829
TRAN~ACTION~OF THE ROYAL SOCETY OF TROPICALMELXCINEAND HYGIENE (1990) 84, 829-831
Diagnosis of Strongyloides and hookworm and duodenal fluid microscopy
infections:
comparison
of faecal
A. K. J. Goka’, D. D. K. Ralston’, V. I. Mathan* and M. J. G. Farthing” ‘Department of Gastroenterology, St Bartholomew’s Hospital, West Smithfield, London, ECIA 7BE, UK; zWellcome Research Unit, Department of Gastroenterology, Christian Medical College Hospital, Vellore, Tamil Nadu, India
Abstract
Faecal microscopical diagnosis of Strongyloides and hookworm infections is insensitive. We have therefore compared duodenal fluid and faecal microscopy for detection of these parasites in a group of 292 patients being investigated for gastrointestinal symptoms who were examined by both techniques. Thirty-three of these patients (8%) were infected with Strongyloides stercoralis and 88 (30%) had hookworm infections. Microscopical examination of up to 3 faecal specimens detected only 33% and 65% of patients with Strongyloides and hookworm infections, respectively. Microsconical examination of a single snecimen of duodenal fluid was more sensitive for detection of strongyloidiasis. identifvina 76% of natients: the oarasite was found exclusively in’ duodena fluid (and not in faeces) in 67% of patients. For hookworm, the diagnostic sensitivity was similar with both techniques but duodenal fluid microscopy detected some patients (35%) who had not been identified by faecal microscopy. This study confirms previous work indicating the insensitivity of faecal microscopy in these infections and emphasizes the need to consider routine examination of duodenal fluid to exclude chronic strongyloidiasis. This may have particular relevance for south-east Asian war veterans and immunocompromised patients. Introduction
The diagnosis of Strongyloides and hookworm infections generally relies on-the detection of larvae or ova in faeces(STURCHLER.1987). Failure to identifv these parasitesin faecesis often acceptedas indicating the absence of infection. However, exhaustive examination of multiple stool specimens is often not feasible and experience in the identification of these parasites is lacking in many diagnostic laboratories, particularly those in the developed world. Further tests are therefore not requested, with the result that diagnosis may be unduly delayed. This is particuarly important for S: stercoralis infection, as there are now many reports of fatal or near-fatal infections usually in war veterans from south-east Asia (PURTILO et aE., 1974; KUBERSKI SIEGMAN et al.,
et al., 1975; GROVE, 1980; IGRA:
1981). although children and immunocompromi’sed patients are-also at risk (BURKE, 1978; MAAYAN et al., 1987). Identification of even very light infection is now considered essential as dissemination and life-threatening complications can occur very rapidly (SMALLMAN et al., 1986). In the course of a limited field study, we noticed that hookworm and Strongyloides ova or larvae were ~~ ‘Author for correspondence.
infreouentlv found in faeces, even in the Presenceof very high -parasite concentrations in duodenal or ieiunal fluid. We therefore decided to comoare the sensitivity of faecal and duodenal fluid micrdscopy in the diagnosis of these parasitic infections. Materials
and Methods
All patients admitted to the Wellcome Research Unit in the Christian Medical College Hospital, Vellore, India, had multiple faecal specimens examined in the course of investigation of gastrointestinal symptoms. As part of the routine clinical examination, some patients also had microscopical examination of duodenal or jejunal fluid. The same experienced parasitologist examined all specimens. During the four year period from June 1981to May 1985,292 patients had microscopical examinations of both duodenal fluid and at least one faecal sample in the same week before any specific therapy had been given. Faecal specimenswere examined fresh, usually within 30 min of collection. Wet preparations in normal saline were examined by direct microscopy at low and high magnification. A further examination was made following flotation on 50% zinc sulphate to concentrate ova and cysts. Aspiration of intestinal fluid was performed in the fasting state; the position of the aspiration tube was confirmed to be in the distal duodenum or proximal jejunum by fhtoroscopy. Aspirates were examined immediately by low and high power microscopy, then centrifuged at 600 g for 10 min followed bv a further microscooical examination of the sediment. Results Stronayloides stercoralis
Larvae were found in 33 of the 292 patients (8%). Of these, the parasite was easily identified in large numbers in duodenal fluid of 25 (76%) of these patients (Table 1). Faecal microscopy was’less sensitive, since only 2 1% of infected patients were detected by one faecal examination, rising to only 33% after examination of 3 specimens. The parasite was found exclusively in duodenal fluid in 22 (67%) of these oatients. The sensitivitv and soecificitv of faecal and duodenal fluid microscopy ark summarized in Table 2. Hookworm
Hookworm ova or hookworm were found in 88 (30%) of the 292 patients examined, manv of them reported as having heavy parasite loads. -Ova were found in 39% of the first faecal samplesfrom infected patients, rising to 65% following examination of 3 faecal specimens(Table 1). Hookworm were found in
Table 1. Comparisonof faecal and duodenalfluid microscopyin the examination of patients infectedwith Stron~loides stercorafis (0=33) and bookworm (0=88) NO.
