Sero-epidemiology of human T-cell lymphotropic viruses-1 and -2 infection among pregnant women attending Abuja Teaching Hospital,Nigeria

Abstract

BACKGROUND:

There is the paucity of HTLV-1/-2 studies on Nigerian pregnant women despite the medical and public health significance of maternal-to-child transmission of HTLV-1/-2.

OBJECTIVE:

This study aims to determine the seroprevalence and risk factors of HTLV-1/-2 infections among pregnant women attending the University of Abuja Teaching Hospital (UATH), Abuja, Nigeria.

MATERIALS AND METHODS:

Blood samples were collected from consented pregnant women and analysed for ant-HTLV-1/-2 total antibodies using a commercial Enzyme-Linked Immunosorbent Assay (ELISA) kit. Pretested structured questionnaires were used to collate participants’ socio-demographic variables and risk factors of HTLV infection.

RESULTS:

Out of the 156 pregnant women tested for HTLV-1/-2 antibodies, 16 (10.3%) were seropositive. There was no significant association between the socio-demographic variables collated and seroprevalence of HTLV-1/-2 infection among pregnant women ( $p>$ 0.05). Pregnant women with HIV infection had a lower prevalence of HLTV-1/-2 infection than those without HIV infections (7.5% versus 11.7%). Pregnant women with multiple sexual partners had a higher risk of HTLV-1/-2 infection than those who had single (OR $=$ 2.08, 95% CI: 0.53–8.18). Women with a history of needles injury had a higher risk of HTLV-1/-2 infection than those who do not (OR $=$ 1.24, 95% CI: 0.38–4.08). The history of blood transfusion was significantly associated with HTLV-1/-2 infection ( $p=$ 0.027). However, no significant association existed between other risk factors of HTLV-1/-2 infection among pregnant women ( $p>$ 0.05).

CONCLUSION:

Considering the 3% pooled national prevalence of HTLV-1/-2 infection in Nigeria, the seroprevalence reported in this study is relatively high. Thus, there is a need for more large cohort studies and routine screening of population at increased risk of infection.

Keywords

Retroviruses vertical transmission serological survey HTLV maternal infection Nigeria

1. Introduction

Just like other human retroviruses, human T cell Lymphotropic virus-1 (HTLV-1) causes a lifelong infection of T-lymphocytes, in particular, CD4 $+$ T cells [1]. However, unlike HIV, the immunological hallmark of HTLV-1-infected individuals is a sustained proliferation of T-cells driven by the HTLV-1-encoded Tax protein [1]. The subsequent transactivation of cellular genes by the Tax-encoded region can result in malignant transformation [1].

Recent researches suggest that the incidence of HTLV-1/2 linked diseases might be even higher than the literature traditionally reports due to the influence of local factors in their pathogenesis [1].

Epidemiologically, there are three main routes of HTLV-1/2 transmission; sexual intercourse, infected blood or blood products, and mother-to-child (vertical transmission – VT). In endemic areas, VT remains the most important mode of transmission, since it occurs in up to 25% of the children who are breastfed by seropositive women. Greater efficacy of VT is associated with the length of breastfeeding, high antibody titers and high proviral load in maternal blood [2].

Mother-to-child transmission (MTCT) is the predominant route in endemic areas. HTLV-1 seroprevalence increase with age, especially among women [3].

The MTCT of HTLV-1 could cause lifelong or persistent infection. At least 5–10 million individuals worldwide are currently living with HTLV-1. Studies of regional variation are required to understand the roles of MTCT to the global burden of HTLV-1/2 infection. Although most infected individuals remain asymptomatic, $\sim$ 10% develop morbidity and 2% mortality [3].

