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Molecular epidemiology of human papillomavirus in pregnant women in Burkina Faso

  • Koudpoko Madeleine Kabre , Djénéba Ouermi EMAIL logo , Théodora Mahoukèdè Zohoncon , Fatié Porzé Wilfried Traore , Ouamini Pulchérie De Prisca Gnoumou , Rogomenoma Alice Ouedraogo , Albert Théophane Yonli , Prosper Bado , Paul Ouedraogo , Teega-Wendé Clarisse Ouedraogo , Tampoula Edwige Yelemkoure , Punya Akouélé Kuassi-Kpede , Dorcas Obiri-Yeboah , Charlemagne Marie Ragnag-Néwendé Ouedraogo and Jacques Simpore
Published/Copyright: December 31, 2022
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Biomolecular Concepts
From the journal Biomolecular Concepts Volume 13 Issue 1

Abstract

Introduction

Genital human papillomavirus (HPV) infection is widespread among sexually active individuals. Several factors may contribute to increased risk of infection in pregnant women. The objective of this study was to determine the high-risk (HR-HPV) and low-risk (LR-HPV) oncogenic HPV genotypes among pregnant women in Ouagadougou.

Methodology

In this study, 100 endocervical samples were collected using a sterile swab on the sterile examination glove used during vaginal examination in pregnant women. DNA from each sample was amplified by PCR followed by hybridization using the HPV Direct Flow Chips kit detecting 36 HPV genotypes.

Results

Twenty-three percent (23%) of pregnant women had HPV infection. Of the 36 genotypes tested, 29 genotypes had been identified with a predominance of HPV 52 (10.34%), HPV 35 (6.89%), and HPV 82 (6.89%) for high risk and HPV 43 (10.34%), HPV 44/55 (6.90%), and HPV 62/81 (6.89%) for low risk.

Conclusion

HPV is common among pregnant women in Burkina Faso. However, the available vaccines do not cover the frequent genotypes found in this study. HPV could therefore constitute a threat for pregnant women and a risk of infection for the newborn.

Keywords: pregnant women; genotypes; HR-HPV; LR-HPV; Burkina Faso

Introduction

Cervical cancer is a public health problem worldwide. In 2020, there were an estimated 604,127 new cases and 341,831 deaths from this cancer worldwide. It is currently the second most common cancer in women [1,2]. The main cause of this cancer is due to human papillomavirus (HPV) infection; the most common sexually transmitted infection (STI) in the world. More than 80% of sexually active individuals acquire this infection at some point in their lives before the age of 45 [3].

Cervical cancer is a major concern for Africa. It is estimated that approximately 84% of all cervical cancers and 88% of all cervical cancer deaths occurred in low-resource countries. It is the second most common cancer in African women aged 15–44 years [1,4].

Although viral clearance occurs in nearly 80% of cases, some HPVs can persist for several years and may have great potential to cause malignancies [5]. Other factors such as parity, prolonged use of oral contraceptives, and the presence of other STIs have been reported as risk factors that may promote the persistence of HPV infection [6]. In pregnant women, in addition to these factors, authors suggest that hormonal and immune changes may increase the risk of HPV infection [7].

The prevalence of HPV infection in pregnant women varies around the world. In Australia, North America, Asia, and Europe, the reported prevalences were 36.60, 30.37, 15.72, and 13.19%, respectively [8]. In Africa, prevalences of 33.3% have been reported in Ghana [9] 5.4% in Nigeria [10]; 5.9% in Tanzania [11], and 13.4% in Cameroon [12].

In Burkina Faso, cervical cancer is the second leading cause of cancer death in women [13]. Several studies that have contributed to the fight against this scourge have reported variations in prevalence and genotypes among populations in several regions [14,15,16,17,18]. However, no HPV studies have focused on the pregnant population.

Recognizing the vulnerability of pregnant women to infection and the possibility of vertical transmission of certain STIs such as HPV, the objectives of our study were: (i) to determine the prevalence of HPV infection in pregnant women, (ii) to investigate the genotypes present in these pregnant women, and (iii) to investigate the risk factors associated with HPV infection in these pregnant women. This study will contribute to the fight against cervical cancer in Burkina Faso in making available data on HPV infection in a vulnerable population, namely pregnant women.

