Proteinuria, hematuria, and leukocyturia in children with mixed urinary and intestinal schistosomiasis

Kidney International, Vol. 28 (1985), pp. 520—525

Proteinuria, hematuria, and leukocyturia in children with mixed urinary and intestinal schistosomiasis EKKEHARD DOEHRING, JOCHEN H. H. EHRICH, UDO VESTER, HERMANN FELDMEIER, ULRICH P000ENSEE, and JOHANNES BRODEHL Department of Pediatric Nephrology and Metabolic Disorders, Medizinische Hochschule, Hannover, and Department of Immunodiagnosis and Immunoparasitology, Landesinstitut fur Tropenmedizin, Berlin, and Department of Tropical Hygiene, Bernhard-Nocht-Insiitut für Schffs und Tropenkrankheiten, Hamburg, Federal Republic of Germany

Protelnuria, hematurla, and leukocyturia in children with mixed sessment

valeurs physiologiques 5 mois aprCs le traitement. Ces résultats sugger-

ent que Ia protéinurie, I'Crythocyturie, et Ia leucocyturie dans La

urinary and intestinal schistosomiasis. Quantitative parasitological as-

and quantitative analysis of proteinuria, hematuria, and

schistosomaise mixte Ctiaent d'origine post'rénale.

leukocyturia were carried out in 182 Sudanese schoolboys with mixed urinary and intestinal schistosomiasis. Pathological proteinuria was found in 73% of patients (median = 380, 95% confidence limits = 200 to

500 mg/liter). The median protein/creatinine ratio was 0.54. SDS polyacrylamide gel electrophoresis showed an excretion of albumin, transferrin, and IgG consistent with a postrenal pattern of proteinuria. Pathological erythrocyturia occurred in 84% of patients (median = 255, 95% CL = 95 to 629 cel1s/s1) and leukocyturia in 77% of patients (median = 148, 95% CL = 93 to 246 cells/pi). Phase contrast microscopy revealed intact erythrocytes, suggestive of postrenal hemorrhage. Proteinuria, erythrocyturia, and leukocyturia correlated significantly with the ova excretion in the urine, but not with egg excretion in the

stool. Oxamniquine reduced ova excretion in the stool but did not

Pathological urine findings such as proteinuna (PU), leukocyturia (LU), and erythrocyturia (EU) have been known to be associated with urinary schistosomiasis since the early description of the disease [1]. Most studies comparing ova output and pathological urine findings have only used test strip analysis for PU, EU, and LU [2—4]. Thus, in this study, the prevalence of PU, EU, and LU in patients with schistosomiasis

influence pathological urine findings. In patients treated effectively with

was investigated by quantitative techniques. To assess the

Praziquantel or Metrifonate, pathological PU, EU, and LU decreased markedly I month post treatment. PU in severely proteinuric patients reached physiological values 5 months post therapy. We suggest that the proteinuria, erythrocyturia, and leukocyturia in mixed schistosomiasis were of postrenal origin.

haematobium and mansoni infection were chosen. The

Protéinurle, hématurie, et leucocyturie chez des enfants atteints de schistosomiase mixte urinaire et intestinale. Une evaluation quantitative parasitaire et une analyse quantitative de Ia protéinurie, de l'hématurie,

et de La leucocyturie ont eté effectuées chez 182 écoliers soudanais atteints de schistosomiase mixte urinaire et intestinale. Une protéinurie

pathologique a éte trouvée chez 73% des malades (mediane = 380, intervalle de confiance 95% = 200 fi 500 mg/litre). Le rapport median

protCine/créatinine Ctait de 0.54. Une électrophorese sur gel de polyacrylamide-SDS a montré une excretion d'albumine, de transferrine, et d'lgG compatibles avec un aspect post'renal de Ia protéinurie. Une erythrocyturie pathologique Ctait présente chez 84% des malades (mediane = 225, 95% CL = 95 it 629 cellules/td) et une leucocyturie chez 77% des malades (mediane = 148, 95% CL = 93 a 246 cellules/.d). La microscopic en contraste de phase a révélé des érythrocytes intacts, suggCrant une hémorragie post-rCnale. La protéinurie, l'erythrocyturie, et Ia leucocyturie étaient significativement corrClées it l'excrCtion

influence of ova excretion in both urine and stool on pathological urine findings, patients suffering from mixed Schistosoma

reversibility of pathological urine findings was assessed after treatment with Praziquantel, Metrifonate, or Oxamniquine, which exert different effects on S. haematobium and S. mansoni ova output. Previous studies support the hypothesis that pathological urine findings have a postrenal origin [3, 5]. In contrast, other authors have raised doubts about the postrenal origin of PU [6] and consider renal lesions to be responsible for PU [7—9]. In this study, qualitative analysis of urinary proteins according to their

molecular weight and phase contrast microscopy of erythrocytes were carried out to determine the origin of PU and EU. Methods