Adequate prevention of MTCT significantly contributes to disproportionately reduction in both the incidence of HTLV-1 and burden of HTLV-1 associated diseases. To successfully avoid MTCT of HTLV, it is essential to understand all the variables that predispose MTCT HTLV infection. Questions remain regarding the frequency and risk factors for in-utero peripartum transmission whilst little is known about the efficacy of prelabor cesarean section to reduce these infections [3]. Understanding the contribution of peripartum infection to the burden of the disease will be essential to gauge the risk-benefit of interventions in this area. Whilst breastfeeding is strongly associated with transmission and avoidance of breastfeeding a proven intervention, little is known about the mechanism of transmission from the breast milk to the infants [3].

Nigeria is as an endemic nation for HTLV-1 infection with seroprevalence that varies considerably between sex, age and region [4, 5]. Given its national dimensions, Nigeria is top 10% countries with the highest number of HTLV-1/2 prevalence in the world [6].

An estimated 3% pooled national prevalence of HTLV-1 in Nigeria was reported from a recent meta-analysis and systematic [6]. However, individual studies have reported as from 0% to 11.5% [7, 8]. Furthermore, even in Africa, the seroprevalence for HTLV-1/2 in pregnant women can vary widely from 0.2% in South Africa, with places of intermediate prevalence such as the Republic of Congo (0.7%) [8, 9]. Such discrepancy in prevalence is a result of both the epidemiological characteristic of the infection, which has endemic clusters alongside low prevalence areas, and the gap in HTLV knowledge since vast areas of the country remain unstudied. Additionally, most of the studies are on potentially biased populations such as low-risk voluntary blood donors or high-risk IV drug users and sex clinic attendees [2, 9].

Intermediate seroprevalence rates have been found in pregnant women [2, 9]. Although not devoid of bias, this group has been proposed to represent a more reliable portrait of the general population since their prevalence data are generally able to characterise geographic areas likely to be endemic [10, 11]. Unfortunately, there is no nationwide data on the seroprevalence of HTLV-1/2 in Nigeria pregnant women since the Ministry of Health does not recommend screening as part of the routine antenatal care.

Intrauterine HTLV1 transmission during childbirth causes less than 5% of vertical transmission, and if breastfeeding was done, the transmission increases up to 25% [10]. Vertical transmission of HTLV1 infection occurs mainly via mother’s milk, and in breastfeeding longer than 6 months, transmission risk is to be 3-fold or more [12].

Since there is currently no cure, effective treatment or immunisation for HTLV-1/2 infection and its complications, more accurate knowledge about its prevalence is helpful in the elaboration of public policies on educational and prophylactic measures to increase awareness and reduce the rates of viral transmission and the incidence of infection-related diseases.

Pregnant women have been demonstrated to undergo immunosuppression due to several factors. An increasing body of evidence suggests that HTLVs may cause some degree of immunosuppression [4], leading to a higher risk of HTLV transmission and expansion. An increased prevalence of the virus infection, as well as higher mortality among pregnant women, is described by a previous study [9]. The relative importance of MTC mode of transmission is still mostly unknown, and most likely, it varies with the population involved. In endemic areas such as Japan, MTC transmission has been described as the primary source of transmission (mainly through breastfeeding) [13]. Only 2.5–5.0% of children are seroconverted in the absence of breastfeeding. In comparison, up to 25% are infected if breastfed for over 12 months [14]. In fact, a Brazilian study found a vertical transmission rate of 50% in children who were breastfed for over 24 months [14]. This study aims to determine the seroprevalence and risk factors of HTLV-1&-2 infection among pregnant women attending the University of Abuja Teaching Hospital, Abuja, Nigeria.

2. Materials and methods

2.1 Study area

This study was conducted at the University of Abuja Teaching Hospital (UATH), Gwagwalada, Federal Capital Territory (FCT) Abuja, Nigeria. Gwagwalada is about 45 km away from the FCT. It is one of the six area council headquarters of the FCT. The town lies in the downstream of River Usuma and is located between latitude 8 ${}^{\circ}$ 55’ and 9 ${}^{\circ}$ 00’N and longitudinal 7 ${}^{\circ}$ 00’ and 7 ${}^{\circ}$ 05’E.

