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Intestinal helminths infections are of major concern in most developing countries where HIV/AIDS cases are endemic. HIV infection has increased the susceptibility of the host to these infections with dire consequences. The introduction of antiretroviral drugs has reduced the prevalence of intestinal helminths infections. However, patients who have low CD4 count still habour these intestinal parasites. While several studies have investigated the occurrences of intestinal helminths infection among patients on HAART, very little is known of these neglected tropical intestinal parasites in the North-central region of Nigeria. This study was undertaken to determine the pattern of intestinal helminths infection among HIV-positive adult patients on HAART and to identify risk factors that increase their susceptibility to these parasites.

A cross sectional study was carried out at Heart to Heart clinic in which one stool sample was  collected from each of three hundred and ten patients and was analyzed by wet mount preparation and the concentration method. A structured questionnaire was administered to collect data of socio-demographic and associated risk factors. Data was entered and analysed using EPI INFO software and logistic regression was used to assess any association between explanatory factors and outcome variable.

The prevalence of intestinal helminth infection was 10.3%. Ascaris lumbricodes accounted for 65.6%,  hookworm 21.9% and Strongyloides stercoralis accounted for the remaining 12.5%. The main risk factors that predispose patients to intestinal helminths infection include severe immune deficiency state (CD4<200 cell/mm3), lack of standard toilet facility, poor hand washing hygiene, lack of safe drinking water and being a farmer. Predictor of intestinal helminths infection in this study was poor hand washing hygiene (OR 2.44)

HIV-infected patients are prone to intestinal helminths infection, despite being on ART. This is more glaring among those who do not have access to portable drinking and good toilet facilities.

Severe immune deficiency is also a risk factor for this infection.


Declaration      -           -           -           -           -           -           -           -           -           -        II

Certification -              -           -           -           -           -           -           -           -           -       III

Dedication       -           -           -           -           -           -           -           -           -           -       IV

Acknowledgement      -           -           -           -           -           -           -           -           -       V

Table of contents         -           -           -           -           -           -           -           -           -       VI

List of tables/Figures -            -           -           -           -           -           -           -           -     IX

Abbreviations  and their meaning - -              -           -           -           -           -           -       X

Summary (Abstract) -             -           -           -           -           -           -           -           -       XII


1.1       Background information         -           -           -           -           -           -                    1

1.2       Statement of the problem        -           -           -          -            -          -                 12

1.3       Aim of the study         -           -           -           -           -             -          -                 13

1.4       Objectives of the study           -           -           -           -           -           -                  13

1.5       Rationale for the study            -           -           -           -           -            -                 13


2.1       Prevalence of intestinal parasitic infection among HIV/AIDS adults -   -   -        15

2.2       Relationship between immune status and intestinal parasitic infection -   -          20

2.3       Risk factors associated with parasitic infection among HIV/AIDS patients -    - 22

2.4         Pathophysiology of  parasitic infection among HIV/AIDS patients on       HAART         -

-          -         -        -                    -           -                -                           -     26

2.5       General clinical manifestations of Helminth infection           -           -                  28

2.6       Diagnosis of helminth infection         -           -           -           -           -            -     29

2.7       Treatment        -           -           -           -      -              -              -            -               31

2.8        Common intestinal parasites  among HIV/AIDS patients  -      -     -   -               31

2.9       Prevention of Helminths infection      -           -           -           -           -                  43


3.1       Study environment      -           -           -           -           -           -             -         -      45

3.2       Study area       -           -           -           -           -           -           -             -        -       45

3.3       Study population         -           -           -           -           -           -           -           -      46

3.4        Ethical consideration -           -           -           -           -           -           -            -     46

3.5       Study design                -           -           -           -            -          -           -          -      46

3.6       Inclusion criteria         -           -           -           -           -           -           -           -      47

3.7       Exclusion criteria        -            -            -          -          -           -           -          -     47

3.8       Sample size calculation           -           -           -           -           -           -            -     47

3.9       Sampling method              -      -           -           -          -            -            -        -     48

3.10     Instruments     -           -           -           -           -             -            -             -       -    48

3.11     Collection of data        -           -           -           -           -               -             -       -   49

3.12     Laboratory investigation         -           -           -           -               -              -           51

3.13     Analysis of data          -           -           -           -           -           -                  -           53

3.14     Study duration -           -           -           -           -           -           -          -                   53


