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Comparative features of double-contrast barium studies in patients with isosporiasis and strongyloidiasis
Clinical Radiology(1998) 53, 764-767
Comparative Features of Double-contrast Barium Studies in Patients With Isosporiasis and Strongyloidiasis K. H I Z A W A , M. IIDA,* K. E G U C H I , t K. A O Y A G I , S. TADA,$ Y. K U W A N O , Y. M O C H I Z U K I and M. F U J I S H I M A
Second Department of Internal Medicine and tSecond Department of Pathology, Faculty of Medicine, Kyushu University, Fukuoka; *Division of Gastroenterology, Department of Medicine, Kawasaki Medical School, Kurashiki; and ~iDivision of Gastroenterology, Department of Medicine, Saiseikai Hospital, Kumamoto, Japan Objective: To compare the gastrointestinal features of isosporiasis and strongyloidiasis. Methods: Two patients with isosporiasis and three patients with strongyloidiasis were assessed by double-contrast radiography of the duodenum and small intestine, with reference to histology of the duodenal biopsy specimens. Results: Both conditions affected the duodenum and the proximal jejunum, and showed similar radiographic changes as the diseases progressed. Thus, three patients with diarrhoea lasting 1 year or less showed only minimal or irregularly thickened mucosal folds, which seemed to result from mucosal inflammation. Two patients with long-standing disease periods (17 years and 30 years) presented a markedly granular mucosal appearance with effacement of the folds on radiography. These chronological differences in the radiographic features seemed to reflect the degree of villous atrophy. Conclusion: Isosporiasis has similar radiographic features of strongyloidiasis. Hizawa, K., Iida, M., Eguchi, K., Aoyagi, K., Tada, S. Kuwano, Y., Mochizuki, Y. & Fujishima, M. (1998). Clinical Radiology 53, 7 6 4 - 7 6 7 . Comparative Features of Double-contrast Barium Studies in Patients With Isosporiasis and Strongyloidiasis
Accepted for Publication 20 May 1998
Since the epidemic of human immunodeficiency virus (HIV) infection began, there has been an increasing awareness of various gastrointestinal pathogens in immunocompromised hosts [1-3]. Isosporiasis and strongyloidiasis are parasitic diseases, caused by infestation with Isospora belli and Strongyloides stercoralis, respectively. Both these pathogens inhabit the duodenum and proximal jejunum, where they produce several inflammatory processes within the mucosa, resulting in various morphological changes [4,5]. Radiographic features of strongyloidiasis have been well documented [5-8]. However, there is no description concerning double-contrast barium studies in patients with isosporiasis. Therefore, we attempt to describe the radiographic features of isosporiasis, in comparison with those of strongyloidiasis.
PATIENTS AND METHODS W e included in this study three patients with strongyloidiasis (patients 1 - 3 ) and two patients with isosporiasis (patients 4,5). All of the patients underwent double-contrast radiographic studies of the duodenum and small intestine, and gastroduodenoscopy. On the basis of the histological detection of S. stercolaris or L belti in the duodenal mucosa sample obtained by endoscopic biopsy, we diagnosed the patients as suffering from these parasitic diseases. Symptoms included diarrhoea in five patients, body-weight loss in
Correspondence to: Dr K. Hizawa, Second Department of Internal Medicine, Faculty of Medicine, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-8582, Japan. 9 1998The RoyalCollegeof Radiologists.
three, epigastric pain in one and intermittent pyrexia in one. The duration of symptoms before diagnosis varied from 1 month to 30 years. Hypoproteinaernia (< 6 g/dl) and hypereosinophilia (> 600//zl) were noted in two patients, respectively. Three patients were serologically positive for human T-cell lymphotropic virus type I (HTLV-1), and four patients undergoing lymphostimulating tests to phytohaemagglutinins and concanavalin-A revealed impairment of their cellular immunity.