Methodology

Study site and population

This study was conducted at the maternity ward of l Saint Camille Hospital of Ouagadougou (HOSCO) over a 3-month period (October to December 2021). A total of 100 consenting, full-term pregnant women were included. Socio-demographic and clinical data were collected using a questioning filled out on the basis of each woman's clinical file, supplemented by responses obtained directly from them.

Collection of samples

During the early stage of labor when the obstetrician gynecologist performed digital vaginal examination, endocervical samples were collected with a sterile swab. These samples were placed in a cooler equipped with an icebox and transported to the Pietro Annigoni Biomolecular Research Center (CERBA) where they were stored at 4°C before molecular analysis.

  1. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance the tenets of the Helsinki Declaration, and has been approved by the Ethics Committee for Health Research of Burkina Faso (Deliberation no 2021-10-239) as well as that of the HOSCO management.

  2. Informed consent: Informed consent has been obtained from all individuals included in this study.

Molecular characterization

This was done by PCR/hybridization using the HPV Direct Flow Chip kit (Vitro Master Diagnóstica). The samples were pre-treated with bi-distilled water and 30 μL of each sample was added to the freeze-dried mix for the PCR on GeneAmp PCR System 9700 (Applied Biosystems) according to the following program: 1 cycle at 25°C for 10 min; 1 cycle at 94°C for 3 min; 15 cycles each consisting of 94°C for 30 s, 47°C for 30 s, 72°C for 30 s; 35 cycles each consisting of 94°C for 30 s, 65°C for 30 s, 72°C for 30 s; and 1 cycle 72°C for 5 min. The obtained amplicons were denatured at 95°C for 10 and the hybridization was done with the HybriSpot12 (Vitro Master Diagnóstica). The image capture, analysis, and reporting of the results were performed using HybriSoft software.

Data analysis

The data were processed and analyzed using IBM SPSS V20.0 and Epi Info version 6 software. The Chi-square test was used for comparisons. The difference was considered statistically significant for P < 0.05.

Table 1

Sociodemographic, sexual, behavioral characteristics and risk factors associated with HPV carriage in pregnant women

Frequencies (%) P-value Statut HPV
Characteristics HPV− N = 77 HPV+ N = 23 Total P-value
Age group (year) <25 25 0.40 17 8 25 0.47
25–29 36 27 9 36
30–34 25 21 4 25
≥35 14 12 2 14
School level Not in school 9 0.17 8 1 9 0.88
Primary 14 11 3 14
Secondary 39 29 10 39
University 38 29 9 38
Occupation Student 22 0.77 16 6 22 0.39
Informal 27 22 5 27
Housewife 20 13 7 20
Employed 31 26 5 31
Number of sexual partners 1 35 0.003 31 4 35 0.04
≥2 65 46 19 65
Age at the first sexual intercourse 12–15 3 0.04 3 0 3 0.30
16–18 39 27 12 39
≥19 54 43 11 54
Missing 4 4 0 4
Parity 1 43 0.15 31 12 43 0.21
≥2 57 46 11 57
Oral contraceptives using Yes 18 <0.001 15 03 1 0.48
No 82 62 20 82
STI history Yes 48 0.68 39 9 48 0.33
No 52 38 14 52
Screened for cervical cancer Yes 19 <0.001 16 3 19 0.40
No 81 62 20 82
Table 2

