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Immunization Coverage Surveys and Linked Biomarker Serosurveys in Three Regions in Ethiopia

Sunday, 6th of March 2016 Print

Immunization Coverage Surveys and Linked Biomarker Serosurveys in Three Regions in Ethiopia

Mark A. Travassos et al.

 

Excerpts below; full text is at http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0149970

 

Abstract

Objective

Demographic and health surveys, immunization coverage surveys and administrative data often divergently estimate vaccination coverage, which hinders pinpointing districts where immunization services require strengthening. We assayed vaccination coverage in three regions in Ethiopia by coverage surveys and linked serosurveys.

Methods

Households with children aged 12–23 (N = 300) or 6–8 months (N = 100) in each of three districts (woredas) were randomly selected for immunization coverage surveys (inspection of vaccination cards and immunization clinic records and maternal recall) and linked serosurveys. IgG-ELISA serologic biomarkers included tetanus antitoxin ≥ 0.15 IU/ml in toddlers (receipt of tetanus toxoid) and Haemophilus influenzae type b (Hib) anti-capsular titers ≥ 1.0 mcg/ml in infants (timely receipt of Hib vaccine).

Findings

Coverage surveys enrolled 1,181 children across three woredas; 1,023 (87%) also enrolled in linked serosurveys. Administrative data over-estimated coverage compared to surveys, while maternal recall was unreliable. Serologic biomarkers documented a hierarchy among the districts. Biomarker measurement in infants provided insight on timeliness of vaccination not deducible from toddler results.

Conclusion

Neither administrative projections, vaccination card or EPI register inspections, nor parental recall, substitute for objective serological biomarker measurement. Including infants in serosurveys informs on vaccination timeliness.

Citation: Travassos MA, Beyene B, Adam Z, Campbell JD, Mulholland N, Diarra SS, et al. (2016) Immunization Coverage Surveys and Linked Biomarker Serosurveys in Three Regions in Ethiopia. PLoS ONE 11(3): e0149970. doi:10.1371/journal.pone.0149970

Editor: Caroline L. Trotter, University of Cambridge, UNITED KINGDOM

Received: September 14, 2015; Accepted: February 7, 2016; Published: March 2, 2016

Copyright: © 2016 Travassos et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and supporting material.

Funding: This work was supported by Bill & Melinda Gates Foundation Grant OPP1017350. The findings and conclusions contained within are those of the authors and do not necessarily reflect positions or policies of the Bill & Melinda Gates Foundation. The Foundation had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. JSI Research & Training Institute Inc. provided support in the form of salaries for authors (ZA, LO, JS, RS). Other than these authors, JSI did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors (ZA, LO, JS, RS) are articulated in the "author contributions" section.

Competing interests: Zenaw Adam, Lisa Oot, Jenny Sequeira and Robert Steinglass are employed by JSI Research & Training Institute Inc. There are no patents, products in development or marketed products to declare. This does not alter the authors´ adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors. Authors from the Center for Vaccine Development of the University of Maryland (CVD) and from the Ethiopian Public Health Institute (EPHI), representing a state academic institution (CVD) and a national governmental institution (EPHI), respectively, declare that they have no competing interests. The role of JSI investigators in the serosurvey study does not alter the authors´ adherence to all PLOS ONE policies on sharing data and materials.

Introduction

Given the contribution of infant immunization to plummeting young child mortality during the past 15 years[1,2], Gavi- the Vaccine Alliance, the Advanced Market Commitment and other donors have supported the introduction of costly new vaccines such as Haemophilus influenzae type b [Hib] conjugate, pneumococcal conjugates and rotavirus vaccines into the Expanded Program on Immunization (EPI) in developing countries [3]. Gavi also strengthens immunization services infrastructure based on a reward system for countries that measurably increase the number of children who receive three doses of diphtheria toxoid/tetanus toxoid/whole cell pertussis vaccine (DTP3 coverage) [3]. Ethiopia´s EPI, launched in 1980, administers BCG and oral polio vaccine (OPV) at birth; OPV, pentavalent vaccine (DTP, Hib conjugate and hepatitis B virus vaccine), and pneumococcal conjugate at ages six, 10 and 14 weeks; and measles vaccine at nine months. Daunting challenges confront the Ethiopian EPI as it grapples to deliver these vaccines to all infants in a timely way in a largely rural population that is sparsely dispersed in mountainous regions and often nomadic in arid areas [4]. Frustratingly, data from sources that should pinpoint districts needing improved immunization services are often starkly conflicting. For example, the Ethiopian national DTP3 coverage in 2010 based on official administrative estimates (number of vaccine doses administered by EPI to the target population divided by the number of target subjects [from census data]) was 86% [5]. In contrast, World Health Organization / United Nations Children´s Fund (WHO/UNICEF) joint reporting estimated 2010 DTP3 coverage at 63% [6,7], and a nationwide Demographic and Health Survey estimated only 37% DTP3 coverage based on sampling vaccination cards and parental recall [8].

