Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 
https://doi.org/10.1186/s41043-018-0157-x
RESEARCH ARTICLE Open Access
Food elimination, food substitution, and
nutrient supplementation among ARV-
exposed HIV-positive persons in southern
Ghana
Amos K. Laar1* , Margaret Y. Lartey2, Augustine Ankomah1, Michael P. K. Okyerefo3, Ernest A. Ampah1,
Demi P. Letsa1, Priscillia A. Nortey4 and Awewura Kwara5
Abstract
Background: Optimal nutrition is a determinant of health in all persons. In persons living with HIV (PLHIV), nutrition
is particularly important. Various factors, including dietary practices, play a role in guaranteeing nutritional health.
Objectives: We investigated multiple non-prescription drugs use among HIV-positive persons receiving antiretroviral
therapy (ART) from four treatment centers in southern Ghana. This paper, however, focuses on nutrient supplement
use, food elimination, and food substitution practices by the PLHIV.
Methods: Using quantitative and qualitative methods, we collected data from 540 HIV-positive persons at the health
facility level. This paper focuses on only the quantitative data. Individual study participants were selected using a
systematic random sampling procedure. Participants were interviewed after informed consent. We used univariate
analysis to generate descriptive tabulations for key variables. Multivariable logistic regression modeling identified
predictors of three practices (nutrient supplementation, food elimination, and food substitution). P value less than 0.05 or
95% confidence intervals facilitated determination of statistical significance. All analyses were performed using IBM SPSS
Statistics for Windows, version 20.0.
Results: The use of nutrient supplements was a popular practice; 72% of the PLHIV used various kinds. The primary motive
for the practice was to boost appetite and to gain weight. A little over 20% of the participants reportedly eliminated certain
foods and beverages, while 17% introduced new foods since their initial HIV diagnosis. All the three practices were largely
driven by the quest for improved health status. We determined predictors of nutrient supplementation to be ART clinic
location and having an ART adherence monitor. Having an ART adherence monitor was significantly associated
with reduced odds of nutrient supplementation (AOR = 0.34; 95% CI 0.12–0.95). The only predictor for food
elimination was education level (AOR = 0.29; 95% CI 0.30–0.92); predictors of food substitution were ART clinic
location (AOR = 0.11; 95% CI 0.02–0.69) and anemia (defined as hemoglobin concentration less than 11.0 g/dl)
(AOR = 0.21; 95% CI 0.12–0.85).
Conclusions: The practice of supplementation is popular among this group of PLHIV. Food elimination and
substitution are practiced, albeit in moderation. The predictors identified may prove helpful in provider-client
encounters as well as local HIV programming.
Keywords: Nutrient supplementation, Food elimination, Food substitution, HIV, ART, Ghana
* Correspondence: alaar@ug.edu.gh
1Department of Population, Family, & Reproductive Health, School of Public
Health, University of Ghana, Accra, Ghana
Full list of author information is available at the end of the article
© The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 2 of 12
Introduction rates of hospitalization, opportunistic infections, pro-
Optimal nutrition is key to health. In the case of persons gression to AIDS, and death [19–21] are confirmed, side
living with HIV (PLHIV), nutrition is particularly im- effects associated with their use can lead to compro-
portant. Nutrition can help boost immune function, mised nutritional status [22]. Adverse side effects of
maximize the effectiveness of antiretroviral therapy ARVs are often related to the gastrointestinal system and
(ART), reduce the risk of other chronic diseases, and include nausea, vomiting, diarrhea, abdominal cramps
contribute to an overall quality of life [1]. Studies have anemia, malabsorption, loss of appetite, and changes in
shown that HIV-positive people with poor diets develop taste of familiar foods. HIV-positive persons also end up
AIDS more quickly [2–5]. The many and multilayered with oral and esophageal lesions, sore throat, and swol-
factors that affect nutrition in HIV are at individual, len glands that result in a reduction of food intake. In an
household, and community levels. Individual-level fac- attempt to mitigate some of the adverse effects of ARVs,
tors include inherent metabolic changes and gastrointes- people often resort to herbs, potions, dietary supple-
tinal disorders [6, 7], effects of various opportunistic ments, and non-prescription remedies [23]. Some of the
infections [5], side effects of medications, and the effect gastrointestinal side effects often drive people to make
of the HIV itself. Household-level factors are related to dietary modifications such as introducing new foods
household attributes such as poverty and food insecurity and/or eliminating others [1, 24, 25].
[8]. Community-level factors relate to socio-political, re- Like ARVs, some dietary supplements play important
ligious, cultural, and structural factors [9, 10]. These fac- roles in the lives of many people living with chronic and
tors can in a linear or in an interactive fashion impact often life-threatening medical conditions. However, there
negatively on the nutritional status of a PLHIV. are concerns about their use. Such concerns generally stem
As other infections do, HIV increases metabolic rate. from the potential for adverse interactions with conven-
The body’ need for energy and protein is increased as it tional medicines and patients replacing evidence-based
struggles to maintain optimal immune function and repair health care with untested remedies [26]. Studies show that
damaged cells [11–13]. The work of Mangili et al. also the most common dietary supplements in PLHIV are aimed
shows that HIV medications increase resting energy ex- at “boosting immune functioning” such as mega-dose vita-
penditure independent of viral load [14]. This translates mins, and anti-oxidants, body cleansing products such as
into increases in nutrient requirements [15]. While in- teas, and herbs such as ginseng [27]. Suffice it to say that
creasing nutrient requirements, HIV infection at the same many of these usually result in the elimination and/or re-
time can lead to reduced food intake. Several pathways ex- striction of certain foods. Others are contraindicated when
plain this. First, reductions in food intake can result from used with antiretroviral medications [27, 28].
painful sores in the mouth and/or esophagus. Side effects In addition to the clinical issues described above, there
of the infection, such as fatigue, depression, and changes are social issues that affect the ability to acquire the kind
in mental state, can affect food intake as well. Further, spe- of food needed to maintain optimal health among
cific nutrient deficiencies, which may be due to HIV infec- PLHIV. Food insecurity and HIV positivity have a cyc-
tion, can affect a person’s appetite and interest in food. lical relationship [29]. Being infected with HIV can limit
Side effects of medications, which include nausea, vomit- productivity, leading, in turn, to loss of income while
ing, diarrhea, abdominal cramps, can also result in sub- healthcare costs continue to increase [30]. The other fac-
optimal dietary intakes. A recent Ghanaian study that tors include housing [31], challenges related to accessing
determined the daily intakes of some important nutrients ART [32], and food assistance [33].
by HIV-positive pregnant women revealed a high preva- While extensive research has been conducted among
lence of inadequate dietary intake among those with nau- PLHIV to explore reasons why they may not adhere to ARV
sea, vomiting, and oral lesions [16]. Another possible medication regimens [34–36], there is relatively little explor-
cause of reduced intake is food insecurity resulting from ation, of whether they receive or adhere to nutritional rec-
HIV-related factors [17, 18]. ommendations from primary healthcare providers. There is
To therefore achieve optimal nutritional health, equally little work done on the extent of food substitution or
HIV-positive persons not only need to eat, they need to food elimination as a practice among PLHIV on ART. This
have access to diverse foods, consume adequate quan- paper assessed the extent and predictors of nutrient supple-
tities, as well as be linked to optimal clinical care. In mentation, the practice of food substitution or elimination
resource-constrained settings, however, many factors among ARV-exposed PLHIV in southern Ghana.
preclude these. As indicated earlier, the very potent
weapon for HIV, antiretroviral (ARV) medications, is Methods
also one of the many clinical precipitators of reduced Design and study sites
food intake. Although ARV efficacy in sustaining durable This study forms part of a larger original study that was
suppression of HIV replication, which in turn reduces conducted to examine non-prescription drug use among
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 3 of 12
HIV+ persons on ART, adherence to ART, and barriers Prior to sampling, the probability proportional to size
HIV+ persons face accessing ART in Ghana. A weighting procedure was employed in the allotment of
cross-sectional study using surveys and in-depth inter- the PLHIV to the four study sites. Study participants
views was conducted to collect data from healthcare were selected using a systematic random sampling with
providers and a total of 540 adult HIV+ persons receiv- random start. To do this, the master list of ART clients
ing ART at four treatment centers in the Eastern and at each facility served as the site-specific sampling frame.
