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Endemicity of Malaria parasites among Tuberculosis infected HIV patients attending Bombo-Military Hospital, Luwero District, Uganda

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Contents

Contents hide
1 Contents
2 end
3 Okello1 P, Agwu2 E, Yona M3
3.1 Abstract
3.1.1 Background
3.1.2 Materials and methods
3.1.3 Results
3.1.4 Conclusion
3.2 INTRODUCTION
3.3 MATERIALS AND METHODS
3.4 Data analysis
3.5 RESULTS
3.6 DISCUSSION OF THE PARASITES STUDY
3.7 References

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Okello1 P, Agwu2 E, Yona M3

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Addresses:

Dept: 1&3: Laboratory Unit, Bombo Military Hospital, Luwero district, Uganda, 2: Department of Medical Microbiology, Kampala International University, Western Campus Ishaka, Box 71, Bushenyi, Uganda.

Correspondence: [email protected]: Tel: +256782101486

Citation 1: Okello P, Agwu E, Yona M. Endemicity of Malaria parasites among Tuberculosis infected HIV patients attending Bombo-Military Hospital, Luwero district, Uganda. Special Parasites Pathogens Journal (SJ-PPJ) 2015, Vol 1, No 1, Pag: 021-28

Citation 2: Okello P, Agwu E, Yona M. Endemicity of Malaria parasites among Tuberculosis infected HIV patients attending Bombo-Military Hospital, Luwero district, Uganda. Spec. para. pathog. j. 2015, Vol 1, No 1, Pag: 021-28  DOI: 10.61915/ppj.289134//10.61915/ppj.012801

DOI: https://doi.org/10.61915/ppj.289134 ; https://doi.org/10.61915/ppj.012801

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Abstract

Background

Malaria parasites, Tuberculosis, and HIV respectively are recognized public health global menace. The prevalence of Tuberculosis and HIV in Malaria endemic regions needs urgent attention to avert catastrophic health consequences. Objective: To evaluate the endemicity of Malaria among Tuberculosis infected HIV patients attending Bombo-Military Hospital.

Materials and methods

This was a laboratory-based cross-sectional study in which 100 HIV patients were screened for malaria parasites and Mycobacterium tuberculosis and parasite density determined using standard Microbiological and parasitology methods. Data generated were tested for statistical significance.

Results

Out of 100 participants (18 females were civilians and 82 males were soldiers), 2.4% of males had malaria, 3.7%) had PTB, 1 (1.2%) had both malaria and PTB.  Of the 18 females, only 1 (5.6%) had PTB. Malaria parasites and TB prevalence of 3.3% were among those aged 21-30 years. The highest 16.7% prevalence of PTB and malaria-PTB co-infections was among those aged 51-60 years. Malaria parasites prevalence among soldiers was 2.4%, and 1.2% had malaria and PTB while 3.7% had PTB alone. Participants’ demographic characteristics (p<0.05; r=0.243) influenced malaria endemicity among Tuberculosis infected HIV patients studied.

Conclusion

Malaria parasites remained endemic even among Tuberculosis infected HIV patients studied Malaria disease surveillance, advocacy on innovative prevention and control strategies, an updated policy that will support effective intervention, are highly recommended.

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INTRODUCTION

Malaria is an acute febrile illness caused by protozoa of the genus Plasmodium (1) which is spread to humans by female Anopheles mosquitoes during blood meals. Four species of malaria parasite which infect humans include Plasmodium falciparum, Plasmodium malariae, Plasmodium vivax, and Plasmodium ovale. Plasmodium causes different types of malaria namely: malignant, quartet, benign and tertian malaria respectively, and P. falciparum is the most deadly of all the strains (1-2).

Falciparum malaria is the most widespread, accounting for up to 80% of malaria cases worldwide (3). Co-infection with malaria and HIV is common where the two diseases coexist in general populations or specific high-risk groups (4). Given these high levels of co-infection, interactions between the two diseases have major implications for treatment, care, and prevention (5).

