Toxoplasma gondii Infection Is Associated with Low Birth Weight: Findings from an Observational Study among Rural Bangladeshi Women
Abstract
:1. Introduction
2. Results
3. Discussion
Limitations and Strengths
4. Materials and Methods
4.1. Study Design, Study Site and Population
4.2. Ethical Approval
4.3. Anthropometric Assessment and Collection of Blood Sample
4.4. Assessment and Definition of Serological Profiles for Toxoplasmosis
4.5. Major Outcome and Co-Variates
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
AIC | Akaike’s information criteria |
AROC | Area under the receiver operating characteristics curve |
BMI | Body mass index |
BIC | Bayesian information criteria |
CI | Confidence interval |
Icddr,b | International Centre for Diarrheal Disease Research, Bangladesh |
Ig | Immunoglobulin |
LBW | Low birth weight |
OR | Odds ratio |
RR | Relative risk |
References
- Hill, D.; Dubey, J. Toxoplasma gondii: Transmission, diagnosis and prevention. Clin. Microbiol. Infect. 2002, 8, 634–640. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Egorov, A.I.; Converse, R.; Griffin, S.M.; Styles, J.; Klein, E.; Sams, E.; Hudgens, E.; Wade, T.J. Environmental risk factors for Toxoplasma gondii infections and the impact of latent infections on allostatic load in residents of Central North Carolina. BMC Infect. Dis. 2018, 18, 421. [Google Scholar] [CrossRef] [PubMed]
- Prasoona, K.R.; Srinadh, B.; Sunitha, T.; Sujatha, M.; Deepika, M.L.; Lakshmi, B.V.; Ramaiah, A.; Jyothy, A. Seroprevalence and Influence of Torch Infections in High Risk Pregnant Women: A Large Study from South India. J. Obstet. Gynaecol. India 2015, 65, 301–309. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pusdekar, Y.V.; Patel, A.B.; Kurhe, K.G.; Bhargav, S.R.; Thorsten, V.; Garces, A.; Goldenberg, R.L.; Goudar, S.S.; Saleem, S.; Esamai, F.; et al. Rates and risk factors for preterm birth and low birthweight in the global network sites in six low-and low middle-income countries. Reprod. Health 2020, 17, 187. [Google Scholar] [CrossRef] [PubMed]
- Shen, Z.Z.; Wang, Y.W.; Ma, S.; Zhan, Y.L.; Wu, S.S.; Feng, Y.H.; Cai, S.Y.; Ma, L.K.; Jiang, Y. Risk factors for preterm birth, low birth weight and small for gestational age: A prospective cohort study. Zhonghua Liu Xing Bing Xue Za Zhi Zhonghua Liuxingbingxue Zazhi 2019, 40, 1125–1129. [Google Scholar] [CrossRef]
- Al-Hakami, A.M.; Paul, E.; Al-Abed, F.; Alzoani, A.A.; Shati, A.A.; Assiri, M.I.; Qasim, A.A.; Riaz, F.; Moosa, R.A.; Chandramoorthy, H.C. Prevalence of toxoplasmosis, rubella, cytomegalovirus, and herpes (TORCH) infections among women attending the antenatal care clinic, maternity hospital in Abha, Southwestern Saudi Arabia. Saudi Med. J. 2020, 41, 757–762. [Google Scholar] [CrossRef]
- Santos, P.C.; Telmo, P.L.; Lehmann, L.M.; Mattos, G.T.; Klafke, G.B.; Lorenzi, C.; Hirsch, C.; Lemos, L.; Berne, M.E.A.; Gonçalves, C.V.; et al. Risk and other factors associated with toxoplasmosis and toxocariasis in pregnant women from southern Brazil. J. Helminthol. 2017, 91, 534–538. [Google Scholar] [CrossRef]
