Sudan Journal of Medical Sciences Volume 17, Issue no. 3, DOI 10.18502/sjms.v17i3.12110 Production and Hosting by Knowledge E Research Article Assessment of Variation in Clinical Presentation of Visceral Leishmaniasis Among Patients Attending the Tropical Diseases Teaching Hospital in Sudan Hammam Abdalrhman Altom Mohammed Ahmed, Ahmed Ali Ahmed Musa, Ahmed Mahmoud Sayed Sayedahmed*, Shiraz Bashir Jabralseed Mohammed, Ehssan Farouk Mohamed Ahmed, Anas Badreldeen Elageb Mohamed, and Abdelsalam Mohamed Ahmed Nail Omdurman Islamic University, Khartoum, Sudan ORCID: Ahmed Ali Ahmed Musa: https://orcid.org/0000-0001-8603-0515 Ehssan Farouk Mohamed Ahmed: https://orcid.org/0000-0001-7862-1606 Shiraz Bashir Jabralseed Mohammed: https://orcid.org/0000-0001-9532-8743 Anas Badreldeen Elageb Mohamed: https://orcid.org/0000-0002-9150-468X Ahmed Mahmoud Sayed Sayedahmed: https://orcid.org/0000-0002-3898-8814 Abstract Background: Visceral leishmaniasis (also known as Kala-azar) is a systemic parasitic infection with many clinical presentations. The present study assesses the variation in presentations among patients who attended the Tropical Diseases Teaching Hospital (TDTH) in Khartoum, Sudan. Methods: This analytical cross-sectional, hospital-based study was conducted at the TDTH between November 2019 and September 2020. Medical records of patients who presented at the TDTH were reviewed using a structured data extraction checklist. The Chi-square test was used to determine the associations between sociodemographic and clinical presentations of patients. P-value < 0.05 was considered as statistically significant. Results: Out of 195 patients, 79.5% were male and 48.2% were <31 years old. Fever was the main clinical presentation (90.2%) while 53.3% presented with weight loss and 72.3% and 39% presented, respectively, with splenomegaly and hepatomegaly. HIV was detected in 4.6% of the patients. RK39 was the main diagnostic test. We found a significant association between the abdominal distention and the age of the patients (P < 0.05) – age groups 11–20 and 41–50 years were more likely to present with abdominal distention than other age groups. Conclusion: There is no exact clinical presentation or routine laboratory findings that are pathognomonic for visceral leishmaniasis; therefore, it should be considered in the differential diagnosis of any patient with fever, weight loss, and abdominal distention, and among patients with HIV. Keywords: visceral leishmaniasis, Sudan, clinical presentations How to cite this article: Hammam Abdalrhman Altom Mohammed Ahmed, Ahmed Ali Ahmed Musa, Ahmed Mahmoud Sayed Sayedahmed*, Shiraz Bashir Jabralseed Mohammed, Ehssan Farouk Mohamed Ahmed, Anas Badreldeen Elageb Mohamed, and Abdelsalam Mohamed Ahmed Nail (2022) “Assessment of Variation in Clinical Presentation of Visceral Leishmaniasis Among Patients Attending the Tropical Diseases Teaching Hospital in Sudan,” Sudan Journal of Medical Sciences, vol. 17, Issue no. 3, pages 341–354. DOI 10.18502/sjms.v17i3.12110 Page 341 Corresponding Author: Ahmed Mahmoud Sayed; email: ahmed1mahmoud111@ gmail.com Received 21 October 2021 Accepted 9 July 2022 Published 30 September 2022 Production and Hosting by Knowledge E Ahmed et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Editor-in-Chief: Prof. Nazik Elmalaika Obaid Seid Ahmed Husain, MD, M.Sc, MHPE, PhD http://www.knowledgee.com https://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/ Sudan Journal of Medical Sciences Ahmed et al 1. Introduction Visceral leishmaniasis (VL; also known as Kala-azar) is a systemic