Greater Accra regions of Ghana. For the purposes of the The sampling interval (n) for each site was derived by
current paper, we focus on and report findings from the dividing the total number of participants on the monthly
quantitative survey. register by the required sample at each site. The total
Surveys were conducted at four health facilities where number of clients needed from a particular study site
ART is offered to HIV-positive clients. These health fa- was interviewed between May 5 and June 30 2014.
cilities are the Fevers Unit of the Korle Bu Teaching Fieldwork was conducted by eight trained research as-
Hospital and the ART center at the Tema General Hos- sistants (RAs). RAs were recruited based on survey ex-
pital (both in the Greater Accra region of Ghana). The perience and knowledge of the local area. Training
Atua Government Hospital and St Martins de Porres entailed introduction to the study objectives, goals,
Hospital ART centers were the other rural sites in the methods, and expected outcomes. There were extensive
Eastern Region of Ghana. The Korle Bu Teaching Hos- role-plays to ensure accuracy during fieldwork. Study
pital is one of the tertiary hospitals in the southern part tools were pretested after the training, and the needed
of Ghana. The Fevers Unit affiliated to the Department validations done prior to the actual data collection.
of Medicine, University of Ghana has the largest popula- With the help of health personnel managing the ART
tion of PLHIV at a single site. At the time of the study, clinics, eligible study participants were identified and
the Fevers Unit of the Korle Bu Teaching Hospital had interviewed. The interview elicited information on the
about 6000 patients on ART. Tema General Hospital (a various medications and remedies used by the ART cli-
regional hospital) had about 1500 HIV-positive clients ents (ART and other approved allopathic and trad-
who were enrolled on ART. The Atua Government Hos- itional/herbal medications, non-prescription drugs,
pital and the St. Martins Hospital had about 4800 and nutrient supplements, etc.). Also recorded as part of the
4000 HIV-positive clients on ART respectively. interview were potential predictors of the three study
outcomes of interest such as “place of residence, sex,
Sample size estimation, sampling, and summary of other age, religious affiliation, level of education of respondent,
field procedures and whether or not respondent had an adherence moni-
The sample size for the quantitative component of the tor.” Clients’ hospital records were also reviewed, and
study was determined using Statcalc in Epi Info 2000 relevant data extracted. The interviews further assessed
package [37]. Both the population-based survey compo- motivations for the various practices (problems with eat-
nent and the unmatched cohort/cross-sectional study ing in general use of nutrient supplements, food elimin-
were used—first to provide at least 95% level of precision ation, food substitutions). Variables measured through
for estimating the prevalence of the three practices of lab-based equipment included body mass index (BMI)
interest (food elimination, food substitution, and nutrient (kg/m2), CD4+ cell count, and hemoglobin concentra-
supplementation) and second to provide power to detect tion (g/dl). All such were determined using standard
predictors of these practices. Neither the exact propor- procedures.
tions of the three key practices (nutrient supplementation,
food elimination, and food substitution) nor the odds of Data management and analysis
engaging in the practices in relation to the potential pre- Interviews were done using paper-based questionnaires.
dictors were known in this population. These were each Our data cleaning protocol required data collectors to re-
assumed to be 50% but could be as low as 45% (worst ac- view all completed data collection forms and correct er-
ceptable level). The sample size from the guesstimated rors/inconsistencies before hand-delivering them to field
proportions was larger than that estimated using odds ra- supervisors. Supervisors further reviewed the forms for ac-
tios. This was thus preferentially chosen. Thus, with an curacy, consistency, and completion. Once the data collec-
alpha of 0.05 and a statistical power of 90%, 434 clients tion forms were considered complete, they were securely
was computed as the minimum sample size. This sample delivered to the principal investigator’s office where they
size was further increased by 20% (to account for contin- were kept in locked filing cabinets. Measures instituted to
gencies such as non-responses or recording errors) and address entry errors included hiring two competent and
rounded up to 521 clients. However, being part of a larger motivated data entry clerks, who then doubly entered data
study with an overall sample size of 540, all of the 540 into pre-programmed data screens designed in CSPro
PLHIV were used for this analysis. (Census and Survey Processing System). Data were
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 4 of 12
exported to IBM SPSS Statistics, version 20, for consistency sample, data on physiologic state was available on 357.
checks and validation. Cleaned and validated data sets were Of these, 3% were pregnant and 4% nursing young chil-
analyzed using the same program. dren. The sampled population was overwhelmingly
We used univariate analysis to generate descriptive Christian (90%). About 80% of them had some form of
tabulations for key variables. To determine predictors of formal education. Close to 50% of the study participants
the key outcomes of interest (nutrient supplement use, either were anemic or had CD4 count of less than 350
food elimination, and food substitution), three independ- cells/mm3. The prevalence of low body mass index/
ent multivariable logistic regression models were con- underweight (indicative of chronic energy undernutri-
structed using various background, socio-demographic, tion) was comparable to the prevalence of obesity among
and clinical attributes of PLHIV as potential predictors. the study sample (Table 1).
Variables with P < 0.25, at the bivariate analysis (data We present in Fig. 1 the extent of nutrient supplement
not shown), or those previously reported to be associ- use, food elimination, and food substitution among the
ated with nutrient supplement use were selected into study sample. Eighty percent of the PLHIV interviewed
the multiple regression models. Several factors were indicated having no problem with eating in general. The
considered potential predictors as per Table 2. A priori 20% with eating problems stated a number of reasons
determined confounders introduced into the models in- for their inability to eat properly. Lack of appetite/nau-
cluded age, place of residence, and educational back- sea/vomiting were the most common problems (men-
ground. We employed a standard logistic regression tioned 34 times), financial challenges were mentioned 12
modeling in SPSS (the “Enter” method) in our analysis. times, and sore throat/pains in the mouth or stomach 11
With this method, all the variables were entered into a times. Heart burn, a bitter taste in the mouth, tasteless-
full model generated in a single step. The attributes of ness of food, and inability to afford the foods they want
the model are included in the tables presented. P value were some other reasons given. Some also complained
< 0.05 was used to denote statistical significance. of distention and pain in the abdomen when eating. To
address this problem, some included more fruits and en-
Ethical considerations ergy drinks in their diets. Many others began eating
Participation in the study conformed to the required small meals at regular intervals and taking unidentified
ethical guidelines for use of human subjects. The study pills and tablets as well as “camphor tablets” to help with
proposal was reviewed and approved by the Ethical Re- abdomen distention. Others forced themselves to eat
view Committee of the Ghana Health Service, Research despite their symptoms. Yet others resorted to nutrient
and Development Division, Accra (Protocol ID NO: supplementation.