The underlying epidemiology of malaria transmission in part predicts the clinical consequences of the interaction between malaria and HIV. A cohort study from rural Uganda indicates that HIV-infected adults have higher levels of asymptomatic parasitemia compared to those without HIV infection (6). About 40% of the world is at risk of malaria; however, 9 out of 10 cases occur in Africa south of the Sahara (7).

An estimated 2-fold risk of clinical malaria in HIV-infected individuals could increase the burden on clinical services in areas where HIV is prevalent and one child dies every 30 seconds (2). Although the major burden of malaria and HIV occurs in the same regions (sub-Saharan Africa, South-East Asia, Latin America, and the Caribbean), the prevalence of malaria and HIV varies widely within each region (6). In a region with an HIV prevalence of 30%, the population-attributable fraction could reach 20% for parasitemia and 35% for clinical malaria (6).

Onyenekwe et al, (8) from South Eastern Nigeria, reported malaria co-infection with HIV-infected individuals as 11.8% and amongst the symptomatic HIV seropositive group as 33.3%. Two subsequent cross-sectional studies of pregnant women from Malawi found that the prevalence of malaria parasitemia on the first prenatal visit was higher among HIV-1–infected women (32% and 54%, respectively) than among HIV-1–seronegative women (19% and 42%, respectively), a trend more pronounced with multigravidity (9-10). The risk of clinically diagnosed malaria (parasitemia and fever) was also higher in HIV-1–infected patients in a cohort of Ugandan adults and rates of clinical malaria were inversely related to CD4 cell counts (6, 11).

Tuberculosis is the leading cause of death among people living with HIV/AIDS (PLWHA) and one of the most common opportunistic infections they experience (12).  The disease burden on the people in the Sub-Saharan African countries is onerous, making economic and political progress difficult (13). AIDS, tuberculosis, and malaria are the three diseases responsible for most of the morbidity and mortality in the (Africa) region (13).

The number of tuberculosis patients co-infected with HIV has risen during the past two years with 30% of the deaths among AIDS patients attributable to tuberculosis (14). The triple scourges of HIV/AIDS, tuberculosis, and malaria pose the greatest threats to the health of the African people (13). HIV and tuberculosis form a lethal combination, each speeding each other’s progress (15). People who are infected with HIV are especially susceptible to developing active tuberculosis (12).

Okodua et al (16) in Edo State, Nigeria, reported a 21.7% of pulmonary tuberculosis disease with pulmonary tuberculosis in males as 54 (26.1%) being higher than that of females at 34 (17.2%).  Thirty-nine (9.6%) patients had HIV-PTB co-infection with higher infection in females 23 (11.6%) than in males 16 (7.7%).

In sub-Saharan African countries the problem of HIV, tuberculosis, and malaria is still very high. Both Mycobacterium tuberculosis (M. tuberculosis) and malaria parasites are known to be increasingly prevalent among HIV/AIDS patients living in Africa. To the best of our knowledge, the exact situation among military personnel in East Africa and Uganda, in particular, is not known.

Again, Mycobacterium tuberculosis and Malaria parasites are known to help HIV-infected persons to degenerate faster to AIDS (17). Interactions between the two diseases may therefore have major implications for the treatment, care, and prevention of both.

There are so many researches on Malaria HIV and tuberculosis, and malaria in East Africa but the exact situation among the military personnel, particularly in Uganda is still not clear. According to Weaver (18), increased funding from the rest of the world for combating Malaria, HIV/AIDS, tuberculosis, and malaria is making a real difference in Uganda. Despite the achievements made in local biomedical research prevalence of tuberculosis and malaria infections among HIV infected and AIDS patients in the Uganda military is still not known.

The study to determine the prevalence of malaria parasites among pulmonary tuberculosis-infected HIV/AIDS patients attending Bombo Military Hospital, and Luwero District, was therefore initiated with the ultimate goal of improving healthcare. The study is significant because the army is vulnerable as reported by Fraser et al (2008). The objective of this study was to determine the endemicity of malaria parasites in pulmonary tuberculosis-infected HIV patients attending Bombo Military Hospital.