Prevalence and distribution of HR-HPV and LR-HPV genotypes in pregnant women

Prevalence of HPV genotypes in pregnant women
HR-HPV n (%) LR-HPV (%)
HPV52 3 (10.34) HPV43 3 (10.34)
HPV35 2 (6.89) HPV44/55 2 (6.90)
HPV82 2 (6.89) HPV62/81 2 (6.89)
HPV16 1 (3.45) HPV6 1 (3.45)
HPV31 1 (3.45) HPV42 1 (3.45)
HPV33 1 (3.45) HPV54 1 (3.45)
HPV45 1 (3.45) HPV61 1 (3.45)
HPV51 1 (3.45) HPV70 1 (3.45)
HPV53 1 (3.45) HPV84 1 (3.45)
HPV56 1 (3.45)
HPV58 1 (3.45)
HPV66 1 (3.45)
Total 1 16 (55.17) Total 2 13 (44.83)
Total 29 (100)
HPV infections types
Isolated infections n (%) Multiple infections n (%)
HPV31 1(4.35) HPV16 +56 1(4.35)
HPV35 1(4.35) HPV43 +54 1(4.35)
HPV51 1(4.35) HPV35 +58 1(4.35)
HPV52 2(8.69) HPV43 +44/55 1(4.35)
HPV53 1(4.35) HPV52+70 1(4.34)
HPV66 1(4.35) HPV45 +62/81 1(4.35)
HPV42 1(4.35) HPV82 +44/55 1(4.35)
HPV43 1(4.35) HPV33 +6 1(4.34)
HPV61 1(4.34) HPV 62/81 1(4.35)
HPV82 1(4.35) Total 2 9 (39.13)
HPV84 1(4.34)
Total 1 12 (52.17)
Total of identified genotypes 21 (21%)
TOTAL of undetermined genotypes UND 2(8.70)
Total 23 (23%)

*UND = undetermined.

Results

  1. Sociodemographic characteristics of the study population

    A total of 100 full-term pregnant women were enrolled. The mean age of the pregnant women was 28.2 ± 5.15 years with a range of 18 and 40 years. The mean number of weeks of amenorrhea was 39.37 ± 1.07. The 25–29 age group was the most represented (36%), while the 35–40 age group was poorly represented (14%). According to the educational level of the women, 14, 39, and 38% had reached elementary school, secondary school, and university, respectively, but 9% of the women in our population had not attended school. In addition, 58% had an income, 22% were students, and 20% were housewives. Age at the first sexual intercourse ranged from 14 to 30 years with an average of 19.51 ± 2.94 years. Sixty-five percent of the women had more than one sexual partner and 35% had had only one partner. However, all women reported having only one sexual partner in the past 12 months. The parity varied from 2 to 7 with an average of 2.05 ± 1.22, of which 57% were multiparous. In addition, 48% of the women had a history of STIs, 18% had used oral contraceptives, and 19% had already been screened for cervical cancer without vaccination (Table 1). Women screened for cervical cancer reported a negative result. In this population, only 3% were not living with their partner, and there were no women who smoked or were HIV positive.

  2. Prevalence of HPV infection (HR-HPV and LR-HPV) and risk factors associated with HPV carriage in pregnant women

    The analyses showed that 23 pregnant women were infected with at least one HPV genotype, for an overall prevalence of 23%. The age group under 30 years was the most affected (17%). No statistically significant association was observed between HPV infection and risk factors such as age, parity, educational level, occupation, age at first sexual intercourse, use of oral contraceptives, and history of STI. Only the number of sexual partners showed a statistically significant difference (Table 1).

  3. Characterization of HPV genotypes in pregnant women

    Of the 23 women who tested positive for HPV, 21 (91.30%) had identifiable genotypes while 2 (8.70%) had indeterminate genotypes. Of these 21 women who had identifiable genotypes, an accumulation of 29 genotypes out of the 36 tested was found (Table 2). The prevalence of high risk genotypes in our general population was 13% (13/100).

    Of the 21 cases of genotype determined infections, 9 (39.13%) were multiple infections and 12 (52.17%) were single infections.

    Of the 36 genotypes tested by the kit, the genotypes found were in decreasing order of frequency: HPV52, 35, 82, 16, 31, 33, 45, 51, 53, 56, 58, and 66 for HR-HPV and for LR-HPV: HPV43, 44/55, 62/81, 6, 42, 54, 61, 70, and 84 (Table 2).

  4. Vaccination coverage according to genotypes found

Of the 29 genotypes identified, only 6.90% were covered by Gardasil®4 available in Burkina Faso, 31.04% were covered by Gardasil®9, and 68.96% were not covered by a HPV vaccine (Figure 1).

Figure 1 HPV vaccination coverage rate according to genotypes found in pregnant women.
Figure 1

HPV vaccination coverage rate according to genotypes found in pregnant women.

Discussion

Overall prevalence of HPV

The overall prevalence of HPV infection in pregnant women in this study was 23%. This prevalence was similar to those reported in the same type of population in China [19], Brazil [20], and Korea [21], which were 24.2, 25.3, and 24.3%, respectively. Our results corroborate those of the meta-analysis by Liu et al. in 2014 who had reported that the prevalence of HPV infection in pregnant women ranged from 9.58 to 46.67% [8].