- Fochi, M.M.; Baring, S.; Spegiorin, L.C.; Vaz-Oliani, D.C.; Galão, E.A.; Oliani, A.H.; de Mattos, L.C.; de Mattos, C.C. Prematurity and Low Birth Weight did not Correlate with Anti-Toxoplasma gondii Maternal Serum Profiles—A Brazilian Report. PLoS ONE 2015, 10, e0132719. [Google Scholar] [CrossRef]
- van der Weiden, S.; de Jong, E.P.; Pas, A.B.T.; Middeldorp, J.M.; Vossen, A.C.; Rijken, M.; Walther, F.J.; Lopriore, E. Is routine TORCH screening and urine CMV culture warranted in small for gestational age neonates? Early Hum. Dev. 2011, 87, 103–107. [Google Scholar] [CrossRef]
- Freeman, K.; Oakley, L.; Pollak, A.; Buffolano, W.; Petersen, E.; Semprini, A.E.; Salt, A.; Gilbert, R. Association between congenital toxoplasmosis and preterm birth, low birthweight and small for gestational age birth. BJOG Int. J. Obstet. Gynaecol. 2005, 112, 31–37. [Google Scholar] [CrossRef]
- Schmidt, D.R.; Hogh, B.; Andersen, O.; Fuchs, J.; Fledelius, H.; Petersen, E. The national neonatal screening programme for congenital toxoplasmosis in Denmark: Results from the initial four years, 1999–2002. Arch. Dis. Child. 2006, 91, 661–665. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, X.-L.; Wei, H.-X.; Zhang, H.; Peng, H.-J.; Lindsay, D.S. A meta analysis on risks of adverse pregnancy outcomes in Toxoplasma gondii infection. PLoS ONE 2014, 9, e97775. [Google Scholar] [CrossRef] [PubMed]
- Naheen, C.R.; Tarafder, S.; Khan, S. Toxoplasma gondii Seropositivity and its Possible Associated Risk Factors among Pregnant Women Attending Antenatal Clinic in a Tertiary Care Hospital of Dhaka, Bangladesh. Mymensingh Med. J. MMJ 2018, 27, 336–343. [Google Scholar] [PubMed]
- Samad, M.A.; Begum, N.; Shamsunahar; Ahmed, M.U. Serological diagnosis of Toxoplasma gondii infection in women associated with gyneco-obstetric problems. Southeast Asian J. Trop. Med. Public Health 1993, 24, 102–106. [Google Scholar] [PubMed]
- Dalimi, A.; Abdoli, A. Latent toxoplasmosis and human. Iran. J. Parasitol. 2012, 7, 1. [Google Scholar]
- Robert-Gangneux, F.; Dardé, M.-L. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin. Microbiol. Rev. 2012, 25, 264–296. [Google Scholar] [CrossRef] [Green Version]
- Al-Adhroey, A.H.; Mehrass, A.A.O.; Al-Shammakh, A.A.; Ali, A.D.; Akabat, M.Y.M.; Al-Mekhlafi, H.M. Prevalence and predictors of Toxoplasma gondii infection in pregnant women from Dhamar, Yemen. BMC Infect. Dis. 2019, 19, 1089. [Google Scholar] [CrossRef] [Green Version]
- Ashrafunnessa; Khatun, S.; Islam, M.N.; Huq, T. Seroprevalence of toxoplasma antibodies among the antenatal population in Bangladesh. J. Obstet. Gynaecol. Res. 1998, 24, 115–119. [Google Scholar] [CrossRef]
- National Nutrition Services (NNS). National Low Birth Weight Survey (NLBWS) Bangladesh, 2015; Dhaka, Bangladesh National Nutrition Services, Institute of Public Health Nutrition, Directorate General of Health Services, Ministry of Health & Family Welfare, Government of the People’s Republic of Bangladesh: Dhaka, Bangladesh, 2017. [Google Scholar]
- World Health Organization. Global Nutrition Targets 2025: Low Birth Weight Policy Brief; World Health Organization: Geneva, Switzerland, 2014. [Google Scholar]
- Bhat, B.V.; Adhisivam, B. Trends and outcome of low birth weight (LBW) infants in India. Indian J. Pediatr. 2013, 80, 60–62. [Google Scholar] [CrossRef]