 MATERIALS AND METHODS

This was a laboratory-based cross-sectional study, designed to determine the endemicity of malaria in pulmonary tuberculosis-infected HIV/AIDS patients attending Bombo Military Hospital situated in Luwero District in the central region of Uganda. Bombo Military Hospital (BMH) has a capacity of 150 beds, serving approximately 15,000 in-patients yearly. Patients attending BMH are mainly military personnel, their families, and civil communities living near the military barracks. Those included in this study were: febrile, HIV seropositive, adult military officers in Uganda People’s Defence Forces with lower respiratory tract infection.

Informed consent was sought and obtained from the Kampala International University Research and Ethics Committee, the patients, and the management of Bombo Military Hospital. The sample size of 100 was obtained using the standard formula: n=Z2P(1-P)/d2 (19) where d = margin of error, a significance level of 0.05 (i.e. 5%), P= prevalence of HIV in Uganda and is known to be 6% (MOH 2004),  Z=Level of significance (1.96) for the confidence interval of 95%. To take care of sampling error, 122 subjects were recruited between April and August 2008.

The participants sampled were given clean, dry, wide-neck, leak-proof containers, and requested to produce deep aspirated early morning sputum for detection of acid and alcohol fast bacilli while blood samples were taken from the participants to confirm their HIV status and determine the malaria prevalence and severity. To confirm HIV seropositivity of the included patient, 3 HIV serological methods: Abbott (Determine), Uni-gold, and Stat pack.

The blood samples were first tested for HIV antibody using Abott Determine HIV kit according to the manufacturer’s instructions (Abbott Company). Those that tested positive were tested with a Uni-Gold HIV kit. Samples that also tested positive with Uni-Gold were reported as positive. Whenever there was disagreement between the two test kits, a third-line test kit, Stat-Pak, was used as a tie-breaker.

Sputum smears for acid-fast bacilli test using Ziehl-Nelseen technique: Briefly, 1-2 ml of deep expectorated early morning sputum was transferred to a screw-cap sputum container of 15-20 ml capacity and an equal volume of concentrated sodium hypochlorite solution (bleach) was added. The sputum was left at room temperature for 10-15 minutes, some quantities of antimucolytic saline were added and mixed well. The sample was centrifuged at 3000g for 15 minutes.

The supernatant was discarded. The sediment was mixed well and a drop was transferred to a clean glass slide, spread to make a thin film, and allowed to air-dry. The air-dried smears were heat-fixed and stained for Acid and Alcohol Fast Bacilli (AAFB) using the Zeel Nelson Techniques. The bacteria were seen as bright slender red rods on a blue background (1). Definite red bacilli seen on the smear was reported as AFB positive (20).

Venous blood was collected aseptically from the subjects using vacutainer tubes containing ethylene diamine tetra-chloro-acetic acid (EDTA) anticoagulant and mixed very well. Thin and thick blood films were made on clean grease-free microscope slides using standard methods and stained with field stain following standard Microbiology protocols. Blood films were examined microscopically using the 40x and 100x objectives. The approximate numbers of parasites (trophozoites, schizonts, and gametocytes) and also whether a malaria pigment was present in white cells (always mentioning when the pigment was in neutrophils) were reported.

To determine the severity of malaria in the study population, malaria parasites were counted in thick blood films and the result was expressed as many parasites per microlitre of blood concerning a predetermined number of leukocytes and result read using standard guidelines (21). Briefly: If, after 200 leukocytes have been counted, 10 or more parasites have been identified, the results were recorded, showing the number of parasites per 200 leukocytes.

If, after 200 leukocytes have been counted, 9 or fewer parasites have been counted, counting was continued until 500 leukocytes have been counted and the results recorded as the number of parasites per 500 leukocytes. The parasite count concerning the leukocyte count was converted to parasites per microlitre using the formula: No. of parasites x 8000/ Number of leukocytes = Number of parasites per μl.

This means that if 200 leukocytes were counted, the number of parasites counted was multiplied by 40 and if 500 leukocytes were counted the number of parasites was multiplied by 16 according to WHO (21). With falciparum infections, because the gametocytes were easily recognized, it was possible to report separately the asexual and sexual forms e.g. P. falciparum trophozoites, gametocytes +, with malaria pigment in white cells (3).

