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Abstract

Objective:

This was a cross-sectional study intended to assess the prevalence and management of helminthiasis (HL) among underfives living with HIV/AIDS (ULHA).

Methodology:

Clinical histories of ULHA were scrutinized for HIV/AIDS status, antiretroviral therapy (ART), HL prevalence, and their management.

Results:

About 364 ULHA were studied, 213 (58.5%) were girls and 151 (41.5%) were boys. Of the 364 ULHA, 171 (47.5%) had HL and 64.3% were treated with albendazole (ABZ). Trichuriasis was ascribed to 23.6% of HL. Majority (72.5%) of ULHA had a CD4 count below 200 cells/mm³. Direct association was observed between CD4 counts and HL. About 55% ULHA were on lamivudine (3TC)-stavudine (d4T)-nevirapine (NVP; LSN) combination therapy. The ABZ-LSN combination was frequently used for HIV/AIDS and HL management.

Conclusion:

High prevalence of HL and vivid correlation between HIV status and HL were observed. The LSN-ABZ combination was frequently employed for management of HIV/AIDS and HL. We recommended prompt diagnosis of HL to avoid acceleration of HIV infection to AIDS.

Keywords

prevalence of helminthiasis underfives living with HIV/AIDS antiretrovirals anthelmintics

Introduction

AIDS caused by HIV is currently one of the most deadly worldwide epidemics.¹ HIV infection has already caused approximately 25 million deaths; and it is estimated that more than 100 million people are harboring the virus.^2,3 Sub-Saharan Africa is the region of the world most severely affected by HIV/AIDS; in this area, the life expectancy has declined drastically, in some countries by 50%, and the infant death rates have doubled.¹

The AIDS epidemic has intersected most notably with tuberculosis (TB), which is the principal cause of death for persons with HIV infection worldwide.^2
–4 But next to TB, the most common infections in the developing countries are helmintic/helminthiasis (HL).^5
–7 About one quarter of the world's population are infected with one or more of the major soil-transmitted helminths, with an estimated number of infected people being over 1.5 billion.^5,8 These infections are more prevalent in tropical and subtropical regions of the developing world where adequate water supply and sanitation are lacking.^7

–10 Many potential HL are eliminated by host defenses; others become established and may persist for prolonged periods, even years. Helminthiasis is a serious problem among children, particularly those under 5 years of age (underfives). One previous study conducted in Tanzania revealed that 1089 (24%) out of 4537 underfives were infected with helminths. Most of the infected underfives (80%) were incidentally found to harbor the worms while seeking medical attention for different ailments than the HL-related ones, and 10% of them remained undiagnosed until they started passing worms in feces or vomit.¹¹

HIV/AIDS has also changed the disease patterns, as a consequence of the emergence of several opportunistic infections/diseases.¹² Because of the immature immune system of the underfives, they become prone to a number of the opportunistic diseases and HL. The prevalence and geographic distribution of HL and HIV/AIDS, particularly in Africa, are remarkably high; possible causal relationships between these infections may also exist. Several studies have reported on the correlation between HIV/AIDS with HL and demonstrated contradictory findings.^2,13,14 Chronic immune activation is one of the hallmarks of HIV infection, which is also present, with close resemblance to individuals with HL.^14,15 Health status of underfives living with HIV/AIDS (ULHA) with HL will definitely deteriorate faster and may negatively affect the progression of the HIV/AIDS infection. This becomes even worse in resource-limited communities/countries, Tanzania inclusive, where malnutrition among underfives is not uncommon.^16
–18 Consequently, this study intended to assess the prevalence and concurrent management of HL and HIV/AIDS among ULHA and to investigate the confounding factors for the disease conditions among the study population.

Materials and Methods

Study Design

This was a retrospective cross-sectional study assessing the prevalence and management of HL using patients’ clinical histories. The target population was all children under the age of 5 years living with HIV/AIDS who were attending health care services at Amana Municipal Hospital (AMH) for a period of 3 years (2004-2006).

Sampling Procedures

A total of 364 ULHA from all 3 districts of Dar es Salaam residing in proximity to AMH were included. Sampling frames for neither the ULHA nor their residences were established. Therefore, all clinical histories that were registered and available in the specified period of time (2004-2006) were sampled and analyzed.

Data Collection

Data were retrospectively collected from the archives of patients’ clinical histories/files, which were scrutinized with more emphasis on HIV status (CD4 counts), prevalence of HL, and their comanagement. Similarly, additional data on demographic characteristics, sex and age of the patients, were collected. Patients’ weights, types of HLs, and the date of antiretroviral therapy (ART) initiation at the AMH clinic for each subject were recorded.

Data Analysis

The acquired information was coded and entered into the database and analyzed using SPSS version 17.0 software package. The nonparametric (chi-square) test was used for statistical comparison of various parameters, and numerical differences were considered significant when P < .05.

