|Year : 2020 | Volume
| Issue : 1 | Page : 64-68
Seroepidemiology of human parvovirus B19 among pregnant women in Erbil, Iraq
Nabaz Ahga1, Kawthar Alharmni2, Zakarea Alkhayat3
1 Department of Prevention Health, Erbil Medical Technical Institute, Erbil Polytechnic University, Erbil, Iraq
2 Department of Anatomy and Histology, College of Medicine, Hawler Medical University, Erbil, Iraq
3 Department of Microbiology, College of Medicine, Hawler Medical University, Erbil, Iraq
|Date of Submission||16-Oct-2019|
|Date of Acceptance||24-Dec-2019|
|Date of Web Publication||17-Mar-2020|
Dr. Zakarea Alkhayat
Department of Microbiology, College of Medicine, Hawler Medical University, Erbil
Source of Support: None, Conflict of Interest: None
Background: Human parvovirus B19 (HPV B19) is a member of the family Parvoviridae. It can be transmitted congenitally from an infected mother to the embryo. The virus has been implicated in hydrops fetalis, spontaneous abortion, aplastic crisis, and acute symmetric polyarthropathy. Objective: The present study was carried out to determine the seroprevalence of HPV B19 immunoglobulin G (IgG) and immunoglobulin M (IgM) antibodies among apparently healthy pregnant women and to define the risk factors associated with. Materials and Methods: Blood samples were collected from consenting pregnant women who were attending Erbil Maternity hospitals from the period between January 2018 and June 2019. The sera were obtained from samples were analyzed for IgG and IgM antibodies of HPV B19 using (EUROIMMUN AG, Luebeck Germany) ELISA Classic Parvovirus B19 IgG/IgM kits. Structured questionnaire was used to obtain data on sociodemography and risk factors. Results: A total of 349 pregnant women were enrolled in this study and were screened for both IgM and IgG antibodies. Overall, 139 (39.8%) were positive for parvovirus B19 IgG and 32 (9.2%) had IgM antibody. Demographics including age group, occupation, number of children, and trimester of pregnancy. The differences of distribution of the Parvovorus IgG in relation to the above-mentioned demography were as follows: age >35 years: highly significant (P ≤ 0.01), second trimester: nonsignificant, homemakers: highly significant (P ≤ 0.01), ≥5 children highly significant (P ≥ 0.01). The differences of distribution of the Parvovorus IgM in relation to the above-mentioned demography were as follows: age <20 years: significant (P ≤ 0.05), second trimester: nonsignificant, homemakers: highly significant (P ≤ 0.01), ≥5 children: significant (P ≥ 0.05). Conclusions: HPV B19 is prevalent in Erbil, Iraq. More than half (51%) of the women were IgG negative, so they are susceptible to the HPV B19 infection. Hence, there is a need for routine screening for B19 IgM antibodies for all women of childbearing age and subsequent clinical management of positive cases.
Keywords: Human parvovirus B19, pregnant women, seroprevalence
|How to cite this article:|
Ahga N, Alharmni K, Alkhayat Z. Seroepidemiology of human parvovirus B19 among pregnant women in Erbil, Iraq. Med J Babylon 2020;17:64-8
| Introduction|| |
Human parvovirus B19 (HPV B19) belongs to the parvovirus genus of the family Parvoviridae, which constitutes the smallest and the simplest of the known DNA viruses. It has a diameter of 23 nm and comprises a single-stranded DNA genome (5.5 kb). The viruses in the parvo-virus genus are species specific and thus human parvovirus B 19 is the only recognized pathogenic parvovirus in humans. HPV B19 causes a number of clinical maladies including infectious erythema (fifth disease), hydrops fetalis, transient aplastic crises, arthropathy, and congenital aplasia. Transmission of infection takes place by means of respiratory route and blood-derived products administered parenterally and vertically from mother to fetus. Assessment of population predisposition to human parvovirus is useful in considering the risk to pregnant women, because primary prevention is not feasible as no vaccines against parvovirus B19 infection are currently approved. On the other hand, the dearth of the exemplary rash pattern in a large portion of patients infected with parvovirus B19 and the resemblance of clinical manifestations to other rash diseases, especially to rubella highlight the difficulty of diagnosing B19 infection clinically alone. In general, diagnosis of parvovirus is based on clinical symptoms and serologic antibody testing for parvovirus immunoglobulin G (IgG) and parvovirus immunoglobulin M (IgM)., Past infection can be assured by the presence of IgG antibodies. Acute infection is revealed by the existence of IgM antibodies., The seroprevalence of HPV B19 appears to be variable worldwide. Various factors are recognized to impact seroprevalence including age, geography, climate, socioeconomic status, occupation, race, parity, and working among children.
