Meningococcal Carriage among Household Contacts of Patients with Invasive Meningococcal Disease in Kathmandu, Nepal: A Longitudinal Study
Abstract
:1. Introduction
2. Results
2.1. Meningococal Carriage Rate among Houshold Contacts
2.2. Serogroup Distribution of Menincococcal Isolates
3. Discussion
4. Materials and Methods
4.1. Study Design
4.2. Sample Size
4.3. Inclusion Criteria
4.4. Exclusion Criteria
4.5. Sample Collection and Processing
4.6. Species Identification
4.7. Serogrouping
4.8. Ethical Approval
4.9. Data Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Basta, N.E.; Stuart, J.M.; Nascimento, M.C.; Manigart, O.; Trotter, C.; Hassan-King, M.; Chandramohan, D.; Sow, S.O.; Berthe, A.; Bedru, A.; et al. Methods for identifying Neisseria meningitidis carriers: A multi-center study in the African meningitis belt. PLoS ONE 2013, 8, e78336. [Google Scholar] [CrossRef]
- Cohn, J.M.A.A. Manual for the Surveillance of Vaccine-Preventable Diseases Chapter 8: Meningococcal Disease. Available online: http://www.cdc.gov/vaccines/pubs/surv-manual/chpt08-mening.html (accessed on 29 July 2016).
- CDC. Epidemiology and Prevention of Vaccine-Preventable Diseases: Meningococcal Disease. Available online: https://www.cdc.gov/vaccines/pubs/pinkbook/mening.html (accessed on 15 April 2019).
- Yazdankhah, S.P.; Caugant, D.A. Neisseria meningitidis: An overview of the carriage state. J. Med. Microbiol. 2004, 53 Pt 9, 821–832. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gonzales, M.L.; Bianco, V.; Vyse, A. Meningococcal carriage in children and young adults in the Philippines: A single group, cross-sectional study. Epidemiol. Infect. 2017, 145, 126–132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Krizova, P.; Kalmusova, J.; Musilek, M.; Felsberg, J.; Haugvicova, R.; Vlckova, J. Study of long-term and multiple carriage of Neisseria meningitidis in a healthy population using molecular biology methods. Epidemiol. Mikrobiol. Imunol. Cas. Spol. Epidemiol. Mikrobiol. Ceske Lek. Spol. JE Purkyne 2004, 53, 25–36. [Google Scholar]
- Trotter, C.L.; Greenwood, B.M. Meningococcal carriage in the African meningitis belt. Lancet Infect. Dis. 2007, 7, 797–803. [Google Scholar] [CrossRef] [Green Version]
- Stephens, D.S. Uncloaking the meningococcus: Dynamics of carriage and disease. Lancet 1999, 353, 941–942. [Google Scholar] [CrossRef]
- Trotter, C.L.; Maiden, M.C. Meningococcal vaccines and herd immunity: Lessons learned from serogroup C conjugate vaccination programs. Expert Rev. Vaccines 2009, 8, 851–861. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kepenekli Kadayifci, E.; Guneser Merdan, D.; Soysal, A.; Karaaslan, A.; Atici, S.; Durmaz, R.; Boran, P.; Turan, I.; Soyletir, G.; Bakir, M. Prevalence of Neisseria meningitidis carriage: A small-scale survey in Istanbul, Turkey. J. Infect. Dev. Ctries. 2016, 10, 413–417. [Google Scholar] [CrossRef] [Green Version]
- Bidmos, F.A.; Neal, K.R.; Oldfield, N.J.; Turner, D.P.; Ala’Aldeen, D.A.; Bayliss, C.D. Persistence, replacement, and rapid clonal expansion of meningococcal carriage isolates in a 2008 university student cohort. J. Clin. Microbiol. 2011, 49, 506–512. [Google Scholar] [CrossRef] [Green Version]
- Basta, N.E.; Berthe, A.; Keita, M.; Onwuchekwa, U.; Tamboura, B.; Traore, A.; Hassan-King, M.; Manigart, O.; Nascimento, M.; Stuart, J.M.; et al. Meningococcal carriage within households in the African meningitis belt: A longitudinal pilot study. J. Infect. 2018, 76, 140–148. [Google Scholar] [CrossRef] [Green Version]
- WHO. Control of Epidemic Meningococcal Disease. WHO Practical Guidelines, 2nd ed.; World Health Organization: Geneva, Switzerland, 1998. [Google Scholar]