On the other hand, our results are lower than those reported in Mexico City [22], India [23], and Ghana [9], which were 35, 39.4, and 33.3%, respectively. This difference found could be due in part to the age of the pregnant women, the technique used, and the size of the population. Indeed in our study population, the women were older than those in the studies of Schulze et al. and Martínez-Leal et al. (28.2 ± 5.15 vs 26.3 ± 6.6 years and 25.7 ± 4.8, respectively) [9,22]. Yet, Liu et al. in 2014 had highlighted a higher prevalence of HPV in pregnant women younger than 25 years than in those older than 25 years [8]. In addition, the techniques used by Schulze et al. and Pandey et al. had a broad spectrum of genotypes absent in our technique. Also, the small population size of Martinez et al. (31 pregnant women) could justify this difference in prevalence observed.

Furthermore, the overall prevalence of infection in this study was higher than that reported by Doh et al. in 2021 in Cameroon which was 13.4% [12] and the prevalence of HR-HPV infection (13%) was higher than that reported by Juliana et al. in 2020 in Tanzania which was 5.9% [11]. This difference in prevalence could be related to differences in geographic regions, variation in risk factors, and exposure to infection.

However, despite the immunosuppressed state which could imply elevated prevalence of HPV infection in pregnant women [7], the prevalence of HR-HPV (13%) reported in this study was low compared to those reported in previous studies of the sexually active female population in our country which ranged from 26.1 to 54.9% [15,17,24,25,26,27]. This could be due to the size of our target study population.

Risk factors associated with HPV infection

In our study, we found that pregnant women who had at least two sexual partners were more infected and this difference was statistically significant. Multiple sexual partners have been reported to increase the risk of HPV infection and therefore may increase the risk of developing precancerous lesions [12,24]. We found no statically significant difference between HPV infection and other risk factors. This observation is similar to those reported in the work of Doh et al. in 2021 for age, education, and occupation; Ouedraogo et al. in 2020 for marital status, parity, and STI history; Ouedraogo et al. in 2020 for age of first sexual intercourse; and Traore et al. in 2016 for oral contraceptives [12,15,24,27]. A healthy sexual lifestyle and a change in sexual behavior would therefore be necessary to win the fight against HPV.

Characterization of genotypes found in pregnant women

The most frequent genotypes in this study were HPV52, HPV35, and HPV82 for high risk and HPV43, HPV44/55, and HPV62/81.

Studies conducted in Mexico City [22] and Ghana [9] on the same type of population had reported the presence of HPV52, HPV35, and HPV82. The HR-HPV82 genotype circulating in the sub-region had not been identified in Burkina. However, HPV35 and HPV52 were found in the non-pregnant female population of several regions/cities: Garango [24], central region, central-eastern region, and high basins [15], Ouagadougou [25], Tenkodogo [26], and Orodora [17]. These two genotypes (HPV35 and HPV52) had also been observed in cases of cervical cancer and cervical intraepithelial neoplasia in Ouagadougou and Parakou [16,28,29].

As for LR-HPV, HPV43 had been identified in pregnant women in Mexico City and Ghana [9,22]. For HPV44, HPV55, HPV62, and HPV81, we cannot affirm their presence with accuracy because the panel used had observed cross-reactions between genotypes 44 and 55 and genotypes 62 and 81. Nevertheless, they were identified as circulating genotypes in the world. HPV44 and HPV55 identified in pregnant women in Ghana and Mexico City [9,22], HPV62 in Mexico [30], and HPV81 in Ghana. These LR genotypes (43, 44, 55, 81, and 62) had not been identified in Burkina Faso given that most HPV studies had looked for HR-HPV and LR genotypes 6 and 11.

The circulating HPV6 genotype, found in our study with a low prevalence had been identified in cervical samples in 2010 and 2011, respectively by Low et al. in Bobo Dioulasso and Djigma et al. in Ouagadougou. In these studies, this genotype was predominant compared to HPV11 [18,31]. This genotype was also identified in pregnant women in Ghana in 2016 [9] and in Cameroon in 2021 [12].

The HPV16 genotype found with a low prevalence had already been found in our country in the female population with also a low prevalence [24,25]. Genotypes 11 and 18 were absent in this study. However, they had been found in pregnant women in Ghana, Cameroon, and in the female population of our country. Their absence could be due to the small size of our population.