parasitic infection caused by Leishmania donovani, L. infatum, and L. chagasi and transmitted via sand fly Phlebotomus arhentipes [1]. Clinical presentations include fever, malaise, anemia, weight loss, splenomegaly, hepatomegaly, bleeding tendency, among other [2], with fever often presenting first [3]. The condition may become worse as some patients may develop hepatic dysfunction or concurrent infections due to pancytopenia which is associated with VL, while some patients may develop post-kalazar dermal infection (PKDL) [4]. According to the World health organization (WHO), 55% of Sudanese patients suffered from PKDL [5]. Of note, the severity of the clinical presentations depends on the interaction between the parasite and its host, so some patients can become asymptomatic carriers or develop symptoms with varying severity due to their inability to control the multiplication of the parasite [4]. Moreover, the fatality rate for untreated cases in developing countries can be as high as 100% within two years [6]. Sudan is suffering from VL since the early 1900s, and several epidemics have occurred and claimed the lives of thousands of people [7]. The first epidemic in Sudan was reported in 1936 in the upper Nile Province, wherein about 300 individuals were infected, and the death rate was nearly 80% [8]. Moreover, a recent study disclosed that about 1.3 million new VL cases are reported yearly, with an estimated 20,000– 40,000 annual deaths [9]. In addition, about 94% of VL cases are from Sudan, South Sudan, Ethiopia, India, Bangladesh, and Brazil [10]. Furthermore, in 2015, 2902 cases of VL were reported in Sudan [11]. Recent reports confirm that Gedaref State is a known hyper-endemic area for VL, while Western Upper Nile, Kordofan State, Central Sudan, and White Nile State are also considered as endemic areas [12]. Good understanding of the broad spectrum presentation in patients with VL and its relation to certain factors can establish a better outcome, as early diagnosis is the core stone in the management of the disease. Although a number of papers have been published, there is still vagueness due to the diversity of data and classifications, and variation in people from different geographical areas. This study can provide additional information to doctors and decision-makers for improving the management of VL patients. The present study therefore assesses the variation in presentation among patients presented at the Tropical Diseases Teaching Hospital (TDTH) in Khartoum State, Sudan. Moreover, it describes the sociodemographic characteristics of patients with VL and identifies the association between the presentations of patients diagnosed with VL and the sociodemographic characteristics. DOI 10.18502/sjms.v17i3.12110 Page 342 Sudan Journal of Medical Sciences Ahmed et al 2. Materials and Methods 2.1. Study design and study area This is analytical, cross-sectional, hospital-based study was conducted to assess the variation in the presentations of VL among Sudanese patients. It was conducted at the TDTH, which is the only tropical hospital in Khartoum State and the biggest in Sudan, between November 2019 and September 2020. 2.2. Study population Medical records of all Sudanese patients who presented with VL at the TDTH from Jan- uary 2016 to March 2020 were studied. However, patients whose files were incomplete were excluded. 