With proper sampling and questionnaires, cluster surveys estimate the proportion of children who have received a particular vaccine [9–11]. However, since such surveys cannot indicate the quality of the vaccines administered nor can they confirm that a child given high-quality vaccine actually mounted an adequate immune response indicating protection, some have referred what coverage surveys measure as “coverage” and what biomarker surveys measure as “effective coverage” [11,12]. For these reasons, serosurveys that measure objective biomarkers performed concomitantly with immunization coverage cluster surveys are complementary tools to assess the performance of immunization services [11,13].

Serological biomarkers selected with respect to age, titer cut-offs and epidemiological facts can gauge immunization services´ effectiveness and timeliness. For example, tetanus antitoxin in toddlers derive only from immunization [14,15]. Whereas Hib anti-capsular polysaccharide [polyribosyl ribitol phosphate (PRP)] in toddlers may have derived from either infection with Hib or cross reacting bacteria, a high titer (≥ 1.0 mcg/ml) of anti-PRP in infants age 6–8 months denotes recent immunization rather than maternal transfer or infection-derived origin and also connotes durable protection [16–18]. Measuring specific antibodies also helps evaluate the integrity of the cold chain that underpins immunization services, since most vaccines must be assiduously maintained in the cold chain, lest they lose potency [15]. Live virus vaccines can be adversely affected by elevated temperatures, while protein-based vaccines can denature if inadvertently frozen [19]. Serosurvey biomarkers estimate objectively the prevalence of immunized (i.e., protected) children, irrespective of the prevalence of inoculated children (i.e., to whom vaccine was administered).

We linked serosurveys to immunization coverage surveys to measure the proportion of children protected against two pentavalent vaccine-preventable diseases (tetanus and invasive Hib) in three regions in Ethiopia [20]. Whereas coverage surveys typically focus on 12–23 month olds [21], we also sampled 6–8 month olds to assess the timeliness of infant immunization [22–24]. Overall, serologic biomarker measurements documented a hierarchy among the woredas, with Hintalo Wajerate (Tigray Region) showing the highest coverage. We found that objective serological biomarker measurements were not adequately estimated by administrative projections, vaccination card or EPI register inspections, or parental recall.

Materials and Methods

In each of three administrative districts (woredas), 400 hundred children (N = 1200 total) were randomly selected to participate in immunization coverage surveys and accompanying serosurveys, from February to April 2013, lasting between 12 to 20 days in each woreda [20]. The selected districts, some of which had recent outbreaks of vaccine-preventable disease, included: Hintalo Wajerate woreda in Tigray Region (primarily agrarian with high administrative estimates of vaccine coverage); Arbegona in Southern Nations, Nationalities, and Peoples´ Region (“SNNPR”) (primarily agrarian, with lower administrative estimates of vaccine coverage); and Assaieta in Afar Region (pastoralist area with nomadic clans and low administrative estimates of vaccine coverage). Each woreda was selected by Ethiopian EPI and JSI Research & Training Institute, Inc. (JSI) to inform a Federal Ministry of Health (FMOH) evidence-based decision on how to pursue nationwide universal child immunization. The coverage survey sample per woreda was 300 toddlers aged 12–23 months and 100 infants aged 6–8 months. The serosurvey enrollment target was 60% of coverage survey enrollment.

The serosurvey protocol and consent procedure were approved by the Ethiopian National Research Ethics Review Committee and the University of Maryland, Baltimore Institutional Review Board. Written informed consent was obtained from parents or caretakers of each child enrolled in the serosurvey. Informed consent was documented by the use of a written consent form approved by the IRBs and signed or thumb printed by the parent or caretaker. Participation in the immunization coverage survey, a routine FMOH public health endeavor, did not require informed consent.