The centrality of this town in relation to other area councils’ headquarters makes it influential and important in various socio-economic activities. The climate condition of this town is not far-fetched from that of the tropics having several climatic elements in common; most especially the wet and dry season characteristic. The temperature of the area ranges from 30 ${}^{\circ}$ C to 37 ${}^{\circ}$ C yearly, with the highest temperature experienced in the month of March and mean total rainfall of approximately 1650 mm/annum.

About 60% of this rain falls between May to August. The area council is an industrial zone of FCT that stands out as the second most cosmopolitan city of the FCT, after the capital city with 10 political wards and consist of over 26 Federal organisations which include the University of Abuja, University of Abuja Teaching Hospital etc. These have brought about the inflow of people into the council.

2.2 Study population

This study comprised of pregnant women $\geqslant$ 18 years attending the UATH. All consenting participants without diabetes and history of Tuberculosis were included in the study. All participants were screened, and their HIV status confirmed using Uni-Gold Recombigen ${}^{\@setsize{\scriptsize}{8pt}{\viipt}{\@viipt}{\textregistered}}$ HIV-1/2 (Trinity Biotech, Wicklow, Ireland) and Determine ${}^{\text{TM}}$ (Alere, Auckland City, New Zealand) proprietary reagents. Non-consenting women and those living with TB infection or diabetes mellitus were excluded from the study.

2.3 Study design

This was a hospital based cross-sectional study.

2.4 Data collection

Data for this study were collected through a structured questionnaire to assess participants’ biodata, socio-demographic, as well as the participants’ medical history.

2.5 Sample size calculation

The sample size was determined using the Fischer’s formula for cross sectional studies:

$n=\frac{Z^{2}Pq}{d^{2}}$ $n=$ minimum sample size $z=$ percentage point of standard normal distribution curve which defines 95% confidence interval as (1.96) constant. $p=$ prevalence from previous study as reported by Udeze et al. [9]; 1.1%. $d=$ sampling error allowed at 95% confidence limit i.e., 0.05. $q=(1-p)1-0.011=0.989$ $n=\frac{(1.96)^{2}0.011\times 0.989}{(0.05)^{2}}$ $n=\frac{0.04286}{0.0025}$ $n=$ 17.1 $n=$ 17 $n=$ 17

Thus, the minimum sample size of participants for this study was calculated as 17. However, this number was increased to a total of 156 pregnant women.

2.6 Participants sampling technique

Participants for the study were randomly enrolled.

2.7 Sample collection, preparation and storage

About 5mls of whole blood were collected aseptically from each participant using standard venipuncture. Samples were dispensed into appropriately labelled screw-capped containers and were left at room temperature for about an hour, after which it was spun at 3,000 rpm for 10 minutes to separate serum from blood clot. Serum was dispensed into corresponding labelled plain containers and stored at $-$ 20 ${}^{\circ}$ C until needed for assay. Samples were collected between from 7 ${}^{\text{th}}$ April to 10 ${}^{\text{th}}$ October 2019. Blood samples were analysed within 1 hour of collection.

2.8 Laboratory analytical procedures

2.8.1 The analytical method for the detection of anti-HTLV1/2

ELISA was carried out according to the method described by the kit manufacturer (Dia.Pro HTLV-I/II Ab Ultra, San Giovanni, Italy) The HTLV ELISA test was a three-incubation process whereby the first incubation involved the coating of the wells with HTLV antigen. During this step, any antibodies that are reactive with the HTLV antigens, bound to the wells. Next, the wells were washed to remove the test sample. At this point Enzyme Conjugate was added. During this second incubation, the Enzyme Conjugate bound to all antibodies present (IgA, IgG or IgM). Before the third incubation step, 3 cycles of washings were done. Then a chromogen (tetramethylbenzidine) was added. With the presence of Enzyme Conjugate and the peroxidase, causing the consumption of peroxide, the chromogen changed to a blue colour. The blue colour turned to a bright yellow colour after the addition of the stop solution, which ends the reaction. ELISA reader was used to the optical density of the final coloured product. Subsequently, the results were calculated. Test effectiveness: the average value of positive control $\geqslant$ 1.00; the average value of negative control $\leqslant$ 0.10. The critical value (CUT OFF) calculation: critical value $=$ the average value of negative control $+$ 0.15 Negative judgement: if the OD value $<$ CUT OFF, the sample is HTLV-1+2 negative. Positive judgement: if the OD value $\geqslant$ CUT OFF, the sample is HTLV-1/-2 positive.

