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Volume 24, Number 7—July 2018

Integrated Serologic Surveillance of Population Immunity and Disease Transmission

Benjamin F. ArnoldComments to Author , Heather M. Scobie, Jeffrey W. Priest, and Patrick J. Lammie
Author affiliations: University of California, Berkeley, California, USA (B.F. Arnold); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (H.M. Scobie, J.W. Priest, P.J. Lammie); Task Force for Global Health, Atlanta (P.J. Lammie)

Main Article

Figure 2

Antibody response to tetanus toxoid and causative agents of malaria and NTDs measured by multiplex bead assay among 2,150 women, Cambodia, 2012. Specimens were measured by using the Luminex platform (Luminex Corporation, Austin, TX, USA) (25). A) Relationship between pairs of antibodies measured by mean antibody response (log10 MFI – bg) in each of the 100 sampling clusters. Scatter plots include nonparametric locally weighted regression fits trimmed to reduce edge effects. Correlation ellipses

Figure 2. Antibody response to tetanus toxoid and causative agents of malaria and NTDs measured by multiplex bead assay among 2,150 women, Cambodia, 2012. Specimens were measured by using the Luminex platform (Luminex Corporation, Austin, TX, USA) (25). A) Relationship between pairs of antibodies measured by mean antibody response (log10 MFI – bg) in each of the 100 sampling clusters. Scatter plots include nonparametric locally weighted regression fits trimmed to reduce edge effects. Correlation ellipses depict the strength of the association on the basis of the Pearson correlation (r estimates). Both axes indicate mean antibody response. B) Heatmap of mean antibody response to tetanus toxoid and pathogens that cause malaria and NTDs in 100 sampling clusters stratified by region and then sorted by mean antibody response. Data set and computational notebook are available through the Open Science Framework ( MFI – bg, mean fluorescence intensity minus background; MSP, merozoite surface protein; NTDs, neglected tropical diseases; SAG2A, surface antigen 2A; VPDs, vaccine-preventable diseases.