Coverage surveys

Data were obtained by “JSI-type” coverage surveys that examine vaccination cards provided by parents/caretakers, record “parental recall” if cards were not available and peruse registers at health facilities where immunizations are administered to identify records of children whose parents claimed that they had been vaccinated but were unable to exhibit immunization cards [20].

Antibody biomarker measurements

Serum IgG antibodies to vaccine antigens measured by ELISA served as biomarkers of acquisition of protective titers from vaccination or from wild type infection [22,25]. Protective titers of tetanus antitoxin in toddlers age 12–23 months denote successful immunization with pentavalent vaccine, which contains tetanus toxoid. A cut-off of ≥ 0.15 IU/ml, which correlates well with toxin neutralization [26], was the biomarker used for denoting subjects immunized with tetanus toxoid [25,27–30].

In infants age 6–8 months, a high (≥ 1.0 mcg/ml) titer of serum Hib IgG anti-PRP constitutes a biomarker that the infant received pentavalent vaccine in an age range approximating the recommended EPI schedule [22]. The anti-PRP biomarker is less useful in toddlers because by that age antibodies may also derive from natural exposure to Hib or similar bacteria [17].

Statistics

A coverage survey child was considered immunized if she/he received three pentavalent vaccine doses via the routine EPI or via outreach or supplemental immunization activities. Results were compared against government administrative estimates of regional vaccine coverage (Health Sector Development Program (HSDP) IV. Woreda Based Health Sector Annual Core Plan); the administrative estimates were treated as constants in this analysis, since no measures of uncertainty were provided with them. The planned sample sizes of 300 toddlers aged 12–23 months and 100 infants aged 6–8 months per woreda for the coverage survey were the largest considered feasible. Assuming a design effect of 2 and 60% of the sample in the serosurvey, the width of exact two-sided 95% confidence intervals (CI´s) for the proportion of 12–23 month olds protected would be 21.5% and 17.4% for observed proportions of 50% and 80%, respectively; the power to show a significant difference from an administrative estimate of 90% would be approximately 0.82 for a true proportion protected of 80%.

Assuming the antibody biomarker gave the true status, positive predictive values (PPV) were calculated as the proportion of children positive by the antibody biomarker among children scored as positive by a coverage survey method of interest (vaccination card, scrutiny of immunization records or maternal recall) (true positives/[true positives + false positives]). Negative predictive values (NPV) were calculated as the proportion of children negative by the antibody biomarker among children scored as negative by a coverage survey method of interest (vaccination card, scrutiny of immunization records or maternal recall) (true negatives/[false negatives + true negatives]).

. . .

Discussion

Gavi and other international agencies are scrutinizing how countries monitor the effectiveness of their immunization services, provide credible data to justify the financial investments, and identify under-performing districts needing improvements. Given this, coupling serosurveys that quantitatively measure biomarkers of immunization (or of seroprotection) with immunization coverage surveys in three rural districts of Ethiopia has yielded revelations of broad implication and utility: 1) corroboration of the inaccuracy of administrative estimates of vaccine coverage, which over-estimate coverage where immunization services are weak, i.e., where improvements are most needed [31]; 2) the erroneousness of parental recall in the rural Ethiopian setting, lending credence to the notion that in certain populations recall data should not be relied upon for decision making [11,13,32]; and 3) scrutinizing EPI registers, in addition to inspecting immunization cards, improves coverage survey accuracy but increases workload and provides no information on the immunization status of children lacking any documentation.

The detection of toddlers having a protective tetanus antitoxin biomarker added an objective benchmark to the survey and EPI register data. This is one of the first serosurveys in a pediatric population that received DTP vaccine bundled within pentavalent vaccine. The serum IgG tetanus antitoxin biomarker in toddlers clearly differentiated the three woredas, with Hintalo Wajerate exhibiting the highest prevalence of pentavalent-immunized toddlers, followed by Arbegona and Assaieta. In all three woredas, toddlers who had documented receipt of 2–3 doses of pentavalent vaccine by immunization card or by EPI register record had a high prevalence of tetanus antitoxin biomarkers.

