Gallbladder Disease in Young Congolese with Sickle Cell Anemia: An Ultrasound Survey
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1 Gallbladder Disease in Young Congolese with Sickle Cell Anemia: An Ultrasound Survey by B. Longo-Mbenza, a R. Ngiyulu, a P. Kizunda, b M. Kaluila, b and Nkiabungu Bikangi c a Division of Ultrasounds, Lomo Medical, Kinshasa/Limete, Democratic Republic of Congo b Centre de Traitement de l Anémie SS, Kinshasa-Yolo, Democratic Republic of Congo c Ceplanut, Kinshasa-Gombe, Democratic Republic of Congo Summary Patients with sickle cell anemia have been shown to present with a high prevalence of gallbladder disease. Relatively few data exist on the prevalence of gallbladder disease in Africans with autosomal recessive gene for sickle hemoglobin. To establish this relationship, we examined the 1-year incidence of gallbladder disease among 190 consecutive children and young adults with sickle cell anemia aged 3 24 years using ultrasound. There were 130 males (68.4 per cent) and 60 females (31.6 per cent). Incidence of cholelithiasis, cholecystitis, hydrops of gallbladder, and biliary sludge were 58.4, 25.3, 18.4, and 2.1 per cent, respectively. Of the 190 patients, 61 (37.3 per cent) presented hepatobiliary symptoms. The incidence of cholelithiasis depended on age. The age group years and leucocytes > 10000/mm 3 were considered as risk factors of the cholelithias onset, while female gender was isolated as a risk factor for the hydrops of the gallbladder outcome. In conclusion, the ultrasonographic examination is recommended for patients with hepatobiliary symptoms with respect to the high prevalence of the autosomal recessive gene for sickle hemoglobin in Congo, Central Africa. Introduction Patients with sickle cell disease (SCD) have been shown to have elevated frequencies of gallbladder disease. Cholelithiasis is present in between 6 and 55 per cent of children with SCD. 1 9 The prevalence of cholelithiasis in adult populations has been reported to be 6 37 per cent. 1,3,4 In sickle cell anemia, the incidence of cholelithiasis increases with age, and it is higher over the age of 10 years. 7 Most studies were concentrated in countries with a low prevalence of carriers of the autosomal recessive gene for sickle hemoglobin. 10 Little research has been conducted on cholelithiasis related to SCD in Africa, except in Nigeria and Congo Brazzaville Patients with chronic hemolytic disease induced by SCD are prone to present with painful crises involving the bones, joints, chest, and abdomen. The aim of this study was to establish the incidence of gallbladder disease in a Acknowledgements This work was supported, in part, by a grant from ODEX Company, Mvumbi Puati; chairman, Kinshasa-Matadi. The authors thank Prof. Dr A. Lurhuma, Dr M. Kabakele and Prof. Dr J. M. Mbuyi Mwamba, the Managing Committee of the Institute in Medical Research, Kinshasa, DRC. Correspondence: Prof. Benjamin Longo-Mbenza, University of Kinshasa, B.P. 783, Kinshasa XI, Congo, République Démocratique du Congo. <longombenza@caramail.com>. larger consecutive number of young Congolese with SCD with abdominal complaints at the time of examination. Materials and Methods Population Patients seen as outpatients at the sickle cell center of Yolo area, Kinshasa, were referred to the Laboratory of ultrasounds at Lomo Medical, Kinshasa Limete, on an unselected basis from January to December Hemoglobin was evaluated by electrophoresis. None of these patients had ever been diagnosed with gallstones in the past. Disease definitions After the patient fasted overnight, the examination consisted of a general physical examination, measurement of height and weight, a collection of venous blood for laboratory testing, an ultrasonography and a roentgenogram of the abdomen. Laboratory evaluation included determinations of hemoglobin, erythrocyte sedimentation rate (ESR), bilirubin, alkaline phosphatase, total cholesterol, and triglycerides. Ultrasonography was performed using a Genesis-Biosound real-time with a 7.5 MHz transducer for evaluation of the gallbladder and related ductal anatomy. Patients were examined in the supine position and Journal of Tropical Pediatrics, Vol. 50, No. 2 Oxford University Press 2004; all rights reserved 73
2 FIG. 1. Age distribution of all patients with sickle cell anemia, and patients with sickle cell anemia and cholethiasis. then on the left lateral decubitus position or in the erect position to assess the mobility of sludge or stones. Gallstones were identified based on characteristic shadowing and movement with gravity. All patients were also investigated by a supine roentgenogram of the abdomen. Gallbladder disease was defined as the presence of gallstones, hydrops of gallbladder, biliary sludge, and cholecystits visualized on ultrasound or as the occurrence of previous cholecytectomy. Sludge was defined as echogenic material within the gallbladder lumen that layered and changed shape and position on moving the patient. The radiological review of images confirmed the disease definitions. Statistical analysis Comparison of means was done using the Student s t-test. To assess pairwise association of overt disease categories, standard 2 statistics were used. We used the analysis of variance techniques to assess the impact of gallbladder disease on quantitative measures. Odds ratios (OR) with 95 per cent confidence intervals (95% CI) were calculated. The Mantel Haenszel test was applied to evaluate the differences between categories. A probability (p) of less than 0.05 was considered as significant. Results The age distribution of these 190 patients ranged from 3 to 24 years and is shown in Fig. 1. Approximately two-thirds of the patients were 15 years of age or older. There were 130 males (68.4 per cent) and 60 females (31.6 per cent) in the series, and the sex ratio was 2.2 men : 1 woman. Table 1 presents the characteristics of the study population. Females were older and heavier than males, while males were taller and had the highest levels of hemoglobin and leucocyte counts. Of the 190 patients, 111 were found, through ultrasonography, to have cholelithiasis (incidence, 58.4 per cent), 48 with cholecytitis (incidence, 25.3 per cent) and 35 with hydrops of gallbladder (incidence, 18.4 per cent). Hepatomegaly and biliary sludge were observed within 155 (81.6 per cent) and four patients (2.1 per cent), respectively. Table 2 depicts the sex-specific incidence of gallbladder disease. The incidences of cholelithiasis and cholecytitis were similar in both males and females. Hydrops and dilated common duct were seen more in females (30 per cent) than in males (13.1 per cent); p < The presence of hepatomegaly was more established in males (88.5 per cent) than in females (66.7 per cent); p < Biliary sludge was present in males (3 per cent; two boys aged 4 years and two boys aged 5 years). Up to the age of 9 years the incidence of cholelithiasis increased by fold, but after 19 years it decreased five-fold (Fig. 1). However, the age group-specific incidences of biliary sludge (stone-in-waiting) and cholelithiasis shown in Table 3 demonstrate the risk of gallbladder disease with increasing age. This risk is highest (81.8 per cent) in the age group years. Odds ratio with 95 per cent CI showed a measure of association between sex, leucocytes count, liver volume, and cholelithiasis incidence. As shown in 74 Journal of Tropical Pediatrics Vol. 50, No. 2
3 TABLE 1 The sex-specific distribution of descriptive statistics Variable Males Females p Gender 68.4% 31.6% <0.001 (n = 130) (n = 60) Age (years) ± ± 2.47 <0.01 Body weight (kg) ± ± <0.001 Height (cm) ± ± <0.05 Hemoglobin (g%) 8.19 ± ± 2.51 <0.001 Leucocytes/mm ± ± <0.001 TABLE 3 Incidence of biliary sludge (stone-in-waiting) and cholelithiasis within age groups Age group N Cholelithiasis (years) n % (n/n) TABLE 2 The sex-specific incidence of gallbladder disease and hepatomegaly Variable Males Females (n = 130) (n = 60) p Cholelithiasis 58.5% 58.3% NS (n = 76) (n = 35) Cholecytitis 27.7% 20% NS (n = 36) (n = 12) Hepatomegaly 88.5% 66.7% <0.001 (n = 115) (n = 40) Hydrops and dilated 13.1% 30% <0.01 common duct (n = 17) (n = 18) Biliary sludge 3% 0% NS (n = 4) (n = 0) NS: not significant, p > Table 4, there was no association between leucocytes count >10 000/mm 3 and cholelithiasis occurrence (RR = 2.26, ), standard levels of statistical significance being reached (p < 0.001). Less than 10 blood transfusions were reported in 129 patients (67.9 per cent) (Fig. 2). The incidence of hydrops and dilated common duct risk was 2.29 (OR = , p < 0.001) for females vs. males. Seventy-one of the 190 patients (37.3 per cent) in this series had clinical symptoms that could be attributed to biliary tract. This included fatty food intolerance, painful abdominal crisis, fever, and jaundice. Discussion Sickle cell anemia is a chronic hemolytic disease resulting from abnormal hemoglobin. The incidence of gallbladder disease in sickle cell anemia is between 6 and 55 per cent. 1 9 This variability depends on the age groups surveyed, and the means used to detect biliary tract disease. Our study of 190 patients represents the largest African series to date with a very high incidence (58.4 per cent) of cholelithiasis. This study suggests that as patients with sickle cell TABLE 4 The incidence and risk of cholelithiasis in sickle cell anemia Exposure Cholelithiasis outcome OR (95% CI) p Sex 1.00 NS Male vs. female ( ) Leucocytes 2.26 <0.001 > /mm 3 vs. <10 000mm 3 ( ) Liver 1.22 NS Hepatomegaly vs. normal volume ( ) NS: not significant. anemia are examined more closely for biliary trace disease by ultrasound, and as they live longer with improved management, the incidence will approach 81 per cent. The decrease of cholelithiasis incidence over the age of 19 years may be explained by the mortality usually observed at that age. When Herrick described sickle cell anemia in 1910, 14 the patient had bilious attacks accompanied by severe epigastric pain, vomiting, dark urine, and yellow sclerae. The etiology of these crises is not clear. The abdominal crises are usually accompanied by an elevation of serum bilirubin and often an increase in serum alkaline phosphatase suggestive of biliary tract obstruction. The sludging of sickled red cells in hepatic sinusoids with subsequent ischemia and necrosis of hepatocytes determines these abdominal crises. In Congolese subjects, a leucocyte count > /mm 3 and the age group years are the risk factors of cholelithiasis outcome. Congolese patients with cholecytitis hydrops, dilated biliary tract, and congested liver presented with similar symptoms. These entities were easily differentiated after sonographic study. The first case of painful abdominal crisis caused by hydrops of the Journal of Tropical Pediatrics Vol. 50, No. 2 75
4 FIG. 2. Distribution of all patients with sickle cell anemia, and patients with sickle cell anemia and cholethiasis with respect to the number of blood transfusions. gallbladder during sickle cell disease was reported in a young black from Togo. 15 The frequency of cholelithiasis is inversely proportional to the number of blood transfusions. Physicians pay attention to prescribing blood transfusion because of the high prevalence of AIDS in Congo. The sludge resolved in three of the four symptomatic boys without stones, but the sludge persisted in one asymptomatic boy. Biliary sludge (a mixture of bile and particulate precipitates as cholesterol monohydrate, calcium bilirubinate, calcium salt, or xenobiotics such as the third-generation cephalosporin ceftriaxone is reported here for the first time in African children with SCD on ultrasound evaluation. The present patients with SCD and biliary sludge presented heptobiliary symptoms as reported by Winter, et al. in American children, 20 and were free of stones as observed by Walker and Serjeant in a cohort of 429 Jamaican children. 21 The pathophysiology of cholelithiasis and biliary sludge is still unclear. Recently, Werlin and Scott suggested that biliary sludge is a stone-in-waiting. 19 Gallstones were present from age 6 years, while biliary sludge was noted in boys aged 4 6 in this study. Young Congolese with SCD are more likely than blacks from the diaspora to receive blood transfusions and antibiotics, to eat a high-fiber diet, and be exposed to sunlight. Red cells of donors are prone to hemolysis and the accelerated hemolysis in SCD increases the production of pigment gallstones. 2 Biliary sludge was transient in 75 per cent of patients and occurred under conditions of gallbladder hypomotility which promotes precipitation of biliary pigment and bile stasis. 22,23 Biliary sludge and hydrops of gallbladder with dilated common duct occurred in the age group 5 10 years and preceded the process of stone formation in young Congolese. However, biliary sludge is uncommon in the present study, as reported in the literature. 7,21 Bansimba (unpublished data) confirmed among children with SCD from Congo-Brazzaville our findings, in which the number of blood transfusions did not influence the cholelithiasis incidence. Conversely, in Jamaicans, Stephens and Scott 24 reported a high incidence of cholelithiasis in SCD with blood polytransfusion. Patients with symptoms not treated conservatively were referred for cholecystectomy as reported in the USA. 20 The ultrasonographic examination is recommended for patients with hepatobiliary symptoms from Congo where the autosomal recessive gene for sickle hemoglobin occurs in 25 per cent of its population. 25 In conclusion, the age group years and leucocyte count > /mm 3 were considered as risk factors of the incidence of cholelithiasis, while the female gender was isolated as risk factor of the hydrops of the gallbladder outcome. References 1. Jordan RA. Cholelithiasis in sickle cell disease. Gastroenterology 1957; 33: Barrett-Connor E. Cholelithiasis in sickle cell anemia. Am J Med 1968; 45: Journal of Tropical Pediatrics Vol. 50, No. 2
5 3. Cameron JL, Maddrey WC, Zwidema GD. Biliary tract disease in sickle cell anemia: Surgical considerations. Ann Surg 1971; 174: Phillips JC, Gerald BE. Incidence of cholelithiasis in sickle cell disease. Am J Roentgenol Radium Ther Nucl Med 1971; 113: Ariyan S, Shesel F, Pickett L. Cholecystitis and cholelithiasis masking as abdominal crises in sickle cell disease. Pediatrics 1976; 58: Lachman BS, Lazerson J, Starshak PJ, Vaughters FM, Merlin SL. The prevalence of cholelithiasis in sickle cell disease as diagnosed by ultrasound and cholecystography. Pediatrics 1979; 64: Sarnajk S, Slovis IL, Corbet DP, Emami A, Whitten CF. Incidence of cholelithiasis in sickle cell anemia using the ultrasonic gray-scale technique. J Pediatr 1980; 96: Cunningham JJ, Houuhan SM, Altay C. Cholecystosonography in children with sickle cell disease: technical approach and clinical results. J Clin Ultrasound 1981; 9: Rennels MB, Dunne MG, Grossman NJ, Schwartz AD. Cholelithiasis in patients with major sickle hemoglobinopathies. Arn J Dis Child 1984; 138: Ranney HM. Clinically important variants of human hemoglobin. New Engl J Med 1970; 282: Akinyanju O, Ladapo F. Cholelithiasis and biliary tract disease in sickle cell disease in Nigerians. Postgrad Med J 1979; 55: Itoua-Ngaporo A, Ngoma-Kadoulou JC. La prevalence de la lithiase biliaire dans la drepanocytose homozygote. Med Chir Dig 1987; 16: Durosinmi MA, Ogunseyinde AO, Olatunji PO, Esa GJF. Prevalence of cholelithiasis in Nigerians with sickle cell disease. Afr J Med Sci 1989; 18: Herrick JB. Peculiar elongated and sickle shaped red blood corpuscles in a case of severe anemia. Arch Intern Med 1910; 6: Cabrol S, Desjardin F, Baruchel S, et al. L hydrocholecyste, cause méconnue de crises douloureuses chez le drépanocytaire. Arch Fr Pediatr 1985; 42: Lee SP, Maiier K, Nicholls IF. Origin and fate of biliary sludge. Gastroenterology 1988; 94: Janowitz P, Kratzer W, Zemmler T, et al. Gallbladder sludge: spontaneous course and incidence of complications in patients without stones. Hepatology 1994; 20: Lee SP, Hayashi A, Kim YS. Biliary sludge: curiosity or culprit (editorial). Hepatology 1994; 20: Werlin SL, Scott P. Is biliary sludge a stone-in-waiting (Editor s column). J Pediatr 1996; 129: Winter S, Kinney TR, Ware RE. Gallbladder sludge in children with sickle cell disease. J Pediatr 1994; 125: Walker TM, Serjeant GR. Biliary sludge in sickle cell disease. J Pediatr 1996; 129: Bouchier IAD. The formation of gallstones. Keio J Med 1992; 41: Everson GT, Nemeth A, Kourourian S, et al. Gallbladder function is altered in sickle hemoglobinopathy. Gastroenterology 1989; 96: Stephens CG, Scott RB. Cholelithiasis in sickle cell anemia. Arch Intern Med 1980; 140: Michaux JL, Debroe M, Vanros G. La sicklanémie de l adulte au Congo-Kinshasa. Ann Soc Belge Med Trop 1969; 49: 137. Journal of Tropical Pediatrics Vol. 50, No. 2 77
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