2.3. Study variables 1. Characteristics of patients: age, gender, education, residence, occupation, income, and marital status 2. Different clinical presentations, past medical history, complications, and treatment 3. Laboratory results (hemoglobin, total white blood cells count, platelet count, albu- min) 2.4. Sampling method and sample size The total coverage method was used for all patients who visited the study center during the study period. 2.5. Data collection 2.6. Secondary data were collected using pretested and structured data extraction checklist from all Sudanese cases reported during the study period and fulfilling the inclusion criteria. Data collectors were the researchers themselves. DOI 10.18502/sjms.v17i3.12110 Page 343 Sudan Journal of Medical Sciences Ahmed et al 2.7. Data analysis Data were reviewed, coded, entered, and then analyzed using the SPSS (statistical package social science), version 25. Descriptive statistics were computed to determine frequencies and percentages. Chi-square test was used to determine the associations between sociodemographic and clinical presentations of patients diagnosed with VL at the TDTH. P-value < 0.05 was considered as statistically significant. 64 22 59 45 21 0 10 20 30 40 50 60 70 2016 2017 2018 2019 2020 VL cases Figure 1: Histogram showing the trend in VL over the 2016–2020 period. 3. Results 3.1. Sociodemographic characteristics Table 1 presents the sociodemographic characteristics of our participants. A total of 195 patients with VL were identified during the study period. Of them, 155 (79.5%) were male and 140 (71.8%) were aged <41 years. Some of the patients suffered from concurrent chronic disease (Table 2). 3.2. Clinical presentations and hematological findings Table 3 presents the clinical manifestations of our participants. Out of 195 patients, 177 (90.2%) presented with fever, while 104 (53.3%) presented with weight loss. The mean hemoglobin value was 8.3 g/dl (SD = 2.2), and 177 (90.8%) participants were anemic (hemoglobin level <12 g/dl). While the mean value of the total white blood cells was 3.5 per microliter (SD = 3.4), the mean value of the platelet count was 122 per microliter (SD = 95) and a mean value of 3 g/dl (SD = 1.1) for the albumin. DOI 10.18502/sjms.v17i3.12110 Page 344 Sudan Journal of Medical Sciences Ahmed et al Table 1: Sociodemographic data of VL patients who were admitted to the TDTH. Variables N (%) Gender Male 155 (79.5) Female 40 (20.5) Age (yr) 0–10 2 (1.1) 11–20 42 (21.5) 21–30 50 (25.6) 31–40 46 (23.6) 41–50 29 (14.9) 15–60 15 (7.7) >60 11 (5.6) Marital status Child 10 (6.7) Single 59 (39.3) Married 80(53.3) Divorced 1 (0.7) Residence Khartoum 51 (26.2) Gadarif 26 (13.3) White Nile 26 (13.3) Blue Nile 8 (4.1) North Kordofan 23 (11.8) South Kordofan 15 (7.7) West Kordofan 5 (2.6) North Darfour 3 (1.5) South Darfour 6 (3.1) West Darfour 4 (2.1) Central Darfour 1 (0.5) Nile River 1 (0.5) Northern State 0 Kassala State 8 (4.1) Aljazeera state 4 (2.1) Red sea 1 (0.5) Sinnar 5 (2.6) Occupation Child 7 (4) Unemployed 2 (1.2) Farmer 37 (21.4) Student 22 (12.7) Shepherd 14 (18.1) Housewife 25 (14.5) Others 66 (38.2) Income Low 88 (74.6) Average 29 (24.6) High 1 (0.8) DOI 10.18502/sjms.v17i3.12110 Page 345 Sudan Journal of Medical Sciences Ahmed et al Table 2: Chronic diseases often observed in patients with VL admitted to the TDTH. Chronic diseases N (%) Human immunodeficiency virus (HIV) 9 (4.6) Diabetes mellitus 7 (3.6) Hypertension 6 (3.1) Hepatitis B virus 8 (4.1) Hepatitis C virus 2 (1) Table 3: Clinical manifestations often observed in patients with VL admitted to the TDTH. Clinical picture N (%) Symptoms Fever 177 (90.2) Weight loss 104 (53.3) Fatigue 63 (32.3) Weakness 3 (1.5) Dyspnea 10 (5.1) Abdominal pain 90 (46.2) Joint pain 11 (5.6) Vomiting 21 (10.8) Signs Hyperpigmentation 7 (3.6) Yellow sclera 16 (8.2) Abdominal distention 26 (13.3) Lower limb edema 23 (11.8) Itching 1 (0.5) Lymphadenopathy 49 (25.1) Splenomegaly 141 (72.3) Hepatomegaly 76 (39) Pallor 81 (41.5) Laboratory findings (Mean ± SD) Hemoglobin (gr/dl) 8.2 ± 2.2 Total white blood cells (per microliter) 3.5 ± 3.4 Platelet count (per microliter) 122 ± 95 Albumin (gr/dl) 3 ± 1.1 Tested N (%) Positive (N) RK39 134 (68.7) 119 RK28 3 (1.5) 2 Bone marrow aspiration 70 (35.9) 62 Lymph node aspiration 46 (20.5) 43 DAT 43 (22) 38 Skin biopsy 2 (1) 2 DOI 10.18502/sjms.v17i3.12110 Page 346 Sudan Journal of Medical Sciences Ahmed et al Table 4: Concurrent infections often detected in patients with VL admitted to the TDTH. Concurrent infections N (%) Tuberculosis 7 (3.6) Gastroenteritis 26 (13.3) Pneumonia 18 (9.2) Malaria 11 (5.6) Otitis media 0 Urinary tract infection 8 (4.1) Esophageal candidiasis 1 (0.5) Table 5: The trend in VL admissions to the TDTH from 2016 to 2020. Year All hospitalizations All leishmaniasis Visceral leishmaniasis Cumulative # of VL cases 2016 78 66 64 - 2017 61 29 22 86 2018 138 81 59 145 2019 86 66 45 190 2020 54 32 21 211 Total 417 274 211 211 Table 6: Early outcomes for VL patients who were admitted to the TDTH. Outcomes N (%) Death (2016 to 2020) 29 (15) Discharged after initial improvement 161 (83.4) Referred (for nonresponse) 1 (0.5) Discharged against medical advice 2 (1) 3.3. Complications Concurrent infections were the main complication in our participants (63, 32.3%). Table 4 demonstrates the most common concurrent infections. Other complications were bleeding tendency (34, 17.4%) and PKDL (8, 4.1%). 3.4. Hospitalization rate Out of 417 admissions to TDTH during the study period, 274 were due to leishmaniasis. This includes only those patients who were admitted to the hospital as inpatient (Table 5). Figure 1 demonstrates the trend in VL over the 2016–2020 period. DOI 10.18502/sjms.v17i3.12110 Page 347 Sudan Journal of Medical Sciences Ahmed et al Table 7: Association between clinical presentations of patients diagnosed with VL at the TDTH and the corresponding age groups. Clinical picture Age (yr) Statistics 0–10 11–20 21–30 31–40 41–50 51–60 > 60 Chi- square P-value Fever 2 40 46 41 26 11 11 8.046 0.235 Weight loss 1 23 26 21 19 8 6 2.906 0.821 Fatigue 0 18 17 15 8 4 1 6.384 0.382 Weakness 0 0 1 0 0 1 1 8.676 0.193 Dyspnea 0 3 2 2 2 1 0 1.501 0.959 Abdominal pain 1 18 16 22 19 7 7 10.007 0.124 Hyperpigmentation0 3 2 2 0 0 0 3.755 0.710 Vomiting 0 2 5 6 5 2 1 3..496 0.744 Joint pain 0 4 5 1 0 1 0 6.554 0.364 Yellow sclera 0 3 6 3 1 3 0 5.996 0.424 Abdominal distention 0 8 1 5 8 3 1 13.140 0.041∗ Lower limb edema 0 1 8 6 3 4 1 8.089 0.232 Itching 0 0 0 1 0 0 0 3.256 0.776 Lymphadenopathy0 7 12 16 6 3 5 7.511 0.276 Splenomegaly 2 33 39 31 20 7 9 8.537 0.201 Hepatomegaly2 17 22 18 8 4 5 6.434 0.376 Pallor 0 20 22 16 12 6 5 3.134 0.792 ∗Significant association 3.5. Diagnosis and treatment RK39 was the most commonly used diagnostic method, used for 134 (68.7%) of our participants. Other diagnostic methods that were used were bone marrow aspiration (70, 35.9%), lymph node aspiration (46, 23.6%), DAT (33, 22.1%), RK28 (3, 1.5%), and skin biopsy (2, 1%). On the other hand, sodium stibogluconate was the main drug used to treat the patients (103, 52.8%), followed by amphotericin B (93, 47.7%) and paromomycin (66, 33.8%). Some patients received antibiotic therapy (36, 18.5%), 180 (92.3%) received multivitamins, while 41 (21%) required blood transfusion. Early outcomes are presented in Table 6. Case fatality