Assessment of Visceral Leishmaniasis Consequences Using Ultrasound ()
1. Introduction
Visceral leishmaniasis (VL), known as kala azar in India, is the cause of much death and disease in developing countries. It is one of several diseases caused by over 20 species of Leishmania; it is transmitted by Sandfly bites [1] . The infection of humans appears with multiple clinical manifestations, including cutaneous (CL), mucocutaneous, diffuse and VL. The latter is responsible for approximately 59,000 deaths per year, a parasitic disease surpassed only by malaria [2] [3] . There are two types of VL, anthroponotic and zoonotic. Zoonotic VL (ZVL) is widespread and occurs in Latin America, Northern Africa, Southern Europe and in areas of the Middle East and Asia [2] -[4] . Two forms of leishmaniasis (VL and CL) present in Europe are caused by Leishmania infantum [4] . While cases of cutaneous leishmaniosis were reported in France, Italy and Spain, ZVL is endemic in all countries bordering the Mediterranean Sea [5] .
Geographically, the distribution of leishmaniasis is limited by the distribution of its vector Sandfly species. The Sandfly vectors are mainly active during the night, and therefore the highest risk for contracting the infective stages of the parasite from Sandfly bites is between dusk and dawn [6] . The reservoirs of the pathogen can be several wild and domestic canid and rodent species, but domestic dogs are considered as the main reservoir of Leishmania infantum playing a key role as the source of human infection. Indeed, there is a clear association between a high rate of infection in dogs and an increased risk of human disease [2] [7] .
VL is endemic in 62 countries, with a total of 200 million people at risk, an estimated 500,000 new cases each year worldwide, and 41,000 recorded deaths in the year 2000 [8] [9] . As is the case for other tropical diseases, epidemiological data are incomplete, and official figures are likely to underestimate grossly the real prevalence of the disease [10] . Both the number of recorded cases and the geographic areas affected have grown in the past two decades [11] .
Delays and difficulty in diagnosis are common due to the long incubation period of the agent, nonspecific symptoms, and the difficulty of identifying the intracellular protozoa (Donovan bodies) in tissue aspirates. It is usually diagnosed by serology or bone marrow examination. Liver biopsy is rarely required for diagnosis [12] . The role of imaging techniques as diagnostic tools remains to be established in VL [13] . This study designed with an aim to assess the consequences of VL in the liver, spleen and pancreas of the affected participants by using ultrasound, which will contribute in the treatment of the disease in an early period, before the exacerbation of complications and the condition become difficult to control.
2. Materials and Methods
2.1. Selection and Description of Participants
This prospective cohort study was performed in the period of January 2012 to March 2014. Participants were scanned in the ultrasound department of Tropical Disease Hospital (TDH) in Khartoum-Sudan. Prior to participants scanning, a formal approval was obtained from Ethics and Scientific Committee of TDH and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and all subsequent revisions.
After the nature of the procedure was fully explained, informed consents were obtained from participants and the ultrasound department. Sudanese participants were included in this study, after they were diagnosed to be affected by VL on the basis of noninvasive laboratory tests, either immunodiagnostic (serological tests) or nonspecific serological tests (Napier’s Aldehyde test). Participants were excluded if they were pregnant or breastfeeding, human immunity virus (HIV) positive, had a serious concurrent infection such as tuberculosis, bacterial pneumonia, malaria or if they had a granulocyte count <1 × 109/l, hemoglobin concentration <40 g/l, or platelet count <40 × 109/l.
2.2. Technical Information Identifies
Abdominal ultrasound scanning was performed using Aloka (SSD-500) portable ultrasound machine equipped with 3.5 MHz convex probe (serial number of 1028924YM7, manufactured date of February 2010 and made by the Yokogawa medical system, Ltd. 7 - 127 Asahigaoka 4-chome Hino-shi Tokyo, Japan). Printing facility issued through the ultrasound-digital graphic-printer (serial number of 3-619-GBI-01 made by Sony CorporationJapan), 100 V; 1.5 A; and 50/60 Hz.
2.3. Abdominal Ultrasound Scanning Technique
Abdominal ultrasound scanning technique used was in accordance with the protocols established by the American Institute of Ultrasound in Medicine (AIUM) [14] . The examination of the liver should include long-axis and transverse views. The liver parenchyma should be evaluated for focal and/or diffuse abnormalities. If possible, the echogenicity of the liver should be compared with that of the right kidney [15] -[17] . Whenever possible, all portions of the pancreas -head, uncinate process, body, and tail-should be identified. Orally administered water may afford better visualization of the pancreas [18] -[20] . Representative views of the spleen in long-axis and transverse projections should be obtained. Splenic length measurement may be helpful in assessing enlargement. Echogenicity of the left kidney should be compared to splenic echogenicity when possible.
An attempt should be made to demonstrate the left hemi diaphragm and the adjacent pleural space [21] [22] . The potential benefits and risks of each examination should be considered. The ALARA (as low as reasonably achievable) principle should be observed when adjusting controls that affect the acoustic output and by considering transducer dwell times.
2.4. Statistical Analysis
Data were initially summarized as mean ± SD in a form of comparison tables. Statistical analysis was performed using the standard Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL, USA) version 15 for windows.
3. Results
Study population comprised 100 positive participants to VL (84% males and 16% females). Participants’ ages ranged from 15 to 45 years; with a mean age of (29.8 ± 2.2) years (Table 1). Out of the scanned participants, a total of 34 subjects were in the age group (35 - 39) years, representatives (34%) of the population. The age group of (40 - 45) years was the smallest and representing only (6%) of the population (Table 1). The highest mean ± SD of ages was (43 ± 1.4) years and found in the age group 40 - 45 years, while the lowest mean ± SD of ages was (18 ± 1.4) years found in the age group 15 - 19 years (Table 1).
Regarding symptoms and signs of VL; abdominal distention was detected in (50%) of participants, while hepato-splenomegaly, weight loss and fever were present in (100%) of participants. Cough and diarrhoea were the least clinical features detected only in (2%) of participants for each (Table 2). Sonographically, hepatic complications of VL were hepatic lesions as hepatomegaly (100%), increased liver echogenicity (18%), dilated portal vein (7%), and shrinkage liver (4%) (Table 3).
In the Spleens of the affected participants, ultrasound detects features of splenomegaly (100%), hypoechoic spleen (19%), and focal splenic lesion (34%). While in pancreas, acute pancreatitis (2%) and decreased pancreatic echogenicity (1%) were the commonest sonographic findings (Table 3). Other complications of VL such as ascites (50%) and lymphadenopathy (35%) were also detected (Table 3).
4. Discussion
Kala azar is a protozoal infection common in developing countries; there are an estimated 500,000 new cases