4.1      Socio-demographic characteristics of the study population -    -   -        -              54

4.2      Relationships between immune status  and intestinal helminths infection -    -    62

4.3      Relationship between sociodemographic factors and helminths infection among the study

subjects -  -   -       -      -       -       -        -      -         -           -     -    -    -   -   -    63

  1. 4 Predictors of intestinal helminth infection-    -     -     -     -        -     -     -   -        67


Discussion       -           -           -           -           -           -           -                       -         -      -     -      68

Predictors of intestinal helminths infection-    -     -     -     -        -     -     -      -      -         81

Conclusion and limitations     -           -           -         -          -              -     -      -    -   -      82

Recommendations     -          -         -           -           -          -         -         -             -        - 84

REFERENCES         -           -           -           -           -           -           -           -        -         85


Ethical clearance from Plateau State Specialist Hospital        -     -        -       -   -    -   -   98

Consent form -            -           -           -           -           -           -             -  -   -      -      -    -99

Questionnaire -           -           -           -           -           -           -    -        -    -      -    -     - 100


                                           CHAPTER ONE


The existence of Human Immunodeficiency Virus (HIV), the causative agent for Acquired Immunodefiency Syndrome (AIDS), dated back to the middle of 1970 according to seroarcheological studies.1The dominant feature of this period was silence, for the HIV was unknown and transmission was not accompanied by signs or symptoms salient enough to be noticed.2 By 1981, increase in the prevalence of some opportunistic diseases such as Pneumocystis  jiroveci pneumonia and Kaposi Sarcoma among homosexuals, began to raise some suspicion about the possible outbreak of an immune deficiency disease among them.3 The Center for Disease Control (CDC) published a report of these occurrences without an identifiable cause.3 The report was regarded as the beginning of the general awareness of AIDS in the United States of America


The media campaign about HIV/AIDS intensified as the disease began to take its toll on the American population.1 In the early, middle and later part of the 80’s, the disease was characterized by rapid spread, rapid progression to AIDS, high morbidity and mortality rate.1 Since the route of transmission was not known, the spread transcended all ages, races, social status and groups.1 Several cases were reported in at least four other continents at the end of 1983.1 On 23rd April

1984, the United States Health and Human Services secretary, Margaret Heckner announced that Dr Robert Gallo of the National Cancer Institute, USA, isolated the virus, HIV, the causative agent for AIDS.4 This discovery led to the formulation of standard, reliable and sensitive procedures for making a definitive laboratory diagnosis in those suspected to have HIV infection.1,4

By the end of 2003, the estimated number of people living with HIV worldwide was put at 40 million, with African countries having 60-70% of the disease.5,6 However, massive campaign on



awareness, universal access to antiretroviral drugs, voluntary counselling and testing and prevention of mother to child transmission (PMTCT) reduced the prevalence to 39.3million in 2006 and 33.1 million in 2010.7 These figures might not reflect the true prevalence of those who have the disease because these are hospital based figures which may not include several unreported cases in most developing countries where stigmatization was still prevalent.

The first case of AIDS-related condition, “slim disease”, in Africa was reported in Kinshasa, Zaire in the late 1970’s.1 Due to ignorance, unhygienic cultural practices and poverty, the spread of the disease was more rapid and resulted in the higher prevalence seen in Africa.8  In 2003, Africa accounted for 62% (25 million) of the global AIDS burden.5 Despite the concerted effort by government and non- governmental organizations, Africa still accounted for 60-70% of this deadly disease at the end of 2010.7

The diagnosis and classification of HIV/AIDS marked a turning point in the control, prevention and management of the disease.5 HIV testing and counselling, over the years, has become the gateway through which all HIV infected patients are identified.5,9 The laboratory testing of HIV infection is either through direct detection of the viral particles or its component or by indirect method of detection of antibodies against the virus.5 The use of indirect method in adults is as reliable as the direct viral detection especially when testing is done while considering the window period after previous exposure to a risk or source of HIV.5

There are three types of HIV indirect or antibody test. (1) Sample or rapid test. (2) Enzyme Linked Immunosorbent Assay ( ELISA). (3) Western blot test.5 The rapid test utilizes blood or serum, does not require special equipments or highly trained staff and are as accurate as ELISA and Western blot test. Rapid test will usually give result in less than 30 minutes and is easy to perform.5

This is the reason why rapid test is widely used in resource limited countries like Nigeria. Figure

1.1 represents a flow chart of the national guideline for serial rapid HIV testing algorithm in Nigeria.5