- Chen, Y.; Li, G.; Ruan, Y.; Zou, L.; Wang, X.; Zhang, W. An epidemiological survey on low birth weight infants in China and analysis of outcomes of full-term low birth weight infants. BMC Pregnancy Childbirth 2013, 13, 242. [Google Scholar] [CrossRef] [Green Version]
- Mukhopadhyay, K.; Malhi, P.; Mahajan, R.; Narang, A. Neurodevelopmental and behavioral outcome of very low birth weight babies at corrected age of 2 years. Indian J. Pediatr. 2010, 77, 963–967. [Google Scholar] [CrossRef] [PubMed]
- Siddiqi, M.N.A.; Muyeed, A.; Haque, M.N.; Goni, M.A.; Shadhana, S.C. Low Birth Weight of Newborns and Its Association with Demographic and Socio-economic Determinants: Findings from Multiple Indicator Cluster Survey (MICS) Bangladesh 2019. Int. J. Health Stud. 2021, 7, 37–42. [Google Scholar]
- Pappas, G.; Roussos, N.; Falagas, M.E. Toxoplasmosis snapshots: Global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int. J. Parasitol. 2009, 39, 1385–1394. [Google Scholar] [CrossRef] [PubMed]
- Mansur, A.M.; Rezaul, K.M.; Mahmudul, H.M. Quality of antenatal care in primary health care centers of bangladesh. J. Fam. Reprod. Health 2014, 8, 175–181. [Google Scholar]
- Jo, Y.; Alland, K.; Ali, H.; Mehra, S.; LeFevre, A.E.; Pak, S.E.; Shaikh, S.; Christian, P.; Labrique, A.B. Antenatal care in rural Bangladesh: Current state of costs, content and recommendations for effective service delivery. BMC Health Serv. Res. 2019, 19, 861. [Google Scholar] [CrossRef]
- Fallahi, S.; Rostami, A.; Shiadeh, M.N.; Behniafar, H.; Paktinat, S. An updated literature review on maternal-fetal and reproductive disorders of Toxoplasma gondii infection. J. Gynecol. Obstet. Hum. Reprod. 2018, 47, 133–140. [Google Scholar] [CrossRef]
- Kieffer, F.; Wallon, M. Congenital toxoplasmosis. Handb. Clin. Neurol. 2013, 112, 1099–1101. [Google Scholar]
- Aqeely, H.; El-Gayar, E.K.; Khan, D.P.; Najmi, A.; Alvi, A.; Bani, I.; Mahfouz, M.S.; Abdalla, S.E.; Elhassan, I.M. Seroepidemiology of Toxoplasma gondii amongst Pregnant Women in Jazan Province, Saudi Arabia. J. Trop. Med. 2014, 2014, 913950. [Google Scholar] [CrossRef] [Green Version]
- van Enter, B.J.; Lau, Y.-L.; Ling, C.L.; Watthanaworawit, W.; Sukthana, Y.; Lee, W.-C.; Nosten, F.; McGready, R. Seroprevalence of Toxoplasma gondii Infection in Refugee and Migrant Pregnant Women along the Thailand–Myanmar Border. Am. J. Trop. Med. Hyg. 2017, 97, 232–235. [Google Scholar]
- Abamecha, F.; Awel, H. Seroprevalence and risk factors of Toxoplasma gondii infection in pregnant women following antenatal care at Mizan Aman General Hospital, Bench Maji Zone (BMZ), Ethiopia. BMC Infect. Dis. 2016, 16, 460. [Google Scholar] [CrossRef] [Green Version]
- Obaidat, M.M.; Al-Sheyab, N.A.; Salman, A.E.B.; Lafi, S.Q. Seroepidemiology and risk factors of Toxoplasma gondii infection in undergraduate university female students in Jordan. Epidemiol. Infect. 2015, 143, 1898–1903. [Google Scholar] [CrossRef] [PubMed]
- Doni, N.Y.; Simsek, Z.; Gurses, G.; Zeyrek, F.Y.; Demir, C. Prevalence and associated risk factors of Toxoplasma gondii in female farmworkers of southeastern Turkey. J. Infect. Dev. Ctries. 2015, 9, 87–93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andiappan, H.; Nissapatorn, V.; Sawangjaroen, N.; Nyunt, M.H.; Lau, Y.-L.; Khaing, S.L.; Aye, K.M.; Mon, N.C.N.; Tan, T.-C.; Kumar, T. Comparative study on Toxoplasma infection between Malaysian and Myanmar pregnant women. Parasites Vectors 2014, 7, 564. [Google Scholar] [CrossRef] [PubMed]