2.9 Statistical analysis

Data obtained were analysed using the Statistical Package for Social Sciences (SPSS) software version 26 (IBM Corporation, Armonk, NY, USA). Continuous variables were presented as mean $\pm$ standard deviation (SD). Chi-squared test was used to compare the association between socio-demographic and risk factors and seroprevalence of HTLV-1/-2 antibodies. Bivariate logistic regression was used to compute the odds ratios (OR) as risk factors of HTLV-1/-2 infection among pregnant women. $p\leqslant$ 0.05 at a confidence interval of 95% were considered statistically significant.

Figure 1.

Seroprevalence of HTLV-1/-2 antibodies among pregnant women under study.

Table 1

Sero-prevalence of HTLV-1/2 by socio-demographic variables of pregnant women ( $n=$ 156)

Variables	Total no. tested	No. HTLV-1/-2 positive (%)		Chi-squared	$p$ value
Mean $\pm$ SD age (range)	29.4 $\pm$ 4.8 (18–43)
Age range (years)
18–28	65	7	(10.8)
29–38	88	9	(10.2)
39–48	3	0	(0.0)	0.36	0.835
Educational level
No formal education	2	0	(0.0)
Primary	13	0	(0.0)
Secondary	47	7	(14.9)
Tertiary	94	9	(9.6)	2.86	0.413
Residential area
Rural	51	7	(14.0)
Suburb	61	5	(8.2)
Urban	44	4	(9.1)	1.22	0.748
Monthly income (US$)
$<$ 100	65	6	(9.2)
100–199	71	10	(14.1)
200–300	16	0	(0.0)
$>$ 300	4	0	(0.0)	3.49	0.322
Occupation
Farmer	3	0
Self-employed	9	1	(11.1%)
Housewife	52	6	(11.5)
Civil servant	50	5	(10.0)
Unemployed	42	4	(9.5)	0.471	0.976
Marital status
Married	123	14	(10.2)
Divorced	6	0	(0.0)
Single	11	2	(15.4)	1.06	0.589
Household density (persons per household)
1–4	107	9	(8.4)
5–8	42	6	(14.3)
$\geqslant$ 9	7	1	(14.3)	1.26	0.533

Table 2

Risk factors analysis of HTLV-1/2 among pregnant women ( $n=$ 156)

Risk factors	HTLV-1/2 negative	HTLV-1/2 positive	OR (95% CI)	$p$ value
History of body tattoo
Yes	2	0 (0.0)	0.596 (0.03–12.9)	0.742
No	138	16 (10.4)	1
History of blood transfusion
Yes	54	11 (16.9)	0.29 (0.09–0.867)	0.027 ${}^{*}$
No	86	5 (5.5)	1
Sexual partner
Single	126	13 (9.4)	2.08 (0.53–8.18)	0.296
Double	14	3 (17.6)	1
Scarification
Yes	25	4 (13.8)	0.65 (0.19–2.19)	0.489
No	115	12 (9.4)	1
HIV status
Seronegative	91	12 (11.7)	0.62 (0.19–2.02)	0.427
Seropositive	49	4 (7.5)	1
History of needle injury
Yes	41	4 (8.9)	1.24 (0.38–4.08)	0.720
No	99	12 (10.8)	1
Parity
3	29	6 (17.1)	0.32 (0.07–1.36)	0.122
2	65	7 (9.7)	0.65 (0.15–2.47)	0.484
1	46	3 (6.1)	1
Trimester
1 ${}^{\text{st}}$	42	6 (12.5)	0.44 (0.07–2.82)	0.388
2 ${}^{\text{nd}}$	78	9 (10.3)	0.49 (0.07–3.28)	0.462
3 ${}^{\text{rd}}$	20	1 (4.8)	1