This study was an attempt to investigate the prevalence and incidence of Human Parvovirus 19 IgG and IgM, respectively, with a possible relation with different demographic factors in a sample of apparently healthy pregnant Iraqi women in Erbil city, Iraq.
| Materials and Methods|| |
This was a cross-sectional study which was performed from the period between January 2018 and June 2019. The study population included pregnant women attending the antenatal clinics in Erbil Maternity hospitals in Erbil city.
This study was approved by the Ethics Committee of Erbil Medical Technical Institute, Erbil Polytechnic University, Iraq, Health Directorate of Erbil, and College of Medicine Hawler Medical University. Informed consent was obtained from each woman in addition to their husbands or relatives before inclusion in the study. Before the blood sample was collected, the procedure was thoroughly explained to every person to ensure that they understood exactly what was going to happen. It was also pointed out to the individuals that they could refuse to participate in the study without prejudice.
Apparently healthy pregnant women with no previous history of abortion were selected by simple random method, ranging in age from 18 to 41 years and at various trimesters of pregnancy were included in this study. All pregnant women whose gestation ages were unknown and who had transfused with blood were excluded from the study. Before sample collection, clinical information, demographic information, and data on possible risk factors were collected from the women using structured questionnaires.
Five milliliters (5 ml) of venous blood was aseptically collected from each subject. Serum was separated into Eppendorf tubes after centrifugation then stored at −20°C till needed for analysis. Quantitative determination of IgG and semi-quantitative determination of IgM antibodies against Parvovirus B19 in human serum were measured using ELISA kits (EUROIMMUN AG, Luebeck Germany). Purified antigens are coated to a micro well plate. Antibodies in the patient samples bind to the antigens and are determined during the second incubation step by using enzyme-labeled anti-human antibodies (the conjugate). The enzyme converts the colorless substrate (H2O2/TMB) to a blue end product. The enzyme reaction is stopped by adding sulfuric acid and the color of the mixture switches from blue to yellow at the same time. The final measurement is carried out at 450 nm on a photometer using a reference wavelength ≥620 nm. Interpretations of the results were done according to the instruction of the manufacturer as follows:
- IgG: Negative (antibody level <0.4 IU/mL), equivocal (antibody level <5.5 IU/mL) positive (antibody level >5.5 IU/mL)
- IgM: Negative (antibody level <0.8 IU/mL), equivocal (<1.1 IU/mL), positive (antibody level >1.1 IU/mL).
The data were expressed as the mean ± standard deviation (SD) or as percentages and ranges as appropriate. Comparisons were made using the Chi-square test using standard equations. The results were reported with P ≤ 0.05 or P ≤ 0.01 as the accepted level of significance accordingly.
| Results|| |
A total of 349 pregnant women were enrolled in this study and were screened for both IgM and IgG antibodies. [Table 1] illustrates the prevalence of both antibodies including the range and mean ± SD in in the study group. Overall, 139 (39.8%) were positive for parvo-virus B19 IgG and 32 (9.2%) had IgM antibody. The remaining 178 (51%) were neither equivocal nor cases with both IgG and IgM.
|Table 1: Prevalence of immunoglobulin G and immunoglobulin M antibodies in the study samples|
Click here to view
Tables 2 delineates the prevalence of IgG and incidence of IgM in relation to the demography. The highest prevalence of HPV B19 IgG according to age, trimester, occupation, and number of children was as follows: >35 years (45, 32.4%), second trimester (52, 47.4%), homemakers (89, 64%), ≥5 children (45, 32.4%). Statically, the differences of distribution of the Parvovorus IgG in relation to above-mentioned demography were as follows: age >35 years: highly significant (P ≤ 0.01), second trimester: nonsignificant, homemakers: highly significant (P ≤ 0.01), ≥5 children: highly significant (P ≥ 0.01). The highest incidence of HPV B19 IgM according to age, trimester, occupation and number of children were as follows: <20 years (13, 40.6%), second trimester (13, 40.6%), homemakers (15, 46.9%), ≥5 children (13, 40.6%). Statically, the differences of distribution of the Parvovorus IgM in relation to above-mentioned demography were as follows: age <20 years: significant (P ≤ 0.05), second trimester: nonsignificant, homemakers: highly significant (P ≤ 0.01), ≥5 children: significant (P ≥ 0.05).