Table 1 - Summaryof the patientswith strongyloidiasisand isosporiasis
Strongyloidiasis
Isosporiasis
Patient
1
2
3
4
5
Age (years)/gender Duration of symptoms HTLV- 1 antibody Total protein (g/dl) Impaired immunity* Radiographic findings Affected sites Fold effacement Granular mncosa Mural rigidity Histological findings Atrophy of the villi Inflammatory infiltrate Eosinophils Oedema Fibrosis
45/F 1 month + 6.3 4-
63/M 1 year 7.0 NE
55,qVl 30 years + 7.1 4-
53/M 1 year 45.7 +
71/M 17 year 5.5 +
D,J .
D,J 4-44-4-
D,J 4-
.
D,J 4.
D,J 4-44-44-
4Jr+ + . .
4++ + 4.
4-44-4+ -
444+
4-4+4+44-
.
.
Impaired response of T-lymphocytes to phytohaemagglutinins.Degree of radiological and histological findings: - , none; +, mild; + +, prominent. NE, not examined; D, duodenum; J, jejunum.
765
ISOSPORIASIS AND STRONGYLOIDIASIS
(a)
(b)
Fig. 1 - Patient 2 (strongyloidiasis). (a) Double-contrast radiography shows irregularly thickened folds with a mild granular appearance in the duodenum. (b) Histological examination reveals parasitic organisms and inflammatory cell infiltration in the oedematous duodenal mucosa with mild villous atrophy (H & E, x 25).
(b)
(a)
(c) Fig. 2 - Patient 3 (strongyloidiasis). (a) Double-contrast radiography shows a granular mueosal appearance with effacement of the duodenal folds. (b) Granular mucosal changes with effaced folds are also evident in the jejunum. (c) Duodenal biopsy reveals mucosal inflammation and remarkable atrophy of the villi, containing parasitic organisms (H & E, x 50). 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 764-767.
766
CLINICAL RADIOLOGY
(a)
(d)
(b)
(e)
Fig. 3 - Patient 5 (isosporiasis). (a) Double-contrast radiography depicts a granular appearance with effacement of the duodenal folds. (b) The jejunal folds are diffusely flattened and effaced with granular mucosal appearance. (c) Duodenoscopy reveals the granular woven mucosal appearance. (d) Histological examination demonstrates remarkable villous atrophy and fibrotic changes within the duodenal mucosa (H & E, x 25). (e) On duodenal biopsy, a merozoite of 1. belli (arrow) is identified in the epithelial cells (H & E, x 132).
9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 764-767.
ISOSPORIASIS AND STRONGYLOIDIASIS
Double-contrast radiography of the duodenum and small intestine was performed as previously described [9]. These radiographic images were reviewed by one radiologist (K.H.). The degree of the histological findings obtained by endoscopic duodenal biopsy was assessed by one pathologist (K.E.). With reference to the endoscopic and histological findings, the radiographic features of isosporiasis were compared to those of strongyloidiasis.
RESULTS Clinicopathological findings in the patients are summarized in Table 2.
Radiographic Manifestations Radiographic findings of strongyloidiasis were more evident when the disease had been of long-standing. Patient 1 with symptoms of only 1 month's duration showed only minimal thickened folds in the duodenum and proximal jejunum. Patient 2 (disease period of I year), in addition, exhibited mild granular changes within the mucosa (Fig. la). In patient 3 (diseased period of 30 years), there was a prominent granular appearance with effacement of the folds in the duodenum (Fig. 2a) and jejunum (Fig. 2b). In patients with isosporiasis, the duodenum and proximal jejunum were also predominantly involved, and the radiographic changes seemed to be similar to those of strongyloidiasis. Thus, patient 4 with a 1-year history of the disease showed mild granular appearances in the duodenum and jejunum. Patient 5 (disease period of 17 years) manifested a granular woven appearance with mild mural rigidity in the duodenum (Fig. 3a), which was also evident on endoscopy (Fig. 3c). On double-contrast radiography of the small intestine, the jejunal folds were diffusely flattened and effaced, showing fine granular mucosal changes (Fig. 3b).