Table 1. Distribution of participant’s ages (years).

Table 2. Distribution of symptoms and signs in VL participants.

Table 3. Ultrasound findings in the liver, spleen and pancrease of VL participants.
every year and there were 41,000 recorded deaths in the year 2000 [23] . From the early 1900s, VL has been among the most important health problems in Sudan, particularly in the main endemic area in the eastern and central regions. Several major epidemics have occurred—in the Western Upper Nile province in southern Sudan, detected in 1988—and the most recent claiming over 100,000 lives [24] .
Delay and difficulty in diagnosis are common, especially in the early stage of the disease, due to non-specific symptomatology and difficulty in demonstrating intracellular protozoa in tissue aspirates [25] . In this study there was a wild diversity in clinical patterns (Table 2) and this was caused because the pathogenicity depends mainly on parasite genotype versus host immungenetic profile [26] .
Study results showed that abdominal ultrasound can detect the changes occur in organ size as well as to demonstrate the echo texture changes—hyper or hypo echogenicity—in case of VL complications in liver, spleen and pancreases (Table 3). Such findings were confirmed in another study of ultrasound findings in patients with VL, where their results showed that abdominal ultrasound can detect the changes in organ size in an appropriate manner as well as to demonstrate the echo texture changes as hyper or hypo echogenicity in case of inflammation as pancreatitis and renal inflammatory diseases resulted from VL [27] .
Also ultrasound findings of hepatosplenomegaly, and abdominal lymphadenopathy secondary to VL had been reported when VL was diagnosed by ultrasound guided fine needle aspiration of an axillary node and when ultrasound is used to study changes occur in the organ parenchyma in VL participants [28] [29] .
Abdominal ultrasound has the capability to diagnose VL and differentiating it from mimicking conditions, in complement with other laboratory tests. Delayed diagnosis due to a typical manifestation can lead to fatal outcome in patients. Instead of relying solely on the classical clinical features of visceral leishmaniasis, simple abdominal ultrasound examination can help to make an early diagnosis even in atypical cases, thereby reducing the mortality of visceral leishmaniasis. The use of ultrasound as a primary model in the diagnosis of patients with VL, and characterization of the signs and complications in Tropical Sudanese hospitals is enlightening.
This study is limited because the obtained results cannot be applied to the whole society in Sudan, because it was conducted only in Khartoum state rather than other states in Sudan.
5. Conclusion
In conclusion, ultrasound scanning presents to be an effective tool in the diagnosis of VL consequences because of its ability to detect these complications in various abdominal organs such as liver, spleen and pancreas, which in turn allowing the possibility of prevent and treat related deterioration in the patient’s health status.
Acknowledgements
The author would like to thank the staff of the ultrasound department at the Tropical Disease Hospital (TDH) for their cooperation and support during data collection.