GHS-ERC 03/11/13). Permission was granted from the Out of the total number of PLHIV interviewed, about
facilities within which the study was conducted. In- 72% of them confirmed using nutrient supplements.
formed consent was obtained from all participants after These supplements include Fersolate, folic acid, B-com-
the objectives and the methodology of the study were plex, Selevite, and multivitamin tablets. The respondents
explained to them. Participation in the study was com- mentioned other trade names of nutrient supplements
pletely voluntary, and no financial or material benefits such as Vitafol, Bioferon, Astymin, Intravita, Selevite,
were given. The privacy and confidentiality of every par- Lutavita, Eleron, Zincovite, Zipferon, Zincolac, and Zin-
ticipant was ensured throughout the study period. Iden- cofer. The primary reason survey respondents gave for
tification numbers (and not names) were used to taking supplements was to “enable them to eat well and
disguise identity. Every member of the data collection to gain weight.” Majority of the respondents reported
and analysis team was cautioned during the training ses- that they began to take supplements upon the advice of
sions to maintain strict confidentiality and anonymity of doctors, nurses, and other health workers.
study data and participants. The participants, who were A little over 20% of the interview participants report-
all adults (18 years or older), further consented to the edly eliminated certain foods and liquids since their HIV
publication of the study findings. diagnosis. The foods or beverages eliminated included
alcoholic beverages, fatty foods, palm oil, meat, milk,
Results cocoyam fufu, and sugary foods. A variety of reasons
Table 1 presents the background, socio-demographic, were given by the respondents for these practices. Such
and selected clinical characteristic of study participants. included to control their blood pressure, reduce heart
Close to half of the study sample (46%) was from the burn, reduce their protein level, live longer, and other
ART centers in the Greater Accra region; the remaining undisclosed personal reasons. Others stopped upon the
54% were from the rural Eastern Region study sites. advice from fellow patients while others wanted relief
About three quarters (74%) of the respondents were fe- from their symptoms such as stomach ache and upset,
male. Of 400 women who formed part of the study inability to sleep, diarrhea, vomiting, severe chest pain,
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 5 of 12
Table 1 Background, socio-demographic, and selected clinical Table 1 Background, socio-demographic, and selected clinical
characteristic of study participants characteristic of study participants (Continued)
ART/study site Frequency Percent ART/study site Frequency Percent
Atua Government Hospital 146 27.0 Class III obesity (BMI > 40.00) 8 1.8
St Martin’s Martins de Porres Hospital 148 27.4 Total 436 100.0
Tema General Hospital 93 17.2 CD4+ cell count3
Fevers Unit, Korle Bu Teaching Hospital 153 28.3 CD4+ cell count < 350 235 47.3
Place of residence CD4+ cell count ≥350 262 52.7
Urban 275 50.9 Total 497 100.0
Rural 265 49.1 Hemoglobin concentration (g/dl)4
Sex of respondent Anemic < 11.0 g/dl 239 46.4
Male 140 25.9 Normal/Hb ≥ 11.0 g/dl 276 53.6
Female 400 74.1 Total 515 100.0
Religious affiliation of respondent 1Mean age is 42.3 age ranged from 18 to > 60 years
2Mean BMI is 23.9335 and ranged from 13.61 to 50.00; 104 of the cases have
Not religious 10 1.9 missing weight or height
3
Christian 485 89.8 Median CD4 cell count is 373; range from 2 to 1663; 43 cases are missing
CD4 measurements
Muslim 43 7.9 4Mean Hb is 11.1 and ranged from 5.8–19.2; 25 cases are missing
Hb measurements
Traditionalist 2 0.4
Respondent’s level of education uncomfortable feeling, and general feeling of weakness.
No formal education 109 20.1 As with nutrient supplement use, many indicated that
Primary 123 22.9 they stopped certain foods upon consulting with nurses,
JHS 170 31.4 doctors, and health workers who advised them to stop
SHS/vocational 102 18.9 since it suppresses the potency of the ARV and reduces
the effectiveness of the ART.
Post secondary/tertiary 36 6.7
Out of a total of 471 PLHIV who responded to the
Total 509 100.0 question on food substitution, only 16.8% had intro-
Age1 duced new foods after their initial HIV diagnosis. These
18–19 5 0.9 foods were mainly fruits (mango, banana, watermelon,
20–24 12 2.2 orange, pawpaw, carrots, pear, apple), vegetables (spin-
25–35 126 23.3 ach leaves or kontomire), “tom brown” (a local cereal
bran made from maize, sorghum, and groundnuts),
36–60 374 69.3
“fufu,” palm nut soup, and dry fish. The primary reason
61 or older 23 4.3 respondents gave for introducing these new foods in to
Does respondent have an adherence monitor their diet was health worker (doctors or nurses) recom-
Yes 293 54.5 mendation. Other reasons given were that it improved
No 245 45.5 their nutritional status, boosts the immune system to
Total 538 100.0 fight off opportunistic infections, and “gives them blood”
and enough strength to work.
Physiologic status of female respondents
We constructed three independent multivariable re-
Pregnant 10 2.8 gression models to predict the practices of nutrient sup-
Lactating 14 3.9 plementation (model 1), food elimination (model 2), and
Not pregnant 333 93.3 food substitution (model 3). The models identified pre-
Total 357 100.0 dictors of the stated outcomes after adjusting for a num-
Body mass index (BMI)2 (kg/m2) ber of covariates.
In model 1, ART clinic location and having an ART
Underweight (BMI < 18.50) 53 12.2
adherence monitor were predictive of nutrient supple-
Normal weight (BMI 18.50–24.99) 236 54.1 ment use. Thus, compared to ART service users from
Overweight (BMI 25.00–29.99) 99 22.7 the Korle Bu Fevers Unit (a teaching hospital setting),
Class I obesity (BMI 30.00–34.99) 29 6.7 those from the Eastern Region ART clinics were signifi-
Class II obesity (BMI 35.00–39.99) 11 2.5 cantly less likely to use nutrient supplements. On the
contrary, PLHIV from the Tema General Hospital (a
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 6 of 12
Fig 1 Nutrient supplement use, food elimination, and food substitution among PLHIV on ART
district hospital located in the city) had nine times to significant predictor of the practice of food substitution.
use nutrient supplements (adjusted odds ratio [AOR] = These key findings are discussed.