- Thiébaut, R.; Leproust, S.; Chêne, G.; Gilbert, R. Effectiveness of prenatal treatment for congenital toxoplasmosis: A meta-analysis of individual patients’ data. Lancet 2007, 369, 115–122. [Google Scholar]
- Tarekegn, Z.S.; Dejene, H.; Addisu, A.; Dagnachew, S. Potential risk factors associated with seropositivity for Toxoplasma gondii among pregnant women and HIV infected individuals in Ethiopia: A systematic review and meta-analysis. PLoS Negl. Trop. Dis. 2020, 14, e0008944. [Google Scholar] [CrossRef]
- Wang, S.; Yao, Z.; Li, H.; Li, P.; Wang, D.; Zhang, H.; Xie, Q.; Zhang, Z.; Li, X. Seroprevalence and risk factors of Toxoplasma gondii infection in primary school children in Henan province, central China. Parasite 2020, 27, 23. [Google Scholar] [CrossRef]
- Khan, M.M.A.; Mustagir, M.G.; Islam, M.R.; Kaikobad, M.S.; Khan, H.T. Exploring the association between adverse maternal circumstances and low birth weight in neonates: A nationwide population-based study in Bangladesh. BMJ Open 2020, 10, e036162. [Google Scholar] [CrossRef]
- Ngandu, C.B.; Momberg, D.; Magan, A.; Chola, L.; Norris, S.A.; Said-Mohamed, R. The association between household socio-economic status, maternal socio-demographic characteristics and adverse birth and infant growth outcomes in sub-Saharan Africa: A systematic review. J. Dev. Orig. Health Dis. 2020, 11, 317–334. [Google Scholar] [CrossRef]
- Frederick, I.O.; Williams, M.A.; Sales, A.E.; Martin, D.P.; Killien, M. Pre-pregnancy body mass index, gestational weight gain, and other maternal characteristics in relation to infant birth weight. Matern. Child Health J. 2008, 12, 557–567. [Google Scholar] [CrossRef]
- Ancira-Moreno, M.; O’Neill, M.S.; Rivera-Dommarco, J.; Batis, C.; Ramírez, S.R.; Sánchez, B.N.; Castillo-Castrejón, M.; Vadillo-Ortega, F. Dietary patterns and diet quality during pregnancy and low birthweight: The PRINCESA cohort. Matern. Child Nutr. 2020, 16, e12972. [Google Scholar] [CrossRef] [Green Version]
- Ko, T.J.; Tsai, L.Y.; Chu, L.C.; Yeh, S.J.; Leung, C.; Chen, C.Y.; Chou, H.C.; Tsao, P.N.; Chen, P.C.; Hsieh, W.S. Parental smoking during pregnancy and its association with low birth weight, small for gestational age, and preterm birth offspring: A birth cohort study. Pediatr. Neonatol. 2014, 55, 20–27. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abdelazim, I.A.; Bekmukhambetov, Y.; Aringazina, R.; Shikanova, S.; Amer, O.O.; Zhurabekova, G.; Otessin, M.A.; Astrakhanov, A.R. The outcome of hypertensive disorders with pregnancy. J. Fam. Med. Prim. Care 2020, 9, 1678–1683. [Google Scholar] [CrossRef] [PubMed]
- Wilson, R.L.; Grieger, J.A.; Bianco-Miotto, T.; Roberts, C.T. Association between Maternal Zinc Status, Dietary Zinc Intake and Pregnancy Complications: A Systematic Review. Nutrients 2016, 8, 641. [Google Scholar] [CrossRef] [Green Version]