The CDC and World Health Organization (WHO) developed a guideline on the immunological and clinical classification of HIV/AIDS especially among resource-constrained nations.5 The immunological classification was based on T-cell part of lymphocyte count while the clinical classification was based on clinical symptoms and signs.5,9 The classification system can be used for surveillance and case definition of AIDS. In 2006 the WHO released a more definitive guideline for staging and immunogical classification of HIV/AIDS. This led to more accurate case definition of HIV/AIDS and an astronomical increase in the prevalence of the disease worldwide.  The following rapid antibody test kits combination shown below are recommended for use as rapid screening, confirmatory and tie breaker test consecutively


Perform test 1 3


  1. Determine Unigold                                     Statpak
  2. Unigold Statpak                                       Determine
  3. Determine Statpak                                        Unigold

A ”screening test” kit was used initially with the use of “confirmatory test” kit only when the result of the first test kit is positive. A “tie breaker test” kit is required to resolve discordance whenever the first two rapid tests differ.




Figure 1.1 Rapid HIV testing algorithm



A confirmed case of HIV infection should be properly staged using the 2006 WHO clinical guideline in order to expedite management and improve his/her quality of life.10 Below is WHO clinical staging of HIV/AIDS.

CLINICAL STAGE 1 Asymptomatic

  • Persistent generalized lymphadenopathy.


  • Unexplained moderate weight loss (<10% of presumed or measured weight)
  • Herpes zoster
  • Recurrent respiratory tract infection
  • Angular cheilitis
  • Recurrent oral ulceration
  • Papular pruritic eruption
  • Fungal nail infection
  • Seborrheic dermatitis.


  • Unexplained severe weight loss (>10% presumed or measured weight loss)
  • Chronic diarrhoea for .4weeks
  • Unexplained persistent fever for > 4weeks (temp >37.50c)
  • Persistent oral candidiasis.
  • Oral hairy leukoplakia
  • Pulmonary tuberculosis


  • Severe bacterial infection.
  • Unexplained anaemia (<8g/dl)
  • Acute necrotizing ulcerative stomatitis


  • HIV wasting syndrome.
  • Pneumocystic pneumonia
  • Recurrent severe bacterial pneumonia
  • Chronic herpes simplex
  • Oesophageal candidiasis
  • Extrapulmonary TB
  • Kaposi sarcoma.
  • Cytomegalovirus infection
  • Central nervous system toxoplasmosis
  • HIV encephalopathy
  • Extrapulmonary cryptococcosis
  • Lymphoma
  • Invasive cervical cancer
  • Atypical disseminated leishmaniasis
  • HIV associated nephropathy and cardiomyopathy.

The first case of HIV infection in Nigeria was reported at an international AIDS conference in 1986.11 The spread was rapid and the case fatality rate was so high that almost all patients who progressed to the advanced stage of the disease hardly survived.11 Factors that mitigate against the control of HIV/AIDS in Nigeria include ignorance, denial, bad cultural practices, poverty and male gender issues with male dominating decision making function.11 Other factors include lack of commitment on the side of government, lack of structure that support people living with HIV/AIDS and poor community mobilization and participation.9,11

At first, the Nigerian government was slow in response to the increasing rate of HIV transmission; it was only in 1991 that the Federal Ministry of Health made their first attempt to know the

Nigeria’s AIDS situation.11 The reports showed that about 1.8% of its population was affected.11 This rose to 3.8% in 1993 and 4.5% in 1998.11

1n 1999 the Federal Government of Nigeria made HIV prevention and control its major priority.11,12  The National Action on AIDS (NACA) was set up and was empowered with resources to combat the scourge of HIV/AIDS through a 3 year HIV Emergency Action plan (HEAP).12 Despite this effort to control the epidemic, the prevalence of the disease rose to 5.8% in 2001 but dropped to 5.0% in 2003. The reason for this drop was largely due to massive campaign by governmental and non-governmental agencies on public orientation.11 However, the estimated seven million Nigerian who were infected by HIV were considered to be at risk of dying from AIDS. As a result, Nigerian government, in conjunction with other NGOs, launched a free antiretroviral therapy program.11 These programs were aimed at improving the quality of life of those living with the disease, preventing transmission from mother to child and reducing the rate of transmission from one infected person to another.11

