Intestinal helminths are amongst the most prevalent chronic human infestations worldwide.^1,2 The World Health Organization (WHO) estimates that around 2 billion people are currently infested, particularly the rural poor in the developing world. About 300 million people have suffered severe and permanent impairment as a consequence.³ Infestations caused by these soil-transmitted helminths (STH) are listed among the Neglected Tropical Diseases (NTDs) that cause substantial illness for more than one billion people globally.⁴ The main species that infest humans are the round worms Ascaris lumbricoides, the whipworm Trichuris trichiura and the hookworms Necator americanus and Ancylostoma duodenale.^5–7 Determinants of Intestinal helminth infestation include environmental factors like water source, sanitary facilities and waste disposal methods; personal hygiene; food hygiene; geographical distribution; socioeconomic status; educational level; walking barefoot and other factors like a routine medical check-up. Thus, persons infested can be continually re-infested as long as they are exposed despite short term interventions of giving chemotherapy to at-risk groups.^1,8

Human immunodeficiency virus (HIV) which is also a chronic infection is common in many of these countries where intestinal helminths are prevalent and both conditions can co-exist thereby maintaining the cycle of poverty and disease.⁹ Several earlier studies reported that Helminth infections were more common in HIV infected than in HIV-uninfected patients.¹⁰ Also, the HIV program in this region is wholistic, such that HIV patients are not only given drugs for the treatment of the disease but other interventions like health talks which expectedly, influence positive health behaviour. Therefore, knowing the determinants of intestinal helminths infection among HIV patients will aid in integrating appropriate interventions into the existing HIV program. On the other hand, assessing the determinants among the HIV negative cohort will give further insights into the wider community factors within the same context and region.

Studies of the interaction between HIV infection and intestinal parasitic infections have suggested that HIV-infected patients who are coinfected with helminths experience a shift in their immune system from a T helper type 1 (Th1) response to a predominantly T helper type 2 (Th2) response as well as an increase in immune system activation.¹¹ Also, the concomitant infection of HIV and intestinal parasites may potentiate the severity and progression of both within the infected person.¹¹ Th1 cells are essential in eradicating intracellular pathogens, and inflammatory responses. Th2 cells, on the other hand, target extracellular pathogens and produce cytokines, which enhance antibody production. The increased Th2 and diminished Th1 responses as well as the chronic immune activation found in patients with intestinal helminth infection have been hypothesised to lead to an increased susceptibility to HIV infection and enhanced HIV replication in helminth-infected individuals.^12,13

Emerging evidence provides a scientific rationale for combining treatment programs for neglected tropical diseases (NTDs) with programs for the treatment of HIV/AIDS (acquired immune deficiency syndrome). Engaging the major stakeholders to establish operational links between HIV/AIDS and NTD control and elimination activities, especially in sub-Saharan Africa, could increase the efficiency and cost-effectiveness of both HIV/AIDS and NTD efforts.¹⁴

A systematic review and meta-analysis to determine the distribution of soil-transmitted helminthic infection in Nigerian children found that over one-third of the studies were published from south-western Nigeria. The south-western region was the only high-risk zone for STH infections while the rest of the regions were low-risk zones.¹⁵

There have been a lot of locally published studies on the prevalence of helminthic infection amongst children^16–18 and a few amongst adults and yet fewer amongst HIV positive adult patients.

The aim of this study was to determine the prevalence of intestinal helminth infection among HIV sero-positive and sero-negative adults in the study area and its determinants.

METHODS

Background of the study area

The study was conducted in Vom Christian Hospital and Barkin Ladi General Hospital. Vom Christian Hospital is located in Vwang District in Jos South Local Government Area (LGA), Plateau state. The District is situated on latitude 10 ⁰ N longitude 9 ⁰ E about 35km south-west of Jos, Plateau state. Vwang covers an area of 155 km² with a population of 121, 284.¹⁹ Barkin-Ladi General Hospital is located in Ropp, a district in Barkin-Ladi LGA, Plateau State. The district is situated at latitude 9⁰32’009’‘N longitude 8⁰54’00’'E. It has an area of 1,032 km² and a population of 175,267 at the 2006 census.²⁰ The immediate communities of Vwang and Ropp are rural and most people in the community are farmers. The dry season is between November and March while the rainy season, April to October.