- Montagnoli, C.; Zanconato, G.; Cinelli, G.; Tozzi, A.E.; Bovo, C.; Bortolus, R.; Ruggeri, S. Maternal mental health and reproductive outcomes: A scoping review of the current literature. Arch. Gynecol. Obstet. 2020, 302, 801–819. [Google Scholar] [CrossRef] [PubMed]
- Wardlaw, T.M. Low Birthweight: Country, Regional and Global Estimates; UNICEF: New York, NY, USA, 2004. [Google Scholar]
- Vyas, S.; Kumaranayake, L. Constructing socio-economic status indices: How to use principal components analysis. Health Policy Plan 2006, 21, 459–468. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zou, G. A modified poisson regression approach to prospective studies with binary data. Am. J. Epidemiol. 2004, 159, 702–706. [Google Scholar] [CrossRef] [PubMed]
Normal Birth Weight (n = 169) | Low Birth Weight (n = 39) | |||
---|---|---|---|---|
N | % | N | % | |
IgM−; IgG− | 132 | 78.1 | 24 | 61.5 |
IgM−; IgG+ | 30 | 17.8 | 15 | 38.5 |
IgG+; IgM+ | 2 | 1.2 | 0 | 0.0 |
IgM+; IgG− | 5 | 3.0 | 0 | 0.0 |
Normal Birth Weight (n = 169) | Low Birth Weight (n = 39) | Unadjusted Relative Risk (95% CI) | |
---|---|---|---|
Age group | |||
<20 years | 18.34 | 17.95 | 1.00 (0.43–2.35) |
20–29 years | 55.03 | 53.85 | Ref. |
≥30 years | 26.63 | 28.21 | 1.07 (0.51–2.21) |
Pregnant women’s education | |||
>9 years of schooling | 32.54 | 20.51 | Ref. |
5–9 years of schooling | 60.36 | 58.97 | 1.45 (0.65–3.24) |
<5 years of schooling | 7.1 | 20.51 | 3.15 (1.18–8.39) |
Wealth quintiles | |||
Poor | 24.85 | 12.82 | Ref. |
Lower middle | 17.16 | 20.51 | 2.03 (0.66–6.21) |
Middle | 15.98 | 28.21 | 2.72 (0.95–7.83) |
Upper middle | 18.93 | 20.51 | 1.88 (0.62–5.75) |
Rich | 23.08 | 17.95 | 1.43 (0.45–4.51) |
Number of under 18 years children | |||
No child | 35.5 | 23.08 | Ref. |
1–2 children | 37.87 | 41.03 | 1.53 (0.68–3.47) |
≥3 children | 26.63 | 35.9 | 1.82 (0.79–4.2) |
Antenatal visit | |||
No | 60.36 | 64.1 | 0.88 (0.46–1.69) |
Yes | 39.64 | 35.9 | Ref. |
Reported anemia | |||
No | 5.92 | 2.56 | Ref. |
Yes | 94.08 | 97.44 | 2.12 (0.29–15.45) |
Mode of delivery | |||
Normal Vaginal Delivery | 47.34 | 71.79 | Ref. |
Caesarian section | 52.66 | 28.21 | 0.42 (0.21–0.85) |
Pregnant women’s education BMI | |||
Normal | 64.5 | 53.85 | Ref. |
Under nutrition | 8.28 | 15.38 | 1.86 (0.75–4.60) |
Over nutrition/obese | 27.22 | 30.77 | 1.28 (0.63–2.60) |
Gestation at enrollment (weeks) * | 19.84 ± 10.08 | 17.84 ± 8.99 | 0.98 (0.95–1.01) |
Term pregnancy (>36 weeks) | |||
No | 80.47 | 43.59 | Ref. |
Yes | 19.53 | 56.41 | 3.60 (2.07–6.27) |
Model 1 | Model 2 | Model 3 | Model 4 | Model 5 | |
---|---|---|---|---|---|
T. gondii | |||||
IgM−; IgG− | Ref. | Ref. | Ref. | Ref. | Ref. |
IgG+ or IgM+ | 1.88 (1.07–3.3) | 1.76 (1.01–3.07) | 1.76 (1.02–3.02) | 1.78 (1.03–3.06) | 2.00 (1.17–3.42) |
Age group | |||||
<20 years | 1.04 (0.5–2.16) | 1.57 (0.65–3.82) | 1.54 (0.59–4.00) | 1.48 (0.43–5.11) | |
20–30 years | Ref. | Ref. | Ref. | Ref. | |
≥30 years | 0.95 (0.5–1.8) | 0.71 (0.3–1.7) | 0.70 (0.32–1.54) | 0.50 (0.24–1.05) | |
Pregnant women’s education | |||||
>9 years of schooling | Ref. | Ref. | Ref. | Ref. | |
5–9 years of schooling | 1.5 0 (0.75–3.02) | 1.29 (0.69–2.44) | 1.34 (0.70–2.56) | 1.02 (0.54–1.93) | |
<5 years of schooling | 3.52 (1.52–8.17) | 2.7 (1.14–6.36) | 3.10 (1.24–7.77) | 2.35 (1.05–5.27) | |
