Hospital-based prospective study of pertussis in infants and close contacts in Tehran, Iran

Gaelle Noel, Masoumeh Nakhost Lotfi, Sajedeh Mirshahvalad, Sedaghatpour Mahdi, David Tavel, Seyed M Zahraei, Roxana Mansour Ghanaie, Tahereh Heidary, Aliahmad Goudarzi, Azardokht Kazemi, Abdollah Karimi, Alireza Nateghian, Mohand Ait-Ahmed, Nicole Guiso, Fereshteh Shahcheraghi, Fabien Taieb, Gaelle Noel, Masoumeh Nakhost Lotfi, Sajedeh Mirshahvalad, Sedaghatpour Mahdi, David Tavel, Seyed M Zahraei, Roxana Mansour Ghanaie, Tahereh Heidary, Aliahmad Goudarzi, Azardokht Kazemi, Abdollah Karimi, Alireza Nateghian, Mohand Ait-Ahmed, Nicole Guiso, Fereshteh Shahcheraghi, Fabien Taieb

Abstract

Background: Pertussis remain a global health concern, especially in infants too young to initiate their vaccination. Effective vaccination and high coverage limit the circulation of the pathogen, yet duration of protection is limited and boosters are recommended during a lifetime. In Iran, boosters are given at 18 months and 6 years old using whole pertussis vaccines for which efficacy is not known, and pertussis surveillance is scant with only sporadic biological diagnosis. Burden of pertussis is not well understood and local data are needed.

Methods: Hospital-based prospective study implementing molecular laboratory testing in infants aged ≤6 months and presenting ≥5 days of cough associated to one pertussis-like symptom in Tehran. Household and non-household contact cases of positive infants were evaluated by comprehensive pertussis diagnosis (molecular testing and serology) regardless of clinical signs. Clinical evaluation and source of infection were described.

Results: A total of 247 infants and 130 contact cases were enrolled. Pertussis diagnosis result was obtained for 199 infants and 104 contact cases. Infant population was mostly < 3 months old (79.9%; 157/199) and unvaccinated (62.3%; 124/199), 20.1% (40/199) of them were confirmed having B. pertussis infection. Greater cough duration and lymphocyte counts were the only symptoms associated to positivity. Half of the contact cases (51.0%; 53/104) had a B. pertussis infection, median age was 31 years old. A proportion of 28.3% (15/53) positive contacts did not report any symptom. However, 67.9% (36/53) and 3.8% (2/53) of them reported cough at inclusion or during the study, including 20.8% (11/53) who started coughing ≥7 days before infant cough onset. Overall, only five samples were successfully cultured.

Conclusion: These data evidenced the significant prevalence of pertussis infection among paucy or poorly symptomatic contacts of infants with pertussis infection. Widespread usage of molecular testing should be implemented to identify B. pertussis infections.

Keywords: Contact; Diagnosis; Infant; Infection; Pertussis; Vaccine compliance; Whole-cell vaccine.

Conflict of interest statement

The authors have declared that no conflict of interests exist.

Figures

Fig. 1
Fig. 1
Flow chart of index (a) and contact (b) cases included in the analysis
Fig. 2
Fig. 2
Distribution of primary (a) and secondary (b) cases with respect to the index case among positive contacts. yo, years old