Study population

Study participants were HIV sero-positive and sero-negative patients who were 18 years and above attending Anti-Retroviral Therapy (ART) and Outpatient clinics of Vom Christian Hospital and Barkin Ladi General Hospital respectively. They were excluded if they had been given any medicine for helminth infection in the preceding six weeks.

Study design and subject recruitment

The study used a cross-sectional design to compare the prevalence and determinants of intestinal helminths in HIV sero-positive and HIV sero-negative adults. HIV sero-positive clients were enrolled from the HIV clinics of Vom Christian Hospital and General Hospital Barkin Ladi while adults who were HIV sero-negative were enrolled from the outpatient clinics of the same hospitals. The study was conducted between January to December 2015.

Sample size

This was a survey of all eligible clients in the study sites and their corresponding controls in the same ratio.

Data collection

Data was collected from study participants using a structured interviewer-administered questionnaire. Four hundred HIV sero-positive participants were recruited each from Vom Christian Hospital and General Hospital Barkin-Ladi with matched controls giving a total of one thousand six hundred participants. Information collected included socio-demographic characteristics and relevant risk factors for STHI such as the source of drinking water, treatment of drinking water, the practice of washing fruits and vegetables before eating, type of toilet facility and hand washing after toilet use. Stool samples were obtained on the same visit and microscopy was done using the Kato-Katz method.²⁰

Data analysis

Data was entered into the IBM SPSS version 25 for analysis. Frequency tables were used to present the bio-socio-demographic and clinical characteristics. A bivariate analysis, (Chi-square test) was used to test for association between the independent (age, sex, educational qualification, occupation, location of residence, main source of drinking water, water treatment and daily hygiene practices) and the dependent variable (the presence or absence of intestinal helminthic infection on stool microscopy). A binary logistic regression was used to assess the determinants of helminthic infection by imputing variables from the bivariate analysis that had a p $\leq$ 0.25 or variables known from theory to be relevant.

Ethics consideration

Ethical approval was obtained from the Ethics Committee of the Jos University Teaching Hospital, Jos. All participants gave written informed consent or a thumbprint using indelible ink on the consent form. Confidentiality of all information obtained from participants was assured. Participants were at liberty to withdraw from the study at any point with no negative consequence to the care they were already receiving. Patients diagnosed to have intestinal helminths were treated.

RESULTS

The study had 400 HIV sero-positive clients recruited from Vom Christian Hospital and 400 HIV sero-positive clients from Barkin Ladi General Hospital with an equal number of matched controls in the two sites. The prevalence of intestinal helminths was found to be 16.3% in the HIV seropositive population and 16.4% in the HIV sero-negative population. The median age of the study participants was 40 years with an interquartile range (IQR=31-50). In the HIV sero-positive population, the age group with the highest rate of STH infection was 31-45 years; 421(52.6%) while the 76-90 years age group had the lowest; 6(0.8%). In the HIV sero-negative arm, the age group with the highest rate of STH infection was 46 -60 years; 236 (29.5%) while the 76 -90 years age group had the lowest; 30 (3.8%). Secondary school education had the highest level of infestation; 316(39.5%) in the HIV sero-positive arm while those with primary school education had the highest level of infestation in the HIV sero-negative arm. About three fifths; 494 (61.7%) of the HIV sero-positive participants were forty years old or below while slightly over two fifths; 345 (43.1%) in the HIV sero-negative arm were forty years and below. About a quarter; 211(26.4% were male and about two fifths; 317(39.6%) were farmers in the HIV sero-positive arm. The HIV sero-negative arm had a quarter as males 204(25.5%) and about two thirds; 527(65.9%) were farmers. Approximately three fifths; 479 (59.9%) did not have more than primary school education and a third; 264 (33.0%) lived in the rural area among HIV sero-positive participants whereas less than two fifths; 307 (38.4%) did not go beyond primary school and about two fifths; 339 (42.4) resided in rural communities in the HIV sero-negative category (Table 1).

Bivariate analysis showed a statistically significant association between the treatment of drinking water and intestinal helminthic infestation in the HIV sero-positive arm. In the HIV sero-negative arm, there was a statistically significant association between the location of residence and the washing of fruits and vegetables before consumption and intestinal helminthic infestation (Table 2).