rate was calculated (Tables 5 & 6) as follows: 29÷ 211 × 100 = 14.9% (from 2016 to 2020). DOI 10.18502/sjms.v17i3.12110 Page 348 Sudan Journal of Medical Sciences Ahmed et al Table 8: Association between clinical presentations of patients diagnosed with VL at the TDTH and their gender. Clinical picture Gender Statistics Male Female Chi- square P-value Fever 141 36 0.036 0.850 Weight loss 79 25 1.699 0.192 Fatigue 51 12 0.123 0.726 Weakness 2 1 0.307 0.579 Dyspnea 8 2 0.002 0.967 Abdominal pain 68 22 1.585 0.208 Hyperpigmentation 6 1 0.173 0.678 Vomiting 17 4 0.031 0.860 Joint pain 10 1 0.933 0.334 Yellow sclera 12 4 0.215 0.643 Abdominal distention 22 4 0.484 0.487 Lower limb edema 21 2 2.233 0.135 Itching 1 0 0.259 0.611 Lymphadenopathy 38 11 0.150 0.698 Splenomegaly 116 25 2.417 0.120 Hepatomegaly 65 11 2.786 0.095 Pallor 65 16 0.049 0.825 3.6. Association between clinical presentations and age groups Table 7 presents the association between clinical presentations of VL patients at the TDTH and the age groups. A significant association was seen between the abdominal distention and the age of the patients (P < 0.05). Age groups 11–20 and 41–50 years were more likely to present with abdominal distention than other age groups. 3.7. Association between clinical presentations and gender Table 8 presents the association between clinical presentations of VL patients in TDTH and gender. None of the clinical presentations was found to be associated with the gender of the patients. DOI 10.18502/sjms.v17i3.12110 Page 349 Sudan Journal of Medical Sciences Ahmed et al Table 9: Association between clinical presentations of patients diagnosed with VL at the TDTH and geographic areas. Clinical picture Geographic areas Statistics Khartoum state Gadarif White Nile Blue Nile North Kordofan South Kordofan South Darfur Kassala state Others Chi- square P-value Fever 48 24 24 8 20 13 6 7 21 5.736 0.766 Weight loss 23 10 16 5 8 11 4 6 16 14.186 0.116 Fatigue 19 8 7 1 6 5 2 6 7 9.767 0.370 Weakness 0 0 0 0 1 0 0 0 1 10.826 0.288 Dyspnea 2 1 2 0 1 1 0 1 2 3.283 0.952 Abdominal pain 23 15 7 1 10 7 4 4 12 15.708 0.073 Hyperpigmentation 2 1 0 0 0 1 0 0 1 13.694 0.134 Vomiting 3 4 4 1 1 2 1 2 3 6.478 0.691 Joint pain 2 0 3 0 1 2 1 0 2 8.408 0.494 Yellow sclera 2 1 5 1 0 1 0 3 3 19.348 0.022∗ Abdominal distention 5 5 4 1 3 2 0 1 2 6.924 0.645 Lower limb edema 6 2 2 2 4 0 2 1 4 9.177 0.421 Itching 0 0 1 0 0 0 0 0 0 6.534 0.686 Lymphadenopathy 15 6 5 2 7 2 3 3 4 6.027 0.737 Splenomegaly 41 18 17 5 12 9 5 7 20 12.251 0.200 Hepatomegaly 17 8 9 4 9 6 3 4 10 7.196 0.617 Pallor 20 6 11 4 11 8 3 5 10 6.917 0.646 ∗Significant association 3.8. Association between clinical presentations and geographical areas Table 9 presents the association between clinical presentations of VL patients in TDTH and their residence. There was a significant association between the yellow sclera and patients’ place of residence (P < 0.05). Patients from the White Nile area were more likely to present with yellow sclera than others. 4. Discussion The clinical features and laboratory findings described here are based on the data from the case files of 195 Sudanese patients diagnosed with VL. We determined that VL is mainly presented by fever, weight loss, splenomegaly, anemia, hepatomegaly, and abdominal pain. In this study, 155 (95%) patients were male, and 140 (71.8%) of them were younger than 41 years. This finding is in agreement with a previous study conducted in Kenya, DOI 10.18502/sjms.v17i3.12110 Page 350 Sudan Journal of Medical Sciences Ahmed et al where 105 (77%) patients were male, and 