3. Results

This cross-sectional study involved women between the age range of 19–43 years and mean $\pm$ SD of 29.4 $\pm$ 4.8 years. Out of the 156 pregnant women screened for HTLV-1/-2 antibodies, 16 (10.3%) were seropositive (Fig. 1). The seroprevalence of anti-HTLV-1/-2 was highest among pregnant women between 18–28 years, 10.8%, followed by those between 29–38 years, 10.2% and none of those between 39–48 years had HTLV-1/-2 antibodies. The seroprevalence of anti-HTLV-1/-2 was highest among pregnant women with secondary education, 14.9%, followed by those with tertiary education, 9.6% and none of those primary and no formal education had HTLV-1/-2 antibodies. The rural resident had the highest seroprevalence of HTLV-1/-2, 14.0% and least in those in the suburban settlements, 8.2%. All the pregnant women with serological evidence of HTLV-1/-2 infection had monthly income of 200 USD, 11.8% whereas none of those with 200 USD monthly income had HTLV-1/-2 antibodies. Women who are full housewives had the highest seroprevalence of HTLV-1/-2, 11.5% and least among farmers (0.0%). Pregnant women who were unmarried singles had relatively higher seroprevalence of HTLV-1/-2, 15.4% than the married ones, 10.2%. However, none of the divorces had detectable HTLV-1/-2 antibodies. It appeared that pregnant women in densely populated households ( $>$ 5 persons) had the highest seroprevalence of HTLV-1/-2, 14.3% than the sparsely populated (1–4 persons) household, 8.5% (Table 1). However, there is no significant association between all the socio-demographic variables and seroprevalence of HTLV-1/-2 infection among pregnant women ( $p>$ 0.05).

Pregnant women with HIV infection had a lower prevalence of HLTV-1/-2 infection that those without HIV infections (7.5% versus 11.7%) (Table 2). As regards the risk factor analysis, after bivariate logistic regression pregnant women who multiple sexual partners had a higher risk of HTLV-1/-2 infection than those who had single (OR $=$ 2.08, 95% CI: 0.53–8.18) (Table 2). Women with a history of needles injury had a higher risk of HTLV-1/-2 infection than those who do not (OR $=$ 1.24, 95% CI: 0.38–4.08) (Table 2). All other risk factors studied showed lesser ORs of HTLV-1/-2 infection among the cases than the controls. The history of blood transfusion was significantly associated with HTLV-1/-2 infection ( $p=$ 0.027). However, no significant association existed between other risk factors of HTLV-1/-2 infection among pregnant women ( $p>$ 0.05) (Table 2).

4. Discussion

Based on available reports, Human T-Cell Lymphotropic Virus -1/-2 (HTLV-1/-2) infections appear to have varied epidemiological pattern among different study populations. However, there is a paucity of studies on pregnant women. In cognisance of the medical and public health significance of maternal-to-child transmission of HTLV-1/-2. Pregnant women are significant sources of transmission of HTLV-1/-2 infection, either to their spouses or fetuses [15]. The seroprevalence of HTLV-1/-2 infection among pregnant women in this study was 10.3%. This value is higher than the previous Nigerian reports from most cross-sectional studies. For instance, 0.5% was reported by Olusola et al. [16], 0% by Iyalla et al. [17], 0.5% Okoye et al. [18] and 3.2% by Hananiya et al. [19]. However, it was lower than the 24.2% reported by Opaleye et al. [20], 14.3% by Abu et al. [21] and 16.7% by Forbi and Odetunde [22].

These variations could be due to changes in the endemicity of HTLV with the time of previous studies, differences in the test performances and accuracies of the commercial kits employed. Most of these studies, including the present study, used enzyme immunoassays. Of which, some detect only a class of the immunoglobulin (either IgM or IgG). However, our detected the total Ig in samples tested. This observation could explain the relatively higher seroprevalence we recorded in our study. For now, there is no ample justification for routine screening of pregnant women for HTLV-1/-2 during antenatal care, as further studies on the cost/benefit will be needful in Nigeria through largescale and comprehensive studies. Even though most HTLV infections are latent and subclinical, there might be cases of underdiagnosis by healthcare professionals.