Importantly, by including Hib PRP antibody biomarker measurement in 6–8 month old infants, invaluable information was derived on the timeliness of immunization with pentavalent vaccine. It is critical to adhere closely to the EPI schedule to maximize prevention of pertussis and invasive Hib disease, since pertussis deaths cluster in the first few months of infancy [33] and in sub-Saharan Africa Hib peaks at age 6–7 months [34]. Ordinarily age 6–8 months represents the nadir for prevalence of PRP antibody titers ≥ 1.0 mcg/ml; thus, absent pentavalent immunization, few African infants this age exhibit this biomarker [17,35]. Even in Hintalo Wajerate, the prevalence of protective PRP titers in infants was only 68% and was only 41% and 31% in the other woredas (Table 1). The infant biomarker measurements indicate that immunizations are being delivered later than scheduled in all woredas [36]. Indeed, in two woredas most 6–8 month olds sampled were vulnerable to pentavalent-vaccine preventable diseases, in contrast to toddlers from the same populations.

Vaccination record-keeping in Arbegona and Assaieta was problematic. In Arbegona, many children were apparently being vaccinated without a record, since 41% of toddlers lacking vaccination records exhibited protective tetanus antitoxin biomarkers. This phenomenon has also been reported in Africa among mothers women post-delivery in whom the prevalence of a history of prenatal tetanus toxoid vaccination was lower than the prevalence of tetanus antitoxin biomarker [37]. These findings can prompt action to improve immunization services in Arbegona. In Assaieta, where a proportion of the population is nomadic, some vaccines (particularly measles) are delivered via supplemental mass campaigns during which vaccination cards are not generally given to caretakers. Failure to issue immunization cards and poor record keeping at EPI vaccination units and during mass immunization campaigns are well-recognized sources of error in trying to interpret immunization coverage [11,32].

The Ethiopian experience of conducting concurrent coverage surveys and biomarker serosurveys in the same populations, a pioneering public health approach in Ethiopia and only rarely undertaken elsewhere [12,13,38], posed substantial logistical and other challenges but provided critical insights into the effectiveness of local EPI programs. In all three regions experienced phlebotomists overcame the challenge of collecting venous blood from infants and toddlers in the field, allowing us to measure tetanus and PRP antibodies in serum, a gold standard. However, to expand the use of serosurveys in developing countries, alternatives to venous blood collection must be considered to enhance practicality and economy. Emerging technologies are providing solutions to accomplish this. For example, collecting dried whole blood spots on filter papers following finger stick entirely avoid the need for skilled pediatric phlebotomists [39,40], having to centrifuge blood under field conditions and having to keep sera frozen. Collecting oral fluid specimens (which contain crevicular fluid rich in IgG) allows testing for IgG tetanus antitoxin [25] and other vaccine antibodies [41–43], while entirely eliminating the need for use of sharps. Indeed, portable point-of-care devices that detect protective IgG antibody biomarkers of vaccination in oral fluid that correlate closely with serum antibody levels are undergoing field trials.

Serosurveys (the term is used broadly here to include surveys that collect oral fluids) that measure tetanus antitoxin in toddlers in different districts can allow public health authorities in developing countries to monitor objectively the proportion of toddlers that have received DPT or pentavalent vaccine. In this way, districts can be assessed comparatively for the quality of the immunization services serving their populations [12]. Including 6–8 month old infants in whom PRP antibody biomarkers are measured can provide insights on the timeliness of immunization with pentavalent vaccine. Under-performing districts can be identified and remedial interventions introduced, while districts with objective biomarker evidence of high vaccination coverage can be studied to try and identify why such districts stand out. Such serosurveys can be carried out with or without an accompanying immunization coverage survey.

Supporting Information

S1 Dataset. Coverage survey findings and serological biomarker measurements of study participants.

doi:10.1371/journal.pone.0149970.s001

(XLSX)

Acknowledgments

We thank the families and communities for their participation in this study; field staff for their hard work and dedication; and the woreda health offices at each site that generously provided facilities, resources, and personnel for the conduct of the study.

Author Contributions

Conceived and designed the experiments: RS MML MAT SOS JDC MFP AK LO JS ZA BB. Performed the experiments: MAT ZA JDC NM SSD TK MR IR JG. Analyzed the data: MAT BB ZA JDC LO JS MR WCB YW MFP RS AK MML. Contributed reagents/materials/analysis tools: WCB YW MFP MML. Wrote the paper: MAT MML BB ZA JDC LO RS AK. Supervised the laboratory assays: MR MFP. Performed laboratory assays: MR IR JG. Data management: MAT BB SSD TK MR MFP WCB YW.