| Discussion|| |
To the best of our knowledge, no published data are available on the prevalence of HPV B19 among pregnant women in Erbil governorate, hence this study can be considered the first study of such quality to deal with and inspect the prevalence and associated risk factors of such an infection among these women. Maternal primary infection with cytomegalovirus (CMV), HPV B19, and rubella virus may give rise to fetus and pregnancy complications. Because the congenital rubella infection is controlled by the vaccine, CMV and HPV B19 are the most paramount causes of clinically significant intrauterine viral infections.
In the present study, the prevalence of IgG antibody against HPV B19 was 39.8%. In addition, the incidence of IgM antibody against HPV B19 was 9.2%, which is a sign of acute infection, and signals that B19 is existent in the population. Thus, more than half (51%) of the women were IgG negative, so they are vulnerable to the HPV B19 infection. HPV B19 infection has been revealed in a number of developed countries throughout the world with adult prevalence rates varying from 30% to 60%. However, few prevalence screening has been conducted in developing countries.
HPV B19-specific IgG antibody was detected in 65 out of 86 (75.6%) of pregnant women in west Iran. In other countries, prevalence of parvovirus B19 antibodies was reported in 59.9% of European and 67.7% of non-European women, without significant differences in demographic parameters. B19 IgG antibodies detected in 46.6% and IgM antibodies in 2.25% of different age groups of childbearing women in Makkah, KSA. In another study involving 231 women in Nigeria, 45 (19.5%) were positive for parvovirus B19 IgG, 10 (4.3%) were positive for parvovirus B19 IgM. IgG prevalence was 61% among the women of childbearing age in Tripoli, Libya, while the incidence of IgM was 5%.
Divergence in the results of the present study and those aforementioned studies may be due to ELISA techniques and populations variables. The seroprevalence of HPV B19 seems to be variable worldwide. Diversified factors are renowned to have an impact on the seroprevalence including age, geography, climate, socioeconomic status, occupation, race, parity, and working among children.
[Table 2] explicates the prevalence and incidence of IgG and IgM, respectively, in relation to different demographics. Concerning the women age, the highest prevalence rate of B19 IgG antibodies in the present study was found to be 32.4%. This finding was observed in pregnant women aged between 35 and 40 years. In addition, it is noted that the prevalence of IgG antibodies to parvovirus B19 increases with age in a highly significant manner (P ≤ 0.01) ranging from 5.8% in women below 20 years of age to as high as 32.4% in women aged between 35 and 40 years age. This finding suggests that the seroprevalence of B19 IgG antibodies is dependent on age, which is in harmony with previous reports., A survey in the USA showed a gradual increase in HPV B19 seropositivity with age, ranging from as low as 19% in children under 10 years of age to 67% in individuals over 49 years of age, suggesting continued exposure to the virus. Other studies in industrialized countries deduced that infection occurs during adult life increasing the seroprevalence rate from ~60% at age 18 years to >80% in geriatric populations.,
|Table 2: Prevalence of immunoglobulin G and immunoglobulin M antibodies in relation to demographics|
Click here to view
Parvovirus B19, seropositivity is a synonym of immunity, the increase in seroprevalence with age denotes that, the proportion of individuals liable to parvovirus B19 decreases with age. Higher incidence of IgM antibodies was detected in the age group of <20 years (40.6%) with a significant difference (P ≤ 0.05). This decrease in the incidence of IgM with age is in accordance with a study done in Syria which had investigated 273 pregnant women, concluded that women aged between 22 and 26 years had the highest incidence rate of IgM antibodies (9.4%) while the lowest rate (0%) was noted in women who are older than 37 years. Another study which had embroiled 231 pregnant women in Oyo State, Nigeria, pointed that highest incidence of parvovirus B19 IgM antibody (10.8%) was in the 22–27 year age group, and lowest was in the 38 years and older age group. The decrease in the incidence of IgM with age had been proclaimed by considerable studies which elucidated the certainty that younger women had never had prior infection as compared with older women.,,,,
Women in their second trimester of pregnancy were found to manifest the highest rates of IgM and IgG antibodies. However, these differences were not statistically significance (P ≤ 0.05). The present result is in unison with the outcome of a study accomplished by Emiasegen et al. in which highest rate of antibodies were noticed in the second trimester with no significant association. Okojokwu et al. concluded that a positive linking between prevalence of IgG antibodies and trimester while there was no association between incidence of IgM antibodies and trimester. Emiasegen et al. indicated that the observation of nonsignificant association between high levels of antibodies and trimesters may be a result of chance, differences in the study design or ELISA techniques discrepancies in specificity and sensitivity. Parvovirus B19 infection in pregnant women especially in the second trimester can result in hydrops fetalis and fetal loss, fetal anemia, spontaneous abortion, and stillbirth. In the present study, 40.6% of the pregnant women had evidence of recent infection in their second trimester, thereby indicating that high number of women who were subjected for the study was at risk and having unfavorable birth outcome. The outcome of the highest incidence (40.6%) and prevalence (47.4%) in the second trimester of the gestational age of pregnancy could possibly be clarified as predisposition to infection may be due to hormonal changes with progress in pregnancy.