Histological Findings Parasitic organisms of various developmental stages were identified within the epithelial cells of the descending duodenum (Figs lb, 2c & 3e). Infiltration of mononuclear cells and eosinophils in the lamina propria was recognized in all patients. Mucosal oedema was identified in patients 2 and 4 (Fig. lb). Atrophy of the villi was present in all patients, but particularly prominent in patients 3 and 5 (Figs 2c & 3d), which had a long-term duration of the disease and manifested a remarkable fold effacement with a granular mucosal appearance. Fibrotic change was evident in patient 5 (Fig. 3d). The granular mucosal appearances seemed to reflect the degree of villous atrophy rather than hypoproteinaemia, mucosal inflammation with eosinophilic infiltration, or fibrotic changes. DISCUSSION Gastrointestinal manifestations in strongyloidiasis have been classically divided into three stages with progression of the infestation, including catarrhal, oedematous and
9 1998 The Royal College of Radiologists, ClinicalRadiology, 53, 764-767.
767
ulcerative enteritis [5]. Affected duodenum and proximal jejunum initially show increased mucosal congestion and mucous secretion. Consequent to inflammatory cell infiltration and oedema in the mucosa, thickening and swelling of the intestinal mucosal folds become evident. The inflammatory process and progress of villous atrophy produce a coarse and granular appearance of the mucosa with effacement of the folds. Finally, the deteriorated mucosa is eroded, presenting superficial ulceration and submucosal fibrosis. This present study indicated that radiographic features of isosporiasis were similar to those of strongyloidiasis. Thus, the duodenum and proximal jejunum were also predominantly involved in patients with isosporiasis. The severity of granular mucosa with effacement of the folds progressed as the disease advanced. These radiographic changes seemed to be non-specific, reflecting the degree of villous atrophy. Therefore, encountering such granular small bowel mucosa on radiography, we should carefully differentiate these conditions from other chronic bowel diseases, including Crohn's disease, radiation enteritis, amyloidosis and coeliac disease [5]. On routine examination, it is occasionally difficult to identify tiny and irregularly excreted parasitic organisms within faecal specimens [2,3]. If multiple stool specimens are nondiagnostic, duodenal biopsy may be useful. In immunologically normal hosts, isosporiasis and strongyloidiasis are asymptomatic or self-limited. However, in patients with impaired cellular-immunity, these infestations tend to be frequent and prolonged, and can occasionally progress to life-threatening diarrhoea if overlooked [1-3]. In Japan, both of the diseases are apt to be complicated in patients with HTLV-1 infection (as our patients). In the countries such as Zambia and Zaire, where there are an estimated 20.4 million individuals with HIV infection, the incidence of I. belli infection in the patients ranges from 7.7% to 12% [1,2]. Therefore, we should pay more attention to these long-standing parasitic diseases presenting granular small bowel mucosa, especially in the patients with immunodeficient conditions such as HIV and HTLV-I infections.
REFERENCES I Harries AD, Gossius G. Protozoal infection of the gut in patients with HIV infection. Lancet 1996;348:1248-1249. 2 Goodgame RW. Understanding intestinal spore-forming protozoa: eryptosporidia, microsporidia, isospora, and cyelospora. Annals of Internal Medicine 1996;124:429-441. 3 Heyworth MF, Parasitic diseases in immunocompromized hosts: cryptosporidiosis, isosporiasis, and strongyloidiasis. Gastroenterology Clinics North America 1996;25:691-707. 4 Trier JS, Moxey PC, Schimmel EM et al. Chronic intestinal coccidiosis in man: morphology and response to treatment. Gastroenterology 1974; 66:923-935. 5 Reeder M, Palmer P. Infections and infestations. In: Margulis A, Burhenne J, eds. Alimentary Tract Radiology, 5th edn. St. Louis: Mosby, 1994:931-933. 6 Berkmen YM, Rabinowitz J. Gastrointestinal manifestations of the strongyloidiasis. American Journal of Roentgenology 1972;115:306-311. 7 Dallemand S, Waxman M, Farman J. Radiological manifestations of Strongyloides stercoralis, Gastrointestinal Radiology 1983;8:45-51. 8 Medina LS, Heiken JP, Gold RP. Pipestem appearance of small bowel in strongyloidiasis is not pathognomonic of fibrosis and irreversibility. American Journal of Roentgenology 1992;159:543-544. 9 Aoyagi K, Iida M, Yao T et al. Intestinal lymphangiectasia: value of doublecontrast radiographic study. Clinical Radiology 1994;49:814-819.