8.99; 95% CI 2.37–34.17) (Table 2). Thus, having an Our data show that 55% of the study respondents had
ART adherence monitor was significantly associated with an ART adherence monitor at the time of the survey and
reduced odds of nutrient supplement use (AOR = 0.34; having an ART adherence monitor was significantly asso-
95% CI 0.12–0.95). ciated with reduced odds of nutrient supplement use
For model 2, only one of the ten potential predictors— (AOR = 0.34; 95% CI 0.12–0.95). Before discussing our
respondent’s level of education—significantly predicted key study findings, it would be useful to present back-
food elimination. Those with no formal education were ground to adherence monitoring. At the time of the study,
less likely to eliminate foods from their usual menus local guidelines relating to “ARV treatment initiation”—in
compared to those with post secondary/tertiary level of line with WHO guidelines—contained both medical/clin-
education (AOR = 0.29; 95% CI 0.03–0.92). ical and non-medical eligibility criteria. Medical eligibility
Model 3 aimed to identify predictors of food substitu- criteria included patients with CD4 count less than 350
tion/introduction of new foods, and confirmed ART cells/ml and/or the patient is symptomatic with HIV in-
clinic location and anemia (defined as hemoglobin con- fection in WHO clinical stages III and IV and patient pre-
centration less than 11.0 g/dl) to be independent predic- sents with severe hepatic liver function tests > 5 times the
tors of the practice. Anemic PLHIV were less likely to upper limit of normal, or end-stage renal disease; a patient
introduce new foods (AOR = 0.45; 95% CI 0.21–0.85). having an acute opportunistic infection is not eligible to
Also compared to the Korle Bu study site, PLHIV from initiate ART. The acute opportunistic infections must be
the Atua Government Hospital (district hospital setting treated before initiation of antiretroviral therapy to avoid,
in a rural area), the St Martin’s (a rural sub-district hos- for example, immune reconstitution syndrome. Therefore,
pital setting), and the Tema General Hospital study sites service providers would provide appropriate adherence
had lower odds of introducing new foods, although only counseling and initiate ART for those who are eligible.
the St Martins ART site retained its predictive power The non-medical eligibility criteria included “do not initi-
after controlling for nine other potential predictors ate treatment, if treatment is not sustainable,” for example
(AOR = 0.11; 95% CI 0.02–0.69) (Table 2). if the person is not able to cope with follow-up visits or fa-
cility is unable to assure continuity of care and if HIV+ is
Discussion found to be unlikely to comply/adhere, PLHIV. For these
This paper presents and discusses the extent of nutrient HIV+ as well as not who are screened off with the medical
supplement use, food elimination, and food substitution eligibility criteria, service providers provide appropriate
practices among PLHIV on ART in Southern Ghana. counseling and defer initiation into ART. For those who
Our data show that majority (72%) of the PLHIV were meet enrollment criteria and are enrolled into ART, ad-
users of nutrient supplements; 23% had eliminated cer- herence monitoring is a life-long initiative, just as ART.
tain foods and beverages upon HIV diagnosis, and 17% Due to limited trained personnel and socio-cultural limita-
had substituted/introduced new foods post their HIV tions, this service may be delivered by trained health ser-
diagnosis. Significant correlates of nutrient supplement vices if their relationship with HIV+ and proximity will
use included location of ART clinic and ART adherence facilitate regular interaction; these are also delivered by
monitoring. Predictors of food elimination were location family members, friends, religious leaders, or other confi-
of ART clinic and level of education. Anemia (defined as dants of the HIV+. In our study, we aimed to assess the
hemoglobin concentration < 11.0 g/dl) was the only association of “service continuity adherence monitors/
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 7 of 12
Table 2 Background, socio-demographic, and clinical correlates of nutrient supplement use, food elimination and substitution
Attribute Nutrient supplement use Eliminated certain foods due to Introduced new/substituted foods
Model 1 HIV diagnosis due to HIV diagnosis
Model 2 Model 3
AOR 95% CI AOR 95% CI AOR 95% CI
LB UB LB UB LB UB
ART site
Atua ART clinic 0.26 0.06 0.61 0.38 0.11 0.95 0.20 0.03 1.20
St Martins de Porres Hospital 0.20 0.05 0.87 0.37 0.10 0.74 0.11 0.02 0.69
Tema General Hospital 8.99 2.37 34.17 0.99 0.17 5.78 0.16 0.02 1.35
Korle Bu Fevers Unit 1.00 1.00 1.00
Sex of respondent
Male 0.39 0.03 4.57 1.83 0.12 28.44 10.23 0.95 71.69
Female 1.00 1.00 1.00
Place of residence
Urban 2.37 0.71 7.91 0.55 0.22 1.41 0.76 0.24 2.48
Rural 1.00 1.00 1.00
Respondent’s level of education
No formal education 1.49 0.16 14.20 0.29 0.03 0.92 0.40 0.04 4.17
Primary 1.02 0.11 9.22 0.20 0.02 1.70 0.67 0.07 6.35
JHS 1.52 0.17 13.73 0.21 0.02 1.85 0.50 0.05 4.86
SHS/vocational 0.82 0.07 9.22 0.16 0.02 1.58 0.68 0.06 7.65
Post secondary/tertiary 1.00 1.00 1.00
Does respondent have an adherence monitor
Yes 0.34 0.12 0.95 1.09 0.36 3.25 0.65 0.16 2.66
No 1.00 1.00 1.00
Physiologic state of female respondent
Pregnant/lactating 1.51 0.67 3.41 1.49 0.77 2.85 1.38 0.68 2.80
Not pregnant 1.00 1.00 1.00
Age categories
< 35 0.85 0.41 1.78 1.17 0.58 2.33 1.22 0.52 2.85
≥ 35 1.00 1.00 1.00
BMI
Underweight 1.24 0.42 3.70 1.33 0.49 3.56 1.85 0.58 5.87
Not underweight 1.00 1.00 1.00
CD4+ cell count
CD4+ cell count < 350 1.08 0.54 2.17 0.83 0.44 1.54 1.12 0.54 2.33
CD4+ cell count ≥ 350 1.00 1.00 1.00
Anemia status
Normal/Hb ≥ 11.0 g/dl 0.75 0.36 1.56 0.89 0.47 1.67 0.47 0.21 0.85
Anemic < 11.0 g/dl 1.00 1.00 1.00
Abbreviations: AOR, adjust odds ratios with accompanying 95% confidence intervals were determined using multiple logistic regression (all variables in this table
were included in the model)
Nutrient supplement use model: Model summary Cox and Snell R2 (0.176), Nagelkerke R2(0.264), −2 Log likelihood 220.832 (estimation terminated at iteration
number 20 because maximum iterations have been reached)
Food elimination model: Model summary Cox and Snell R2 (0.125), Nagelkerke R2 (0.180), −2 Log likelihood 264.135 (estimation terminated at iteration number 20
because maximum iterations have been reached)
Model for food substitution: Model summary Cox and Snell R2 (0.109), Nagelkerke R2 (0. 176), −2 Log likelihood 198.231 (estimation terminated at iteration
number 6 because parameter estimates changed by less than 0.001)
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 8 of 12
counsellors” and the three study outcomes (nutrient sup- infections. Infections cause and exacerbate poor nutrition.
plementation, food elimination, food substitution), and Poor nutrition makes it impossible for PLHIV to stay
not receipt of adherence counseling during initiation into healthy and productive much worse if this state of poor
ART (as all HIV+ do receive). The variable was nutrition pre-exists. To offset such undesirable clinical as
self-reported—in response to a survey question on well as physical manifestations, PLHIV turn to alternative
whether or not HIV+ currently had an adherence and complimentary medications: among which are herbs
counselor/monitor. That 45% of the PLHIV on ART did and nutrient supplement [52, 53].