129 (89%) were younger than 45 years [13]. Moreover, a previous study conducted in India concluded that the male gender is a risk factor for VL [14]. Males from a young age are more likely to sleep outside (in yards and farms), so they are more exposed to sand-fly bites [15, 16]. Moreover, a majority of patients in our study presented with fever (90.2%), splenomegaly (72.3%), weight loss (53.3%), or hepatomegaly (39%). In a study con- ducted in Brazil and Mexico, the patients mainly presented with hepatomegaly (98%), splenomegaly (97.8%), or fever (97.7%) [17]. Moreover, we found that 4.6% of our patients were diagnosed with HIV. This finding is in agreement with another study conducted in Brazil, where 5.5% of VL patients were co-infected with HIV [18]. Owing to the lack of facilities or poor reporting systems, VL/HIV co-infection is underreported in many endemic areas [19]. VL is a common opportunistic infection in HIV patients, as they are more vulnerable to VL infection, and HIV replication is accelerated in VL patients [19]. Most of our patients were treated with sodium stibogluconate (52%), followed by amphotericin B (47.7%) or a combination of paromomycin and sodium stibogluconate. On the other hand, >60% of patients in Brazil and Bulgaria were treated with Meglumine Antimoniate [18, 20]. Due to parasites’ drug resistance, liposomal amphotericin B is now the drug of choice for VL [21]. In our study, RK39 was the most used diagnostic test; about 61% of our patients were diagnosed by it. RK39 is a widely used test because it is a simple, sensitive, specific, and economical test [17]. In this study, bone marrow aspiration and lymph node aspiration were done for 70 and 46 patients, respectively, and no patient had undergone splenic aspiration. The splenic aspirate is more sensitive than bone marrow or lymph node aspirate; however, the splenic aspirate is a complicated procedure and associated with a risk of fatal hemorrhage [22, 23]. Regarding limitations of this study, data were available in a paper-based database, this type of database is difficult to deal with, and it can be lost or damaged easily. 5. Conclusion In conclusion, we found that fever was the main clinical finding, followed by splenomegaly, weight loss, and hepatomegaly. However, there is no exact clinical presentation or routine laboratory findings that are pathognomonic for VL; therefore, it should be considered in the differential diagnosis of any patient presenting with an unusual presentation from the endemic areas or with a history of recent travel. HIV is commonly associated with VL, so VL patients must be investigated for HIV infection. 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DOI 10.18502/sjms.v17i3.12110 Page 354 Introduction Materials and Methods Study design and study area Study population Study variables Sampling method and sample size Data collection Secondary data were collected using pretested and structured data extraction checklist from all Sudanese cases reported during the study period and fulfilling the inclusion criteria. Data collectors were the researchers themselves. Data analysis Results Sociodemographic characteristics Clinical presentations and hematological findings Complications Hospitalization rate Diagnosis and treatment Association between clinical presentations and age groups Association between clinical presentations and gender Association between clinical presentations and geographical areas Discussion Conclusion Acknowledgements Ethical Considerations Competing Interests Availability of Data and Material Funding References