References

  1. 1. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 2012 May 10. doi: 10.1016/s0140-6736(12)60560-1
  2. 2. Bhutta ZA, Black RE. Global maternal, newborn, and child health—so near and yet so far. N Engl J Med 2013 Dec 5;369(23):2226–35. doi: 10.1056/NEJMra1111853. pmid:24304052
  3. 3. Orenstein WA, Seib K, Graham-Rowe D, Berkley S. Contemporary vaccine challenges: improving global health one shot at a time. Sci Transl Med 2014 Sep 10;6(253):253ps11. doi: 10.1126/scitranslmed.3009848. pmid:25210061
  4. 4. Okwaraji YB, Mulholland K, Schellenberg JR, Andarge G, Admassu M, Edmond KM. The association between travel time to health facilities and childhood vaccine coverage in rural Ethiopia. A community based cross sectional study. BMC Public Health 2012 Jun 22;12:476. doi: 10.1186/1471-2458-12-476.:476–12. pmid:22726457
  5. 5. UNICEF. State of the World´s Children 2012. Children in an Urban World. 1–142. 2012. New Jersey, Hatteras Press.
  6. 6. WHO and UNICEF. Ethiopia: WHO and UNICEF estimates of immunization coverage: 2013 revision. 2014.
  7. 7. Burton A, Monasch R, Lautenbach B, Gacic-Dobo M, Neill M, Karimov R, et al. WHO and UNICEF estimates of national infant immunization coverage: methods and processes. Bull World Health Organ 2009 Jul;87(7):535–41. pmid:19649368 doi: 10.2471/blt.08.053819
  8. 8. Central Statistical Agency EaIICM. Ethiopia Demographic and Health Survey 2011. Calverton, MD: ICF International; 2012 Mar.
  9. 9. World Health Organization VAaMTDoIVaB. Immunization coverage cluster survey—Reference manual. 2005. Geneva, WHO Document Production Services.
  10. 10. Henderson RH, Sundaresan T. Cluster sampling to assess immunization coverage: a review of experience with a simplified sampling method. Bull World Health Organ 1982;60(2):253–60. pmid:6980735
  11. 11. Cutts FT, Izurieta HS, Rhoda DA. Measuring coverage in MNCH: design, implementation, and interpretation challenges associated with tracking vaccination coverage using household surveys. Plos Med 2013;10(5):e1001404. doi: 10.1371/journal.pmed.1001404. pmid:23667334
  12. 12. Colson KE, Zuniga-Brenes P, Rios-Zertuche D, Conde-Glez CJ, Gagnier MC, Palmisano E, et al. Comparative Estimates of Crude and Effective Coverage of Measles Immunization in Low-Resource Settings: Findings from Salud Mesoamerica 2015. PLoS ONE 2015 Jul 2;10(7):e0130697. doi: 10.1371/journal.pone.0130697. pmid:26136239
  13. 13. MacNeil A, Lee CW, Dietz V. Issues and considerations in the use of serologic biomarkers for classifying vaccination history in household surveys. Vaccine 2014 Sep 3;32(39):4893–900. doi: 10.1016/j.vaccine.2014.07.005. pmid:25045821
  14. 14. Borrow R, Balmer P, Roper MH. Module 3: Tetanus. Update 2006. 1–51. 2007. Geneva, World Health Organization. The Immunological Basis for Immunization Series.
  15. 15. Levine MM. "IDEAL" vaccines for resource poor settings. Vaccine 2011 Dec 30;29 Suppl 4:D116–25. doi: 10.1016/j.vaccine.2011.11.090.:D116-D125. pmid:22486974
  16. 16. Sow SO, Tapia MD, Diallo S, Keita MM, Sylla M, Onwuchekwa U, et al. Haemophilus influenzae Type B conjugate vaccine introduction in Mali: impact on disease burden and serologic correlate of protection. Am J Trop Med Hyg 2009 Jun;80(6):1033–8. pmid:19478272
  17. 17. Hutter J, Pasetti MF, Sanogo D, Tapia MD, Sow SO, Levine MM. Naturally acquired and conjugate vaccine-induced antibody to Haemophilus influenzae type b (Hib) polysaccharide in Malian children: serological assessment of the Hib immunization program in Mali. Am J Trop Med Hyg 2012 Jun;86(6):1026–31. doi: 10.4269/ajtmh.2012.11-0807. pmid:22665612