Binary logistic regression revealed that those that drink untreated water were more likely to be infected with intestinal helminths compared with those that do not (OR=1.60, CI=1.06-2.42) in the HIV sero-positive respondents. In the HIV sero-negative arm, those that had more than a primary school education were less likely to have intestinal helminths compared with those that did not (OR=0.61, CI=0.38–0.97) and those that reside in rural areas were more likely to be infected with intestinal helminths compared with those that do not (OR=1.78, CI=1.21-2.60) (Table 3).

DISCUSSION

We found that the prevalence of intestinal helminths among the HIV sero-positive population was 16.3% whereas that in the HIV sero-negative population was 16.4% and there was no statistically significant difference between the two. The prevalence of intestinal helminths in our study is much lower than that obtained in an earlier study in Plateau State, Nigeria which documented a prevalence of 33.3% among HIV- seropositives and 21.9% in HIV-seronegatives.²¹ Subjecting this difference to further statistical analysis (chi-square test), showed that this difference in prevalence is statistically significant. In recent years, there has been more education on the risk factors of intestinal helminths, routine deworming, the use of Anti-Retroviral Therapy (ART) and the use of Sulphdoxine-Trimethoprim as prophylaxis and these may explain the reduction in prevalence particularly among HIV patients.²² Most importantly, the uptake of ART and linkage to care of HIV patients has significantly increased over the past couple of years in this region. HIV treatment and prevention programs provide several health-related benefits to clients via health education on diverse topics, counselling and home visits. These have led to an improvement in their immunity and a reduction of opportunistic infection. Some participants in the study may not have been treatment naïve to antihelminths and this may have affected the results obtained in the study.

The prevalence of intestinal helminths found in this study is comparable to that obtained in Nairobi Kenya where the prevalence of intestinal helminth among HIV sero-positive adults was found to be 16.1%,²³ while that in a district facility was 19.3%.²⁴ The finding in this study is also comparable to the prevalence of intestinal parasites obtained in North-East Ethiopia where 16.0% was found in HIV sero-positive persons and 10.0% in HIV sero-negative persons.²⁵

Some studies had a higher prevalence than ours but these studies examined intestinal parasites as a whole and therefore more likely to have many more pathogens.^26–31 The prevalence values obtained in our study were nonetheless higher than those from other studies carried out where intestinal parasites were evaluated.^32–34 This is difficult to explain but may be related to a relatively lower level of the helminths in such geographical locations, differences in methodology or host risk factors.

In most of the studies where the prevalence of intestinal parasites was assessed amongst adult HIV sero-positive and sero-negative sub-populations, the prevalence was found to be higher and often significantly so in the HIV sero-positive arm compared to the HIV sero-negative arm.^{25,27–29,31–33,35–37} HIV sero-positive adults with low immunity are predisposed to gastro-intestinal opportunistic infections accounting for a higher prevalence of intestinal parasites compared to HIV sero-negative adults. This implies the importance of ensuring that HIV patients are tested and linked to ART particularly in rural settings where the risk of getting intestinal helminths is prevalent. Regarding HIV care, treatment centres must integrate treatment of intestinal helminths in high-risk rural areas as part of routine care, especially for newly enrolled clients. This is in line with the UNAIDS 2025 targets which emphasizes that 90% of people living with HIV are linked to context specific-integrated services.³⁸

We found an association between having drinking water treated or not and intestinal helminthiasis in the HIV sero-positive population and this was also found in the studies in Benin and Kenya.^33,39 The location of residence and whether fruits and vegetables are washed or not before eating were associated with having intestinal helminths in the HIV sero-negative population. This is also corroborated by findings in the study done in Kenya.³⁹ Drinking adequate amounts of water and the intake of fruits and vegetables are very important in the maintenance of the body’s biological processes however, food hygiene is critical for the prevention of intestinal helminths.^40,41 It appears that because the HIV sero-positive population had a higher proportion of person who lived in urban/semi-urban locations and had more access to potable water, a lesser proportion treat their drinking water and this may have resulted in the association between having water treated or not and intestinal helminths. The HIV sero-negative population had a higher proportion of persons who used the bush and pit latrines and also had more farmers and persons involved in farming activities and this may be responsible for the association between the intake of fruits and vegetables and intestinal helminths. Studies have shown that between 42.6 – 57.8% of fruits and vegetables collected in the market were contaminated with intestinal parasites.^42,43 This typifies how wider social determinants like potable drinking water, availability of sewage disposal facilities, food and personal hygiene underpin the prevalence of intestinal helminths in rural settings. This underscores the urgent need for interventions in this regard to reduce this social inequality in low- and middle-income countries. Such interventions will positively impact both HIV positive and negative people as a broader community benefit.