- Cardeñosa, N.; Domínguez, A.; Orcau, A.; Pañella, H.; Godoy, P.; Minguell, S.; Camps, N.; Vázquez, J.A. Carriers of Neisseria meningitidis in household contacts of meningococcal disease cases in Catalonia (Spain). Eur. J. Epidemiol. 2001, 17, 877–884. [Google Scholar] [CrossRef]
- Cartwright, K.A.; Stuart, J.M.; Robinson, P.M. Meningococcal carriage in close contacts of cases. Epidemiol. Infect. 1991, 106, 133–141. [Google Scholar] [CrossRef] [Green Version]
- Simmons, G.; Martin, D.; Stewart, J.; Jones, N.; Calder, L.; Bremner, D. Carriage of Neisseria meningitidis among household contacts of patients with meningococcal disease in New Zealand. Eur. J. Clin. Microbiol. Infect. Dis. 2001, 20, 237–242. [Google Scholar] [CrossRef]
- Caugant, D.A.; Maiden, M.C. Meningococcal carriage and disease—Population biology and evolution. Vaccine 2009, 27 (Suppl. 2), B64–B70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Serra, L.; Presa, J.; Christensen, H.; Trotter, C. Carriage of Neisseria Meningitidis in Low and Middle Income Countries of the Americas and Asia: A Review of the Literature. Infect. Dis. Ther. 2020, 9, 209–240. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bhatta, D.R.; Gokhale, S.; Sharma, A.L.; Gupta, U.; Gaur, A.; Gowda, S.; Raut, S.; Thapa, S.; Khadka, R. Carrier state of Haemophilus influenzae type b (Hib), Streptococcus pneumoniae, Streptococcus pyogenes, Neisseria meningitidis and Corynebacterium diphtheriae among school children in Pokhara, Nepal. Asian Pac. J. Trop. Dis. 2014, 4, 45–49. [Google Scholar] [CrossRef]
- Thapa, S.; Gokhale, S.; Sharma, A.L.; Sapkota, L.B.; Ansari, S.; Gautam, R.; Shrestha, S.; Neopane, P. Burden of bacterial upper respiratory tract pathogens in school children of Nepal. BMJ Open Respir. Res. 2017, 4, e000203. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Manigart, O.; Okeakpu, J.; Odutola, A.; Jarju, S.; Foster-Nyarko, E.; Diallo, K.; Roca, A.; Kampmann, B.; D’Alessandro, U.; Sow, S.; et al. Alternative Molecular Methods for Improved Detection of Meningococcal Carriage and Measurement of Bacterial Density. J. Clin. Microbiol. 2016, 54, 2743–2748. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caugant, D.A.; Tzanakaki, G.; Kriz, P. Lessons from meningococcal carriage studies. FEMS Microbiol. Rev. 2007, 31, 52–63. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sharma, S.; Acharya, J.; Banjara, M.R.; Ghimire, P.; Singh, A. Comparison of acridine orange fluorescent microscopy and gram stain light microscopy for the rapid detection of bacteria in cerebrospinal fluid. BMC Res. Notes 2020, 13, 29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sharma, S.; Acharya, J.; Caugant, D.A.; Banjara, M.R.; Ghimire, P.; Singh, A. Detection of Streptococcus pneumoniae, Neisseria meningitidis and Haemophilus influenzae in Culture Negative Cerebrospinal Fluid Samples from Meningitis Patients Using a Multiplex Polymerase Chain Reaction in Nepal. Infect. Dis. Rep. 2021, 13, 173–180. [Google Scholar] [CrossRef]
- Cooper, L.V.; Kristiansen, P.A.; Christensen, H.; Karachaliou, A.; Trotter, C.L. Meningococcal carriage by age in the African meningitis belt: A systematic review and meta-analysis. Epidemiol. Infect. 2019, 147, e228. [Google Scholar] [CrossRef] [PubMed]
- MenAfriCar-Consortium. Household transmission of Neisseria meningitidis in the African meningitis belt: A longitudinal cohort study. Lancet Glob. Health 2016, 4, e989–e995. [Google Scholar] [CrossRef] [Green Version]
- Christensen, H.; May, M.; Bowen, L.; Hickman, M.; Trotter, C.L. Meningococcal carriage by age: A systematic review and meta-analysis. Lancet Infect. Dis. 2010, 10, 853–861. [Google Scholar] [CrossRef]
- Claus, H.; Maiden, M.C.; Wilson, D.J.; McCarthy, N.D.; Jolley, K.A.; Urwin, R.; Hessler, F.; Frosch, M.; Vogel, U. Genetic analysis of meningococci carried by children and young adults. J. Infect. Dis. 2005, 191, 1263–1271. [Google Scholar] [CrossRef]