  18. 18. Kayhty H, Peltola H, Karanko V, et al. The protective level of serum antibodies to the capsular polysaccharide of Haemophilus influenzae type b. J Infect Dis 1983;147:1100. pmid:6602191 doi: 10.1093/infdis/147.6.1100
  19. 19. Chen D, Tyagi A, Carpenter J, Perkins S, Sylvester D, Guy M, et al. Characterization of the freeze sensitivity of a hepatitis B vaccine. Hum Vaccin 2009 Jan;5(1):26–32. pmid:18971625 doi: 10.4161/hv.5.1.6494
  20. 20. Travassos MA, Beyene B, Adam Z, Campbell JD, Mulholland N, Diarra SS, et al. Strategies for Coordination of a Serosurvey in Parallel with an Immunization Coverage Survey. Am J Trop Med Hyg 2015 Jun 8;15–0198. doi: 10.4269/ajtmh.15-0198
  21. 21. World Health Organization. Immunization coverage cluster survey—Reference manual. Geneva: WHO Document Production Services; 2005 Jun.
  22. 22. Sow SO, Tapia MD, Diallo S, Keita MM, Sylla M, Onwuchekwa U, et al. Haemophilus influenzae type b conjugate vaccine introduction in Mali: Impact on disease burden and serologic correlate of protection. Am J Trop Med Hyg 2009;80(6):1033–8. pmid:19478272
  23. 23. Fadnes LT, Nankabirwa V, Sommerfelt H, Tylleskar T, Tumwine JK, Engebretsen IM. Is vaccination coverage a good indicator of age-appropriate vaccination? A prospective study from Uganda. Vaccine 2011 Apr 27;29(19):3564–70. doi: 10.1016/j.vaccine.2011.02.093. pmid:21402043
  24. 24. Babirye JN, Engebretsen IM, Makumbi F, Fadnes LT, Wamani H, Tylleskar T, et al. Timeliness of childhood vaccinations in Kampala Uganda: a community-based cross-sectional study. PLoS ONE 2012;7(4):e35432. doi: 10.1371/journal.pone.0035432. pmid:22539972
  25. 25. Tapia MD, Pasetti MF, Cuberos L, Sow SO, Doumbia MN, Bagayogo M, et al. Measurement of tetanus antitoxin in oral fluid: a tool to conduct serosurveys. Pediatr Infect Dis J 2006 Sep;25(9):819–25. pmid:16940841 doi: 10.1097/01.inf.0000232629.72160.bb
  26. 26. Simonsen O, Bentzon MW, Heron I. ELISA for the routine determination of antitoxic immunity to tetanus. J Biol Stand 1986 Jul;14(3):231–9. pmid:3759998 doi: 10.1016/0092-1157(86)90008-9
  27. 27. Gergen PJ, McQuillan GM, Kiely M, Ezzati-Rice TM, Sutter RW, Virella G. A population-based serologic survey of immunity to tetanus in the United States. N Engl J Med 1995 Mar 23;332(12):761–6. pmid:7862178 doi: 10.1056/nejm199503233321201
  28. 28. Hayney MS, Love GD, Carlberg BM, Buck JM, Muller D. Tetanus seroprevalence among farmers: a preliminary study. J Rural Health 2003;19(2):109–12. pmid:12696846 doi: 10.1111/j.1748-0361.2003.tb00549.x
  29. 29. Redwan e, Al-Awady MK. Prevalence of tetanus immunity in the Egyptian population. Hum Antibodies 2002;11(1–2):55–9. pmid:12237476
  30. 30. Yuan L, Lau W, Thipphawong J, Kasenda M, Xie F, Bevilacqua J. Diphtheria and tetanus immunity among blood donors in Toronto. CMAJ 1997 Apr 1;156(7):985–90. pmid:9099166
  31. 31. Lim SS, Stein DB, Charrow A, Murray CJ. Tracking progress towards universal childhood immunisation and the impact of global initiatives: a systematic analysis of three-dose diphtheria, tetanus, and pertussis immunisation coverage. Lancet 2008 Dec 13;372(9655):2031–46. doi: 10.1016/S0140-6736(08)61869-3. pmid:19070738