Data analysis                                                                                                         

Correlation and regression were the statistical tools used to analyze the data generated. Linear correlation and linear regression (22 were used to describe the relationship between two quantitative variables (e.g. Occupation and prevalence of malaria infection). The former is a statistic that measures the strength of a bivariate association while the latter is a prediction equation that estimates the value of y for any given x. The correlation coefficient (r), which is a measure of the strength of the linear association between two variables was used to describe the relationship between occupation, age, gender, and sex against malaria endemicity, Tuberculosis, and malaria-TB co-infection.

 RESULTS

One hundred subjects (18 females and 82 males) were included in the study. Out of the 82 males 2 (2.4%) had malaria, 3 (3.7%) had PTB, 1 (1.2%) had both malaria and PTB.  Of the 18 females, only 1 (5.6%) had PTB. Eighty-two (82%) of the 100 subjects involved in this study were males and 18 (18%) were females.  (Table 1). Table 2 below shows that the least prevalence of malaria and TB was among subjects in the age group of 21-30 years old.

Out of the 30 subjects tested in this age group, 1 (3.3%) had malaria and 1 (3.3%) had PTB. The table reveals the highest prevalence of PTB and malaria-PTB co-infections among age groups of 51-60 years. Out of the 6 subjects sampled 1 (16.7%) had PTB and 1 (16.7%) had malaria-PTB co-infection. From (Table 3), Two (2.4%) of the soldiers had malaria, 3 (3.7%) had PTB, and 1(1.2%) had both malaria and PTB. Of the 18 civilians, 1 (5.6%) had PTB. Exactly 82% of the subjects recruited in the study were military personnel and 18% were civilians.

In (Table 4) below, malaria was found to be more prevalent among the Banyoro at 1 (25%) of the 20 subjects; followed by the Iteso at 1 (6.25%) out of the 16 subjects. PTB was found to be least prevalent among the Banyankole at 1 (5.0%) of the 20 subjects sampled but highest among the Bakiga at 1 (7.0%) of the 7 subjects examined.

The prevalence of malaria parasiteswas significantly (p < 0.01) dependent on Tb infection among HIV/AIDS patients. Occupation, gender, age, and tribe significantly (p < 0.05) influenced the rate of malaria distribution among the studied HIV/AIDS patients. Positive regression (r = 0.243) was found to exist when the relationship between the age of patients sampled and the prevalence of malaria parasite, TB, and malaria/TB was compared.  In febrile HIV patients with malaria the prevalence of TB infection was significantly dependent on malaria (p < 0.01).

The prevalence of malaria parasite and malaria/TB co-infection was significantly dependent on occupation and the burden of: TB, malaria, HIV/AIDS, age and gender (p < 0.01; r=0.107, r=0.234). There was a significant statistical difference (p<0.05) when the relationship between occupation and the mean prevalences of malaria, TB, and malaria/TB were compared. On the other hand, there was no significant statistical difference (p>0.05) when the relationship between age, gender tribe, and the mean prevalences of malaria, TB, and malaria/TB were compared among the studied HIV population.

                                                                                                                   

DISCUSSION OF THE PARASITES STUDY

Microscopic examinations of stained blood films and sputum stained smears are the main laboratory techniques used for the diagnosis of malaria and tuberculosis in most developing countries. This is because microscopy is a reliable and affordable routine diagnostic technique in resource-poor countries when performed by experienced and trained microscopists. The prevalence of malaria, MTB, and malaria/MTB co-infection among HIV-infected patients in this study was found to be 2.0%, 4.0%, and 1.0% respectively.

The prevalence of P. falciparum (2.0%) in this study is lower than 18.9% reported by Onyenekwe et al (8) in southeastern Nigeria. This difference could be because environmental and socio-economical factors favoring malaria prevalence may be more predominant in the West African region of south Eastern Nigeria than here in East Africa. It could also be due to differences in the study population. This study involved mainly soldiers who have easy access to health facilities whereas the study in Southeastern Nigeria involved civilians some of whom may not have easy access to health facilities.