References

    1. Yeung KHT, Duclos P, Nelson EAS, Hutubessy RCW. An update of the global burden of pertussis in children younger than 5 years: a modelling study. Lancet Infect Dis. 2017;17(9):974–980. doi: 10.1016/S1473-3099(17)30390-0.
    1. World Health Organization Pertussis vaccines: WHO position paper. Wkly Epidemiol Rec 2010. 2010;85:385–400.
    1. World Health Organization Pertussis vaccines: WHO position paper. Wkly Epidemiol Rec 2015. 2015;90:433–458.
    1. von Koenig CHW, Guiso N. Global burden of pertussis: signs of hope but need for accurate data. Lancet Infect Dis. 2017;17(9):889–890. doi: 10.1016/S1473-3099(17)30357-2.
    1. WHO UNICEF estimates time series for Iran (Islamic Republic of) (IRN). WHO vaccine-preventable diseases: monitoring system. 2020 global summary. Available from: . Accessed 30 Oct 2020.
    1. World Health Organization: Incidence time series for Iran (Islamic Republic of) (IRN). WHO vaccine-preventable diseases: monitoring system. 2020 global summary. Available from: . Accessed 30 Oct 2020.
    1. Safarchi A, Octavia S, Nikbin VS, Lotfi MN, Zahraei SM, Tay CY, Lamichhane B, Shahcheraghi F, Lan R. Genomic epidemiology of Iranian Bordetella pertussis: 50 years after the implementation of whole cell vaccine. Emerg Microbes Infect. 2019;8(1):1416–1427. doi: 10.1080/22221751.2019.1665479.
    1. Sedaghat M, Nakhost Lotfi M, Talebi M, Saifi M, Pourshafie MR. Status of pertussis in Iran. Jundishapur J Microbiol. 2014;7(11):e12421. doi: 10.5812/jjm.12421.
    1. Khazaei S, Ayubi E, Mansori K, Khazaei S. Pertussis incidence by time, province and age Group in Iran, 2006-2011. Iran J Public Health. 2016;45(11):1525–1527.
    1. Noel G, Badmasti F, Nikbin VS, Zahraei SM, Madec Y, Tavel D, Aït-Ahmed M, Guiso N, Shahcheraghi F, Taieb F. Transversal sero-epidemiological study of Bordetella pertussis in Tehran, Iran. PLoS One. 2020;15(9):e0238398. doi: 10.1371/journal.pone.0238398.
    1. Ghanaie RM, Karimi A, Sadeghi H, Esteghamati A, Fallah F, Armin S, Fahimzad SA, Ghanaie MM, Shamshiri A, Shiva F. Frequency of pertussis in iranian school-age children. J Pediatr Infect Dis. 2013;08(01):001–005. doi: 10.3233/JPI-130380.
    1. World Health Organization . Laboratory manual for the diagnosis of whooping cough caused by Bordetella pertussis/Bordetella parapertussis. In. Edited by WHO/IPV/14.03. 2014.
    1. Riffelmann M, Wirsing von König CH, Caro V, Guiso N, for the Pertussis PCRCG Nucleic acid amplification tests for diagnosis of Bordetella infections. J Clin Microbiol. 2005;43(10):4925–4929. doi: 10.1128/JCM.43.10.4925-4929.2005.
    1. Katfy K, Guiso N, Diawara I, Zerouali K, Slaoui B, Jouhadi Z, Zineddine A, Belabbes H, Elmdaghri N. Epidemiology of pertussis in Casablanca (Morocco): contribution of conventional and molecular diagnosis tools. BMC Infect Dis. 2017;17(1):348. doi: 10.1186/s12879-017-2452-3.
    1. Njamkepo E, Bonacorsi S, Debruyne M, Gibaud SA, Guillot S, Guiso N. Significant finding of Bordetella holmesii DNA in nasopharyngeal samples from French patients with suspected pertussis. J Clin Microbiol. 2011;49(12):4347–4348. doi: 10.1128/JCM.01272-11.
    1. Riffelmann M, Thiel K, Schmetz J, Wirsing von Koenig CH. Performance of commercial enzyme-linked Immunosorbent assays for detection of antibodies to Bordetella pertussis. J Clin Microbiol. 2010;48(12):4459–4463. doi: 10.1128/JCM.01371-10.
    1. Gill CJ, Gunning CE, MacLeod W, Mwananyanda L, Thea D, Pieciak R, et al. Asymptomatic Bordetella pertussis infections in young African infants and their mothers identified within a longitudinal cohort. medRxiv : the preprint server for health sciences, 2020.11.18.20231423. 10.1101/2020.11.18.20231423. Preprint.
    1. World Health O. WHO child growth standards : length/height-for-age, weight-for-age, weight-for-length, weight -for-height and body mass index-for-age : methods and development. Geneva: World Health Organization; 2006.
    1. Shojaei J, Saffar M, Hashemi A, Ghorbani G, Rezai M, Shahmohammadi S. Clinical and laboratory features of pertussis in hospitalized infants with confirmed versus probable pertussis cases. Ann Med Health Sci Res. 2014;4(6):910–914. doi: 10.4103/2141-9248.144911.