No. positive (cumulative
examined
no. positive)
CUtUUlatiVe percentage positive
1st
33
2nd 3rd
29 20
7 (7) 5 (8) 4(11) 25
21 24 33 76
34 (34) 32~) 22 (57) 60
39 s2 65 68
Specimen strlmgvloides
Faeces Duodenalfluid Hookworm Faeces
33
1st 2nd 3rd
88 78 53
Duodenal fluid
88
Table 2. Sensitivity and specilicity of duodenal hid and faecal microscopy in the detection of infections due to Shoagyloides stercomlis and hookworm
Duodenal fluid examination s. stemrazis Hookworm
Positive Negative Total PositiveNegative Total
Faecalexamination Positive 3
8 0 8
Negative
Total
::
11
29
28
22 33
31 60
0 28
57 31 88
fluid
Faeces
Duodenal fluid
Sensitivity(%)
76
33
68
65
Specificity (%)
100
100
100
100
Duodenal
Faeces
duodenal fluid in a similar proportion of patients (68%) but, in 31 (35%) of the hookworm infected patients, the parasite was detected only in the sample of duodenal aspirate and not in faecal specimens. The sensitivity and specificity of faecal and duodenal fluid microscopy are summarized in Table 2. Discussion
The present study indicates that microscopical examination of a single sample of duodenal fluid can identify patients with Strongyloides and hookworm infections for whom multiple stool examinations were negative for these parasites, despite the use of a concentration technique. The findings were particularly striking for Snungyloides, as more than 60% of infected patients had the parasite detected exclusively in duodenal fluid. Previous studies have also shown the low sensitivity of faecal microscopy for diagnosis of strongyloidiasis (JONES, 1950; JONES & ABADIE, 1954). Sensitivity may be increased by using concentration techniques, by examining large volumes of stool., and by obtnning at least 4 or 5 separatefaecal specnnens; under these circumstances the detection rate rises to ~80% (BURKE, 1978; GROVE, 1980) and may reach 90% if each faecal preparation is examined for 5 h or more (PELLETIER, 1984). Thus, exclusion of Strong&ides infection by faecal microscopy is a highly labour-intensive process. It is alarming, however, that 33% of a group of American BurmaThailand ex-prisoners of war with creeping eruption had negative stool examinations for Strongyloides
(PELLETIER, 1984), suggesting that even aggressive faecal microscopy was failing to identify a sub-group of infected patients. Use of the Baermann technique and agar plate culture increases the sensitivity of faecal examination for S. stercoralis (GENTA et al., 1987), although the method is not widely used in most routine laboratories. Although it might be argued that we have not pursued faecal microscopical diagnosis to the same extent as some investigators (PELLETIER, 1984), we consider our findings are likely to reflect current practice in the majority of competent, busy diagnostic laboratories. Our findings with respect to the diagnosis of hookworm infection are also similar, although we found that a smaller proportion (35%) had the parasite exclusively in duodenal fluid. Clearly the potential risks of missing hookworm infection are markedly less than for Strongyloides, although thesefindings emphasize the principle that competent stool microscopy does not exclude infection with these hehninths. The implications of the present study, and of previous work by PELLETIER (1984) and BURKE (1978), is that war veterans from south-east Asia, particularly those who worked on the Burma-Thai railroad, should not be screenedby faecal microscopy alone. This is particularly important with individuals in whom there is strong clinical suspicion of chronic strongyloidiasis, such asthose with creeping eruption, many of whom may still be undetected (GILL & BELL, 1987). Similarly, immunocompromised individuals, including patients with human immunodeficiency virus infection, in whom Strongyloides infection is considered a diagnostic possibility should also be screened by both faecal and duodenal fluid microscopy. Our findings indicate that these 2 approachesto diagnosis are complementary since neither appear to detect all infected patients. The enzyme-linked immunosorbent assayfor specific S. stercoralis antibodies will have an increasingly important part to play in the screening of these patients (GENTA, 1988), particularly as the assaybecomesmore widely available, but we consider at present that microscopical examination of duodenal fluid is a valuable alternative approach to diagnosis in patients suspected of having strongyloidiasis. Acknowledgements M.J.G.F. is a Wellcome Trust senior lecturer. We
gratefully acknowledgefinancial support by the Wellcome Trust.
References Burke, J. A. (1978). Strongyloidiasis in childhood. American Journal of Disease in Childhood, 132, 1130-1136. Genta, R. A. (1988). Predictive value of an enzyme-linked immunosorbent assay (ELISA) for the serodiagnosis of strongyloidiasis. Amerkan Journal of Clinical Pathology, 89, 391-394. Genta, R. M., Weesner, R., Deuce, R. W., HuirgerO’Connor, J. & Waltzer, P. D. (1987). Strongyloidiasis in United States veterans and other wars. Journal of the American Medical Association, 258, 4%52.