In a study conducted by Ndyomugyenyi et al (23) in Western Uganda, only 24.8% of studied 1627 patients had malaria and more than 75% of this population were misdiagnosed as malaria positive and treated for malaria while they had no malaria. This finding surprisingly contradicts the report of this parasite in HIV study because Western Uganda is expected to have a lower prevalence of malaria due to the topography and cold climate which do not favor the survival of mosquitoes that transmit P.falciparum infection (Githeko et al (24). Another reason for the discrepancy could be because this study was restricted to only adults who were HIV positive thus compromising the actual prevalence of malaria in the whole population.

The population-attributable fraction of adult malaria due to HIV-1 would be expected to rise in parallel with HIV-1 prevalence. In a region with an HIV-1 prevalence of 30%, such as parts of southern Africa, the population-attributable fraction could reach 20% for parasitemia and 35% for clinical malaria (25). Any interaction between malaria and HIV infections will have a significant public health effect, even if the statistical effect is modest.

On a population basis, an increased prevalence of malaria parasites and increased parasite density in HIV-infected individuals could lead to increased malaria transmission affecting both HIV-positive and -negative individuals (6). The overall prevalence of malaria in this study was generally low although the area of study is in the northern part of Lake Victoria where the duration of the transmission is usually throughout the year. This observation could be because this study was conducted in non-malaria transmission seasons which are usually August to October and September to April (26).

Another reason for the low prevalence of malaria parasite among HIV patients attending BMH could be due to increased use of insecticide-treated nets. HIV-infected individuals are put on co-trimoxazole as a prophylaxis measure against opportunistic infections and this could reduce the chance of malaria parasite infection. There could also be a possibility that most of the subjects in the study could have tried self-medication for malaria before coming to the hospital thus reducing the chance of positive malaria tests.

The prevalence of malaria parasites among the Banyoro who were HIV positive and attending BMH was 25%. This figure is greater than that of the Iteso (6.25%) attending the same clinic in BMH. The prevalence of MTB does not rhyme with the reports of studies conducted in East and South Africa in which tuberculosis was diagnosed in 27%–34% of consecutive HIV-1–infected patients admitted to hospitals in Kenya (27) and South Africa (28), 39% of rural Tanzanians presenting with respiratory symptoms (29), and 61% of Burundian patients with AIDS (30).

This parasite in HIV study report is also different from the study reports from Ekpoma (33.3%) (31), Abia (9.0%), Kano (12.0%), Enugu (14.0%), Borno (27.0%), Plateau (30.0%), and Benue (35.0%) States in Nigeria (32). In Sub-Sahara Africa, MTB has been diagnosed in 19-44% of patients with AIDS (33). However, the prevalence rate of MTB in this study was in line with the study report from Oyo State (4.0%) in Nigeria (32). This could mean both the study population in Oyo State in Nigeria and Bombo Military Hospital share certain factors that affect the spread of MTB.

Migliori et al (34) reported that Most HIV/TB patients lived in the town of Arua (50% vs. 7% in rural areas peripheral to Arua and 1.6% in a rural area near the district border). This trend tends to agree with the present study. The significantly low prevalence rate of MTB in this study could be due to increased awareness of MTB transmission and behavioral change to positive living among HIV-infected patients.

This is probably a consequence of an intense campaign against malaria, TB, and HIV by the Uganda Government and Chieftaincy of Medical Services-UPDF in particular. Most of the patients live in the military barracks where general cleanliness and high standard of hygiene are strictly observed thereby reducing the rate of transmission of MTB and malaria. In a study conducted by Okodua et al (16), on the Incidence of HIV Related Pulmonary Tuberculosis in Edo State in Nigeria females were found to have a higher HIV-MTB co-infection (11.6%) than males (7.7%).

In this parasite in HIV study, the low values could be because most of the patients attending BMH are soldiers who are mainly males. This could be true because the predisposing factors for Mycobacterium tuberculosis seem to favor the males more than the females especially in most developing countries in Africa where overpopulation in military camps, prison, construction sites, and factories are dominated by males (16).  The prevalence of MTB/ HIV co-infection in this study was slightly greater than 0.18% reported by Dye et al (35).