  32. 32. Miles M, Ryman TK, Dietz V, Zell E, Luman ET. Validity of vaccination cards and parental recall to estimate vaccination coverage: a systematic review of the literature. Vaccine 2013 Mar 15;31(12):1560–8. doi: 10.1016/j.vaccine.2012.10.089. pmid:23196207
  33. 33. Preziosi MP, Yam A, Wassilak SG, Chabirand L, Simaga A, Ndiaye M, et al. Epidemiology of pertussis in a West African community before and after introduction of a widespread vaccination program. Am J Epidemiol 2002 May 15;155(10):891–6. pmid:11994227 doi: 10.1093/aje/155.10.891
  34. 34. Sow SO, Diallo S, Campbell JD, Tapia MD, Keita T, Keita MM, et al. Burden of invasive disease caused by Haemophilus influenzae type b in Bamako, Mali: impetus for routine infant immunization with conjugate vaccine. Pediatr Infect Dis J 2005 Jun;24(6):533–7. pmid:15933564 doi: 10.1097/01.inf.0000164768.28135.0d
  35. 35. Campagne G, Garba A, Schuchat A, Boulanger D, Plikaytis BD, Ousseini M, et al. Response to conjugate Haemophilus influenzae B vaccine among infants in Niamey, Niger. Am J Trop Med Hyg 1998 Nov;59(5):837–42. pmid:9840608
  36. 36. Clark A, Sanderson C. Timing of children´s vaccinations in 45 low-income and middle-income countries: an analysis of survey data. Lancet 2009 May 2;373(9674):1543–9. doi: 10.1016/S0140-6736(09)60317-2. pmid:19303633
  37. 37. Deming MS, Roungou JB, Kristiansen M, Heron I, Yango A, Guenengafo A, et al. Tetanus toxoid coverage as an indicator of serological protection against neonatal tetanus. Bull World Health Organ 2002;80(9):696–703. pmid:12378286
  38. 38. Hayford KT, Shomik MS, Al-Emran HM, Moss WJ, Bishai D, Levine OS. Measles vaccination coverage estimates from surveys, clinic records, and immune markers in oral fluid and blood: a population-based cross-sectional study. BMC Public Health 2013 Dec;%20;13:1211. doi: 10.1186/1471-2458-13-1211.:1211–3. pmid:24359402
  39. 39. Riddell MA, Byrnes GB, Leydon JA, Kelly HA. Dried venous blood samples for the detection and quantification of measles IgG using a commercial enzyme immunoassay. Bull World Health Organ 2003;81(10):701–7. pmid:14758429
  40. 40. Colson KE, Potter A, Conde-Glez C, Hernandez B, Rios-Zertuche D, Zuniga-Brenes P, et al. Use of a commercial ELISA for the detection of measles-specific immunoglobulin G (IgG) in dried blood spots collected from children living in low-resource settings. J Med Virol 2015 Sep;87(9):1491–9. doi: 10.1002/jmv.24136. pmid:25988945
  41. 41. Nokes DJ, Enquselassie F, Nigatu W, Vyse AJ, Cohen BJ, Brown DW, et al. Has oral fluid the potential to replace serum for the evaluation of population immunity levels? A study of measles, rubella and hepatitis B in rural Ethiopia. Bull World Health Organ 2001;79(7):588–95. pmid:11477961
  42. 42. Ohuma EO, Okiro EA, Bett A, Abwao J, Were S, Samuel D, et al. Evaluation of a measles vaccine campaign by oral-fluid surveys in a rural Kenyan district: interpretation of antibody prevalence data using mixture models. Epidemiol Infect 2009 Feb;137(2):227–33. doi: 10.1017/S0950268808000848. pmid:18544176
  43. 43. Nigatu W, Samuel D, Cohen B, Cumberland P, Lemma E, Brown DW, et al. Evaluation of a measles vaccine campaign in Ethiopia using oral-fluid antibody surveys. Vaccine 2008 Sep 2;26(37):4769–74. doi: 10.1016/j.vaccine.2008.07.005. pmid:18644417

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www.measlesinitiative.org
www.technet21.org
www.polioeradication.org
www.globalhealthlearning.org
www.who.int/bulletin
allianceformalariaprevention.com
www.malariaworld.org
http://www.panafrican-med-journal.com/