Ethical Consideration

Ethical clearance was sought from the Muhimbili University of Health and Allied Sciences Ethical Committee and relevant District/Municipal authorities. Prior to the commencement of the study, confidentiality of the accessed data was taken into account by not revealing names or any personal information that could disclose the participants’ identity.

Results

Demographic Characteristics of Study Population

A total of 364 ULHA (213 boys and 151 girls) who had been receiving health care services at Amana District Hospital were retrospectively studied for the presence of helmintic infections and its concurrent management with HIV/AIDS. The participants’ ages ranged from less than 1 year to 5 years, with a median age of 2 years (Table 1 ). The majority (86.3%; n = 314) of the ULHA resided in Ilala municipality where AMH is located, whereas a few, 29 (7.9%) and 21 (5.7%), came from Kinondoni and Temeke municipalities, respectively.

Table 1.

Demographic Characteristics of Underfives in Relation to the Prevalence of Helminthiasis.

Variable		Types of Helminthiasis (%)
Variable		Trichuris	Hookworm	Ascaris	None
Age, y	<1	25 (6.8)	13 (3.6)	18 (4.8)	62 (17.0)
	2	15 (4.1)	9 (2.5)	8 (2.2)	33 (9.1)
	3	16 (4.4)	4 (1.1)	12 (3.3)	40 (11.0)
	4	22 (6.0)	9 (2.5)	6 (1.6)	44 (12.1)
	5	8 (2.2)	4 (1.1)	2 (0.5)	14 (3.8)
Sex	Female	49 (13.5)	26 (7.1)	23 (6.3)	115 (31.6)
Sex	Male	37 (10.1)	13 (3.6)	23 (6.3)	78 (21.4)

Prevalence of HL among Underfives Living with HIV/AIDS

Of the 364 ULHA, 171 (47%) were harboring at least 2 helminths. Between 2004 and 2006, the most prevalent HL among the ULHA was trichuriasis (23.6%), while 193 (53%) underfives were free from HL. Male and female underfives were equally infected with helminths exception to ascariasis, 26 versus 13, respectively (P < .05). There was an increase in HL from 2004 to 2005; this coincides with an increased number of underfives on ART at the hospital as shown in Table 2.

Table 2.

Prevalence of Helminthiasis among Underfives from 2004 to 2006.

Year	Sex	Types of Helminthiasis (%)				Total
Year	Sex	Trichuris	Hookworm	Ascaris	None	Total
2004	Female	9	3	9	13	34
2004	Male	4	7	4	16	31
2005	Female	22	6	8	49	85
2005	Male	26	9	9	61	105
2006	Female	6	4	6	16	32
2006	Male	19	10	10	38	77
Total		86 (23.6)	39 (10.7)	46 (12.6)	193 (53)	364 (100.0)

HIV/AIDS Status of Underfives and Concurrent Management of HIV/AIDS and HL

Results showed that the majority (72.5%; n = 264) of the ULHA had CD4 counts below 200 cells/mm³, of those 125 (47.3%) had HL. Slightly more than half (53%; n = 35) of ULHA whose CD4 counts ranged from 201 to 400 cells/mm³ had HL, while only 1 underfive whose CD4 count was over 601 cells/mm³ had HL (trichuriasis) as shown in Table 3. On the other hand, the weight of the underfives ranged from 2.8 to 16 kg with a median weight of 3 kg; and in most cases, these were below the normal growth weights (Table 4).

Table 3.

Prevalence of Helminthiasis in Relation to HIV/AIDS Status (CD4 Counts).

CD4 Counts	Helminthiasis (%)
CD4 Counts	Trichuris	Hookworm	Ascaris	None	Total
<100	5 (1.4)	2 (0.6)	2 (0.5)	14 (3.8)	23 (6.4)
101-200	50 (13.7)	31 (8.5)	35 (9.6)	125 (34.3)	241 (66.2)
201-400	21 (5.8)	6 (1.6)	8 (2.2)	31 (8.5)	66 (18.2)
401-500	7 (1.9)	0 (0.0)	1 (0.3)	13 (3.6)	21 (5.8)
501-600	2 (0.5)	0 (0.0)	0 (0.0)	4 (1.1)	6 (1.6)
601-700	1 (0.3)	0 (0.0)	0 (0.0)	6 (1.6)	7 (1.9)
Total	86 (23.6)	39 (10.7)	46 (12.6)	193 (53.0)	364

Table 4.

Comparison of Underfives Ages and Weight against Healthy Growth Weights.