not have adherence monitors that could be interpreted as According to available research, WHO recommends a
adherence monitoring continuity relapse. This is a daily dose of the recommended nutrient intake (RNI) for
phenomenon worth investigating in a separate follow-up all micronutrients [54], especially for PLHIV. The current
study. study looked primarily at the prevalence of nutrient sup-
plementation, although and earlier Ghanaian study in the
Nutrient supplementation setting of the current study reported suboptimal intake of
We found a high prevalence of micronutrient supplemen- various nutrients among female PLHIV [16]. Further ex-
tation by the survey participants, and this is in keeping ploration is needed to determine if our research popula-
with previous research studies [38–42]. These studies not tion meets this recommended standard in the dosing,
only report on the extent of nutrient supplement use by amount, and quality of their micronutrient supplementa-
PLHIV, they also report on several benefits of supplemen- tion. Our data also show that about one out of three of
tation in PLHIV. Kaiser et al. in 2006 established that the respondents took other non-prescription remedies in-
micronutrient supplementation in PLHIV on ARTs had cluding herbal concoctions (data not shown). Although
an increase in CD4 cell count and the supplements were these were named, our research did not examine their
generally well tolerated. Nutrient supplementation in Afri- chemical composition. Several studies [26, 27, 47, 55, 56]
can women with HIV significantly improved CD4 count have reported on micronutrient supplementation [55, 56],
and had a sustained effect for a median of 5 years in the and its adverse interaction with prescription drugs like
population studied [43]. Bormann et al. in their study re- ARVs have also been put forth [26, 27, 47]. It remains en-
ported commonly used nutrient supplements to be tirely possible that PLHIV on ARVs in our geographic area
mega-dose vitamins, anti-oxidants, teas, and herbs. These might suffer adverse consequences due to their concur-
were primarily aimed at boosting immune function [27]. rent use of prescription medications and non-prescription
Majority of the respondents in the current study reported herbal supplements of unknown chemical composition.
such trade names as Selevite, Zincovite, and Zincolac. The study determined significant correlates of non-pre-
Two main reasons were given in support of nutrient sup- scribed nutrient supplement use to include location of
plementation—“to increase appetite” and “to gain weight.” ART clinic. Our collective experience supports this find-
Generally, nutrient supplements were well tolerated and ing. We believe that practices by service providers and ser-
no adverse clinical effects were reported among partici- vice users in a cosmopolitan city/teaching hospital versus
pants who took supplements. The high usage of nutrient those at the district level will differ in many respects. The
supplement in our study agrees with many [38–42], but ART clinic at the Korle Bu Teaching Hospital is manned
not all studies. Bukusuba et al. observed in their study by a team highly specialized physicians, pharmacists, and
conducted among HIV women in Eastern Uganda that clinical psychologists. Second, the clientele of the clinic
only about 20.3% of them added nutrient supplement to are likely to be better placed to reprimand and negative
their regular diets [44]. Work done by Vorster et al. and feedback for services given outside orthodox practices and
Holcomb did link urbanization to an increase in micronu- treatment guidelines. This is in contrast to clinics run by
trient uptake and consumption of diverse food categories nurses who with patients are one large family and are
[45, 46]. Kalichman et al. reported that 69% of more tolerant to certain behaviors. Of note, the model
HIV-positive men used complementary medicine prod- could explain about 26% of the variability in the practice
ucts and practices [47]. Fawzi et al. in their research (Nagelkerke R2 = 0.26; Table 2).
among Tanzania PLHIV hinted that supplementation may
be an important yet, inexpensive prophylactic and thera- Food elimination and food substitutions
peutic measure for HIV-1-infected people [48]. Deficien- Majority (80%) of respondents in this study had no
cies of vitamins A, E, B6 B12, zinc, and selenium have been problem with eating. Nevertheless, being HIV positive
shown to have adverse clinical outcomes during HIV in- and on ART did prove to be problematic for some of the
fections and a higher mortality rate [43, 49]. HIV affects respondents. The HIV state paradoxically causes height-
nutritional status from the onset of infection and in all ened nutritional need but early satiety in individuals
stages of the disease [38, 50, 51]. HIV progressively [24]. This compounded with clinical manifestations of
weakens the immune system, leading to opportunistic oral lesions, sore throat, esophageal infections, and
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 9 of 12
malabsorption impede and impair swallowing of food many foods had been added on because of health profes-
[24]. A study by Laar et al. among HIV-positive pregnant sional advice. In a study by Nti et al. [58] among PLHIV
adolescents in Ghana corroborates the observation in in Ghana, it was found that majority had fair to adequate
this study. Their study found out that participants with knowledge of healthy nutritional options; however, this
oral lesions or experiencing nauseate feeling and vomit- did not translate into a higher quality of diet and overall
ing had a very low intake of nutrients compared to the nutritional status. This gap between knowledge and prac-
others who had no such complications. Such feeling can tice can be linked to social and cultural determinants re-
precipitate food elimination or substitution. lated to food insecurity. Many of the foods added were
In addition to the above, people on ARVs tend to suf- fruits, vegetables, proteins, and plant-based highly nutri-
fer from adverse side effects of the medications that are tional foods such as sorghum, groundnuts, and millet. It is
mainly related to the gastrointestinal system such as therefore a matter of concern that majority of the respon-
diarrhea, vomiting, upset stomach, and nausea. These dents, although having adequate knowledge of nutrition,
adverse medication effects can itself lead to compro- are unable to add these healthier food options to their
mised nutritional status [22]. Many PLHIV therefore are current diet. Of note, the practices reported are not en-
unable to ingest food while experiencing these adverse tirely attributed to the HIV disease or the side effects of
effects of ARVs. the ARVs. Socio-cultural, religious, and economic factors
Almost a quarter of the respondents reported that they may motivators. A recent Ghanaian study [59] reported
experienced gastrointestinal adverse effects related to their that the family, culture, and the economic status of a
ARV medications and/or certain foods that they con- household influence food choices and portion sizes. Sztam
sumed. Examples of foods that had been eliminated were et al. have explained that the economic strain causes poor
fatty foods, starchy foods, and some animal protein quality of life and decreased work productivity of families
sources. Care however needs to be taken since these and individuals, thus forcing them to opt for cheaper food
self-reported food eliminations could affect their overall choices [60]. In the current study, location of ART clinic
nutritional status over the long term. To the best of our and level of education significantly predicted food elimin-
knowledge, these food categories that the respondents had ation practices, but not the studied religious or
self-eliminated had not been replaced by options that were socio-cultural variables.
better tolerated; therefore, there is the risk of an unbal-
anced diet that does not have adequate proportions of all
food groups. As far as we know, no studies have explored Conclusions and recommendations
the long-term nutritional effects of food elimination by The use of nutrient supplements is popular among this
PLHIV based solely on adverse side effects and not on group of PLHIV. Food elimination and substitution are
evidence-based health professional advice. practiced, albeit in moderation. The only significant pre-
PLHIV on ARVs have an increased risk for developing dictor for food elimination was education level, whereas
lipodystrophy and associated metabolic problems, including ART clinic location and anemia (defined as hemoglobin
dyslipidemia and insulin resistance [57]. This may increase concentration less than 11.0 g/dl) significantly predicted
their risk for chronic health problems such as coronary food substitution behaviors. The identified predictors may
heart disease and diabetes. Lifestyle modifications, healthy prove helpful in provider-client encounters as well as local
diet, and regular exercise have been shown to significantly HIV programming. Given the association between clinic
reduce the risk of these chronic diseases. In our study, cer- location and ability to substitute health-promoting foods,
tain food eliminations were based on healthy lifestyle and patients and care providers at rural sites may need educa-
wellbeing choices. Respondents reported that they had tion about potential health-promoting benefits of the
given up certain food items in order to “feel better, sleep practice. Efforts at providing and scaling-up ART to all
well, decrease their blood pressure, and live longer.” Many HIV+ persons ought to recognize these food and
others reported that they presently refrain from alcohol, to- nutrition-related dynamics and thus embed interventions
bacco, and cigarettes. These overall lifestyle changes could that address them. Among others, we recommend the
increase the overall prognosis of PLHIV. institutionalization of individualized nutrition assessment
One of the objectives of this paper was to explore and care and long-term investment to improve nutrition
whether PLHIV receive and/or adhere to nutritional rec- literacy of both care providers and their clients.