Vaccination coverage

In this study, 68.96% of the identified genotypes were not covered by the vaccines available in Burkina Faso. In addition to the HPV82 and HPV53 genotypes not investigated in previous studies, all HR-HPV genotypes in our study had been reported in Burkina Faso and more than half were not covered by available vaccines [15,26]. These results support the idea that vaccination in adolescence with the recently introduced quadrivalent Gardasil in Burkina Faso would not protect against the predominant genotypes and that the nonavalent vaccine that includes the predominant HPV52 in Burkina Faso would be beneficial for women [15,24].

Conclusion

Current cervical cancer screening in Burkina Faso has not yet included pregnant women. However, our study showed that they are vulnerable to HPV infection and could transmit the virus vertically to their babies. The glove used during vaginal examination may be a good option for collecting samples for HPV detection without risk of harm in pregnant women. Nonavalent vaccine including genotypes 6, 11, 16, 18, 31, 33, 45, 52, and 58 would be beneficial to protect women against HPV infection in Burkina Faso. This study is a first in Burkina Faso and demonstrates the need for further investigation of this vulnerable population.

Acknowledgements

The authors thank the Saint Camille Hospital of Ouagadougou (HOSCO) and the CERBA/LABIOGENE of the University Joseph KI-ZERBO for collecting, analyzing, and interpreting the data and writing this article.

  1. Funding information: This research received no external funding.

  2. Author contributions: Study concept and design: DO, TMZ and JS. Sampling and Laboratory analysis: FPWT, OPDPG, ATY, RAO, KMK, PB, TCO, TEY and PAK. Statistical analysis and interpretation of data: DO, TMZ, KMK, RAO and PB. Drafting of the manuscript: DO, TMZ, KMK, RAO, PB, PO, CMRO and DO. Critical revision of the manuscript for important intellectual content: DO, TMZ, DO and JS. Administrative, technical, and material support: ATY, DO, TMZ, PO and JS. Study supervision: DO, TMZ and JS. Manuscript Approval: All authors have read and approved the manuscript.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2022-11-20
Accepted: 2022-12-08
Published Online: 2022-12-31

© 2022 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  4. Effect of omega-3 fatty acids on the telomere length: A mini meta-analysis of clinical trials
  5. Analysis of differentially expressed genes and signaling pathways involved in atherosclerosis and chronic obstructive pulmonary disease
  6. The epigenetic dimension of protein structure
  7. Gamma-induced mutants of Bacillus and Streptomyces display enhanced antagonistic activities and suppression of the root rot and wilt diseases in pulses
  8. Corticosterone potentiates ochratoxin A-induced microglial activation
  9. Supercomplex supercomplexes: Raison d’etre and functional significance of supramolecular organization in oxidative phosphorylation
  10. Insights into functional connectivity in mammalian signal transduction pathways by pairwise comparison of protein interaction partners of critical signaling hubs
  11. The effects of supplementation of Nannochloropsis oculata microalgae on biochemical, inflammatory and antioxidant responses in diabetic rats
  12. Molecular epidemiology of human papillomavirus in pregnant women in Burkina Faso
  13. Review Articles
  14. Interaction of cervical microbiome with epigenome of epithelial cells: Significance of inflammation to primary healthcare
  15. Seaweeds’ pigments and phenolic compounds with antimicrobial potential
  16. The capture of host cell’s resources: The role of heat shock proteins and polyamines in SARS-COV-2 (COVID-19) pathway to viral infection
  17. Erratum
  18. Erratum to “Plant growth-promoting properties of bacterial endophytes isolated from roots of Thymus vulgaris L. and investigate their role as biofertilizers to enhance the essential oil contents”
  19. Special Issue on XXV Congress of the Italian Society for Pure and Applied Biophysics
  20. Low-temperature librations and dynamical transition in proteins at differing hydration levels
  21. The phosphoinositide PI(3,5)P2 inhibits the activity of plant NHX proton/potassium antiporters: Advantages of a novel electrophysiological approach
  22. Targeted photoimmunotherapy for cancer
  23. Calorimetry of extracellular vesicles fusion to single phospholipid membrane
  24. Calcium signaling in prostate cancer cells of increasing malignancy
  25. Oxygen diffusion pathways in mutated forms of a LOV photoreceptor from Methylobacterium radiotolerans: A molecular dynamics study
  26. A photosensitizing fusion protein with targeting capabilities
  27. Ion channels and neuronal excitability in polyglutamine neurodegenerative diseases
  28. Is styrene competitive for dopamine receptor binding?
  29. Diffusion of molecules through nanopores under confinement: Time-scale bridging and crowding effects via Markov state model
  30. Quantitative active super-resolution thermal imaging: The melanoma case study
  31. Innovative light sources for phototherapy
  32. Electrophysiological study of the effects of side products of RuBi-GABA uncaging on GABAA receptors in cerebellar granule cells
  33. Subcellular elements responsive to the biomechanical activity of triple-negative breast cancer-derived small extracellular vesicles
https://doi.org/10.1515/bmc-2022-0026
Keywords for this article
pregnant women; genotypes; HR-HPV; LR-HPV; Burkina Faso
Creative Commons
BY 4.0

