative results for three of the eight stool specimens from the patients with biopsy-confirmed microsporidiosis.
Epidemiologic Evaluation
The results of the prospective examination of 215 stool specimens from 134 HIV-infected persons are summarized in Table 1. Microsporidiosis was not diagnosed in any of the patients with acute diarrhea or no diarrhea. However, four patients with debilitating chronic watery diarrhea, weight loss, and low CD4 counts (range 0.003 to 0.029 × 109 per liter [3 to 29 per cubic millimeter]) had microsporidia spores (170 to 2460 spores per 100 oil-immersion fields) in all of 14 consecutively examined stool specimens. In all four patients, the diagnosis of intestinal microsporidiosis was subsequently confirmed by light microscopy of jejunal tissue, in which gram-positive spores were identified in supranuclear locations of infected enterocytes (Fig. 4Figure 4
Jejunal Tissue Containing Gram-Positive Spores (Arrow) within a Sloughing Enterocyte at the Top of a Blunted Villus (Brown—Brenn Stain, × 1750).). Electron microscopy confirmed the presence of typical spore ultrastructure in three patients but revealed no microsporidia spores in the fourth patient, in whom few parasites were detected in tissue sections by light microscopy and fewer microsporidia spores were found in both stool specimens and duodenal aspirates. Among eight patients with unexplained chronic diarrhea whose stool examinations revealed no microsporidia spores, no cause of the diarrhea was determined in subsequently examined specimens of small bowel. In one of these patients, cytomegalovirus colitis was diagnosed by colonoscopic biopsy. Stool specimens from another two of nine patients with unexplained chronic diarrhea who did not undergo endoscopic evaluation had low numbers of microsporidia spores (1 to 16 spores per 100 oil-immersion fields).Detection of Spores in Duodenal Aspirates
When four patients in the prospective study who had stool specimens containing microsporidia spores underwent endoscopy, spores were found in small-bowel tissue and duodenal aspirates. The number of microsporidia spores detected in concentrated duodenal aspirates ranged from 50 to several hundred per slide, whereas the number of spores in smears of unconcentrated aspirates ranged from 0 to 20. Microsporidia spores were found on slides stained with Gram's and Giemsa stain and our new stain. The chromotrope-based stain revealed a staining pattern similar to that observed in spores from fecal specimens. Gram's staining resulted either in refractile spores that stained partially gram-positive or in gram-negative spores that had gram-positive poles. Giemsa staining demonstrated spores as previously described in touch preparations of small-bowel tissue.32 Slides stained with our technique were easier to interpret than those stained with the Gram's and Giemsa techniques, which were associated with difficulty in distinguishing spores from background debris. Microsporidia spores in both unfixed and formalin-fixed duodenal aspirates did not stain with Kinyoun carbolfuchsin and stained very weakly with trichrome or toluidine.
The presence of microsporidia spores in duodenal aspirates was confirmed by electron microscopy in one patient with biopsy-confirmed intestinal microsporidiosis. Of eight patients with chronic diarrhea and negative small-bowel biopsies who underwent endoscopy, the seven for whom duodenal aspirates were available had no microsporidia spores or other parasites.
Discussion
Gastrointestinal symptoms are common among patients with AIDS,33 34 35 36 37 and HIV-associated chronic diarrhea frequently remains unexplained despite a comprehensive stool examination.33 34 35 36 37 Hence, reliable, noninvasive techniques for the rapid detection of intestinal parasites are needed. Recent studies with invasive diagnostic procedures in HIV-infected persons with chronic diarrhea and negative stool examinations indicate that the intestinal microsporidian E. bieneusi may be one of the most frequent pathogens.3 , 4 , 25 , 36 , 37 E. bieneusi infects enterocytes of the small intestine and has been identified only in patients with AIDS.4 Recent reports provide strong evidence that this parasite is a leading cause of chronic diarrhea in HIV-infected patients.25 , 37
The diagnosis of E. bieneusi microsporidiosis has depended on invasive procedures and the identification of organisms in biopsy specimens of the small intestine.2 , 13 14 15 , 22 , 23 , 25 , 35 The detection of microsporidia by light-microscopical examination of small-intestinal tissue has been well described.25 , 32 However, the identification of the species and diagnostic confirmation have required the use of transmission electron microscopy.2 , 13 14 15 , 22 , 23 , 25 , 35 Light microscopy of small-bowel tissue was sometimes insensitive; when present in low numbers, microsporidia were detected by light microscopy only in specimens that had been determined to be positive by electron microscopy.25 , 35 , 36
Although electron microscopy is considered the gold standard for diagnostic confirmation of microsporidiosis, its sensitivity is unknown. Our negative findings on an examination by transmission electron microscopy of specimens from one patient in whom microsporidia spores were detected in stool samples, duodenal aspirate, and small-bowel tissue by light microscopy suggest that electron microscopy may also fail to detect microsporidia in small-bowel tissue when few organisms are present. The variable sensitivity of both light and electron microscopy may be due to the apparent focal distribution of infected enterocytes, the small amount of tissue obtained with standard pinch biopsies, and the inability of endoscopists to select biopsy sites in infected tissue effectively.