ommendations from primary care providers. Nearly 20%
of them had introduced specific foods post HIV diagnosis. Abbreviations
Many participants reported that they had eliminated cer- AIDS: Acquired immune deficiency syndrome; ART: Antiretroviral therapy;
tain foods from their diet based on health professional ad- ARV : Antiretroviral; CSPro: Census and Survey Processing System; HIV
: Human immunodeficiency virus; PLHIV: Persons living with human
vice that it was contraindicated with ARV use and/or immunodeficiency virus; RAs : Research assistants; SPSS : Statistical Package
suppressed ARV effectiveness. They also confirmed that for the Social Science; TB: Tuberculosis; WHO: World Health Organization
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 10 of 12
Acknowledgements two general areas of sociological inquiry, cultural sociology and sociology of
To all the HIV-positive persons who voluntarily participated in the survey and religion. He is the principal investigator in a research on Religious and Health
to the management of the Fevers Unit of the Korle Bu Teaching Hospital, Beliefs and Practices of Prayer Group members in Achimota Forest, Accra.
the Tema General Hospital, the Atua Government Hospital, and the St Mar- Margaret Y. Lartey is a professor of Medicine and has been working closely
tin’s de Porres Hospital, we are grateful. The study was supported by the Uni- with HIV-infected patients in the area of clinical management. In Ghana, she
versity of Ghana Research Fund administered and managed by the Office of is the most experienced HIV Clinician managing the single largest clinic with
Research, Innovation and Development under Grant Number URF/6/ILG-019/ 15,000 patients on roll and 6000 on antiretrovirals. She contributes actively to
2012-2013. drawing of guidelines and policies on management of HIV infection and in-
volved in the training of all cadres of health workers in HIV care as well as
Funding supervising and monitoring other sites.
The study was supported by the University of Ghana Research Fund Ernest A. Ampah is a biochemist and holds a Master’s degree in Public
administered and managed by the Office of Research, Innovation and Health from the University of Belgrade, Serbia. He has depth of knowledge
Development under Grant Number URF/6/ILG-019/2012-2013. Grant in quality assurance and current good manufacturing practices in the
Recipient: Dr. Amos K. Laar. The funder however played no role in the pharmaceutical industry. He also has experience with drug and food
design, data collection, analysis, interpretation of data, writing of the regulation, having worked with the Food and Drugs Authority (FDA) Ghana.
manuscript, and the decision to submit the manuscript for publication. He is currently a research assistant at the School of Public Health, University
of Ghana, Legon. His current research interests span malaria, HIV, and
Availability of data and materials nutrition.
The authors agree that the dataset on which the conclusions of this
manuscript rely be deposited in publicly available repositories. Ethics approval and consent to participate
The study’s protocol was reviewed and approved by the Ethical Review
Authors’ contributions Committee of the Ghana Health Service (Protocol ID NO: GHS-ERC 03/11/13).
AKL conceived the grant idea and discussed with PAN, AA, MPKO, AK, and Permission was granted from the facilities within which the study was con-
ML for inputs. PAN, AA, MPKO, and AK are co-investigators of the grant from ducted. These facilities were the St. Martins de Porres Hospital, Atua Govern-
which the paper metamorphosed. AK and ML led the clinical components of ment Hospital, the Tema General Hospital, and the Fevers Unit of the Korle
the study design and tool development. PAN, AA, and MPKO all contributed Bu Teaching Hospital. Informed consent was obtained from all participants
to the study tool development. AKL supervised the fieldwork at three of the after the objectives and the methodology of the study were explained to
four sites. ML supervised the fieldwork at the Korle Bu Teaching Hospital. AKL them. In addition, participants were assured of privacy and confidentiality.
conducted the data analysis and drafted the first version of the manuscript.
AA and PAN contributed to the methods section of the paper. ML and AK Consent for publication
contributed to the interpretation of the clinical data. AK, ML, PAN, AA, and Participants’ consent was also obtained for the purposes of publishing the
MPKO all contributed equally to the discussion of the findings. DPL and EA results from the study. All the authors also consented to the study results to
contributed to the literature review and discussion sections of the manu- be published in the form presented in the final version of this manuscript.
script. All authors read and approve the final version of the manuscript.
Competing interests
Authors’ information The authors declare that they have no competing interests.
Amos Laar has demonstrated research interests spanning HIV, maternal,
infant, and young child nutrition. He has experience in planning,
implementing, and disseminating community-based research. He has been a Publisher’s Note
co-investigator of ten successful research grants at the University of Ghana Springer Nature remains neutral with regard to jurisdictional claims in
and has published several articles in refereed journals. published maps and institutional affiliations.
Awewura Kwara is an infectious diseases specialist, with training in Public
Health and Tropical Medicine. He is an associate professor of Medicine at Author details
1
Warren Alpert Medical School of Brown University. His clinical and research Department of Population, Family, & Reproductive Health, School of Public
2
interest is in management of HIV and TB coinfection. His research in the area Health, University of Ghana, Accra, Ghana. Department of Medicine,
of TB and HIV treatment has made important contributions to international University of Ghana School of Medicine & Dentistry, University of Ghana,
3
research efforts in the field of pharmacokinetics, pharmacogenetics, and Accra, Ghana. Department of Sociology, University of Ghana, Accra, Ghana.
4
drug-drug interactions between antiretrovirals and anti-TB drugs. Department of Epidemiology and Disease Control, School of Public Health,
5
Priscillia A. Nortey is a lecturer at the Department of Epidemiology and University of Ghana, Accra, Ghana. Department of Medicine, Warren Alpert
Disease Control, School of Public Health, University of Ghana, Accra, Ghana. Medical School of Brown University, Providence, RI, USA.
She is a clinical pharmacist who worked most of her professional life in the
public health delivery service of Ghana. In the last 10 years of her time in this Received: 28 December 2015 Accepted: 21 November 2018
service, she was mostly involved in the training of health personnel. She has
been part of the teams involved in the development of several health
management guidelines, notably guidelines for HIV and AIDS comprehensive References
care, pharmaceutical service, tuberculosis (TB), malaria, and training health 1. Onyango AC, Walingo MK, Mbagaya G, Kakai R. Assessing nutrient intake
personnel in the provision of these services. She has also been a core and nutrient status of HIV seropositive patients attending clinic at
member of the clinical team for renal transplant and scoliosis surgery. Chulaimbo Sub-District Hospital, Kenya. J Nutr Metab. 2012;2012:306530.
Augustine K. Ankomah is an associate professor of Public Health at the 2. Greene JB. Clinical approach to weight loss in the patient with HIV
Department of Population, Family & Reproductive Health, School of Public infection. Gastroenterol Clin N Am. 1988;17:573–86.