Main Article

  1. Dowell  SF, Blazes  D, Desmond-Hellmann  S. Four steps to precision public health. Nature. 2016;540:18991. DOIGoogle Scholar
  2. World Health Organization. Global vaccine action plan 2011-2020. Geneva: The Organization; 2013 [cited 2017 Nov 22].
  3. World Health Organization. Global technical strategy for malaria 2016–2030. Geneva: The Organization; 2015 Nov 4 [cited 2017 Nov 22].
  4. World Health Organization. Global health sector strategy on HIV 2016–2021. Report no. WHO/HIV/2016.05. Geneva: The Organization; 2016 [cited 2017 Nov 22].
  5. 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:e1001404. DOIPubMedGoogle Scholar
  6. MacNeil  A, Lee  C-W, Dietz  V. Issues and considerations in the use of serologic biomarkers for classifying vaccination history in household surveys. Vaccine. 2014;32:4893900. DOIPubMedGoogle Scholar
  7. Cutts  FT, Hanson  M. Seroepidemiology: an underused tool for designing and monitoring vaccination programmes in low- and middle-income countries. Trop Med Int Health. 2016;21:108698. DOIPubMedGoogle Scholar
  8. Drakeley  C, Cook  J. Chapter 5. Potential contribution of sero-epidemiological analysis for monitoring malaria control and elimination: historical and current perspectives. Adv Parasitol. 2009;69:299352. DOIPubMedGoogle Scholar
  9. Simonsen  J, Strid  MA, Mølbak  K, Krogfelt  KA, Linneberg  A, Teunis  P. Sero-epidemiology as a tool to study the incidence of Salmonella infections in humans. Epidemiol Infect. 2008;136:895902. DOIPubMedGoogle Scholar
  10. Teunis  PFM, Falkenhorst  G, Ang  CW, Strid  MA, De Valk  H, Sadkowska-Todys  M, et al. Campylobacter seroconversion rates in selected countries in the European Union. Epidemiol Infect. 2013;141:20517. DOIPubMedGoogle Scholar
  11. Exum  NG, Pisanic  N, Granger  DA, Schwab  KJ, Detrick  B, Kosek  M, et al. Use of pathogen-specific antibody biomarkers to estimate waterborne infections in population-based settings. Curr Environ Health Rep. 2016;3:32234. DOIPubMedGoogle Scholar
  12. Moss  DM, Priest  JW, Hamlin  K, Derado  G, Herbein  J, Petri  WA Jr, et al. Longitudinal evaluation of enteric protozoa in Haitian children by stool exam and multiplex serologic assay. Am J Trop Med Hyg. 2014;90:65360. DOIPubMedGoogle Scholar
  13. Goodhew  EB, Priest  JW, Moss  DM, Zhong  G, Munoz  B, Mkocha  H, et al. CT694 and pgp3 as serological tools for monitoring trachoma programs. PLoS Negl Trop Dis. 2012;6:e1873. DOIPubMedGoogle Scholar
  14. Hamlin  KL, Moss  DM, Priest  JW, Roberts  J, Kubofcik  J, Gass  K, et al. Longitudinal monitoring of the development of antifilarial antibodies and acquisition of Wuchereria bancrofti in a highly endemic area of Haiti. PLoS Negl Trop Dis. 2012;6:e1941. DOIPubMedGoogle Scholar
  15. Lammie  PJ, Moss  DM, Brook Goodhew  E, Hamlin  K, Krolewiecki  A, West  SK, et al. Development of a new platform for neglected tropical disease surveillance. Int J Parasitol. 2012;42:797800. DOIPubMedGoogle Scholar
  16. Poirier  MJP, Moss  DM, Feeser  KR, Streit  TG, Chang  G-JJ, Whitney  M, et al. Measuring Haitian children’s exposure to chikungunya, dengue and malaria. Bull World Health Organ. 2016;94:817825A. DOIPubMedGoogle Scholar
  17. Feeser  KR, Cama  V, Priest  JW, Thiele  EA, Wiegand  RE, Lakwo  T, et al. Characterizing reactivity to Onchocerca volvulus antigens in multiplex bead assays. Am J Trop Med Hyg. 2017;97:66672. DOIPubMedGoogle Scholar
  18. Curtis  KA, Kennedy  MS, Charurat  M, Nasidi  A, Delaney  K, Spira  TJ, et al. Development and characterization of a bead-based, multiplex assay for estimation of recent HIV type 1 infection. AIDS Res Hum Retroviruses. 2012;28:18897. DOIPubMedGoogle Scholar
  19. Metcalf  CJE, Farrar  J, Cutts  FT, Basta  NE, Graham  AL, Lessler  J, et al. Use of serological surveys to generate key insights into the changing global landscape of infectious disease. Lancet. 2016;388:72830. DOIPubMedGoogle Scholar
  20. Hens  N, Shkedy  Z, Aerts  M, Damme  CFPV, Beutels  P. Modeling infectious disease parameters based on serological and social contact data: a modern statistical perspective. New York: Springer-Verlag New York; 2012.
  21. Solomon  AW, Engels  D, Bailey  RL, Blake  IM, Brooker  S, Chen  J-X, et al. A diagnostics platform for the integrated mapping, monitoring, and surveillance of neglected tropical diseases: rationale and target product profiles. PLoS Negl Trop Dis. 2012;6:e1746. DOIPubMedGoogle Scholar
  22. van Gageldonk  PGM, van Schaijk  FG, van der Klis  FR, Berbers  GAM. Development and validation of a multiplex immunoassay for the simultaneous determination of serum antibodies to Bordetella pertussis, diphtheria and tetanus. J Immunol Methods. 2008;335:7989. DOIPubMedGoogle Scholar
  23. Scobie  HM, Mao  B, Buth  S, Wannemuehler  KA, Sørensen  C, Kannarath  C, et al. Tetanus immunity among women aged 15 to 39 years in Cambodia: a national population-based serosurvey, 2012. Clin Vaccine Immunol. 2016;23:54654. DOIPubMedGoogle Scholar
  24. Arnold  BF, van der Laan  MJ, Hubbard  AE, Steel  C, Kubofcik  J, Hamlin  KL, et al. Measuring changes in transmission of neglected tropical diseases, malaria, and enteric pathogens from quantitative antibody levels. PLoS Negl Trop Dis. 2017;11:e0005616. DOIPubMedGoogle Scholar