    1. Muloiwa R, Nicol MP, Hussey GD, Zar HJ. Diagnostic limitations of clinical case definitions of pertussis in infants and children with severe lower respiratory tract infection. PLoS One. 2020;15(7):e0235703. doi: 10.1371/journal.pone.0235703.
    1. Tozzi AE, Gesualdo F, Rizzo C, Carloni E, Russo L, Campagna I, Villani A, Reale A, Concato C, Linardos G, Pandolfi E. A data driven clinical algorithm for differential diagnosis of pertussis and other respiratory infections in infants. PLoS One. 2020;15(7):e0236041. doi: 10.1371/journal.pone.0236041.
    1. Loeffelholz M. Towards improved accuracy of Bordetella pertussis nucleic acid amplification tests. J Clin Microbiol. 2012;50(7):2186–2190. doi: 10.1128/JCM.00612-12.
    1. Rejali M, Mohammadbeigi A, Mokhtari M, Zahraei SM, Eshrati B. Timing and delay in children vaccination; evaluation of expanded program of immunization in outskirt of Iranian cities. JRHS. 2015;15(1):54–58.
    1. Merdrignac L, Aït El Belghiti F, Pandolfi E, Jané M, Murphy J, Fabiánová K, García Cenoz M, Flem E, Guillot S, Tozzi AE, et al. Incidence and severity of pertussis hospitalisations in infants aged less than 1 year in 37 hospitals of six EU/EEA countries, results of PERTINENT sentinel pilot surveillance system, December 2015 to December 2018. Euro Surveill. 2021;26(4):1900762. doi: 10.2807/1560-7917.ES.2021.26.4.1900762.
    1. Ghanaie RM, Karimi A, Sadeghi H, Esteghamti A, Falah F, Armin S, Fahimzad A, Shamshiri A, Kahbazi M, Shiva F. Sensitivity and specificity of the World Health Organization pertussis clinical case definition. Int J Infect Dis. 2010;14(12):e1072–e1075. doi: 10.1016/j.ijid.2010.07.005.
    1. Siriyakorn N, Leethong P, Tantawichien T, Sripakdee S, Kerdsin A, Dejsirilert S, Paitoonpong L. Adult pertussis is unrecognized public health problem in Thailand. BMC Infect Dis. 2016;16:25. doi: 10.1186/s12879-016-1357-x.
    1. Barkoff A-M, Gröndahl-Yli-Hannuksela K, He Q. Seroprevalence studies of pertussis: what have we learned from different immunized populations. Pathog Dis. 2015;73(7):ftv050. doi: 10.1093/femspd/ftv050.
    1. Wiley KE, Zuo Y, Macartney KK, McIntyre PB. Sources of pertussis infection in young infants: a review of key evidence informing targeting of the cocoon strategy. Vaccine. 2013;31(4):618–625. doi: 10.1016/j.vaccine.2012.11.052.
    1. Baptista PN, Magalhães V, Rodrigues LC, Rocha MÂW, Pimentel AM. Source of infection in household transmission of culture-confirmed pertussis in Brazil. Pediatr Infect Dis J. 2005;24(11):1027. doi: 10.1097/01.inf.0000186293.85867.e8.
    1. Esposito S, Principi N. Immunization against pertussis in adolescents and adults. Clin Microbiol Infect. 2016;22:S89–S95. doi: 10.1016/j.cmi.2016.01.003.
    1. Mansour Ghanaie R, Moradi-Lakeh M, Karimi A, Yaghoubi M, Amiraslany A, Gill A, Zahraei SM. Future strategic plan for national immunisation program in Iran: cost effectiveness of acellular pertussis versus whole-cell. Int J Foresight Innov Policy. 2018;13(1/2):136. doi: 10.1504/IJFIP.2018.095865.
    1. Romanin V, Acosta AM, Juarez MDV, Briere E, Sanchez SM, Cordoba BL, Sevilla ME, Lucion MF, Urrutia A, Sagradini S, Skoff TH, Vizzotti C. Maternal vaccination in Argentina: tetanus, diphtheria, and Acellular pertussis vaccine effectiveness during pregnancy in preventing pertussis in infants <2 months of age. Clin Infect Dis. 2020;70(3):380–387. doi: 10.1093/cid/ciz217.
    1. De Barros ENC, Nunes AA, Abreu AJL, Furtado BE, Cintra O, Cintra MA, Coelho EB. Pertussis epidemiological pattern and disease burden in Brazil: an analysis of national public health surveillance data. Hum Vaccin Immunother. 2020;16(1):61–69. doi: 10.1080/21645515.2019.1634991.
    1. Hincapié-Palacio D, Hoyos MC, Ochoa J, Montoya N, García D, Osorio E. Effect of maternal immunization against pertussis in Medellin and the metropolitan area, Colombia, 2016–2017. Vaccine. 2018;36(27):3984–3991. doi: 10.1016/j.vaccine.2018.05.020.
    1. Switzer C, D'Heilly C, Macina D. Immunological and clinical benefits of maternal immunization against pertussis: a systematic review. Infect Dis Ther. 2019;8(4):499–541. doi: 10.1007/s40121-019-00264-7.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe