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Abdominal ultrasonography in HIV/AIDS patients in southwestern Nigeria

Abdominal ultrasonography in HIV/AIDS patients in southwestern Nigeria Background: Though the major target of the HIV-virus is the immune system, the frequency of abdominal disorders in HIV/AIDS patients has been reported to be second only to pulmonary disease. These abdominal manifestations may be on the increase as the use of antiretroviral therapy has increased life expectancy and improved quality of life. Ultrasonography is an easy to perform, non invasive, inexpensive and safe imaging technique that is invaluable in Africa where AIDS is most prevalent and where sophisticated diagnostic tools are not readily available. Purpose: To describe the findings and evaluate the clinical utility of abdominal ultrasonography in HIV/AIDS patients in Ibadan, Nigeria Methods: A Prospective evaluation of the abdominal ultrasonography of 391 HIV-positive patients as well as 391 age and sex-matched HIV-negative patients were carried out at the University College Hospital, Ibadan. Results: Of the 391 cases studied, 260 (66.5%) were females; the mean age was 38.02 years, (range 15–66 years). The disease was most prevalent in the 4th decade with an incidence of 40.4%. Compared with the HIV-negative individuals, the HIV+ group of patients had a significantly higher proportion of splenomegaly (13.5% vs. 7.7%; p < 0.01), lymphadenopathy (2.0% vs. 1.3%; p < 0.70), and renal abnormalities (8.4% vs. 3.8%; p < 0.02). There were no differences in hepatic and pancreatic abnormalities between the HIV+ and HIV- groups. There were significantly fewer gallstones in the HIV+ group (1.4% vs. 5.1%; p < 0.01). Conclusion: AIDS is a multi-systemic disease and its demographic and clinical pattern remains the same globally. Ultrasonography is optimally suited for its clinical management especially in Africa. Its accuracy and sensitivity may be much improved with clinico-pathologic correlation which may not be readily available in developing countries; further studies may provide this much needed diagnostic algorithms. Page 1 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 HIV-negative adults who were enrolled as age and sex- Background The Acquired Immune-Deficiency Syndrome (AIDS), the matched controls. These included relations of patients, clinical entity resulting from HIV infection is an increas- hospital staff and patients admitted for non-abdominal ingly important disease that has become a social phenom- illnesses. enon. The Sub-Saharan African region is by far the worst affected in the world by the AIDS epidemic. It is actually The ultrasound scans were performed after an overnight home to over 60% of all people living with HIV [1]. fast of at least 12 hours with patients lying supine and Though the major target of this deadly virus is the using a 3.5–5.0 MHz frequency curvilinear probe on an immune system, the frequency of abdominal disorders in ALOKA 1700-SSD ultrasound machine. Non-fasting patients with AIDS has been reported to be second only to patients, children, and patients with incomplete ultra- pulmonary disease [2-4]. These abdominal manifesta- sound examinations were excluded from the study. Two tions may now be on the increase as the discovery and use radiologists performed all sonographic examinations. of antiretroviral therapy has prolonged life expectancy and improved quality of life [2,5]. The presence of the following abnormalities were noted, splenomegaly; (with or without hypo or hyperechoic HIV/AIDS is known to have a wide variety of clinical man- lesions), hepatomegaly; (with or without single or multi- ifestations from involvement of various organs. Ultra- ple focal lesions), lymphadenopathy, gallbladder and bile sonography (US) is a versatile imaging tool, which can duct abnormality, ascites, renal abnormalities with dif- evaluate most of the abdominal organs affected by the dis- fusely increased echogenicity, pancreatic changes, and bil- ease; furthermore, it can guide biopsies allowing the cyto- iary duct dilatation. The extrahepatic bile duct was histological and microbiological investigations needed to identified at the level of the portal vein, where the hepatic obtain a definitive diagnosis. artery crosses perpendicularly between them. When bowel gas obscured a part of the suprapancreatic segment, the Other imaging methods particularly Computed Tomogra- patient was asked to take several deep breaths and hold phy (CT) can explore these organs in more detail than US. the inspiratory phase. Color Doppler sonography was However, CT may often be considered a second choice in used to confirm the identification of the vascular and duc- abdominal imaging for the following reasons; it utilizes tal anatomy. The common bile duct was measured in the radiation, it is more expensive, less readily available and most distal aspect of the head of the pancreas. In this loca- often yields results comparable to US [3-5]. tion, anteroposterior measurements from inner border to inner border were obtained. This is particularly true in developing countries where the absence or the high cost of the procedure makes abdomi- The radiologist initially recorded the data on paper and nal US a suitable alternative diagnostic tool in the radio- later transferred it to a computer, where it was stored logical investigation of HIV infected individuals. throughout the period of the study before statistical anal- ysis. To our knowledge, there is a dearth of reports in the West African Sub-region on imaging in HIV/AIDS especially in The following definitions were used, lymphadenopathy: sonographic evaluation of the abdomen in this large pop- nodes larger than 1 cm in diameter [6], splenomegaly: ulation of HIV/AIDS. The purpose of this prospective spleen larger than 12 cm at its longest axis [7], hepatome- study is to describe the abdominal findings in these galy: liver measuring more than 15 cm at its longitudinal patients and evaluate the clinical utility of abdominal US axis, extrahepatic duct dilatation: common bile duct in HIV/AIDS patients in Ibadan, a southwestern town of diameter (CBD) >7 mm. Electronic calipers were used for Nigeria. all measurements on the ultrasound machine. Demographic data were obtained from patients' record Methods Abdominal ultrasound scans were prospectively per- file. Each patient gave an informed consent. formed over a one-year period (April 2005–March 2006) on 391 consecutive eligible HIV-positive adults (aged 15– Data Management 66 years) referred from the Antiretroviral Clinic at the SPSS 11.0 for windows software (SPSS, Inc. Chicago, Illi- University College Hospital, Ibadan to the Department of nois) was used for data analysis. Continuous variables Radiology for routine diagnostic imaging. At our facility, were expressed as mean ± standard deviation with student HIV-positive patients routinely have a chest X-ray and an T-test analysis for comparison. Categorical variables were abdominal US for early detection of abnormality and expressed as percentages and comparison was by chi- achievement of a base line. During the same period, 391 square analysis. Two tailed p-value < 0.05 was considered abdominal ultrasound examinations were performed on significant. Page 2 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 tically significant. There was also no significant difference Results Of the 391 cases, 260 (66.5%) were females; the mean age in the renal length in both groups (Table 3). One patient was 38.02 years, (range 15–66 years). The modal age in the HIV+ group had a congenital absence of the right group was the 4th decade with a frequency of 40.4% kidney while crossed ectopia was noted in another. (Table 1). Of the control group, 64% were females and 36% males with a mean age of 36 years (age range = 15– Enlarged para-aortic and periportal lymph nodes were 64 years). more common in the HIV+ group having eight (2.0%) versus five (1.3%) in the HIV-seronegative group (Figs. 3 Sonographic Findings and 4). Free fluid (ascites) within the abdomen was seen The significant abdominal US findings seen are shown in more frequently in HIV-seronegative patients; 22 of Table 2. Of the study population normal abdominal find- 391(5.6%) against five of 391(1.3%) in HIV+ patients. ing were comparable in both groups. Splenomegaly was common in both groups, although it was considerably Discussion more common in the HIV+ group; 57(14.6%) compared HIV/AIDS has now reached epidemic proportion in all with 30(7.7%) in the HIV- group (p < 0.01). The spleen Sub-Saharan African countries endangering not just the showed homogeneous enlargement except in two of the lives of its victims but also the social and economic fabric HIV+ cases, which showed solitary hypo-echoic areas. of society. Most health institutions in the sub region including Nigeria are not adequately equipped to prop- Enlargement of the liver was also not significantly differ- erly evaluate the HIV/AIDS patient and the complications ent in both groups: 52(13.3%) in cases versus 58(14.8%) that often arise from the condition. Its infectious and non- in controls, these patients showed mostly non specific infectious complications can be overwhelming and may findings such as high parenchyma echogenicity compati- be impossible to diagnose accurately in developing coun- ble with fatty infiltration of the liver (Fig. 1). Evidence of tries because of lack of diagnostic facilities [3-5]. Evalua- cholelithiasis was noted in 6(1.5%) HIV+ cases but was tion of the abdomen by ultrasound is the alternative tool significantly more in the control group, being present in to CT scan, producing cross-sectional images of high diag- 20 of 391(5.1%) patients (p < 0.01). Extrahepatic bile nostic quality. Although US does not provide a definitive duct dilatation was also noted in 10 of 391 (2.6%) cases diagnosis, it may show areas of abnormal anatomy and with a mean of 4.28 ± 1.18 mm. The width of the com- pathology that may facilitate achieving a tissue diagnosis mon bile duct ranged from 1.0 to 8.6 mm among HIV+ or add further support to the decisions on commencing cases and 1.0 to 6.5 mm among the control group. No ext- empirical treatment. This is highlighted by the spectrum rahepatic bile duct dilatation was recorded in the control of findings in our study as listed in Table 3. The female group. prevalence and mean age of 38.02 years shows a slight var- iance from a comparable study by Tshibwabwa et al in a Renal US findings were diverse, renal parenchymal similar environment [3]. Their study showed a higher changes as evidenced by increased echo texture of both male prevalence and a lower mean age. Findings in our cortex and medulla (Fig. 2) were recorded in normal sized study confirm previous documentation of the wide range kidneys in 33(8.4%) of HIV+ cases compared with of abdominal manifestations of HIV/AIDS and reveal that 15(3.8%) in controls which showed similar changes (p < while abdominal abnormalities occur frequently, they are 0.03). Biochemical tests confirmed increased Urea level in usually nonspecific, with splenomegaly, lymphadenopa- 27% (9\33) of the HIV+ patients while Creatinine level thy, biliary tract abnormalities, and hepatomegaly occur- was equally high in 4 of the 33 patients corresponding to ring most commonly. Splenomegaly was the most those with the highest urea levels. Other renal findings in common abnormal finding in our study, with a frequency both groups include hydronephrosis, nephrolithiasis, and of 13%. This relatively high incidence agrees with previ- simple renal cysts. However the difference was not statis- ous reports [3,5,8,9]. Yee et al [10] and Geoffray et al [11], identified splenomegaly in 45% and 32.5% of their Table 1: Age group distribution in HIV+ Patients patients respectively. As is the case with the non-AIDS population, hepatosplenomegaly is a nonspecific finding. Age-group(years) Frequency Percentage (%) Other abnormalities of the spleen in our study occurred far less commonly. The two cases of focal hypoechoic 10–19 3 0.8 20–29 78 19.9 splenic areas may have been due to splenic lymphoma. 30–39 158 40.4 Focal splenic lymphomas are commonly depicted as a 40–49 89 22.8 hypoechoic lesion and are often seen in association with 50–59 52 13.3 splenomegaly [12] as in the cases identified. ≥60 11 2.8 Total 391 100.0 Page 3 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 Table 2: Abdominal Ultrasound Findings in 782 Nigerian Adults* HIV Status Number HIV + 391 HIV-(Control) 391 P-value Ultrasound Finding Freq % Freq % Normal 228 58.3 256 65.5 0.045 Splenomegaly 57 14.6 30 7.7 0.011 Hepatomegaly 52 13.3 58 14.8 0.381 Renal parenchymal disease 33 8.4 15 3.8 0.025 Extrahepatic duct dilatation 10 2.6 0 0 - Lymphadenopathy 8 2.0 5 1.3 0.701 Cholelithiasis 6 1.5 20 5.1 0.006 Hydronephrosis 5 1.3 5 1.3 0.844 Ascites 5 1.3 22 5.6 0.001 * Since some patients had more than one finding the total frequency is greater than the number of patients. However, the echogenicity of the remaining cases of sity in 35% of this group of patients. The latter is splenomegaly were essentially homogeneous. In the cate- compatible with the well documented fatty changes in gory of patients with hepatomegaly, 49 of 52 (94%) were AIDS patients [3,5,8,9]. According to Fortgang et al, [13] homogeneous. The only solid hyperechoic mass recorded this fatty change of the liver has a low sonographic diag- was not biopsied for lack of appropriate facility. This find- nostic accuracy. This could account for the possibility of ing is at variance with the study from central Africa, [3] underreporting in our study. where intrinsic mass lesions, namely AIDS – related lym- phoma, Kaposi sarcoma of the liver, diffuse nodular Gall bladder wall thickening was not associated with the regenerative hyperplasia, multiple hyperechoic nodules presence of calculi. Acalculous cholecystitis was also not from extra pulmonary pneumocystitis carinii, and mycetic recorded. Extrahepatic dilatation was found in 10(2.6%) abscesses were found. The absence of these hepatic patients; this finding has been reported as a sequel of changes in our patients may suggest an improved quality AIDS Related Sclerosing Cholangitis (ARSC) [4]. How- of life consequent to the administration of the Highly- ever, such patients had associated findings of gall bladder Active Antiretroviral Therapy (HAART). There was how- wall thickening which were not demonstrated in our ever sonographic evidence of increased parenchymal den- cases. Since these patients had no symptoms referable to the biliary system, no further diagnostic procedures were H Figure 2 IV nephropathy in a 34-year-old man Lo increased p ing (*) compatible wit Figure 1 ngitudinaa l s renchyma onogram hl echogenic o fatty infiltration f liver showing hepatomegaly and ity with posterior shadow- HIV nephropathy in a 34-year-old man. Longitudinal Longitudinal sonogram of liver showing hepatomeg- sonogram demonstrates normal sized right kidney with aly and increased parenchymal echogenicity with increased cortical echogenicity. Diffuse increased cortical posterior shadowing (*) compatible with fatty infil- echogenicity is associated with a poor prognosis. tration. Page 4 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 Table 3: Renal measurements of 782 patients Renal Dimensions Right kidney Left kidney HIV+ HIV- HIV+ HIV- Mean ± SD Mean ± SD p-value Mean ± SD Mean ± SD p-value Length 10.55 ± 0.97 10.60 ± 1.18 0.517 10.73 ± 1.11 10.64 ± 0.87 0.207 AP diameter 4.32 ± 0.68 4.53 ± 1.07 0.001 3.97 ± 0.31 4.07 ± 0.53 0.001 performed. The cause of this finding therefore remains largely made up of patients on admission in the hospital. unknown. These were patients with surgical or other medical condi- tions who required screening for HIV as part of their diag- Gall stones were seen significantly less in the HIV+ group, nostic laboratory work up. Healthy individuals in our similar findings were reported by Tshibwabwa et al [3] in environment, usually even with counseling do not readily central Africa consequently this pattern is probably com- submit themselves for HIV screening. The higher inci- mon to all sub-Saharan African countries. dence of ascites in the non-HIV population is therefore most likely due to other pathological causes such as Ultrasound is valuable in the assessment of lymph nodes, malignancy and cirrhosis, which are the commonest with a 3.5 MHz. transducer; deep lymph nodes can be known risk factors. evaluated. Ultrasound allows assessment of location, number and sizes of pathological lymph nodes. It also The association of renal abnormality with HIV has been permits evaluation of their shape, presence or absence of known since the early days of the disease [13]. In 1984, hilum/mediastinum. The lymph nodes recorded in our Rao et al [14] described progressive nephropathy in adults study were greater than 1 cm, mostly oval shaped with an with HIV/AIDS, characterized by proteinuria and renal echogenic hilum and a narrow symmetric cortex suggest- failure. HIV-associated nephropathy may develop in ing that they were benign. An ultrasound guided fine nee- patients with asymptomatic HIV infection, AIDS-related dle aspiration could have further characterized these complex, or AIDS. Patients typically have mild hyperten- nodes, but this could not be carried out in our centre sion and large kidneys and then early and rapidly progres- because of unavailability of appropriate needles. sive renal failure. Studies now show increased prevalence of renal complication because of prolonged survival and Ascites was reported more frequently in the HIV seroneg- increased frequency of HIV transmission among Intrave- ative group. Perhaps the higher frequency in this group is in part due to selection bias, in that the control group was Tr th Figure 3 y in ansver a HIV+ patient se sonogram with non-H showing extensive periportal adenopa odgkin lymphoma - Transverse sonogram showing extensive periportal L neal lymph node adjac asymptom Figure 4 ongitudinatic HIV+ al sonogram of pa etient nt to liver the gall showing a l bladder arge retroperi in a 27 yeart -old o- adenopathy in a HIV+ patient with non-Hodgkin lym- Longitudinal sonogram of liver showing a large retro- phoma. AO-aorta, H-hepatic artery, SP-splenic artery, LN- peritoneal lymph node adjacent to the gall bladder in lymph node. a 27 year-old asymptomatic HIV+ patient. Page 5 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 nous drug abusers [15-18]. The sonographic correlates of References 1. 2006 report on the global AIDS epidemic, UNAIDS. 2006. this disease are nephromegaly and increased cortical 2. Idoko J: The challenge of providing antiretroviral therapy in echogenicity [3,5,14,18]. The number of HIV+ cases in resource poor countries. Archives of Ibadan Medicine 2004, our study who showed such renal abnormality was more 5:26-30. 3. Tshibwabwa ET, Mwaba P, Bogle-Taylor J, Zumla A: Four-year than double the number of the controls. However, overall study of abdominal ultrasound in 900 Central African adults renal sizes were within normal limits among both groups with AIDS referred for diagnostic imaging. Abdom Imaging 2000, 25:290-296. (Table 3). Renal failure was evident in a quarter of the 4. Brunetti E, Brigada R, Poletti F, Maiocchi L, Garlaschelli A, Gulizia R, cases with parenchymal changes. Nonetheless, a direct Filice C: The current role of abdominal ultrasound in the clin- correlation between the extent of renal disease and the ical management of patients with AIDS. Ultraschall in Med 2006, 27:20-33. degree of echogenicity does not exist [19]. This strongly 5. Smith FJ, Matheson JR, Cooperberg PL: Abdominal abnormalities contrasts with the finding of previous studies [10,12,19] in AIDS: detection at ultrasound in a large population. Radi- which found nephromegaly to be associated with HIV ology 1994, 192:691-695. 6. Lee JK: Retroperitoneum. In Computed body tomography with MRI nephropathy, even though this finding is most common correlation 2nd edition. Edited by: Lee JK, Sagel SS, Stanley RJ. New among black males [20,21]. The higher female prevalence York, NY: Raven; 1989:707-753. 7. Matheson JR, Cooperberg PL: The Spleen. In Diagnostic ultrasound in the study group may have accounted for this. Edited by: Rumack CL, Wilson SR, Charbonneau WJ. St Louis, Mo: Mosby-Year Book; 1991:87-105. Our data supports the fact that manifestations and 8. Langer R, Langer M, Schutze B, Zwicker C, Wakat JP, Felix R: Abdominal Sonographic findings in patients with AIDS. Ront- changes seen on abdominal ultrasound of HIV/AIDS genblatter 1989, 42:121-125. patients appear to be uniform across countries in sub- 9. N'Zi PK, Coulibaly A, N'Dri K, Quattara ND, Diabate SA, Zunon- Saharan Africa. However a wide range of features are seen kipre E, Djedje AT: Ultrasound aspects of abdominal involve- ment in adults with HIV infections in the Ivory Coast: apro- in both HIV+ and HIV- individuals which in the absence pos of 146 cases. Sante 1999, 9:85-88. of histological confirmation makes the clinical usefulness 10. Yee JM, Raghavendra BN, Horii SC, Ambrosino M: Abdominal Sonography in AIDS: A Review. J Ultrasound Med 1989, of ultrasound imaging quite limited. In experienced 8:705-714. hands the radiologist may be able to provide a narrow 11. Geoffray A, Binet A, Cassuto JP, Dujardin P, Coussement A: Sonog- range of diagnostic possibilities that would enhance raphy of abdominal adenopathies in patients with anti-HIV- positive serology. In Imaging of AIDS Edited by: Troto P. Philadel- patient management and care in African communities phia, Pa: Decker; 1991:189-194. where the burden of HIV/AIDS remains astonishingly 12. Townsend RR, Laing FC, Jeffrey RB Jr, Bottles K: Abdominal lym- high. phoma in AIDS: evaluation with US. Radiology 1989, 171:719-724. 13. Fortgang IS, Belitsos PC, Chaisson RE, Moore RD: Hepatomegaly Conclusion and steatosis in HIV infected patients receiving nucleoside analog antiretroviral therapy. Am J Gastroenterol 1995, Ultrasonography is a versatile tool for evaluating abdom- 90:1433-1436. inal organs affected by HIV/AIDS. The sonographic find- 14. Miller F, Patrikh S, Gore R, Nemcek A, Fitzgerald S, Vogelzang R: ings in HIV/AIDS patients in Ibadan, Nigeria are Renal Manifestations of AIDS. RadioGraphics 1993, 13:587-596. 15. Rao TK, Filippone EJ, Nicastri AD, Landesman SH, Frean E, Chen CK, comparable to that from other sub-Saharan African com- Friedman EA: Associated focal and segmental glomeruloscle- munities. However, provision and availability of suffi- rosis in the Acquired Immunodeficiency Syndrome. N Engl J Med 1984, 310:669-673. cient clinico-pathologic data in the future would improve 16. Frassetto L, Schwenfeld P, Humphrey M: Increasing incidence of the quality of ultrasonographic diagnosis and treatment human Immunodeficiency virus – associated nephropathy at in these patients. San Francisco General Hospital. Am J Kidney Dis 1991, 18:655-659. 17. Vella S, Giuliano M, Pezzotti P, Agresti MG, Tomino C, Floridia M, Competing interests Greco D, Moroni M, Visco G, Milazzo Fl: Survival of zidovudine- The author(s) declare that they have no competing inter- treated patients with AIDS compared with that of contem- porary untreated patients. Italian Zidovudine Evaluation ests. Group. JAMA 1992, 267:1232-1236. 18. Gold JWN: HIV infection: diagnosis and management. Med Clin North Am 1992, 76:1-18. Authors' contributions 19. Schaffer RM, Schwartz GE, Becker JA, Rao TKS, Shih YH: Renal OMO and AYA conceived the study. AOM and AAM par- ultrasound in acquired immunodeficiency syndrome. Radiol- ticipated in its design. OYU and AAJ performed the ultra- ogy 1984, 153:511-513. 20. Valeri A, Neusy AJ: Acute and chronic renal disease in hospital- sound examinations. OSA and OMA participated in the ized AIDS patients. Clin Nephrol 1991, 35:110-118. recruitment of subjects and collated the data. AYA and IFA 21. Bourgoignie JJ, Meneses R, Ortiz C, Jaffe D, Pardo V: The clinical spectrum of renal disease associated with human immuno- coordinated the recruitment of subjects. OMO and AOA deficiency virus. Am J Kidney Dis 1988, 12:131-137. organized the ultrasound examinations. OMO, OGI and AAT managed the data, performed statistical analysis and Pre-publication history drafted the manuscript. All authors read and approved the The pre-publication history for this paper can be accessed final manuscript. here: http://www.biomedcentral.com/1471-2342/8/5/prepub Page 6 of 6 (page number not for citation purposes) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Medical Imaging Springer Journals

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Medicine & Public Health; Imaging / Radiology
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Abstract

Background: Though the major target of the HIV-virus is the immune system, the frequency of abdominal disorders in HIV/AIDS patients has been reported to be second only to pulmonary disease. These abdominal manifestations may be on the increase as the use of antiretroviral therapy has increased life expectancy and improved quality of life. Ultrasonography is an easy to perform, non invasive, inexpensive and safe imaging technique that is invaluable in Africa where AIDS is most prevalent and where sophisticated diagnostic tools are not readily available. Purpose: To describe the findings and evaluate the clinical utility of abdominal ultrasonography in HIV/AIDS patients in Ibadan, Nigeria Methods: A Prospective evaluation of the abdominal ultrasonography of 391 HIV-positive patients as well as 391 age and sex-matched HIV-negative patients were carried out at the University College Hospital, Ibadan. Results: Of the 391 cases studied, 260 (66.5%) were females; the mean age was 38.02 years, (range 15–66 years). The disease was most prevalent in the 4th decade with an incidence of 40.4%. Compared with the HIV-negative individuals, the HIV+ group of patients had a significantly higher proportion of splenomegaly (13.5% vs. 7.7%; p < 0.01), lymphadenopathy (2.0% vs. 1.3%; p < 0.70), and renal abnormalities (8.4% vs. 3.8%; p < 0.02). There were no differences in hepatic and pancreatic abnormalities between the HIV+ and HIV- groups. There were significantly fewer gallstones in the HIV+ group (1.4% vs. 5.1%; p < 0.01). Conclusion: AIDS is a multi-systemic disease and its demographic and clinical pattern remains the same globally. Ultrasonography is optimally suited for its clinical management especially in Africa. Its accuracy and sensitivity may be much improved with clinico-pathologic correlation which may not be readily available in developing countries; further studies may provide this much needed diagnostic algorithms. Page 1 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 HIV-negative adults who were enrolled as age and sex- Background The Acquired Immune-Deficiency Syndrome (AIDS), the matched controls. These included relations of patients, clinical entity resulting from HIV infection is an increas- hospital staff and patients admitted for non-abdominal ingly important disease that has become a social phenom- illnesses. enon. The Sub-Saharan African region is by far the worst affected in the world by the AIDS epidemic. It is actually The ultrasound scans were performed after an overnight home to over 60% of all people living with HIV [1]. fast of at least 12 hours with patients lying supine and Though the major target of this deadly virus is the using a 3.5–5.0 MHz frequency curvilinear probe on an immune system, the frequency of abdominal disorders in ALOKA 1700-SSD ultrasound machine. Non-fasting patients with AIDS has been reported to be second only to patients, children, and patients with incomplete ultra- pulmonary disease [2-4]. These abdominal manifesta- sound examinations were excluded from the study. Two tions may now be on the increase as the discovery and use radiologists performed all sonographic examinations. of antiretroviral therapy has prolonged life expectancy and improved quality of life [2,5]. The presence of the following abnormalities were noted, splenomegaly; (with or without hypo or hyperechoic HIV/AIDS is known to have a wide variety of clinical man- lesions), hepatomegaly; (with or without single or multi- ifestations from involvement of various organs. Ultra- ple focal lesions), lymphadenopathy, gallbladder and bile sonography (US) is a versatile imaging tool, which can duct abnormality, ascites, renal abnormalities with dif- evaluate most of the abdominal organs affected by the dis- fusely increased echogenicity, pancreatic changes, and bil- ease; furthermore, it can guide biopsies allowing the cyto- iary duct dilatation. The extrahepatic bile duct was histological and microbiological investigations needed to identified at the level of the portal vein, where the hepatic obtain a definitive diagnosis. artery crosses perpendicularly between them. When bowel gas obscured a part of the suprapancreatic segment, the Other imaging methods particularly Computed Tomogra- patient was asked to take several deep breaths and hold phy (CT) can explore these organs in more detail than US. the inspiratory phase. Color Doppler sonography was However, CT may often be considered a second choice in used to confirm the identification of the vascular and duc- abdominal imaging for the following reasons; it utilizes tal anatomy. The common bile duct was measured in the radiation, it is more expensive, less readily available and most distal aspect of the head of the pancreas. In this loca- often yields results comparable to US [3-5]. tion, anteroposterior measurements from inner border to inner border were obtained. This is particularly true in developing countries where the absence or the high cost of the procedure makes abdomi- The radiologist initially recorded the data on paper and nal US a suitable alternative diagnostic tool in the radio- later transferred it to a computer, where it was stored logical investigation of HIV infected individuals. throughout the period of the study before statistical anal- ysis. To our knowledge, there is a dearth of reports in the West African Sub-region on imaging in HIV/AIDS especially in The following definitions were used, lymphadenopathy: sonographic evaluation of the abdomen in this large pop- nodes larger than 1 cm in diameter [6], splenomegaly: ulation of HIV/AIDS. The purpose of this prospective spleen larger than 12 cm at its longest axis [7], hepatome- study is to describe the abdominal findings in these galy: liver measuring more than 15 cm at its longitudinal patients and evaluate the clinical utility of abdominal US axis, extrahepatic duct dilatation: common bile duct in HIV/AIDS patients in Ibadan, a southwestern town of diameter (CBD) >7 mm. Electronic calipers were used for Nigeria. all measurements on the ultrasound machine. Demographic data were obtained from patients' record Methods Abdominal ultrasound scans were prospectively per- file. Each patient gave an informed consent. formed over a one-year period (April 2005–March 2006) on 391 consecutive eligible HIV-positive adults (aged 15– Data Management 66 years) referred from the Antiretroviral Clinic at the SPSS 11.0 for windows software (SPSS, Inc. Chicago, Illi- University College Hospital, Ibadan to the Department of nois) was used for data analysis. Continuous variables Radiology for routine diagnostic imaging. At our facility, were expressed as mean ± standard deviation with student HIV-positive patients routinely have a chest X-ray and an T-test analysis for comparison. Categorical variables were abdominal US for early detection of abnormality and expressed as percentages and comparison was by chi- achievement of a base line. During the same period, 391 square analysis. Two tailed p-value < 0.05 was considered abdominal ultrasound examinations were performed on significant. Page 2 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 tically significant. There was also no significant difference Results Of the 391 cases, 260 (66.5%) were females; the mean age in the renal length in both groups (Table 3). One patient was 38.02 years, (range 15–66 years). The modal age in the HIV+ group had a congenital absence of the right group was the 4th decade with a frequency of 40.4% kidney while crossed ectopia was noted in another. (Table 1). Of the control group, 64% were females and 36% males with a mean age of 36 years (age range = 15– Enlarged para-aortic and periportal lymph nodes were 64 years). more common in the HIV+ group having eight (2.0%) versus five (1.3%) in the HIV-seronegative group (Figs. 3 Sonographic Findings and 4). Free fluid (ascites) within the abdomen was seen The significant abdominal US findings seen are shown in more frequently in HIV-seronegative patients; 22 of Table 2. Of the study population normal abdominal find- 391(5.6%) against five of 391(1.3%) in HIV+ patients. ing were comparable in both groups. Splenomegaly was common in both groups, although it was considerably Discussion more common in the HIV+ group; 57(14.6%) compared HIV/AIDS has now reached epidemic proportion in all with 30(7.7%) in the HIV- group (p < 0.01). The spleen Sub-Saharan African countries endangering not just the showed homogeneous enlargement except in two of the lives of its victims but also the social and economic fabric HIV+ cases, which showed solitary hypo-echoic areas. of society. Most health institutions in the sub region including Nigeria are not adequately equipped to prop- Enlargement of the liver was also not significantly differ- erly evaluate the HIV/AIDS patient and the complications ent in both groups: 52(13.3%) in cases versus 58(14.8%) that often arise from the condition. Its infectious and non- in controls, these patients showed mostly non specific infectious complications can be overwhelming and may findings such as high parenchyma echogenicity compati- be impossible to diagnose accurately in developing coun- ble with fatty infiltration of the liver (Fig. 1). Evidence of tries because of lack of diagnostic facilities [3-5]. Evalua- cholelithiasis was noted in 6(1.5%) HIV+ cases but was tion of the abdomen by ultrasound is the alternative tool significantly more in the control group, being present in to CT scan, producing cross-sectional images of high diag- 20 of 391(5.1%) patients (p < 0.01). Extrahepatic bile nostic quality. Although US does not provide a definitive duct dilatation was also noted in 10 of 391 (2.6%) cases diagnosis, it may show areas of abnormal anatomy and with a mean of 4.28 ± 1.18 mm. The width of the com- pathology that may facilitate achieving a tissue diagnosis mon bile duct ranged from 1.0 to 8.6 mm among HIV+ or add further support to the decisions on commencing cases and 1.0 to 6.5 mm among the control group. No ext- empirical treatment. This is highlighted by the spectrum rahepatic bile duct dilatation was recorded in the control of findings in our study as listed in Table 3. The female group. prevalence and mean age of 38.02 years shows a slight var- iance from a comparable study by Tshibwabwa et al in a Renal US findings were diverse, renal parenchymal similar environment [3]. Their study showed a higher changes as evidenced by increased echo texture of both male prevalence and a lower mean age. Findings in our cortex and medulla (Fig. 2) were recorded in normal sized study confirm previous documentation of the wide range kidneys in 33(8.4%) of HIV+ cases compared with of abdominal manifestations of HIV/AIDS and reveal that 15(3.8%) in controls which showed similar changes (p < while abdominal abnormalities occur frequently, they are 0.03). Biochemical tests confirmed increased Urea level in usually nonspecific, with splenomegaly, lymphadenopa- 27% (9\33) of the HIV+ patients while Creatinine level thy, biliary tract abnormalities, and hepatomegaly occur- was equally high in 4 of the 33 patients corresponding to ring most commonly. Splenomegaly was the most those with the highest urea levels. Other renal findings in common abnormal finding in our study, with a frequency both groups include hydronephrosis, nephrolithiasis, and of 13%. This relatively high incidence agrees with previ- simple renal cysts. However the difference was not statis- ous reports [3,5,8,9]. Yee et al [10] and Geoffray et al [11], identified splenomegaly in 45% and 32.5% of their Table 1: Age group distribution in HIV+ Patients patients respectively. As is the case with the non-AIDS population, hepatosplenomegaly is a nonspecific finding. Age-group(years) Frequency Percentage (%) Other abnormalities of the spleen in our study occurred far less commonly. The two cases of focal hypoechoic 10–19 3 0.8 20–29 78 19.9 splenic areas may have been due to splenic lymphoma. 30–39 158 40.4 Focal splenic lymphomas are commonly depicted as a 40–49 89 22.8 hypoechoic lesion and are often seen in association with 50–59 52 13.3 splenomegaly [12] as in the cases identified. ≥60 11 2.8 Total 391 100.0 Page 3 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 Table 2: Abdominal Ultrasound Findings in 782 Nigerian Adults* HIV Status Number HIV + 391 HIV-(Control) 391 P-value Ultrasound Finding Freq % Freq % Normal 228 58.3 256 65.5 0.045 Splenomegaly 57 14.6 30 7.7 0.011 Hepatomegaly 52 13.3 58 14.8 0.381 Renal parenchymal disease 33 8.4 15 3.8 0.025 Extrahepatic duct dilatation 10 2.6 0 0 - Lymphadenopathy 8 2.0 5 1.3 0.701 Cholelithiasis 6 1.5 20 5.1 0.006 Hydronephrosis 5 1.3 5 1.3 0.844 Ascites 5 1.3 22 5.6 0.001 * Since some patients had more than one finding the total frequency is greater than the number of patients. However, the echogenicity of the remaining cases of sity in 35% of this group of patients. The latter is splenomegaly were essentially homogeneous. In the cate- compatible with the well documented fatty changes in gory of patients with hepatomegaly, 49 of 52 (94%) were AIDS patients [3,5,8,9]. According to Fortgang et al, [13] homogeneous. The only solid hyperechoic mass recorded this fatty change of the liver has a low sonographic diag- was not biopsied for lack of appropriate facility. This find- nostic accuracy. This could account for the possibility of ing is at variance with the study from central Africa, [3] underreporting in our study. where intrinsic mass lesions, namely AIDS – related lym- phoma, Kaposi sarcoma of the liver, diffuse nodular Gall bladder wall thickening was not associated with the regenerative hyperplasia, multiple hyperechoic nodules presence of calculi. Acalculous cholecystitis was also not from extra pulmonary pneumocystitis carinii, and mycetic recorded. Extrahepatic dilatation was found in 10(2.6%) abscesses were found. The absence of these hepatic patients; this finding has been reported as a sequel of changes in our patients may suggest an improved quality AIDS Related Sclerosing Cholangitis (ARSC) [4]. How- of life consequent to the administration of the Highly- ever, such patients had associated findings of gall bladder Active Antiretroviral Therapy (HAART). There was how- wall thickening which were not demonstrated in our ever sonographic evidence of increased parenchymal den- cases. Since these patients had no symptoms referable to the biliary system, no further diagnostic procedures were H Figure 2 IV nephropathy in a 34-year-old man Lo increased p ing (*) compatible wit Figure 1 ngitudinaa l s renchyma onogram hl echogenic o fatty infiltration f liver showing hepatomegaly and ity with posterior shadow- HIV nephropathy in a 34-year-old man. Longitudinal Longitudinal sonogram of liver showing hepatomeg- sonogram demonstrates normal sized right kidney with aly and increased parenchymal echogenicity with increased cortical echogenicity. Diffuse increased cortical posterior shadowing (*) compatible with fatty infil- echogenicity is associated with a poor prognosis. tration. Page 4 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 Table 3: Renal measurements of 782 patients Renal Dimensions Right kidney Left kidney HIV+ HIV- HIV+ HIV- Mean ± SD Mean ± SD p-value Mean ± SD Mean ± SD p-value Length 10.55 ± 0.97 10.60 ± 1.18 0.517 10.73 ± 1.11 10.64 ± 0.87 0.207 AP diameter 4.32 ± 0.68 4.53 ± 1.07 0.001 3.97 ± 0.31 4.07 ± 0.53 0.001 performed. The cause of this finding therefore remains largely made up of patients on admission in the hospital. unknown. These were patients with surgical or other medical condi- tions who required screening for HIV as part of their diag- Gall stones were seen significantly less in the HIV+ group, nostic laboratory work up. Healthy individuals in our similar findings were reported by Tshibwabwa et al [3] in environment, usually even with counseling do not readily central Africa consequently this pattern is probably com- submit themselves for HIV screening. The higher inci- mon to all sub-Saharan African countries. dence of ascites in the non-HIV population is therefore most likely due to other pathological causes such as Ultrasound is valuable in the assessment of lymph nodes, malignancy and cirrhosis, which are the commonest with a 3.5 MHz. transducer; deep lymph nodes can be known risk factors. evaluated. Ultrasound allows assessment of location, number and sizes of pathological lymph nodes. It also The association of renal abnormality with HIV has been permits evaluation of their shape, presence or absence of known since the early days of the disease [13]. In 1984, hilum/mediastinum. The lymph nodes recorded in our Rao et al [14] described progressive nephropathy in adults study were greater than 1 cm, mostly oval shaped with an with HIV/AIDS, characterized by proteinuria and renal echogenic hilum and a narrow symmetric cortex suggest- failure. HIV-associated nephropathy may develop in ing that they were benign. An ultrasound guided fine nee- patients with asymptomatic HIV infection, AIDS-related dle aspiration could have further characterized these complex, or AIDS. Patients typically have mild hyperten- nodes, but this could not be carried out in our centre sion and large kidneys and then early and rapidly progres- because of unavailability of appropriate needles. sive renal failure. Studies now show increased prevalence of renal complication because of prolonged survival and Ascites was reported more frequently in the HIV seroneg- increased frequency of HIV transmission among Intrave- ative group. Perhaps the higher frequency in this group is in part due to selection bias, in that the control group was Tr th Figure 3 y in ansver a HIV+ patient se sonogram with non-H showing extensive periportal adenopa odgkin lymphoma - Transverse sonogram showing extensive periportal L neal lymph node adjac asymptom Figure 4 ongitudinatic HIV+ al sonogram of pa etient nt to liver the gall showing a l bladder arge retroperi in a 27 yeart -old o- adenopathy in a HIV+ patient with non-Hodgkin lym- Longitudinal sonogram of liver showing a large retro- phoma. AO-aorta, H-hepatic artery, SP-splenic artery, LN- peritoneal lymph node adjacent to the gall bladder in lymph node. a 27 year-old asymptomatic HIV+ patient. Page 5 of 6 (page number not for citation purposes) BMC Medical Imaging 2008, 8:5 http://www.biomedcentral.com/1471-2342/8/5 nous drug abusers [15-18]. The sonographic correlates of References 1. 2006 report on the global AIDS epidemic, UNAIDS. 2006. this disease are nephromegaly and increased cortical 2. Idoko J: The challenge of providing antiretroviral therapy in echogenicity [3,5,14,18]. The number of HIV+ cases in resource poor countries. Archives of Ibadan Medicine 2004, our study who showed such renal abnormality was more 5:26-30. 3. Tshibwabwa ET, Mwaba P, Bogle-Taylor J, Zumla A: Four-year than double the number of the controls. However, overall study of abdominal ultrasound in 900 Central African adults renal sizes were within normal limits among both groups with AIDS referred for diagnostic imaging. Abdom Imaging 2000, 25:290-296. (Table 3). Renal failure was evident in a quarter of the 4. 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In Diagnostic ultrasound in the study group may have accounted for this. Edited by: Rumack CL, Wilson SR, Charbonneau WJ. St Louis, Mo: Mosby-Year Book; 1991:87-105. Our data supports the fact that manifestations and 8. Langer R, Langer M, Schutze B, Zwicker C, Wakat JP, Felix R: Abdominal Sonographic findings in patients with AIDS. Ront- changes seen on abdominal ultrasound of HIV/AIDS genblatter 1989, 42:121-125. patients appear to be uniform across countries in sub- 9. N'Zi PK, Coulibaly A, N'Dri K, Quattara ND, Diabate SA, Zunon- Saharan Africa. However a wide range of features are seen kipre E, Djedje AT: Ultrasound aspects of abdominal involve- ment in adults with HIV infections in the Ivory Coast: apro- in both HIV+ and HIV- individuals which in the absence pos of 146 cases. Sante 1999, 9:85-88. of histological confirmation makes the clinical usefulness 10. Yee JM, Raghavendra BN, Horii SC, Ambrosino M: Abdominal Sonography in AIDS: A Review. J Ultrasound Med 1989, of ultrasound imaging quite limited. In experienced 8:705-714. hands the radiologist may be able to provide a narrow 11. Geoffray A, Binet A, Cassuto JP, Dujardin P, Coussement A: Sonog- range of diagnostic possibilities that would enhance raphy of abdominal adenopathies in patients with anti-HIV- positive serology. In Imaging of AIDS Edited by: Troto P. Philadel- patient management and care in African communities phia, Pa: Decker; 1991:189-194. where the burden of HIV/AIDS remains astonishingly 12. Townsend RR, Laing FC, Jeffrey RB Jr, Bottles K: Abdominal lym- high. phoma in AIDS: evaluation with US. Radiology 1989, 171:719-724. 13. Fortgang IS, Belitsos PC, Chaisson RE, Moore RD: Hepatomegaly Conclusion and steatosis in HIV infected patients receiving nucleoside analog antiretroviral therapy. Am J Gastroenterol 1995, Ultrasonography is a versatile tool for evaluating abdom- 90:1433-1436. inal organs affected by HIV/AIDS. The sonographic find- 14. Miller F, Patrikh S, Gore R, Nemcek A, Fitzgerald S, Vogelzang R: ings in HIV/AIDS patients in Ibadan, Nigeria are Renal Manifestations of AIDS. RadioGraphics 1993, 13:587-596. 15. Rao TK, Filippone EJ, Nicastri AD, Landesman SH, Frean E, Chen CK, comparable to that from other sub-Saharan African com- Friedman EA: Associated focal and segmental glomeruloscle- munities. However, provision and availability of suffi- rosis in the Acquired Immunodeficiency Syndrome. N Engl J Med 1984, 310:669-673. cient clinico-pathologic data in the future would improve 16. Frassetto L, Schwenfeld P, Humphrey M: Increasing incidence of the quality of ultrasonographic diagnosis and treatment human Immunodeficiency virus – associated nephropathy at in these patients. San Francisco General Hospital. Am J Kidney Dis 1991, 18:655-659. 17. Vella S, Giuliano M, Pezzotti P, Agresti MG, Tomino C, Floridia M, Competing interests Greco D, Moroni M, Visco G, Milazzo Fl: Survival of zidovudine- The author(s) declare that they have no competing inter- treated patients with AIDS compared with that of contem- porary untreated patients. Italian Zidovudine Evaluation ests. Group. JAMA 1992, 267:1232-1236. 18. Gold JWN: HIV infection: diagnosis and management. Med Clin North Am 1992, 76:1-18. Authors' contributions 19. Schaffer RM, Schwartz GE, Becker JA, Rao TKS, Shih YH: Renal OMO and AYA conceived the study. AOM and AAM par- ultrasound in acquired immunodeficiency syndrome. Radiol- ticipated in its design. OYU and AAJ performed the ultra- ogy 1984, 153:511-513. 20. Valeri A, Neusy AJ: Acute and chronic renal disease in hospital- sound examinations. OSA and OMA participated in the ized AIDS patients. Clin Nephrol 1991, 35:110-118. recruitment of subjects and collated the data. AYA and IFA 21. Bourgoignie JJ, Meneses R, Ortiz C, Jaffe D, Pardo V: The clinical spectrum of renal disease associated with human immuno- coordinated the recruitment of subjects. OMO and AOA deficiency virus. Am J Kidney Dis 1988, 12:131-137. organized the ultrasound examinations. OMO, OGI and AAT managed the data, performed statistical analysis and Pre-publication history drafted the manuscript. All authors read and approved the The pre-publication history for this paper can be accessed final manuscript. here: http://www.biomedcentral.com/1471-2342/8/5/prepub Page 6 of 6 (page number not for citation purposes)

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