Similar studies had found HIV sero-positive status as a determinant of intestinal parasitic infection in Benin while HIV status, poor educational status and the quality of water for drinking were determinants in Cameroun.^33,37,44 Rural residence and lack of flush toilets were determinants in Kenya,^23,24 while poor personal hygiene were determinants in Eastern Ethiopia.²⁵ A recent visit to a rural area, food shortage and prior history of helminth infection were predictors of existing helminth infection in Zambia,⁴⁵ whereas HIV sero-positive status and poor personal hygiene were determinants in rural China.³⁴ In Zambia, a recent visit to a rural area, food shortage, and prior history of helminth infection were significant predictors of current helminth status,⁴⁵ while in China, an HIV sero-positive status, poor personal hygiene habits were determinants.³⁴ This highlights the opinion that the determinants of intestinal helminths seem to be related to the rural poor and are recurrent.

There is a paucity of studies that compared the determinants of intestinal helminth in the HIV sero-positive and sero-negative sub-populations and reported the findings of the sero-negative population as such implying that future research needs to focus on this gap.

Limitation of the study

The Kato-Katz technique is a highly accurate and rapid method for Ascaris lumbricoides and Trichuris trichiura; however not so much for hookworm due to the fast degeneration of the rather delicate eggs if the slides are viewed beyond I hour of preparation. Kato-Katz technique is preferred because it is the WHO standard for the diagnosis of STHI. This limitation is not likely to influence the study results since deliberate efforts were made in reading the slide within the recommended time frame of 1 hour. The study duration was longer than envisaged because of some civil disturbances that occurred at the time of the study which affected patient turn out in the hospitals.

The study groups were matched in age, sex, educational qualification, main occupation and a number of other variables, however the study design, observational, may not be able to control for some possible indices for good health. Even though persons who had taken an antihelminth in the previous six weeks before the study commenced were excluded, some participants in the study may not have been treatment naïve to anti-helminths and this may have affected the results obtained in the study.

CONCLUSIONS

The prevalence of intestinal helminths was found to be similar among HIV positive and HIV negative arm, but they differed in the risk factors. The HIV programs in rural areas should intensify efforts to increase uptake of ART and integrate intestinal helminths treatment into ongoing care. Wider social problems and living conditions need to be urgently addressed as a broader benefit to improve the health status of rural populations.

Acknowledgements

We are grateful to the facilities where the study was conducted, the clients, research assistants and notably, the microscopists, Mr Emmanuel Richard of the Plateau State Epidemiological Unit and Mr Sati Bitrus of Vom Christian Hospital. Thanks to AIDS Prevention Initiative in Nigeria who have supported HIV treatment, prevention and support at the study sites.

Funding

The authors are most appreciative of the Tertiary Education Trust Fund (TETFUND) Nigeria who provided funds for the study and the University of Jos for managing the entire grant process.

Authorship contributions

M.G., H.A., G.A., M.D., and A.M designed the study, contributed to the acquisition of data, analysed the data and co-wrote the manuscript. S.M., and J.D., contributed to the analysis of data and co-wrote the manuscript. D.M., D.S., and H.S., appraised the study and co-wrote the manuscript. All authors provided critical feedback and approved the final version of the manuscript.

Competing interests

The authors completed the Unified Competing Interest form at www.icmje.org/coi_disclosure.pdf (available upon request from the corresponding author) and declare no conflicts of interest.

Correspondence to:

Dr Suleiman E Mshelia MBBS, MPH(Sheffield), DiPM (Uk)

Department of Community Medicine

Jos University Teaching Hospital

Plateau State, Nigeria.

[email protected]