The current study clarified that occupation and number of children may have an influence on the prevalence and incidence of IgG and IgM respectively. The prevalence of IgG was higher (P ≤ 0.01) in homemakers and in women living in families with ≥ 5 children (89,64%; 45,32.4%). The incidence of IgM which denote recent infection was higher (P ≤ 0.01) in homemakers and in women living in families with ≥5 children (P ≤ 0.05) (15,46.9%; 13,40.6%). Diversified studies had announced the impact of occupation and family size on the prevalence and incidence of IgG and IgM respectively. Abiodun et al. and Emiasegen et al. determined that the rate of IgG and IgM antibodies was significantly highest among full-time homemakers, followed by women working in nursery schools, after-school clubs, or day-care centers. Jegede et al. deduced that high positivity observed among full time homemakers could be due to the fact that women are always in touch with children both at home and outside the home. Another possible elucidation for this observation which was suggested by Röhrer et al. and Ghazi  is that children are more prone to infection with this agent and that full-time homemakers are with their children all day; therefore, their environment potentiates recurrent contact for dissemination by mean of aerosols. The impact of number of children on the prevalence and incidence of IgG and IgM, respectively, had been recorded by numerous studies. Sharifi et al. recalled that the risk of infection compared with nulliparous women increases about several times in women with three or more children. Habibzadeh et al. had concluded that the hazard of infection in pregnant women with one child are three times more than nulliparous women, but this risk for women with three or more children are 7.5 times more. Elnifro et al. and Okojokwu et al. stated that the proportion of the women who had demonstrated IgM and IgG antibodies in a highly significant manner (P < 0.05) increased with the number of children in a household. Khameneh et al. assumed that children are the leading sources of transmission and outbreaks can persist for months in schools and day care centers due to the relatively large number of seronegative children that come in close contact with children within this environment. Ergaz and Ornoy  notified that the infection is commonly passed through respiratory tract secretions from adjacent personal contact. This justifies the present finding that those women with more children were more likely to be infected.
| Conclusions|| |
Nearly 51% of women are susceptible to infection. In addition, IgM antibodies were positive in 9.2% of women, indicating that there is an active transmission of the virus in our population, while 39.8% of women are resistant to infection. A correlation was found between prevalence and incidence of parvovirus infection with the age of the women, number of children in the family, and the occupation of the women.
The authors would like to thank the Health and Education Directorates of Erbil. The authors are grateful to all women who participated in the study and to the doctors and technicians who helped during sample collection in different hospitals.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Mossong J, Hens N, Friederichs V, Davidkin I, Broman M, Litwinska B, et al
. Parvovirus B19 infection in five European countries: Seroepidemiology, force of infection and maternal risk of infection. Epidemiol Infect 2008;136:1059-68.
Watt AP, Brown M, Pathiraja M, Anbazhagan A, Coyle PV. The lack of routine surveillance of parvovirus B19 infection in pregnancy prevents an accurate understanding of this regular cause of fetal loss and the risks posed by occupational exposure. J Med Microbiol 2013;62:86-92.