Study area and patients

d'oeufs dans les urines, mais non avec L'excrétion d'oeufs dans les selles. L'oxamniquine a rCduit l'excrétion d'oeufs dans les selles mais

The investigations were conducted in Heibeika, a village in

efficacement avec du Praziquantel ott du Métrifonate, PU, EU, et LU pathologiques ont diminué de facon marquee un mois aprCs le traitement. PU chez les malades sevérement protCinuriques a atteint des

be highly endemic for Schistosomiasis haematobium and

n'a pas influence les anomalies urinaires. Chez des malades traitCs the Gezira-irrigated area of the Sudan. This region is known to

mansoni [10]. One-hundred eighty-two patients with an age range of 6 to 13

years who presented with a mixed S. haematobium and mansoni infection were admitted to the study. Received for publication October 24, 1984, and in revised form March 8, 1985

© 1985 by the International Society of Nephrology

Informed consent. Informed consent was obtained in the Arabic language through parents or family representatives at an introductory assembly.

520

Proteinuria, hematuria, and leukocyturia in schistosomiasis

521

Table 1. Percentage of patients with mixed schistosomiasis and Clinical and blood investigations. All patients underwent a compathological urine findings plete physical examination. Thick and thin blood smears were done, and the hematocrit was determined by a battery-operated hematocrit Non-infected Infected children children centrifuge. Serum specimens were kept at a temperature of —20°C N=182 N=17 and investigated later for electrolytes, creatinine, BUN, total protein, and cholesterol by routine methods. Proteinuria, Urine and stool collections. At 11:00 A. M. all patients re> 100 mg/liter 0/17 133/182 (73.1%) ceived a 250 ml soda drink to minimize day-to-day variation of Protein/creatinine ratio, Not Done > 0.2 13 1/182 (72%) ova output [11]. Urine was collected under surveillance 45 mm later. After that, the patients were instructed to deliver a stool Erythrocyturia, 1/17 153/182 (84.1%) > 5 per pi specimen for parasitological examination. Leukocyturia, 0/17 140/182 (76.9%) > 20 per s1 Urine examination. After reagent strip analysis (Combur 9, Ova excretion in urine Boehringer, Mannheim, Federal Republic of Germany), egg 0/17 and stool 182/182 (100%) excretion in the urine was determined quantitatively on 3

consecutive days using the filtration-trypan-blue-staining technique [12]. Using a Neubauer Chamber, quantitative analyses of eryth-

rocyte and leukocyte counts per jsl urine were carried out

within 1 hr after the voiding of urine on 2 consecutive days. A

phase contrast microscope was used to assess erythrocyte morphology according to the criteria published by Birch et al [13].

were computed from the whole study group and 95% confidence limits (95% CL) as well as ranges were given. Progression analysis was carried out after transformation of data from individual urine specimens according to the formula x' = log (x + 1). The non-parametric Wilcoxon matched-pairs signed rank test

To measure PU, aliquots of urine were centrifuged. A 2 ml was used to assess the significance of differences, where sample was deep-frozen and kept at a temperature of —20°C appropriate. until processed in Germany 4 wks later. Proteinuria was deterResults mined quantitatively by the Coomassie blue-dye binding test Physical examination was uneventful except for two cases of [14]. Qualitative characterization of urinary proteins according to moderate splenomegaly. The patients were not anemic and no their molecular weight was achieved in unconcentrated urine malaria parasites were detected in the blood. Serum creatinine, specimens by SDS polyacrylamide gel electrophoresis [15]. The

BUN, and electrolytes were within normal limits, as were serum protein and cholesterol. Urinary test reagent strips

(mg/liter) and creatinine concentration (mg/liter), PU in excess of 100 mg/liter and a protein/creatinine ratio of more than 0.2 were considered to be pathological [161. More than 5 erythrocytes and 20 leukocytes/pi of urine were regarded as abnormal. Stool examination. Ova excretion in the stool was quantified using a modification of the Kato thick smear technique [17]. Three thick smears were prepared on each of the 3 consecutive days. Results were expressed as number of ova per g stool. Treatment. Patients were allotted at random to 4 different groups. Group A was treated with a single dose of Praziquantel (40 mg/kg); Group B with Metrifonate (twice in a dose of 10 mg/kg with a 2-wk interval), and Group C with a single dose of Oxamniquine (60 mg/kg). Group D received a multivitamin tablet as placebo. Those children still excreting viable ova at the end of the study were treated with Praziquantel (40 mg/kg). All patients received a complete tetanus vaccination. Control Group. Since the prevalence of infection in Heibeika was very high in the age group under investigation, 17 male students were chosen from a neighboring village 20 km away. Ova output in those students was excluded by repeated thorough parasitological examinations.