- Goldschneider, I.; Gotschlich, E.C.; Artenstein, M.S. Human immunity to the meningococcus. II. Development of natural immunity. J. Exp. Med. 1969, 129, 1327–1348. [Google Scholar] [CrossRef]
- MacLennan, J.; Kafatos, G.; Neal, K.; Andrews, N.; Cameron, J.C.; Roberts, R.; Evans, M.R.; Cann, K.; Baxter, D.N.; Maiden, M.C.; et al. Social behavior and meningococcal carriage in British teenagers. Emerg. Infect. Dis. 2006, 12, 950–957. [Google Scholar] [CrossRef] [Green Version]
- Blakebrough, I.S.; Greenwood, B.M.; Whittle, H.C.; Bradley, A.K.; Gilles, H.M. The epidemiology of infections due to Neisseria meningitidis and Neisseria lactamica in a northern Nigerian community. J. Infect. Dis. 1982, 146, 626–637. [Google Scholar] [CrossRef] [PubMed]
- Mueller, J.E.; Sangare, L.; Njanpop-Lafourcade, B.M.; Tarnagda, Z.; Traore, Y.; Yaro, S.; Borrow, R.; Gessner, B.D.; Nicolas, P. Molecular characteristics and epidemiology of meningococcal carriage, Burkina Faso, 2003. Emerg. Infect. Dis. 2007, 13, 847–854. [Google Scholar] [CrossRef] [PubMed]
- De Wals, P.; Gilquin, C.; De Maeyer, S.; Bouckaert, A.; Noel, A.; Lechat, M.F.; Lafontaine, A. Longitudinal study of asymptomatic meningococcal carriage in two Belgian populations of schoolchildren. J. Infect. 1983, 6, 147–156. [Google Scholar] [CrossRef]
- Kristiansen, P.A.; Ba, A.K.; Ouedraogo, A.S.; Sanou, I.; Ouedraogo, R.; Sangare, L.; Diomande, F.; Kandolo, D.; Saga, I.M.; Misegades, L.; et al. Persistent low carriage of serogroup A Neisseria meningitidis two years after mass vaccination with the meningococcal conjugate vaccine, MenAfriVac. BMC Infect. Dis. 2014, 14, 663. [Google Scholar] [CrossRef] [Green Version]
- Mbaeyi, S.; Sampo, E.; Dinanibè, K.; Yaméogo, I.; Congo-Ouédraogo, M.; Tamboura, M.; Sawadogo, G.; Ouattara, K.; Sanou, M.; Kiemtoré, T.; et al. Meningococcal carriage 7 years after introduction of a serogroup A meningococcal conjugate vaccine in Burkina Faso: Results from four cross-sectional carriage surveys. Lancet Infect. Dis. 2020, 20, 1418–1425. [Google Scholar] [CrossRef]
- Tzeng, Y.L.; Thomas, J.; Stephens, D.S. Regulation of capsule in Neisseria meningitidis. Crit. Rev. Microbiol. 2016, 42, 759–772. [Google Scholar] [PubMed] [Green Version]
- Sharma, S.; Acharya, J.; Caugant, D.A.; Thapa, J.; Bajracharya, M.; Kayastha, M.; Sharma, S.; Chalise, B.S.; Karn, R.; Banjara, M.R.; et al. Meningococcal Meningitis: A Multicentric Hospital-based Study in Kathmandu, Nepal. Open Microbiol. J. 2019, 13, 273–278. [Google Scholar] [CrossRef] [Green Version]
- BCCDC. Communicable Disease Control Meningococcal Disease. Available online: http://www.bccdc.ca/resource-gallery/Documents/Guidelines%20and%20Forms/Guidelines%20and%20Manuals/Epid/CD%20Manual/Chapter%201%20-%20CDC/Meningococcal.pdf (accessed on 1 December 2017).
- Patrick, D.M.; Champagne, S.; Goh, S.H.; Arsenault, G.; Thomas, E.; Shaw, C.; Rahim, T.; Taha, F.; Bigham, M.; Dubenko, V.; et al. Neisseria meningitidis carriage during an outbreak of serogroup C disease. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2003, 37, 1183–1188. [Google Scholar] [CrossRef] [Green Version]
- Maiden, M.C.; Bygraves, J.A.; Feil, E.; Morelli, G.; Russell, J.E.; Urwin, R.; Zhang, Q.; Zhou, J.; Zurth, K.; Caugant, D.A.; et al. Multilocus sequence typing: A portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 1998, 95, 3140–3145. [Google Scholar] [CrossRef] [Green Version]
- Forbes, B.A.; Sahm, D.F.; Weissfeld, A.S. Bailey and Scott’s Diagnostic Microbiology, 12th ed.; Mosby Elsvier: Beijing, China, 2007. [Google Scholar]
- CDC. Meningococcal Disease. Available online: https://www.cdc.gov/meningococcal/index.html (accessed on 15 January 2017).