Health, University of Ghana, Legon, Accra. He has blend of academic, 3. Keating J, Bjarnason I, Somasundaram S, Macpherson A, Francis N, Price AB,
program implementation, research and consultancy experience in HIV and Sharpstone D, Smithson J, Menzies IS, Gazzard BG. Intestinal absorptive
reproductive health, with particular reference to most-at-risk populations. capacity, intestinal permeability and jejunal histology in HIV and their
Over the past 20 years, Professor Ankomah has conducted individual re- relation to diarrhoea. Gut. 1995;37:623–9.
search, led international multi-center collaborative research and evaluation, 4. Macallan DC: Dietary intake and weight loss patterns in HIV infection. In.,
published in peer-reviewed international journals, and presented at several edn.; 1999.
international conferences. 5. Villamor E, Saathoff E, Mugusi F, Bosch RJ, Urassa W, Fawzi WW. Wasting
Michael P.K. Okyerefo is a senior lecturer, Department of Sociology, University and body composition of adults with pulmonary tuberculosis in relation to
of Ghana. A trained sociologist with varied research interests, including a HIV-1 coinfection, socioeconomic status, and severity of tuberculosis. Eur J
focus on the nexus of religion and a host of socio-economic, political, and Clin Nutr. 2006;60:163–71.
health processes in contemporary Ghana, Dr. Okyerefo’s research centers on 6. Kotler DP. HIV infection and the gastrointestinal tract. AIDS. 2005;19:107–17.
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 11 of 12
7. Weiser SD, Fernandes KA, Brandson EK, Lima VD, Anema A, Bangsberg DR, 28. Liu JP, Manheimer E, Yang M. Herbal medicines for treating HIV infection
Montaner JS, Hogg RS. The association between food insecurity and and AIDS. Cochrane Database Syst Rev. 2005;3:CD003937.
mortality among HIV-infected individuals on HAART. J Acquir Immune Defic 29. Bonnard P. HIV/AIDS mitigation: using what we already know. Technical
Syndr. 2009;52:342–9. Note No. 5. Washington, DC.: Food and Nutrition Technical Assistance
8. Lemke S. Nutrition security, livelihoods and HIV/AIDS: implications for Project, Academy for Educational Development; 2002.
research among farm worker households in South Africa. Public Health 30. Boudreau T, Holleman C. Household food security and HIV/AIDS: exploring
Nutr. 2005;8:844–52. the linkages. The Food Economy Group; 2002.
9. Laar AK, Aryeetey R. Nutrition of women and children: focus on Ghana and 31. Tenkorang EY, Owusu AY, Laar AK. Housing and health outcomes of
HIV/AIDS. In: Stein N, editor. Public health nutrition principles and practice persons living with HIV/AIDS (PLWHAs) in the Lower Manya Krobo District,
in community and global health. Burlington MA: Jones & Bartlett; 2014. p. Ghana. J Health Care Poor Underserved. 2017;28(1):191–215. https://doi.org/
187–210. 10.1353/hpu.2017.0017.
10. Laar AK, Andrews NAE, Amoah-Ampah E, Laar M. Coping and hoping in 32. Ankomah A, Ganle JK, Lartey MY, Kwara A, Nortey PA, Okyerefo MPK,
HIV: the struggles of the Ghanaian HIV-positive. In: Marcus Bachman Laar AK. ART access-related barriers faced by HIV-positive persons linked
(Eds). Coping strategies and health. New York, NY: Nova Science Pub to care in southern Ghana: a mixed method study. BMC Infect Dis.
Inc; 2015. p. 87–126. 2016;16(1):738.
11. Blossner M, de Onis M. Malnutrition: quantifying the health impact at 33. Laar AK, El-Adas A, Amenyah RN, Atuahene K, Asare E, Tenkorang EY, Laar
national and local levels. WHO Environ Burden Dis Ser. 2005;12:1–43. M, Adjei AA, Quakyi I. Food and nutrition assistance to HIV-infected and
12. Grunfeld C, Pang M, Shimizu L, Shigenaga JK, Jensen P, KR F. Resting energy affected populations in Ghana: a situational analysis and stakeholder views.
expenditure, caloric intake, and short-term weight change in human Afr Geogr Rev. 2015;34(1):69–82.
immunodeficiency virus infection and the acquired immunodeficiency 34. Geocze L, Mucci S, De Marco MA, Nogueira-Martins LA, Citero Vde A.
syndrome. Am J Clin Nutr. 1992;55:455–4560. Quality of life and adherence to HAART in HIV-infected patients. Rev Saude
13. Hommes MJ, Romijn JA, Godfried MH, Schattenkerk JK, Buurman WA, Endert Publica. 2010;44(4):743–9.
E, Sauerwein HP. Increased resting energy expenditure in human 35. Lovejoy TI, Suhr JA. The relationship between neuropsychological
immunodeficiency virus-infected men. Metab Clin Exp. 1990;39:1186–90. functioning and HAART adherence in HIV-positive adults: a systematic
14. Mangili A, Murman DH, Zampini AM, Wanke CA. Nutrition and HIV infection: review. J Behav Med. 2009;32(5):389–405.
review of weight loss and wasting in the era of highly active antiretroviral 36. Malta M, Magnanini MM, Strathdee SA, Bastos FI. Adherence to antiretroviral
therapy from the nutrition for healthy living cohort. Clin Infect Dis. 2006;42: therapy among HIV-infected drug users: a meta-analysis. AIDS Behav. 2010;
836–42. 14(4):731–47.
15. Woods MN. Dietary recommendations for the HIV/AIDS patient. In: Miller TI, 37. Kish L, editor. Survey sampling 1985. New York: John Wiley & Sons; 1985.
Gorbach SL, editors. Nutritional aspects of HIV infection. New York: Oxford 38. Baum MK, Shor-Posner G, Lu Y, Rosner B, Sauberlich HE, Fletcher MA,
University Press; 1999. Szapocznik J, Eisdorfer C, Buring JE, Hennekens CH. Micronutrients and HIV-
16. Laar AK, Ampofo W, Tuakli JM, Wonodi C, Asante RK, Quakyi IA. Factors 1 disease progression. Aids. 1995;9(9):1051–6.
associated with suboptimal intake of some important nutrients among HIV- 39. Tang AM, Graham NM, Kirby AJ, McCall LD, Willett WC, Saah AJ. Dietary
positive pregnant adolescents from two Ghanaian districts. J Ghana Sci micronutrient intake and risk of progression to acquired immunodeficiency
Assoc. 2009;11:25–39. syndrome (AIDS) in human immunodeficiency virus type 1 (HIV-1)-infected
17. Laar AK, Tandoh A. Not infected but affected: the burden of aids-induced homosexual men. Am J Epidemiol. 1993;138(11):937–51.
food insecurity among HIV-affected households in Ghana. In: Garner R, 40. Meydani SN, Meydani M, Blumberg JB, Leka LS, Siber G, Loszewski R,
editor. Food insecurity: patterns, prevalence and risk factors. New York, NY: Thompson C, Pedrosa MC, Diamond RD, Stollar BD. Vitamin E
Nova Science Pub Inc; 2016. supplementation and in vivo immune response in healthy elderly subjects.