Comparative Features of Double-contrast Barium Studies in Patients With Isosporiasis and Strongyloidiasis K. H I Z A W A , M. IIDA,* K. E G U C H I , t K. A O Y A G I , S. TADA,$ Y. K U W A N O , Y. M O C H I Z U K I and M. F U J I S H I M A
Second Department of Internal Medicine and tSecond Department of Pathology, Faculty of Medicine, Kyushu University, Fukuoka; *Division of Gastroenterology, Department of Medicine, Kawasaki Medical School, Kurashiki; and ~iDivision of Gastroenterology, Department of Medicine, Saiseikai Hospital, Kumamoto, Japan Objective: To compare the gastrointestinal features of isosporiasis and strongyloidiasis. Methods: Two patients with isosporiasis and three patients with strongyloidiasis were assessed by double-contrast radiography of the duodenum and small intestine, with reference to histology of the duodenal biopsy specimens. Results: Both conditions affected the duodenum and the proximal jejunum, and showed similar radiographic changes as the diseases progressed. Thus, three patients with diarrhoea lasting 1 year or less showed only minimal or irregularly thickened mucosal folds, which seemed to result from mucosal inflammation. Two patients with long-standing disease periods (17 years and 30 years) presented a markedly granular mucosal appearance with effacement of the folds on radiography. These chronological differences in the radiographic features seemed to reflect the degree of villous atrophy. Conclusion: Isosporiasis has similar radiographic features of strongyloidiasis. Hizawa, K., Iida, M., Eguchi, K., Aoyagi, K., Tada, S. Kuwano, Y., Mochizuki, Y. & Fujishima, M. (1998). Clinical Radiology 53, 7 6 4 - 7 6 7 . Comparative Features of Double-contrast Barium Studies in Patients With Isosporiasis and Strongyloidiasis
Accepted for Publication 20 May 1998
Since the epidemic of human immunodeficiency virus (HIV) infection began, there has been an increasing awareness of various gastrointestinal pathogens in immunocompromised hosts [1-3]. Isosporiasis and strongyloidiasis are parasitic diseases, caused by infestation with Isospora belli and Strongyloides stercoralis, respectively. Both these pathogens inhabit the duodenum and proximal jejunum, where they produce several inflammatory processes within the mucosa, resulting in various morphological changes [4,5]. Radiographic features of strongyloidiasis have been well documented [5-8]. However, there is no description concerning double-contrast barium studies in patients with isosporiasis. Therefore, we attempt to describe the radiographic features of isosporiasis, in comparison with those of strongyloidiasis.
PATIENTS AND METHODS W e included in this study three patients with strongyloidiasis (patients 1 - 3 ) and two patients with isosporiasis (patients 4,5). All of the patients underwent double-contrast radiographic studies of the duodenum and small intestine, and gastroduodenoscopy. On the basis of the histological detection of S. stercolaris or L belti in the duodenal mucosa sample obtained by endoscopic biopsy, we diagnosed the patients as suffering from these parasitic diseases. Symptoms included diarrhoea in five patients, body-weight loss in
Correspondence to: Dr K. Hizawa, Second Department of Internal Medicine, Faculty of Medicine, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-8582, Japan. 9 1998The RoyalCollegeof Radiologists.
three, epigastric pain in one and intermittent pyrexia in one. The duration of symptoms before diagnosis varied from 1 month to 30 years. Hypoproteinaernia (< 6 g/dl) and hypereosinophilia (> 600//zl) were noted in two patients, respectively. Three patients were serologically positive for human T-cell lymphotropic virus type I (HTLV-1), and four patients undergoing lymphostimulating tests to phytohaemagglutinins and concanavalin-A revealed impairment of their cellular immunity.
Table 1 - Summaryof the patientswith strongyloidiasisand isosporiasis
Strongyloidiasis
Isosporiasis
Patient
1
2
3
4
5
Age (years)/gender Duration of symptoms HTLV- 1 antibody Total protein (g/dl) Impaired immunity* Radiographic findings Affected sites Fold effacement Granular mncosa Mural rigidity Histological findings Atrophy of the villi Inflammatory infiltrate Eosinophils Oedema Fibrosis
45/F 1 month + 6.3 4-
63/M 1 year 7.0 NE
55,qVl 30 years + 7.1 4-
53/M 1 year 45.7 +
71/M 17 year 5.5 +
D,J .