Several studies have been able to identify socio-demographic variables such as age, sex, education, household socio-economic condition as critical determinants of contracting of HTLV [4, 18]. Findings from the present showed that the seroprevalence of HTLV-1/-2 declined with the age of participants. Of which the highest seroprevalence was in women between 18–28 years. However, it was not statistically associated with the prevalence of HTLV-1/-2 antibodies. This finding is consistent with that of Hananiya et al. [19] who reported higher seroprevalence among pregnant women aged 15–25 years.

In relation to marital status, a higher seroprevalence was observed among pregnant women who were single than the married ones. This status may give room for multiple sexual partners. This was further buttressed by the higher prevalence of HTLV-1/-2 in women with dual sexual partners than those with single. Similar findings have been reported by Zehender et al. [23] and Fox et al. [24]. This highlights the role of sexual intercourse in the transmission of HTLV infection in pregnant women.

In this study, history of blood transfusion was a significant risk factor of HTLV-1/-2 infection. Similar findings were reported by Iyalla et al. [17]. The time interval between blood transfusion and development of HTLV-1-associated myelopathy is also short in immunocompromised individuals [25, 26]. This represents another area of further research on transfusion transmissible HTLV infection in immunocompromised person due to physiological process such as pregnancy. Although, Nigeria’s policy on blood transfusion is still restricted to only hepatitis-B, -C viruses, HIV and treponema pallidum, there need to consider the inclusion of other life-threatening pathogens such as HTLV to ensure blood transfusion safety.

From this study, the prevalence of HIV and HTLV-1/ -2 coinfection was 7.5%. However, the seroprevalence of HTLV-1/-2 was higher in HIV seronegative women. This is lower than the 32.6% and 25.7% anti-HTLV-IgG and -IgM the reported by Adeoye et al. [27], but higher than the 4.1% reported by Nasir et al. [4]. Furthermore, we reported more HTLV-1/-2 seroprevalence among HIV patients than HIV seronegative women. First, the variations in seroprevalence of HIV/HTLV-1/-2 in these studies could be due to the antiretroviral statuses of the subjects. Secondly, the lesser HTLV-1/-2 seroprevalence in HIV seropositive women in our study could be the influence of ART on both pathogens. It has been demonstrated that the current highly active antiretroviral therapy (HAART) regimen could contain the replication of HIV and other retroviruses such as HTLV [28].

5. Conclusion

Considering the 3% pooled national prevalence of HTLV-1/-2 infection in Nigeria, the seroprevalence reported in this study is quite high. Thus, there is a need for larger cohort studies and routine screening of population at high risk of infection with the view to monitor its endemicity.

Availability of data and material

The data that support the findings of this study are available from the corresponding author on reasonable request.

Ethics declaration and consent to participate

Before the commencement of this study, ethical approval was obtained from the human research ethical committee of the University of Abuja Teaching Hospital, Gwagwalada, Abuja, Nigeria. All the study procedures were done in accordance with the Helsinki Declaration of Human experimental research as revised in 2003. Written and signed informed consent was provided by all participants.

Consent for publication

All subjects gave approval for publication of data.

Competing interests

Authors declare that they have no competing interests.

Authors contributions

AD, INA (Overall Study implementation coordinator). AM, INA, OMAB and AUE conceived the study. INA and AD oversaw implementation of the study. INA, AUE, AUA, JMA, PEG, and OSA performed the analysis. INA, AUE, AUA, JMA, OMAB, PEG, and OSA wrote the first and final draft. All authors read and approved the final manuscript.

Funding

None received.

Footnotes

Acknowledgments

Authors appreciate the technical support provided by the University of Abuja Teaching Hospital and staff of Labcrest laboratory, Abuja.

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