18. Garcia J, Hromi-Fiedler A, Mazur RE, Marquis G, Sellen D, Lartey A, Perez- A randomized controlled trial. Jama. 1997;277(17):1380–6.
Escamilla R. Persistent household food insecurity, HIV, and maternal stress in 41. Beharka A, Redican S, Leka L, Meydani SN. Vitamin E status and immune
peri-urban Ghana. BMC Public Health. 2013;13:215. function. Methods Enzymol. 1997;282:247–63.
19. Lima VD, Harrigan R, Bangsberg DR, Hogg RS, Gross R, Yip B, Montaner JS. 42. Kaiser JD, Campa AM, Ondercin JP, Leoung GS, Pless RF, Baum MK.
The combined effect of modern highly active antiretroviral therapy Micronutrient supplementation increases CD4 count in HIV-infected individuals
regimens and adherence on mortality over time. J Acquir Immune Defic on highly active antiretroviral therapy: a prospective, double-blinded, placebo-
Syndr. 2009;50(5):529–36. controlled trial. J Acquir Immune Defic Syndr. 2006;42(5):523–8.
20. Laar AK, Kwara A, Nortey PA, Ankomah A, Okyerefo MP, Lartey MY. Use of 43. Fawzi WW. The benefits and concerns related to vitamin a
non-prescription remedies by Ghanaian HIV-positive persons on supplementation. J Infect Dis. 2006;193(6):756–9.
antiretroviral therapy. Front Public Health. 2017;5:115. 44. Bukusuba J, Kikafunda JK, Whitehead RG. Nutritional knowledge, attitudes,
21. Roca B, Gomez CJ, Arnedo A. A randomized, comparative study of and practices of women living with HIV in eastern Uganda. J Health Popul
lamivudine plus stavudine, with indinavir or nelfinavir, in treatment- Nutr. 2010;28(2):182–8.
experienced HIV-infected patients. Aids. 2000;14(2):157–61. 45. Vorster HH, Venter CS, Wissing MP, Margetts BM. The nutrition and health
22. Shevitz AH, Knox TA. Nutrition in the era of highly active antiretroviral transition in the north West Province of South Africa: a review of the THUSA
therapy. Clin Infect Dis. 2001;32(12):1769–75. (Transition and Health during Urbanisation of South Africans) study. Public
23. FAO/WHO. Living well with HIV/AIDS: a manual on nutritional care and Health Nutr. 2005;8(5):480–90.
support for people living with HIV/AIDS. Rome. Available at URL: http:// 46. Holcomb CA. Positive influence of age and education on food consumption
www.fao.org/3/a-y4168e.pdf. Accessed June, 2015; 2002. p. 97. and nutrient intakes of older women living alone. J Am Diet Assoc. 1995;
24. Weiser SD, Young SL, Cohen CR, Kushel MB, Tsai AC, Tien PC, Hatcher AM, 95(12):1381–6.
Frongillo EA, Bangsberg DR. Conceptual framework for understanding the 47. Kalichman SC, Cherry C, White D, Jones M, Kalichman MO, Detorio MA,
bidirectional links between food insecurity and HIV/AIDS. Am J Clin Nutr. Caliendo AM, Schinazi RF. Use of dietary supplements among people living
2011;94(6):1729S–39S. with HIV/AIDS is associated with vulnerability to medical misinformation on
25. Ibeh BO, Omodamiro OD, Ibeh U, Habu JB. Biochemical and haematological the internet. AIDS Res Ther. 2012;9(1):1.
changes in HIV subjects receiving winniecure antiretroviral drug in Nigeria. J 48. Fawzi WW, Msamanga GI, Spiegelman D, Urassa EJ, McGrath N, Mwakagile
Biomed Sci. 2013;20:73. D, Antelman G, Mbise R, Herrera G, Kapiga S, et al. Randomised trial of
26. Mills E, Wu P, Johnston BC, Gallicano K, Clarke M, Guyatt G. Natural health effects of vitamin supplements on pregnancy outcomes and T cell counts
product-drug interactions: a systematic review of clinical trials. Ther Drug in HIV-1-infected women in Tanzania. Lancet. 1998;351(9114):1477–82.
Monit. 2005;27(5):549–57. 49. Semba RD, Tang AM. Micronutrients and the pathogenesis of human
27. Bormann JE, Uphold CR, Maynard C. Predictors of complementary/ immunodeficiency virus infection. Br J Nutr. 1999;81(3):181–9.
alternative medicine use and intensity of use among men with HIV 50. Sachdeva RK, Sharma A, Wanchu A, Dogra V, Singh S, Varma S. Dietary
infection from two geographic areas in the United States. J Assoc Nurses adequacy of HIV infected individuals in north India--a cross-sectional
AIDS Care. 2009;20(6):468–80. analysis. Indian J Med Res. 2011;134(6):967–71.
Laar et al. Journal of Health, Population and Nutrition           (2018) 37:26 Page 12 of 12
51. Baum MK, Shor-Posner G, Zhang G, Lai H, Quesada JA, Campa A, Jose-
Burbano M, Fletcher MA, Sauberlich H, Page JB. HIV-1 infection in women is
associated with severe nutritional deficiencies. J Acquir Immune Defic Syndr
Hum Retrovirol. 1997;16(4):272–8.
52. Coodley GO, Loveless MO, Merrill TM. The HIV wasting syndrome: a review.
J Acquir Immune Defic Syndr. 1994;7(7):681–94.
53. Gorbach SL, Knox TA. Weight loss and human immunodeficiency virus
infection: cachexia versus malnutrition. Infect Dis Clin Pract. 1992;1(4):224–9.
54. WHO. Micronutrients and HIV infection: a review of current evidence.
Geneva: World Health Organisation; 2005. p. 55.
55. Dewey KG, Domellof M, Cohen RJ, Landa Rivera L, Hernell O, Lonnerdal B.
Iron supplementation affects growth and morbidity of breast-fed infants:
results of a randomized trial in Sweden and Honduras. J Nutr. 2002;132(11):
3249–55.
56. Sazawal S, Black RE, Ramsan M, Chwaya HM, Stoltzfus RJ, Dutta A, Dhingra
U, Kabole I, Deb S, Othman MK, et al. Effects of routine prophylactic
supplementation with iron and folic acid on admission to hospital and
mortality in preschool children in a high malaria transmission setting:
community-based, randomised, placebo-controlled trial. Lancet. 2006;
367(9505):133–43.
57. Shah M, Tierney K, Adams-Huet B, Boonyavarakul A, Jacob K, Quittner C,
Dinges W, Peterson D, Garg A. The role of diet, exercise and smoking in
dyslipidaemia in HIV-infected patients with lipodystrophy. HIV Med. 2005;
6(4):291–8.
58. Nti CA, Hayford J, Opare-Obisaw C. Nutrition knowledge, diet quality and
nutritional status of people living with HIV (PLHIV) in Ghana. Food Public
Health. 2012;2(6):219–27.
59. Laar A, Manu A, Laar M, El-Adas A, Amenyah R, Atuahene K, Quarshie D,
Adjei AA, Quakyi I. Coping strategies of HIV-affected households in Ghana.
BMC Public Health. 2015;15:166.
60. Sztam KA, Fawzi WW, Duggan C. Macronutrient supplementation and food
prices in HIV treatment. J Nutr. 2010;140(1):213S–23S.