  25. Priest  JW, Jenks  MH, Moss  DM, Mao  B, Buth  S, Wannemuehler  K, et al. Integration of multiplex bead assays for parasitic diseases into a national, population-based serosurvey of women 15-39 years of age in Cambodia. PLoS Negl Trop Dis. 2016;10:e0004699. DOIPubMedGoogle Scholar
  26. Frenk  J. The global health system: strengthening national health systems as the next step for global progress. PLoS Med. 2010;7:e1000089. DOIPubMedGoogle Scholar
  27. Sturrock  HJW, Bennett  AF, Midekisa  A, Gosling  RD, Gething  PW, Greenhouse  B. Mapping malaria risk in low transmission settings: challenges and opportunities. Trends Parasitol. 2016;32:63545. DOIPubMedGoogle Scholar
  28. Zhou  X-N, Bergquist  R, Tanner  M. Elimination of tropical disease through surveillance and response. Infect Dis Poverty. 2013;2:1. DOIPubMedGoogle Scholar
  29. United Nations. Sustainable development goals [cited 2017 Feb 14].
  30. Woolhouse  ME, Hagan  P. Seeking the ghost of worms past. Nat Med. 1999;5:12257. DOIPubMedGoogle Scholar
  31. Hotez  PJ, Alvarado  M, Basáñez  M-G, Bolliger  I, Bourne  R, Boussinesq  M, et al. The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis. 2014;8:e2865. DOIPubMedGoogle Scholar
  32. Kroidl  I, Saathoff  E, Maganga  L, Makunde  WH, Hoerauf  A, Geldmacher  C, et al. Effect of Wuchereria bancrofti infection on HIV incidence in southwest Tanzania: a prospective cohort study. Lancet. 2016;388:191220. DOIPubMedGoogle Scholar
  33. Salgame  P, Yap  GS, Gause  WC. Effect of helminth-induced immunity on infections with microbial pathogens. Nat Immunol. 2013;14:111826. DOIPubMedGoogle Scholar
  34. Blackwell  AD, Tamayo  MA, Beheim  B, Trumble  BC, Stieglitz  J, Hooper  PL, et al. Helminth infection, fecundity, and age of first pregnancy in women. Science. 2015;350:9702. DOIPubMedGoogle Scholar
  35. Moore  SM, Azman  AS, Zaitchik  BF, Mintz  ED, Brunkard  J, Legros  D, et al. El Niño and the shifting geography of cholera in Africa. Proc Natl Acad Sci U S A. 2017;114:443641. DOIPubMedGoogle Scholar
  36. Kovats  RS, Bouma  MJ, Hajat  S, Worrall  E, Haines  A. El Niño and health. Lancet. 2003;362:14819. DOIPubMedGoogle Scholar
  37. Scobie  HM, Patel  M, Martin  D, Mkocha  H, Njenga  SM, Odiere  MR, et al. Tetanus immunity gaps in children 5–14 years and men >15 years of age revealed by integrated disease serosurveillance in Kenya, Tanzania, and Mozambique. Am J Trop Med Hyg. 2017;96:41520. DOIPubMedGoogle Scholar
  38. Mulders  MN, Serhan  F, Goodson  JL, Icenogle  J, Johnson  BW, Rota  PA. Expansion of Surveillance for Vaccine-preventable Diseases: Building on the Global Polio Laboratory Network and the Global Measles and Rubella Laboratory Network Platforms. J Infect Dis. 2017;216(suppl_1):S32430. DOIPubMedGoogle Scholar
  39. Corran  P, Coleman  P, Riley  E, Drakeley  C. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol. 2007;23:57582. DOIPubMedGoogle Scholar
  40. Masson  J, Douglass  J, Roineau  M, Aye  KS, Htwe  K, Warner  J, et al. Concordance between plasma and filter paper sampling techniques for the lymphatic filariasis bm14 antibody ELISA. Trop Med Infect Dis. 2017;2:6. DOIGoogle Scholar
  41. Formenti  F, Buonfrate  D, Prandi  R, Marquez  M, Caicedo  C, Rizzi  E, et al. Comparison of S. stercoralis serology performed on dried blood spots and on conventional serum samples. Front Microbiol. 2016;7:1778. DOIPubMedGoogle Scholar
  42. Snijdewind  IJM, van Kampen  JJA, Fraaij  PLA, van der Ende  ME, Osterhaus  ADME, Gruters  RA. Current and future applications of dried blood spots in viral disease management. Antiviral Res. 2012;93:30921. DOIPubMedGoogle Scholar
  43. Jacobson  JO, Cueto  C, Smith  JL, Hwang  J, Gosling  R, Bennett  A. Surveillance and response for high-risk populations: what can malaria elimination programmes learn from the experience of HIV? Malar J. 2017;16:33. DOIPubMedGoogle Scholar
  44. Chipeta  MG, Terlouw  DJ, Phiri  KS, Diggle  PJ. Adaptive geostatistical design and analysis for prevalence surveys. Spat Stat. 2016;15:7084. DOIGoogle Scholar
  45. Helb  DA, Tetteh  KKA, Felgner  PL, Skinner  J, Hubbard  A, Arinaitwe  E, et al. Novel serologic biomarkers provide accurate estimates of recent Plasmodium falciparum exposure for individuals and communities. Proc Natl Acad Sci U S A. 2015;112:E443847. DOIPubMedGoogle Scholar
  46. Osgood-Zimmerman  A, Millear  AI, Stubbs  RW, Shields  C, Pickering  BV, Earl  L, et al. Mapping child growth failure in Africa between 2000 and 2015. Nature. 2018;555:417. DOIPubMedGoogle Scholar
  47. Takahashi  S, Metcalf  CJE, Ferrari  MJ, Tatem  AJ, Lessler  J. The geography of measles vaccination in the African Great Lakes region. Nat Commun. 2017;8:15585. DOIPubMedGoogle Scholar
  48. Gething  PW, Casey  DC, Weiss  DJ, Bisanzio  D, Bhatt  S, Cameron  E, et al. Mapping Plasmodium falciparum mortality in Africa between 1990 and 2015. N Engl J Med. 2016;375:243545. DOIPubMedGoogle Scholar
  49. Solomon  AW, Pavluck  AL, Courtright  P, Aboe  A, Adamu  L, Alemayehu  W, et al. The Global Trachoma Mapping Project: methodology of a 34-country population-based study. Ophthalmic Epidemiol. 2015;22:21425. DOIPubMedGoogle Scholar
  50. Moyes  CL, Temperley  WH, Henry  AJ, Burgert  CR, Hay  SI. Providing open access data online to advance malaria research and control. Malar J. 2013;12:161. DOIPubMedGoogle Scholar

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