Number of Underfives (%)
	Weight, kg
Age, y	<4	4.1-8	8.1-12	12.1-16	Healthy Weight^a
≤1	25 (6.8)	73 (20.0)	18 (4.9)	2 (0.6)	9.85 ± 0.3
2	1 (0.3)	19 (5.2)	42 (11.5)	3 (0.8)	12.25 ± 0.3
3	0 (0.0)	8 (2.2)	49 (13.5)	15 (4.1)	14.35 ± 0.3
4	1 (0.3)	12 (3.3)	44 (12.1)	24 (6.6)	16.35 ± 0.5
5	0 (0.0)	0 (0.0)	13 (3.6)	15 (4.1)	18.2 ± 0.5

Abbreviations: LSN, lamivudine–stavudine–neverapine; LZE, lamivudine–zidovudine–efavirenz; LSE, lamivudine–stavudine–efavirenz.

^a Weight per height and weight for children calculator.

However, no significant differences were observed among the ULHA with regard to weights and CD4 counts (F = 4.405; df = 3; P = .05). Likewise, no significant differences were noted among the analyzed age groups wtih respect to CD4 counts (F = 1.529; df = 4; P = .193). Helminthiases were mainly managed by 3 anthelmintics viz, albendazole (ABZ), mebendazole (MBZ), and praziquantel (PRP) as summarized in Figure 1. Of the 171 ULHA who were diagonized with HL, 110 (64.3%) were treated with either ABZ alone or a combination of ARV drugs. Three main ARV drug combinations were employed for ART namely lamivudine (3TC)-stavudine (d4T)-nevirapine (NVP; LSN); 3TC-zidovudine (ZDV)-efavirenz (EFV; LZE); and 3TC-d4T-EFV (LSE). For the concurrent management of HIV/AIDS and HL, about 65 (17.8%) and 15 (4.1%) ULHA were prescribed with LSN-ABZ and LZE)-ABZ combinations, respectively, while 8 (2.2%) were given prophylactic ABZ (Figure 1). Results also show that only 49 (13.5%) and 14 (3.8%) ULHA were administered MBZ and PRP, respectively. Approximately 51.5% (n = 187) of the ULHA who had HL were not on ART, despite 17 (9.1%) of them having CD4 counts below 200 cells/mm³ (Figure 1).

Figure 1.

Concurrent helminthiasis and HIV/AIDS among underfives.

Discussion

According to the Tanzania Standard Treatment Guidelines,¹⁹ any confirmed HIV-positive individual is entitled to commence ART when the CD4 counts are about 200 cells/mm³. Usually, determination of CD4 count percentage is the preferred measurement of HIV/AIDS status in children <5 years old, as it varies and is less than that in the older children. However, because of limited resources, CD4 count in cells/mm³ was adopted.²⁰ Findings from the present study are in agreement with a previous observation,²¹ which also indicated that HL are more pronounced in ULHA with CD4 counts below 200 cells/mm³. The underfives’ debilitated and ineffective defense mechanism to invasive pathogens, helminths inclusive, could partially explain these findings. Over-reactivation of the immune system as a result of chronic HL could have attributed to further depletion of CD4 counts, thus failing to properly coordinate and undertake the defensive function.²² This might have been caused by the poorly functioning cell-mediated mechanism that is responsible for fighting parasitic worms.^22,23

A study conducted in 2006 in Tanzania showed that ocassionally underfives harbor parasitic infections without knowledge of caregivers.¹¹ Nonetheless, this becomes a major health concern when the hosts are ULHA. The present study has revealed that more than half (53%) of the underfives were provided with prophylactic anthelmintics; however, in order to scale-down the observed problem of HL among the study population, more emphasis should be on prompt diagnosis and initiation of the deworming process. In comparison to PRP and MBZ, ABZ has the broader anthelmintic spectrum because of its higher bioavailability, which could be one of the reasons for it being more frequently prescribed for HL treatment.²⁴ However, little information is available on the ideal drug combination of ARVs and anthelmintics.^25
–27 On the other hand, the management of HIV/AIDS largely depends on the established treatment guidelines (whether they are the first- or second-line ARV drugs).¹⁹ Because of the nature of this study, ULHA caregivers were not interviewed and thus their opinions on the treatment outcomes of HIV/AIDS and HL could not be ascertained, which could be one of the drawbacks. Nevertheless, a correlation between HIV plasma viral load and HL (excretion of worm eggs in stool) had previously been documented, which also resulted in the reduction in HIV/AIDS-related symptoms like pallor, abdominal pains, diarrhea, and mean increase in CD4 count.²⁵ This is a clear indication of safety and usefulness of ARV drugs and anthelmintics in the comanagement of HIV/AIDS and HL, which results not only in expulsion of helminths but also viral load suppression.²⁵