Simms RA, Liebling RE, Patel RR, Denbow ML, Abdel-Fattah SA, Soothill PW, et al
. Management and outcome of pregnancies with parvovirus B19 infection over seven years in a tertiary fetal medicine unit. Fetal Diagn Ther 2009;25:373-8.
Röhrer C, Gärtner B, Sauerbrei A, Böhm S, Hottenträger B, Raab U, et al
. Seroprevalence of parvovirus B19 in the German population. Epidemiol Infect 2008;136:1564-75.
Ergaz Z, Ornoy A. Parvovirus B19 in pregnancy. Reprod Toxicol 2006;21:421-35.
Enders M, Weidner A, Enders G. Current epidemiological aspects of human parvovirus B19 infection during pregnancy and childhood in the western part of Germany. Epidemiol Infect 2007;135:563-9.
van Rijckevorsel GG, Bovée LP, Damen M, Sonder GJ, Schim van der Loeff MF, van den Hoek A. Increased seroprevalence of IgG-class antibodies against cytomegalovirus, parvovirus B19, and varicella-zoster virus in women working in child day care. BMC Public Health 2012;12:475.
Alanen A, Kahala K, Vahlberg T, Koskela P, Vainionpää R. Seroprevalence, incidence of prenatal infections and reliability of maternal history of varicella zoster virus, cytomegalovirus, herpes simplex virus and parvovirus B19 infection in South-Western Finland. BJOG 2005;112:50-6.
Khameneh ZR, Hanifian H, Barzegari R, Sepehrvand N. Human parvovirus B19 in Iranian pregnant women: A serologic survey. Indian J Pathol Microbiol 2014;57:442-4.
] [Full text]
Suárez González A, Otero Guerra L, De La Guerra GV, La Iglesia M, Solís Sánchez G, Rodríguez Fernández A. Varicella and parvovirus B19 immunity among pregnant women in Gijón, Spain. Med Clin (Barc) 2002;119:171-3.
Ghazi HO. Prevalence of antibodies to human parvovirus b19 in Saudi women of childbearing age in makkah. J Family Community Med 2007;14:15-7.
Abiodun I, Opaleye OO, Ojurongbe O, Fagbami AH. Seroprevalence of parvovirus B19 IgG and IgM antibodies among pregnant women in Oyo State, Nigeria. J Infect Dev Ctries 2013;7:946-50.
Elnifro E, Nisha AK, Almabsoot M, Daeki A, Mujber N, Muscat J. Seroprevalence of parvovirus B19 among pregnant women in Tripoli, Libya. J Infect Dev Ctries 2009;3:218-20.
Sharifi P, Khodabandehloo M, Rahimiyan-Zarif B. Seroprevalence of parvovirus B19 antibodies in young women Sanandaj Iran. Iran J Virol 2013;7:1-6.
Emiasegen SE, Nimzing L, Adoga MP, Ohagenyi AY, Lekan R. Parvovirus B19 antibodies and correlates of infection in pregnant women attending an antenatal clinic in central Nigeria. Mem Inst Oswaldo Cruz 2011;106:227-31.
Kelly HA, Siebert D, Hammond R, Leydon J, Kiely P, Maskill W. The age-specific prevalence of human parvovirus immunity in Victoria, Australia compared with other parts of the world. Epidemiol Infect 2000;124:449-57.
Gilbert NL, Gyorkos TW, Béliveau C, Rahme E, Muecke C, Soto JC. Seroprevalence of parvovirus B19 infection in daycare educators. Epidemiol Infect 2005;133:299-304.
Buhtori MM. Seroprevalence of parvovirus B19 among pregnant women in Damascus Syria. Int J Pharm Sci Rev Res 2015;30:227-9.
Okojokwu OJ, Adebayo MB, Abubakar BS, Yusuf IA, Anejo-Okopi JA. Seroepidemiology of human parvovirus B19 infection among pregnant women in Abuja Nigeria. Hosts Viruses 2018;5:57-62.
Jegede A, Aminu M, Ella EE. Sero-prevalence of human parvovirus B19 among patients attending some hospitals in Kano metropolis, Nigeria. Afr J Clin Exp Microbiol 2014;15:21-6.
Habibzadeh S, Peeri-Doghaheh H, Mohammad-Shahi J, Mobini E, Shahbazzadegan S. The prevalence of parvovirus B19 infection among pregnant women of Ardabil in 2013. Iran J Microbiol 2016;8:214-8.
[Table 1], [Table 2]