The government’s national strategic framework from 2003 to 2009 (later to 2015)  set out to provide ARVs to 80% of all adults and children living with advanced HIV infection and 80% of HIV positive pregnant women. NACA in conjunction with other Implementing Partners (IP) such as the Presidential Emergency Fund For Aids Relief (PEPFAR), Bill and Melinda Gates foundation and AIDS Preventive Initiative in Nigeria (APIN), were able to make anti-retroiviral drugs available to about 5.8% of the over 5 million people living with HIV at the end of 2010.13 This was far below the initial target. Factors such as corruption, diversion of funds and materials, lack of political will, discrimination and lack of funds had been figured as the major factors militating against making the drug universally accessible to those who needed it.10 Majority of the patients seen at the ART clinic in Plateau State Specialist Hospital (PSSH), Jos, are presently on

ARVs.  This was because of the review of the current WHO guideline for the commencement of ART which raised the cut off CD4 count to 350 cells/uL from 200 cells/uL and the untiring effort on the part of IPs and government agencies.10

Africa has also been identified as a continent being ravaged by Intestinal Parasitic Infection (IPI).14 Intestinal parasitic infection has been described as the greatest single cause of illness and disease worldwide.15,16,17 IPIs are linked to lack of sanitation, lack of access to safe drinking water and poor hygiene; therefore they occur wherever there is poverty.16 IPIs deprive the poorest of the poor of health, contributing to economic instability and social marginalization.14 The poor people in under-developed nations experience a cycle where under-nutrition and repeated infestation lead to excess morbidity that continues from generation to generation.14

About one third of the world i.e more than two billion people, is infested with intestinal parasites and approximately 3 million people are severely ill with these worms.14,18 IPIs rarely cause death but because of the size of the problem, the global number of related death from IPIs is substantial.14,17,18. The consequence of IPIs is measured in DALY (Disability-Adjusted Life Years) and one DALY represent one year of equivalent health.14,17 About 39 million DALYs are attributed to IPIs and thus these infections represent substantial economic burden.17

Ascaris lumbricoides, Trichuris tricuria and hookworm (Ancylostoma duodenale and Necator americanus) collectively referred to as soil transmitted helminths (STHs) are the most common intestinal parasites worldwide.19 Globally, millions of people suffer from intestinal parasitic infection such as Ascaris lumbricoides (1.2 billion), Trichuris trichuria (795 million), hookworm (740 million), Entamoeba histolytica (50 million) and Gardia lamblia (2.8 million).14,19 The faecooral route is significant in the transmission of parasitic infection to humans because of poor personal hygiene, poor environmental condition like contamination of soil and water source with infected human faeces and poor sewage disposal such as use of  human sewage as fertilizer.17,20 When the soil becomes contaminated, the eggs in the soil can be transferred onto vegetables, then onto hands and transferred directly into the mouth or ingested by eating raw vegetable.17,21  The ova of intestinal parasites have been found to adhere to vegetable, fruits, utensils, door handle and money.21 The risk of IPIs is higher among inhabitants of towns in developing countries where there is poor disposal of garbage, poor health system and overcrowding.17 

Intestinal parasites are classified into protozoas and helminthes. Helminths have plagued man before the earliest recorded history.22 The eggs of intestinal helminths can be found in the mummified faeces of human dating back to thousand of years.23,24 There are 3 major phyla of helminth. These include nematodes (roundworms), the cestode (tapeworm) and the trematodes

(flukes).22 The nematodes are further divided into intestinal nematodes and the tissue nematodes. This study is however concerned with intestinal nematode otherwise known as intestinal helminths.

The most common intestinal helminths include Ascaris lumbricoides, Trichuris trichiuria, and hookworm.22,25 It has been reported that people in sub-Sahara Africa are infected with more than one helminth at a time.22 Practically speaking, this means that the inhabitant of rural, impoverished villages throughout the tropics and subtropics are often chronically infected with several different species of parasitic worms; i.e. they are polyparasitized.26 Helminths are known to cause iron deficiency anaemia, hypoproteinemia, malnutrition and intestinal obstruction.22

Adding to the global morbidity that results from human helminths infections, are the observation that it has both direct and indirect effect on HIV/AIDS in developing countries.22,26 Such coinfection has an additive effect resulting in anemia, reduced immunity and malnutrition.28 It also has a synergistic effect with increased transmission of HIV as well as exacerbating progression of

this killer disease.28,29

A study in China reported a 24% prevalence of intestinal parasitic infection among HIV/AIDS patients prior to the commencement of HAART.30 The prevalence in developing countries was much higher ranging between 38% and 64%.31,32,33  Factors such as source of drinking water, educational status, occupation, and personal hygiene have been identified as reasons for increase

in IPI seen in developing countries.34,35

The introduction of free Antiretroviral drugs in 1996 among resource limited countries marked a major turning point in the management of HIV/AIDS in Nigeria, Africa and the world over.1 Studies have revealed a marked reduction in the progression of the HIV infection to AIDS.1 The population of those accessing ART has been on the increase in our adult ART clinic. With the reviewed criteria for commencement of ART, 60-80% of the patients seen at our clinic are presently on ART. Unfortunately, these patients are not immune to intestinal helminthes especially when other risk factors have not been eliminated.