D,J 4-44-4-
D,J 4-
.
D,J 4.
D,J 4-44-44-
4Jr+ + . .
4++ + 4.
4-44-4+ -
444+
4-4+4+44-
.
.
Impaired response of T-lymphocytes to phytohaemagglutinins.Degree of radiological and histological findings: - , none; +, mild; + +, prominent. NE, not examined; D, duodenum; J, jejunum.
765
ISOSPORIASIS AND STRONGYLOIDIASIS
(a)
(b)
Fig. 1 - Patient 2 (strongyloidiasis). (a) Double-contrast radiography shows irregularly thickened folds with a mild granular appearance in the duodenum. (b) Histological examination reveals parasitic organisms and inflammatory cell infiltration in the oedematous duodenal mucosa with mild villous atrophy (H & E, x 25).
(b)
(a)
(c) Fig. 2 - Patient 3 (strongyloidiasis). (a) Double-contrast radiography shows a granular mueosal appearance with effacement of the duodenal folds. (b) Granular mucosal changes with effaced folds are also evident in the jejunum. (c) Duodenal biopsy reveals mucosal inflammation and remarkable atrophy of the villi, containing parasitic organisms (H & E, x 50). 9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 764-767.
766
CLINICAL RADIOLOGY
(a)
(d)
(b)
(e)
Fig. 3 - Patient 5 (isosporiasis). (a) Double-contrast radiography depicts a granular appearance with effacement of the duodenal folds. (b) The jejunal folds are diffusely flattened and effaced with granular mucosal appearance. (c) Duodenoscopy reveals the granular woven mucosal appearance. (d) Histological examination demonstrates remarkable villous atrophy and fibrotic changes within the duodenal mucosa (H & E, x 25). (e) On duodenal biopsy, a merozoite of 1. belli (arrow) is identified in the epithelial cells (H & E, x 132).
9 1998 The Royal College of Radiologists, Clinical Radiology, 53, 764-767.
ISOSPORIASIS AND STRONGYLOIDIASIS
Double-contrast radiography of the duodenum and small intestine was performed as previously described [9]. These radiographic images were reviewed by one radiologist (K.H.). The degree of the histological findings obtained by endoscopic duodenal biopsy was assessed by one pathologist (K.E.). With reference to the endoscopic and histological findings, the radiographic features of isosporiasis were compared to those of strongyloidiasis.
RESULTS Clinicopathological findings in the patients are summarized in Table 2.
Radiographic Manifestations Radiographic findings of strongyloidiasis were more evident when the disease had been of long-standing. Patient 1 with symptoms of only 1 month's duration showed only minimal thickened folds in the duodenum and proximal jejunum. Patient 2 (disease period of I year), in addition, exhibited mild granular changes within the mucosa (Fig. la). In patient 3 (diseased period of 30 years), there was a prominent granular appearance with effacement of the folds in the duodenum (Fig. 2a) and jejunum (Fig. 2b). In patients with isosporiasis, the duodenum and proximal jejunum were also predominantly involved, and the radiographic changes seemed to be similar to those of strongyloidiasis. Thus, patient 4 with a 1-year history of the disease showed mild granular appearances in the duodenum and jejunum. Patient 5 (disease period of 17 years) manifested a granular woven appearance with mild mural rigidity in the duodenum (Fig. 3a), which was also evident on endoscopy (Fig. 3c). On double-contrast radiography of the small intestine, the jejunal folds were diffusely flattened and effaced, showing fine granular mucosal changes (Fig. 3b).