Articles in the same Issue

  1. Research Articles
  2. Diagnostic accuracy of genetic markers for identification of the Lr46/Yr29 “slow rusting” locus in wheat (Triticum aestivum L.)
  3. NADPH-derived ROS generation drives fibrosis and endothelial-to-mesenchymal transition in systemic sclerosis: Potential cross talk with circulating miRNAs
  4. Effect of omega-3 fatty acids on the telomere length: A mini meta-analysis of clinical trials
  5. Analysis of differentially expressed genes and signaling pathways involved in atherosclerosis and chronic obstructive pulmonary disease
  6. The epigenetic dimension of protein structure
  7. Gamma-induced mutants of Bacillus and Streptomyces display enhanced antagonistic activities and suppression of the root rot and wilt diseases in pulses
  8. Corticosterone potentiates ochratoxin A-induced microglial activation
  9. Supercomplex supercomplexes: Raison d’etre and functional significance of supramolecular organization in oxidative phosphorylation
  10. Insights into functional connectivity in mammalian signal transduction pathways by pairwise comparison of protein interaction partners of critical signaling hubs
  11. The effects of supplementation of Nannochloropsis oculata microalgae on biochemical, inflammatory and antioxidant responses in diabetic rats
  12. Molecular epidemiology of human papillomavirus in pregnant women in Burkina Faso
  13. Review Articles
  14. Interaction of cervical microbiome with epigenome of epithelial cells: Significance of inflammation to primary healthcare
  15. Seaweeds’ pigments and phenolic compounds with antimicrobial potential
  16. The capture of host cell’s resources: The role of heat shock proteins and polyamines in SARS-COV-2 (COVID-19) pathway to viral infection
  17. Erratum
  18. Erratum to “Plant growth-promoting properties of bacterial endophytes isolated from roots of Thymus vulgaris L. and investigate their role as biofertilizers to enhance the essential oil contents”
  19. Special Issue on XXV Congress of the Italian Society for Pure and Applied Biophysics
  20. Low-temperature librations and dynamical transition in proteins at differing hydration levels
  21. The phosphoinositide PI(3,5)P2 inhibits the activity of plant NHX proton/potassium antiporters: Advantages of a novel electrophysiological approach
  22. Targeted photoimmunotherapy for cancer
  23. Calorimetry of extracellular vesicles fusion to single phospholipid membrane
  24. Calcium signaling in prostate cancer cells of increasing malignancy
  25. Oxygen diffusion pathways in mutated forms of a LOV photoreceptor from Methylobacterium radiotolerans: A molecular dynamics study
  26. A photosensitizing fusion protein with targeting capabilities
  27. Ion channels and neuronal excitability in polyglutamine neurodegenerative diseases
  28. Is styrene competitive for dopamine receptor binding?
  29. Diffusion of molecules through nanopores under confinement: Time-scale bridging and crowding effects via Markov state model
  30. Quantitative active super-resolution thermal imaging: The melanoma case study
  31. Innovative light sources for phototherapy
  32. Electrophysiological study of the effects of side products of RuBi-GABA uncaging on GABAA receptors in cerebellar granule cells
  33. Subcellular elements responsive to the biomechanical activity of triple-negative breast cancer-derived small extracellular vesicles
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