Others have reported finding microsporidia spores in duodenal fluid by examining aspirates embedded in paraffin or plastic sections.38 Our experience suggests that such processing is unnecessary; simple centrifugation and staining of duodenal aspirates can readily allow diagnosis of intestinal microsporidiosis.
Our simplified diagnostic technique prospectively detected microsporidia spores on light microscopy of unconcentrated formalin-fixed fecal material from four patients in whom the diagnosis was subsequently confirmed by biopsy. The spores showed a characteristic staining pattern and could be distinguished readily from bacteria and fecal debris. In our experience, the screening of 100 oil-immersion fields per slide was sufficient to establish a diagnosis. We suspect that screening fewer fields would permit false negative results in patients who are excreting small numbers of spores.
We were unable to concentrate spores by using any of the procedures we tested or by varying the elements of these procedures, such as the relative centrifugal force, centrifugation time, or specific gravity of flotation solutions. Our data suggest that stool-concentration procedures are not necessary and that direct smears may be adequate for the diagnosis of clinically important intestinal microsporidiosis. Gram's stain, Giemsa stain, toluidine blue O, and Calcofluor (a chemofluorescent optical brightening agent) all stained microsporidia spores but were not specific enough to differentiate spores from bacteria or other fecal elements.
Our epidemiologic data indicate that E. bieneusi is a likely cause of chronic diarrhea in patients with AIDS. The prevalence of microsporidiosis was 22 percent among the patients with chronic diarrhea (6 of 27 patients) and 29 percent among those with unexplained chronic diarrhea (6 of 21 patients). These findings are consistent with those of endoscopic studies in similar patients.25 , 35 36 37
The incidence, risk factors, origin of infection, modes of transmission, clinical manifestations, and treatment of human microsporidiosis have yet to be adequately studied. The new technique that we describe will serve as a practical means of noninvasive diagnosis of intestinal microsporidiosis. It will simplify monitoring of trials of treatments and improve the ability to follow the natural course of this disease.
Supported in part by the Swiss National Science Foundation, by the Department of Veterans Affairs, and by funds from the National Center for Infectious Diseases, Centers for Disease Control.
The use of trade names in this article is for identification only and does not imply endorsement by the Public Health Service or by the Department of Health and Human Services.
We are indebted to Jeremy J. Berge, M.D., Stephen L. Becker, M.D., Alison G. La Voy, M.D., and Richard A. Sundberg, M.D., for providing clinical specimens; to Harold J. Steger, Anthony J. Piazza, Henry S. Bishop, Billie Swisher, and Carey Callaway for technical assistance; to Molly Eaton and Carolyn Bryan for interviewing and examining patients; and to the staff of the infectious diseases clinics of Grady Memorial Hospital, Crawford Long Hospital, and the Veterans Affairs Medical Center, Atlanta.
Source Information
From the Parasitic Diseases Branch, Division of Parasitic Diseases (R.W., R.T.B., G.S.V.), and the Pathology Branch, Scientific Resources Program (L.G.), National Center for Infectious Diseases, Centers for Disease Control, Atlanta; the Cell Biology and Aging Section, Veterans Affairs Medical Center, San Francisco (R.L.O.); and the Division of Gastroenterology, Department of Internal Medicine, Emory University School of Medicine, Grady Memorial Hospital, Atlanta (C.M.W.). Address reprint requests to Dr. Bryan at the Parasitic Diseases Branch, Mailstop F-13, Centers for Disease Control, 1600 Clifton Rd., Atlanta, GA 30333.
* The other members of the Enteric Opportunistic Infections Working Group are listed in the Appendix.
Appendix
The members of the Enteric Opportunistic Infections Working Group, in addition to the authors, are D.D. Juranek, D.G. Addiss, H.C. Spencer, A.W. Hightower, J.M. Stewart, J.M. Roberts, S.P. Wahlquist, C.R. Horsburgh, Jr., K.G. Castro, R.V. Tauxe, D.J. Vugia, and R.I. Glass, Centers for Disease Control, Atlanta; S.E. Thompson, III, and D.A. Schwartz, Emory University School of Medicine—Grady Memorial Hospital, Atlanta; P. E. Kozarsky, J.P. Steinberg, J.A. Shulman, R.M. Dismukes, M.H. DuPuis, and J.F. Nickerson, Emory University School of Medicine—Crawford Long Hospital, Atlanta; D. Rimland, S.E. Hogan, and A. Johnson, Emory University School of Medicine—Veterans Affairs Medical Center, Atlanta; and N. Elliott, Crawford Long Hospital, Atlanta.
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