Gill, G. V. & Bell, D. R. (1987). Strongyloides stercoralis Infection in Burma Star veterans. British MedicalJournal, 294, 1003-1004. Grove, D. I. (1980). Strongyloidiasis in allied ex-prisoners of war in south-east Asia. British Medical ~oumal, i, 598-601. Igra-Siegman, Y,. Kapila, R., Sen, P., Kaminski, Z. C. & Louria, D. B. (1981). Syndrome of hyperinfection with
831 Strongvloides stercoralis.Reviews of Infectious Diseases, 3,
397-407. Jones? C. A. (1950). Clinical studies in human strongyloidiasis. I. Semeiology. Gastroenrerology,16, 743-756. Jones, C. A. & Abadie, S. H. (1954). Studies in human strongyloidiasis. II. A comparison of the efficacy of diagnosis by examination of feces and duodenal fluid. American Journal of Clinical Pathology, 24, 1154-1158. Kuberski, T. T., Gabor, E. P. & Boudreaux, D. (1975). Disseminated strongyloidiasis. A complication of the immunosuppressed host. Western Journal of Medicine, 122, 504-509. Maayan, S., Wormser, G. I’., Widerhorn, J., Sy, E. R., Kim. Y. H. &Ernst, 1. A. (1987). Stron~loidesstercoralis hyperinfection in a- patient with acquired immune deficiency syndrome. American Journal of Medicine, 83, 945-948.
Pelletier, L. L. (1984). Chronic strongyloidiasis in world war II Far East ex-prisoners of war. American Journal of Tropical Medicine and Hygiene, 3, 55-61. Purtilo, D. T., Meyers, W. M. & Connor, D. H. (1974). Fatal strongyloidiasis in immunosuppressed patients. American Journal of Medicine, 56, 488-493. Smallman, L. A., Young, J. A., Shot&rid-Webb, W. R., Carey, M. P. & Michael, J. (1986). Strongyloides stercoralis hyperinfestation syndrome with Escherichia coli meningitis: report of two cases. 3oumal of Clinical Pathology, 39, 366370.
Sturchler, D. (1987). Parasitic diseaseof the small intestinal tract. In: Baillihe’s Clinical Gastroenterology, vol. 1. London: Bail&e Tmdall, pp. 397-424. Received 9 November 1989; revised 4 June 1990; accepted for publication S June 1990
TRANSACTIONS OFTHEROYALSOCIETY OFTROPICAL MEDICINE ANDHYGIENE
1 Short Report 1 Albendazole in the therapy cutaneous larva migrans
of
S. Sanguigni, M. Marangi, A. Teggi and F. De Rosa Department of Tropical and Infectious Diseases, University of Rome ‘La Sapienza’, Rome, Italy
Cutaneous larva migrans is characterized by the invasion of human shin by nematode larvae which are not normal parasites of man, such as Ancylostoma caninum, A. bras&we or Strongyloididae such as Strong+ides myopotami, S. procyonis and others. All these larvae are unable to complete their life cycle and migrate for a long time, at least one year, causing creeping eruption. The disease is widespread in Africa, South and Central America, southern USA, India, and southeast Asia, and some cases have also been reported from southern France, Spain and Australia (MANSONBAHR & BELL, 1987). The therapy of this illness is usually based on local freezing with ethyl chloride or liquid nitrogen, local application of preparations such as benzimtdazole carbamates(usually mebendazole) in petroleum jelly, or the administration of thiabendazole orally (MANSON-BAHR& BELL, 1987). In our experience local treatments are time consuming and liquid nitrogen Correspondence to Professor Sergio Sanguigni, Istituto di Clinica delle Malattie Tropicali e Infettive, Policlinico Umberto I, Via de1 Policlinico, 00162 Rome, Italy.
(1990) 84, 831
may cause severe necrosis, while oral thiabendazole may cause frequent side effects such as dizziness, nausea, hypotension and rashes. In the past few years we have observed 26 casesof cutaneous larva migrans. All were Italian tourists from South and Central America (18 cases)and Africa (7 cases) or south-east Asia (1 case). ’ Basedon the above considerations we administered to these 26 patients the new benzoimidazole carbamate albendazole, which is absorbed orally and is relatively free of serious side-effects (SAIMOTet al., 1983). Albendazole was given at dosage of 400 mg/d, divided into 2 doses,for 5 d. From the 2nd to 3rd day of therapy all clinical manifestations such as itching and cutaneous reactions disappeared and the larvae stopped moving. In only 2 cases, where the larvae were clearly in hypobiosis, was it necessaryto repeat the treatment at the same dosage, as the larvae remained obviously alive:, the second course of treatment was fully effective. No side effects were recorded and no relapseswere observed after 6 months follow-up. In our opinion albendazole is a real improvement in the therapy of this extremely troublesome, and sometimes severe, illness. References Manson-Bahr, P. E. C. & Bell, D.R., editors (1987). Mason’s Tropical Diseases, 19th edition. London: Bailhere Tindall. Saimot, A. G., Cremieux, A. C., Hay, J. M., Meulemans, A., Giovanangeli, M. D., Delaitre, B. & Coulad, J. P. (1983). Albendaxole as a wtential treatment for human hydatidosis. Lancet, ii, 655-656. y;;ived
18 April 1990; accepted fm publication 3 May