revealed nitrite excretion in only two cases. Abnormal proteinuria was found in 73.1% of patients. Pathological hematuria occurred in 84.1% and leukocyturia in 76.9% (Table I). Except for one case of microhematuria, physiological values were found in the control group (Table 1). Median ova output in the urine was 84.4 per 10 ml (range = 0.1 to 9009). Median ova excretion per g stool was 680 (range = 8 to 4849). Accordingly, a marked pathological PU was found (median of urinary protein concentration 0.38 g/liter, range = 0.02 to 6.37; median protein/creatinine ratio = 0.54, range = 0.02 to 8.15). Median EU was 255 cells per jd (range = 0 to 35,568) and median LU 148 cells per l of urine (range = 0 to 7,632). There was a significant correlation between PU, EU and LU with ova excretion in the urine (Fig. 1). The correlation coefficients were 0.86 for PU and 0.84 and 0.83 for EU and LU. In contrast, there was no significant correlation between pathological urine findings and ova output in the stool. In all patients with a PU of more than 100 mg/liter, qualitative electrophoretic assessment of urinary proteins exhibited a high molecular weight pattern consisting mainly of albumin, trans-

protein/creatinine ratio was calculated from urinary protein

Statistical evaluation

The medians of urinary ova output and PU were calculated for each patient from urine samples collected on 3 consecutive days. Accordingly, medians of EU and LU were calculated from 2 urine samples. Medians of median individual urinary findings

ferrin, and IgG (Fig. 2). The albumin/transferrin ratio was similar to that in the serum. A protein band of about 45,000 daltons appeared in most of the electrophoreses carried out. The protein pattern resembled the one found in the serum. Low molecular weight proteins such as a 1 microglobulin, lysozyme

or f3 2 microglobulin were absent in all patients studied. A protein band of 15,000 daltons could be identified as hemoglobin chains. Phase contrast microscopy of EU revealed normal disc

forms indicating postrenal bleeding. Deformed erythrocytes,

522

Doehring et a! A

urine findings reversed after treatment with Praziquantel and Metrifonate (Table 2). PU, EU, and LU were within physiolog-

10

ical limits 1 month alter therapy with Praziquantel. After

a)

0)

C a)

0

0

0.1

—

0 86

___________________________________________

0.01

100

10

1

1,000

10,000

B

Discussion

a)

C

1,000 a)

0. U)

a)

0

almost negligible ova excretion at that point in time. PU reached physiological values 5 months post treatment.

Ova output per 10 ml urine

'-a

Metrifonate treatment, there was a marked decrease in pathological urine findings, but no return to physiological values. In contrast, no significant reduction in urinary egg output and urine findings occurred after treatment with Oxamniquine or placebo. Table 3 depicts those patients who had a high PU before therapy, that is, in excess of 1 g/liter and who were effectively treated for S. haematobium ova excretion in the urine. Median ova excretion was 1,257 per 10 ml before treatment and decreased to 5.4 and 2.8, 1 and 5 months post therapy, respectively. PU, EU, and LU I month post treatment were reduced drastically, but were still markedly pathological despite

100

-C

P<0.0001

U.!

10

Patients with urinary schistosomiasis frequently have pathological proteinuria, hematuria, and leukocyturia [2, 18, 19]. The previously reported hypothesis of a correlation between ova output and pathological urine findings has so far been based upon a urine analysis using reagent strip tests to assess PU, EU, and LU [2, 31. However, these tests are semiquantitative only, and accuracy is limited by a number of interfering agents [20]. The main disadvantage of the previously used reagent strip index [2] for differentiating physiological from pathological urinary findings in patients with urinary schistosomiasis is the

relatively rough score which renders the interpretation of individual results difficult. These limiting factors of reagent strip tests were eliminated in the present study by using quantitative measurements. The only other quantitative data so far reported

10

100

1000

10,000

were provided by Dukes et al. [21] who found a correlation between LU and urinary ova output similar to the one reported

Ova output per 10 ml urine

here. The close correlation between urinary ova output and pathological urine findings as assessed quantitatively thus pro-

vides the basis for the use of reagent strips as an indirect 10,000

diagnostic tool in screening programs for urinary schistosomiasis. The origin of PU in urinary schistosomiasis has so far been controversial. Glomerular changes have been incriminated as a

a)

C

0

1,000

source of PU [9, 22, 23], possibly on the basis of immune complex glomerulonephritis [61. These results contrast with

a)

0. (a

100

I

10

10

100

1,000

10,000

Ova output per 10 ml urine

Fig. 1. Linear correlation between PU (A), EU (B), LU(C) and ova

excretion in the urine (N = 182).