The prevalence of MTB/HIV co-infection was very low compared to WHO and Global Fund’s 40% reports from Burma (36). The differences in prevalence may also depend on the Uganda Government’s willingness to fight the epidemic. Burma has been rated by ‘WHO’ as moving far too slowly to adequately control TB due to a lack of political will and commitment (37). This is contrary to Uganda which has been at the forefront of the fight against the HIV scourge.

The global burden of tuberculosis remains enormous, mainly because of poor control in Southeast Asia, sub-Saharan Africa, and Eastern Europe, and because of high rates of M. tuberculosis and HIV co-infection in some African countries (36). These parasites in the HIV study reveals the highest relative prevalence of PTB (16.7%) and malaria-PTB (16.7%) co-infections among the age group of 51-60 years. This could be due to decreasing immunity with age in association with the devastating effect of HIV/AIDS.

In this parasites in HIV study, the prevalence of MTB among the Bakiga and the Banyoro attending the same clinic in BMH was at 7.0% and 5.0% respectively. The difference in the prevalence of malaria and MTB among the various tribes studied could be due to stigmatization occasioned by low levels of counseling on the HIV/AIDS pandemic. The low prevalence of MTB in this study agrees with the report of WHO (38) that some East African countries with high rates of HIV infections show a declining proportion of smear-positive TB cases.

This is expected because smear-negative TB is more frequent among HIV-positive due to better prevention and control methods. It could also be that a decline in diagnostic performance, despite the emphasis placed on sputum smear microscopy in Directly Observed Treatment (DOT) programs (38). The low prevalence of malaria and MTB among HIV patients attending BMH could be because of the intensive campaign against the three inter-related diseases (i.e. malaria, tuberculosis, and HIV) by the UPDF Medical Services in conjunction with the Ministry of Health, CDC, and other NGOs such as Population Service International (PSI), and AMREF.

In febrile HIV patients with malaria parasites, the prevalence of TB infection is significantly dependent on malaria and the prevalence of malaria/TB is significantly (p<0.05) dependent on TB. Occupation, gender, age, and tribe were significant (p<0.05) factors that contribute to the rate of spread of HIV, malaria, and TB. The observed prevalence of malaria, MTB, and malaria/MTB co-infection among HIV patients in this study could be a signal of other underlying factors affecting the campaign against HIV spread in the military.

The parasites in HIV study would therefore be of importance to the UPDF Medical Services in planning and laying strategies for managing HIV patients who have malaria and/ or TB in Bombo Military Hospital. The strategies laid by the UPDF Medical Services to combat malaria, tuberculosis, and HIV appear to be effective and need to be supported and encouraged by the stakeholders in UPDF and the Government as a whole. Microscopy could be accompanied by other diagnostic methods such as serological or X-rays to improve the detection rate of TB infection. Rapid malaria test (Parasight F) could also be used to detect P. falciparum antigens in the blood.

In conclusion, Malaria parasites remain prevalent among the studied Tuberculosis infected HIV/AIDS patients. Progression of HIV disease was high among malaria patients and malaria disease progression was high among HIV/AIDS disease. While occupation was a significant factor (p<0.05) influencing the prevalence of HIV/AIDS while age, gender tribe was not. Therefore, from the observations made in this study, all patients attending TB clinic should be tested for HIV infection and all HIV patients should be tested for TB and malaria.

The interesting aspect of this parasite in HIV survey is the emergence of malaria parasites among HIV-infected and AIDS patients together with TB infection. This complex relationship between Malaria, HIV/AIDS, and tuberculosis, when carefully studied may shed light on the role of malaria disease in complicating the management of HIV patients especially those infected with tuberculosis. Prompt diagnosis, correct treatment, high standard of hygiene, and avoidance of overcrowding are emphasized. Commanders in the military should be enlightened about the rights to get prompt medical treatment. They should also be educated on the interventions of preventing malaria, tuberculosis, and HIV transmission.

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Endemicity of Malaria parasites among Tuberculosis infected HIV patients attending Bombo-Military Hospital, Luwero District, Uganda

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