Immune activation of an HIV-infected individual is the most critical determinant in the pathogenesis of HIV infection. Similarly, HLs are characterized by chronic immune activation of their hosts, which may account for higher prevalence rates of HIV/AIDS in tropical developing countries.^2,14 The immune activation and dysregulation are characterized by specific patterns of cytokine production, expression of membrane-activated molecules on cells of the immune system, and changes in the levels of several immune parameters in the blood. Since many worms are chronic that means the resultant helminth infestation-related inflammatory changes become irreversible and may lead to malfunction of affected tissues. Unfortunately, this also results in chronic activation and/or dysregulation of the immune system leading to immunological tolerance of the host.²⁸ Furthermore, helminths have large surface areas that allow them to interact with myriad effector cells of the immune system to produce large amounts of antigenic materials. This in turn leads to massive stimulation of CD4 T and CD8 T cells of which some can divert the immune response or locally exhaust the immune potential. Moreover, HL like HIV/AIDS are associated with decreased CD4 counts, despite increased HIV-specific CD8 cells.^15,28,29Presumably, the reduction in the production of opsonizing antibodies toward the helminth surface antigens could stimulate the CD8 cytolytic T cells.²²

Several studies have related ARV drugs, particularly ZDV, to anemia^30
–32 which is aggravated by HL.^2,13 Anemia has also been associated with stunted growth in children, which is one of the risk factors for dwarfism.^16
–18 Other causes of anemia in children include iron deficiency and parasitic infections.¹⁷ This ultimately may lead to the exacerbation of ULHA health and thus increase susceptibility to opportunistic infections like candidiasis, pneumocystis carnii, and cryptoccosis.³³

It is also well recognized that in Tanzania, like in other developing countries, HL are the major sources of morbidity and mortality among underfives.^34,35 Moreover, since most of HLs are asymptomatic, severe pathological conditions can occur.³⁴ Some of the obvious forms of damages are those resulting from blockage of internal organs or direct pressure exerted by growing parasites. Likewise, many helminths undergo extensive migrations through various body tissues, thus causing tissue damage and initiating hypersensitivity reactions. Systemic changes such as eosinophilia, edema, and joint pain reflect local allergic responses to the parasites. Helminthiasis are also attributable to growth retardation among children, which could be due to aggravated malnutrition and other worm-invasive mechanisms.^18,35 Hence, in order to ameliorate the situation, the underfives should be periodically dewormed, which may increase ULHA survival. Our present study shows that the ULHA were provided with prophylactic anthelmintics. Nevertheless, the prevalence of HL was relatively higher (47.5%) as opposed to 29% and 24% discovered among non-HIV/AIDS underfives and HIV/AIDS participants, respectively.^11,21 Delayed initiation of ART and poor HIV/AIDS status (low CD4 counts) and/or its management may be one of the factors attributed to the high prevalence rate of HL.

Relatively lower body weights were observed among ULHA as compared with the established standard “normal” growth weight. Although the study did not investigate the potential causes of lower body weight among the ULHA, this could be attributed to malnutrition, which is common in developing countries as a consequence of HIV/AIDS on decreased productivity of affected households. The confounding factors and complications underlying HIV and HL coinfections might be another reason for underweight in ULHA.³⁶ Helminthiasis in ULHA may also exacerbate diarrhea, which is one of the debilitating disease conditions for HIV/AIDS. Consequently, proper care of ULHA such as feeding, regular deworming, and adherence to ART are of paramount importance because of their direct impacts on the health of the children. The study shows an association between HIV status and HL among the study population.

Conclusion

From a pharmaceutical point of view, it is undoubtedly clear that proper management of HL may greatly improve the health of ULHA who are already debilitated by HIV infection. The high prevalence rate of HL was observed among the ULHA. Direct association was observed between HIV status and HL. The LSN-ABZ combination was the most preferred and used combination therapy for concurrent management of HIV/AIDS and HL. This study recommends prompt diagnosis and closer monitoring of HIV/AIDS status as well as prophylaxis of HL among ULHA, since the 2 infections seem to potentiate each other and can accelerate the progression of HIV infection to AIDS.

Footnotes

Acknowledgments

Authors would like to extend their heartfelt gratitude to the Ministry of Higher Education Science and Technology (Tanzania) for facilitating the study and Amana Municipal Hospital Authorities for permission to conduct this study.

Declaration of Conflicting Interests

The author declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author received no financial support for the research, authorship, and/or publication of this article.

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Prevalence and Management of Helminthiasis among Underfives Living with HIV/AIDS at Amana Hospital,Tanzania

Abstract

Objective:

Methodology:

Results:

Conclusion:

Keywords

Introduction

Materials and Methods

Study Design

Sampling Procedures

Data Collection

Data Analysis

Ethical Consideration

Results

Demographic Characteristics of Study Population

Prevalence of HL among Underfives Living with HIV/AIDS

HIV/AIDS Status of Underfives and Concurrent Management of HIV/AIDS and HL

Discussion

Conclusion

Footnotes

Acknowledgments

Declaration of Conflicting Interests

Funding

References