those of other authors [24, 25] who found no significant association between urinary schistosomiasis and nephrotic syndrome. Nenna, Bouvry, and Delon [26] considered chronic renal insufficiency due to glomerulonephritis and interstitial nephritis to be an exceptional presentation of the disease. Mott et al [3] showed that the level of PU was related to the intensity of infection and a postrenal origin was therefore suggested. This is in accordance with Wilcocks and Manson-Bahr [27] who regarded the PU of up to three grams per liter as loss from the

bladder wall. Radiographic as well as postmortem studies demonstrated the primary involvement of the bladder and lower ureter in urinary schistosomiasis [28, 29]. The present data indicate that the associated pathological PU may be of postrenal origin. A glomerular PU appears to be most

indicative of transglomerular blood loss, were detected in only unlikely because of the results of SDS-PAGE analysis: the a minority of total erythrocytes. Along with the diminution of urinary ova output, pathological albumin/transferrin ratio in the urine was equal to that in the

523

Proteinuria, hematuria, and leukocyturia in schistosomiasis

Unconcentrated urines of four patients

Albumin standard

1

2

4

3

IgG

Transferrin

Albumin

Fig. 2. The characterization of urinary proteins according to their molecular weight shows a pattern similar to the one in the serum. Table 2. Results of ova output and urine findings before and 1 month after therapy for four different groups categorized according to pharmacological therapy Group A

Group B (N 42)

(N = 56) Ova excretion, per 10 ml urine Ova excretion,

perg stool Proteinuria, g per liter Erythrocyturia,

perpi

Leukocyturia,

per 1.d

BT

AT

68 39 to 125 744 581 to 836 0.42 0.22 to 0.62

0.9 0.2 to 2.8 0.09 0.05 to 0.12

159 34 to 627

0 to 2

0 0 toO 1

144

4

54 to 296

1 to 13

BT

Group C

Group D

(N = 58) AT

(N = 26)

BT

AT

BT

AT

140 14 to 263 680 365 to 1338 0.24

72 24 to 243 675 265 to 1150

106

0.5

54

38 to 315 542 462 to 722 0.44 0.2 to 0.73 503 72 to 930 264 72 to 645

0.1 to 1.5

24 to 166

49 22 to 80

610 345 to 790

698 537 to 823 0.26 0.11 to 0.56

0 to 10 0.32 0.21 to 0.46

0.09 0.07 to 0.15

0

31

241

96

ito 112

21 to 873

36 to 384

0.09 to 0.59 290 54 to 1224

0.32 0.14 to 0.35 323 51 to 864

19

117

173

145

161

3 to 50

30 to 246

65 to 300

22 to 457

57 to 268

Definitions are: Group A, treated with Praziquantel; Group B, treated with Metrifonate; Group C, treated with Oxamniquine; and Group D, treated with vitamins as placebo. Numbers indicate medians and 95% confidence limits. Abbreviations are: BT, before therapy; AT, one month after therapy.

serum; second, a protein band of around 45,000 daltons ap- complex glomerulonephritis occurs in patients with liver fipeared, which can be found with postrenal serum leakage [30]. brosis and portal hypertension only [32, 33]. The pathogenesis Tubular PU could be ruled out by the absence of typical low may be comparable in part to the IgA-glomerulonephritis that molecular weight proteins in the urine [311. The close correla- occurs in patients with alcohol toxic liver cirrhosis and portal tion between rapid reverse of urinary egg excretion and PU hypertension [34]. None of the patients reported here had liver after treatment, as also reported by Wilkins et al. [4], favors cirrhosis and portal hypertension as proven by clinical and postrenal PU. However, I month post treatment PU had not yet laboratory data. Species-specific treatment of S. mansoni parreverted to normal, despite the fact that ova output was asites with Oxamniquine did not influence the urinary protein comparable to those patients who initially presented with PU loss or excretion of cells in the urine. Thus it was concluded less than 100 mg/liter before therapy. It can be suggested that that the concomitant S. mansoni infection in our patients did PU in heavily infected patients may not only be caused by ova not contribute substantially to PU, EU, and LU. penetration but also by bladder lesions which may take longer The close correlation between urinary ova output and PU to heal. suggests that PU may be caused directly by penetration of ova The association between glomerulonephritis and S. mansoni through the bladder mucosa. This is supported by the temporal infection seems to be established [321. Yet, the pathogenic relation between circadian variation of ova excretion and PU mechanism remains unclear, and it may well be that immune [35] and the cystoscopical findings of Abdel-Salam and Ehsan

Doehring et a!

524

Table 3. Results of parasitological and urine analyses of patients with

heavy PU (N = 23)

Ova excretion, per 10 ml

Before therapy

One month post therapy

Five months post therapy

1257

5.4 3.4 to 22 Oto9O

2.8 1.2 to 7.7

References

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144

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