A study done in Sao Jose,Brazil, showed a marked decrease in the prevalence of IPIs from 63.9 to 24% before and after commencement of HAART respectively.33 Mar et al and Dimitra et al also agreed to this assertion.37,38Strongyloides stercoralis was the common intestinal helminths isolated from the stool samples of patients on HAART in Brazil.33 Other helminths include Ascaris lumbricoides, Trichuris trichiuria and hookworms.33

HIV infected patients, whether on HAART or not, are still considered to have depressed immunity

especially those with low CD4 count and are prone to all sort of infections including IPIs.33, 34, A pilot study of those receiving HAART at our clinic reveals that most of them are living below the poverty level. When this is added to poor environmental hygiene, lack of safe drinking water and poor sewage disposal system in Jos, our patients are invariably prone to helminthic infestation.
















At the end of 2008, about 1.26 million cummulative deaths and an estimated 118,390 annual deaths from AIDS were recorded in Nigeria.39 This was largely due to comorbidities that arose from bacterial, viral, fungal and parasitic infections.39 In 2010, Plateau state recorded an all time high prevalence of 7.7% (8.6% in Jos) of HIV infection, which was higher than the national prevalence.40 However, there was limited data on the number of deaths from AIDS in Jos and environment.  Similarly, IPIs is endemic in Jos, Plateau state, especially among immunocompromised patients who had low socioeconomic status, poor educational background, lacked access to good drinking water and practiced improper hygiene.41 Onyekwena , in an unpublished work, reported a 27% prevalence of IPIs among people living with HIV/AIDS (PLWHA) at the Heart to Heart unit of Plateau Specialist Hospital (PSSH) during the  pre-HAART era.42 Despite the commencement of HAART at the adult ART clinic, HIV-patients are still at risk of IPIs considering the poor living condition of most of them, the overt nature of IPIs among them and the fact that anti-helminths and other preventive measures have not been part of our therapeutic package. Patients with CD4+ count <200cell/mm3 are particularly susceptible to severe form of IPIs despite being on ART.36 In its insidious form, intestinal helminthes infections may lead to malabsorption, nutrient deficiency and protein energy malnutrition.31 Malnutrition and helminths infection are significant cause of depressed immunity among patients on antiretroviral therapy. These may be the source of several cases of worsening clinical conditions seen among some patients on HAART in a study done in Zambia.43 Due to scarcity of data on the prevalence of these parasites among patients on HAART in Jos, this study sets out to determine the pattern and prevalence of these infections among them.


1.3 AIM

To determine the pattern of intestinal helminths infection among HIV/AIDS adult patients on ART at the Infectious Disease Unit of PSSH, Jos, with the aim of making recommendation that will not only reduce the prevalence of these parasites but improve their quality of life.


  • To determine the prevalence and pattern of intestinal helminths infection among HIV positive adults patients who were taking HAART at PSSH, Jos.
  • To determine the relationship between immune status (using CD4+ count) and intestinal helminths infection in the study population.
  • To assess the relationship between intestinal helminths infection and sex, age, occupation, contact with animals, type of toilet facility, hand washing, level of literacy and source drinking of water among them.


A good knowledge of the pattern and prevalence of intestinal helminths among HIV patients on ART especially in our environment will be of great help in the following ways:

  • Help the patient and his/her family to instill some good hygienic practices in order to prevent these infections.
  • Help the primary care physician to maximize care for better outcome for the patient.
  • Help government/donor agencies plan, in terms of policy formulation and availability of drugs/facilities that will be of help as far as their care is concerned.

Just as the use of cotrimoxazole prophylaxis has helped curtail opportunistic infections, knowledge of the prevalence and the type of helminths infections in HIV patients may help determine the need for prophylaxis. The overall morbidity and mortality of adults on HAART will be reduced and the quality of life of the clients will be improved.


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