Histological Findings Parasitic organisms of various developmental stages were identified within the epithelial cells of the descending duodenum (Figs lb, 2c & 3e). Infiltration of mononuclear cells and eosinophils in the lamina propria was recognized in all patients. Mucosal oedema was identified in patients 2 and 4 (Fig. lb). Atrophy of the villi was present in all patients, but particularly prominent in patients 3 and 5 (Figs 2c & 3d), which had a long-term duration of the disease and manifested a remarkable fold effacement with a granular mucosal appearance. Fibrotic change was evident in patient 5 (Fig. 3d). The granular mucosal appearances seemed to reflect the degree of villous atrophy rather than hypoproteinaemia, mucosal inflammation with eosinophilic infiltration, or fibrotic changes. DISCUSSION Gastrointestinal manifestations in strongyloidiasis have been classically divided into three stages with progression of the infestation, including catarrhal, oedematous and
9 1998 The Royal College of Radiologists, ClinicalRadiology, 53, 764-767.
767
ulcerative enteritis [5]. Affected duodenum and proximal jejunum initially show increased mucosal congestion and mucous secretion. Consequent to inflammatory cell infiltration and oedema in the mucosa, thickening and swelling of the intestinal mucosal folds become evident. The inflammatory process and progress of villous atrophy produce a coarse and granular appearance of the mucosa with effacement of the folds. Finally, the deteriorated mucosa is eroded, presenting superficial ulceration and submucosal fibrosis. This present study indicated that radiographic features of isosporiasis were similar to those of strongyloidiasis. Thus, the duodenum and proximal jejunum were also predominantly involved in patients with isosporiasis. The severity of granular mucosa with effacement of the folds progressed as the disease advanced. These radiographic changes seemed to be non-specific, reflecting the degree of villous atrophy. Therefore, encountering such granular small bowel mucosa on radiography, we should carefully differentiate these conditions from other chronic bowel diseases, including Crohn's disease, radiation enteritis, amyloidosis and coeliac disease [5]. On routine examination, it is occasionally difficult to identify tiny and irregularly excreted parasitic organisms within faecal specimens [2,3]. If multiple stool specimens are nondiagnostic, duodenal biopsy may be useful. In immunologically normal hosts, isosporiasis and strongyloidiasis are asymptomatic or self-limited. However, in patients with impaired cellular-immunity, these infestations tend to be frequent and prolonged, and can occasionally progress to life-threatening diarrhoea if overlooked [1-3]. In Japan, both of the diseases are apt to be complicated in patients with HTLV-1 infection (as our patients). In the countries such as Zambia and Zaire, where there are an estimated 20.4 million individuals with HIV infection, the incidence of I. belli infection in the patients ranges from 7.7% to 12% [1,2]. Therefore, we should pay more attention to these long-standing parasitic diseases presenting granular small bowel mucosa, especially in the patients with immunodeficient conditions such as HIV and HTLV-I infections.
REFERENCES I Harries AD, Gossius G. Protozoal infection of the gut in patients with HIV infection. Lancet 1996;348:1248-1249. 2 Goodgame RW. Understanding intestinal spore-forming protozoa: eryptosporidia, microsporidia, isospora, and cyelospora. Annals of Internal Medicine 1996;124:429-441. 3 Heyworth MF, Parasitic diseases in immunocompromized hosts: cryptosporidiosis, isosporiasis, and strongyloidiasis. Gastroenterology Clinics North America 1996;25:691-707. 4 Trier JS, Moxey PC, Schimmel EM et al. Chronic intestinal coccidiosis in man: morphology and response to treatment. Gastroenterology 1974; 66:923-935. 5 Reeder M, Palmer P. Infections and infestations. In: Margulis A, Burhenne J, eds. Alimentary Tract Radiology, 5th edn. St. Louis: Mosby, 1994:931-933. 6 Berkmen YM, Rabinowitz J. Gastrointestinal manifestations of the strongyloidiasis. American Journal of Roentgenology 1972;115:306-311. 7 Dallemand S, Waxman M, Farman J. Radiological manifestations of Strongyloides stercoralis, Gastrointestinal Radiology 1983;8:45-51. 8 Medina LS, Heiken JP, Gold RP. Pipestem appearance of small bowel in strongyloidiasis is not pathognomonic of fibrosis and irreversibility. American Journal of Roentgenology 1992;159:543-544. 9 Aoyagi K, Iida M, Yao T et al. Intestinal lymphangiectasia: value of doublecontrast radiographic study. Clinical Radiology 1994;49:814-819.