Wealth quintiles | |||||
Poor | Ref. | Ref. | Ref. | Ref. | |
Lower middle | 1.83 (0.63–5.3) | 1.77 (0.6–5.21) | 1.72 (0.60–4.92) | 1.02 (0.36–2.91) | |
Middle | 3.05 (1.16–8.02) | 3.27 (1.2–8.91) | 3.31 (1.19–9.22) | 3.15 (1.18–8.41) | |
Upper middle | 2.18 (0.76–6.28) | 2.41 (0.84–6.89) | 2.71 (0.89–8.28) | 1.36 (0.45–4.07) | |
Rich | 1.87 (0.61–5.78) | 2.18 (0.68–7.01) | 2.43 (0.72–8.14) | 2.04 (0.63–6.61) | |
Number of under 18 years children | |||||
No children | Ref. | Ref. | Ref. | ||
1–2 children | 1.96 (0.8–4.8) | 2.00 (0.77–5.18) | 1.78 (0.56–5.63) | ||
≥3 children | 2.3 (0.78–6.81) | 2.28 (0.76–6.79) | 2.58 (0.74–9.00) | ||
Antenatal visit | Ref. | ||||
No | 0.76 (0.42–1.39) | 0.72 (0.38–1.35) | 0.59 (0.34–1.05) | ||
Yes | Ref. | Ref. | |||
Reported anemia | |||||
No | Ref. | Ref. | Ref. | ||
Yes | 1.76 (0.31–9.97) | 1.57 (0.26–9.57) | 1.40 (0.19–10.27) | ||
Mode of delivery | |||||
Normal Vaginal Delivery | Ref. | Ref. | Ref. | ||
Caesarian section | 0.48 (0.25–0.93) | 0.46 (0.24–0.9) | 0.29 (0.14–0.59) | ||
Pregnant women’s BMI | |||||
Normal | Ref. | Ref. | |||
Under nutrition | 1.54 (0.59–4.00) | 1.68 (0.87–3.26) | |||
Over nutrition/obese | 0.70 (0.32–1.54) | 1.96 (0.94–4.09) | |||
Gestation at enrollment (weeks) | 0.99 (0.96–1.02) | ||||
Term pregnancy (>36 weeks) | |||||
No | 4.66 (2.51–8.68) | ||||
Yes | Ref. | ||||
Model fitness | |||||
Pseudo R-squared | 0.016 | 0.062 | 0.097 | 0.109 | 0.195 |
AIC | 209.142 | 215.731 | 218.265 | 219.661 | 205.758 |
BIC | 215.817 | 249.106 | 268.328 | 276.401 | 269.171 |
Pearson goodness-of-fit (p-value) | 0.972 | 0.931 | 0.941 | 0.874 | 0.948 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Parvin, I.; Das, S.K.; Ahmed, S.; Rahman, A.; Shahid, A.S.M.S.B.; Shahrin, L.; Afroze, F.; Ackhter, M.M.; Alam, T.; Jahan, Y.; et al. Toxoplasma gondii Infection Is Associated with Low Birth Weight: Findings from an Observational Study among Rural Bangladeshi Women. Pathogens 2022, 11, 336. https://doi.org/10.3390/pathogens11030336
Parvin I, Das SK, Ahmed S, Rahman A, Shahid ASMSB, Shahrin L, Afroze F, Ackhter MM, Alam T, Jahan Y, et al. Toxoplasma gondii Infection Is Associated with Low Birth Weight: Findings from an Observational Study among Rural Bangladeshi Women. Pathogens. 2022; 11(3):336. https://doi.org/10.3390/pathogens11030336
Chicago/Turabian StyleParvin, Irin, Sumon Kumar Das, Shahnawaz Ahmed, Aminur Rahman, Abu Sadat Mohammad Sayeem Bin Shahid, Lubaba Shahrin, Farzana Afroze, Mst. Mahmuda Ackhter, Tahmina Alam, Yasmin Jahan, and et al. 2022. "Toxoplasma gondii Infection Is Associated with Low Birth Weight: Findings from an Observational Study among Rural Bangladeshi Women" Pathogens 11, no. 3: 336. https://doi.org/10.3390/pathogens11030336
APA StyleParvin, I., Das, S. K., Ahmed, S., Rahman, A., Shahid, A. S. M. S. B., Shahrin, L., Afroze, F., Ackhter, M. M., Alam, T., Jahan, Y., Palit, P., Sarker, M. H. R., Das, J., Hoque, M. E., Magalhães, R. J. S., Mamun, A. A., Faruque, A. S. G., Ahmed, T., & Chisti, M. J. (2022). Toxoplasma gondii Infection Is Associated with Low Birth Weight: Findings from an Observational Study among Rural Bangladeshi Women. Pathogens, 11(3), 336. https://doi.org/10.3390/pathogens11030336