Age Group | Male Number (%) | Female Number (%) | Total Number | ||
---|---|---|---|---|---|
Participants | Meningococcal Carriers | Participants | Meningococcal Carriers | ||
Child (1–10 years) | 4 (50) | - | 4 (50) | - | 8 |
Adolescent (10–19 years) | 3 (30) | - | 7 (70) | - | 10 |
Adults (19–45 years) | 26 (41) | 2 (8) | 38 (59) | 5 (13) | 64 |
Adults (above 45 years) | 23 (53) | 7 (30) | 20 (47) | 5 (25) | 43 |
Total Number | 56 | 9 | 69 | 10 | 125 |
Number of Visit | Day of Sample Collection | Participants Positive for Meningococci | |
---|---|---|---|
Number | Percentage | ||
1st | 0 | 19 | 15 |
2nd | 15 | 8 | 7 |
3rd | 30 | 5 | 4 |
4th | 45 | 2 | 2 |
5th | 60 | 2 | 2 |
6th | 90 | 0 | - |
7th | 120 | 0 | - |
8th | 150 | 0 | - |
9th | 180 | 0 | - |
Carrier Number | Visit No. (Day of Throat Swab Sample Collection) | ||||||||
---|---|---|---|---|---|---|---|---|---|
1st (0) | 2nd (15) | 3rd (30) | 4th (45) | 5th (60) | 6th (90) | 7th (120) | 8th (150) | 9th (180) | |
1 | A | A | A | A | A | - | - | - | - |
2 | A | - | A | - | - | - | - | - | - |
3 | A | - | - | - | - | - | - | - | - |
4 | NG | NG | NG | - | - | - | - | - | - |
5 | NG | - | - | - | - | - | - | - | - |
6 | NG | - | - | - | - | - | - | - | - |
7 | A | - | A | - | - | - | - | - | - |
8 | NG | NG | - | - | - | - | - | - | - |
9 | NG | - | - | - | - | - | - | - | - |
10 | A | A | A | A | A | - | - | - | - |
11 | NG | NG | - | - | - | - | - | - | - |
12 | NG | NG | - | - | - | - | - | - | - |
13 | NG | - | - | - | - | - | - | - | - |
14 | A | A | - | - | - | - | - | - | - |
15 | NG | - | - | - | - | - | - | - | - |
16 | A | A | - | - | - | - | - | - | - |
17 | NG | - | - | - | - | - | - | - | - |
18 | A | - | - | - | - | - | - | - | - |
19 | NG | - | - | - | - | - | - | - | - |
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Sharma, S.; Acharya, J.; Caugant, D.A.; Aryal, S.; Banjara, M.R.; Ghimire, P.; Singh, A. Meningococcal Carriage among Household Contacts of Patients with Invasive Meningococcal Disease in Kathmandu, Nepal: A Longitudinal Study. Pathogens 2021, 10, 781. https://doi.org/10.3390/pathogens10070781
Sharma S, Acharya J, Caugant DA, Aryal S, Banjara MR, Ghimire P, Singh A. Meningococcal Carriage among Household Contacts of Patients with Invasive Meningococcal Disease in Kathmandu, Nepal: A Longitudinal Study. Pathogens. 2021; 10(7):781. https://doi.org/10.3390/pathogens10070781
Chicago/Turabian StyleSharma, Supriya, Jyoti Acharya, Dominique A. Caugant, Shreedhar Aryal, Megha Raj Banjara, Prakash Ghimire, and Anjana Singh. 2021. "Meningococcal Carriage among Household Contacts of Patients with Invasive Meningococcal Disease in Kathmandu, Nepal: A Longitudinal Study" Pathogens 10, no. 7: 781. https://doi.org/10.3390/pathogens10070781
APA StyleSharma, S., Acharya, J., Caugant, D. A., Aryal, S., Banjara, M. R., Ghimire, P., & Singh, A. (2021). Meningococcal Carriage among Household Contacts of Patients with Invasive Meningococcal Disease in Kathmandu, Nepal: A Longitudinal Study. Pathogens, 10(7), 781. https://doi.org/10.3390/pathogens10070781