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Effect of Population Partitioning on the Probability of Silent Circulation of Poliovirus

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Abstract

Polio can circulate unobserved in regions that are challenging to monitor. To assess the probability of silent circulation, simulation models can be used to understand transmission dynamics when detection is unreliable. Model assumptions, however, impact the estimated probability of silent circulation. Here, we examine the impact of having distinct populations, rather than a single well-mixed population, with a discrete-individual model including environmental surveillance. We show that partitioning a well-mixed population into networks of distinct communities may result in a higher probability of silent circulation as a result of the time it takes for the detection of a circulation event. Population structure should be considered when assessing polio control in a region with many loosely interacting communities.

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Data Availability

Not applicable.

Code availability

The code is available at https://github.com/celestevallejo/polio under the Metapopulation_model folder. The C++ folder contains the simulation model code and the code to calculate the silent circulation statistic using model output. The Model_output folder contains zipped files of all simulation model output used to generate the figures or the silent circulation statistic. The Plotting_scripts folder contains all R scripts used to generate the figures in the manuscript. The SC_statistic_output folder contains zipped files of all output generated from the silent circulation C++ code in the C++ folder.

References

  • Andreasen V, Christiansen FB (1989) Persistence of an infectious disease in a subdivided population. Math Biosci 96(2):239–253. https://doi.org/10.1016/0025-5564(89)90061-8

    Article  MathSciNet  MATH  Google Scholar 

  • Baig IA, Ahmad RN, Baig SA, Ali A (2019) Rural business hub: framework for a new rural development approach in rain-fed areas of Pakistan - A Case of Punjab Province. SAGE Open. https://doi.org/10.1177/2158244019885133

    Article  Google Scholar 

  • Bawa S, Shuaib F, Saidu M, Ningi A, Abdullahi S, Abba B, Idowu A, Alkasim J, Hammanyero K, Warigon C, Tegegne SG, Banda R, Korir C, Yehualashet YG, Bedada T, Martin C, Nsubuga P, Adamu US, Okposen B, Braka F, Wondimagegnehu A, Vaz RG (2018) Conduct of vaccination in hard-to-reach areas to address potential polio reservoir areas, 2014–2015. BMC Public Health 18(4):1312. https://doi.org/10.1186/s12889-018-6194-y

    Article  Google Scholar 

  • Brouwer AF, Eisenberg JNS, Pomeroy CD, Shulman LM, Hindiyeh M, Manor Y, Grotto I, Koopman JS, Eisenberg MC (2018) Epidemiology of the silent polio outbreak in Rahat, Israel, based on modeling of environmental surveillance data. PNAS 115(45):E10625–E10633

    Article  Google Scholar 

  • Demographia World Urban Areas. http://www.demographia.com/db-worldua.pdf. Accessed: 2020-05-16

  • Duintjer Tebbens RJ, Thompson KM (2018) Evaluation of proactive and reactive strategies for polio eradication activities in Pakistan and Afghanistan. Risk Anal 39(2):389–401. https://doi.org/10.1111/risa.13194

    Article  Google Scholar 

  • Duintjer Tebbens RJ, Pallansch MA, Kalkowska DA, Wassilak SGF, Cochi SL, Thompson KM (2013) Characterizing poliovirus transmission and evolution: insights from modeling experiences with wild and vaccine-related polioviruses. Risk Anal 33(4):703–749. https://doi.org/10.1111/risa.12044

    Article  Google Scholar 

  • Duintjer Tebbens R, Pallansch M, Cochi S, Ehrhardt D, Farag N, Hadler S, Hampton L, Martinez M, Wassilak S, Thompson K (2018) Modeling poliovirus transmission in Pakistan and Afghanistan to inform vaccination strategies in undervaccinated subpopulations. Risk Anal 38(8):1701–1717. https://doi.org/10.1111/risa.12962

    Article  Google Scholar 

  • Duintjer Tebbens R, Kalkowska D, Thompson K (2019) Global certification of wild poliovirus eradication: insights from modelling hard-to-reach subpopulations and confidence about the absence of transmission. BMJ Open 9(1):e023938

    Article  Google Scholar 

  • Eichner M, Dietz K (1996) Eradication of Poliomyelitis: When Can One Be Sure That Polio Virus Transmission Has Been Terminated? Am J Epidemiol 143(8):816–822

    Article  Google Scholar 

  • Etienne RS, Heesterbeek J (2000) On optimal size and number of reserves for metapopulation persistence. J Theor Biol 203(1):33–50. https://doi.org/10.1006/jtbi.1999.1060

    Article  Google Scholar 

  • Gillespie DT (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81(25):2340–2361

    Article  Google Scholar 

  • Grassly NC, Fraser C (2006) Seasonal infectious disease epidemiology. Proc R Soc B: Biol Sci 273(1600):2541–2550. https://doi.org/10.1098/rspb.2006.3604

    Article  Google Scholar 

  • Hagenaars T, Donnelly C, Ferguson N (2004) Spatial heterogeneity and the persistence of infectious diseases. J Theor Biol 229(3):349–359. https://doi.org/10.1016/j.jtbi.2004.04.002

    Article  MathSciNet  MATH  Google Scholar 

  • Henderson R (1989) The World Health Organization’s plan of action for global eradication of poliomyelitis by the year 2000. Ann N Y Acad Sci 569(1):69–85

    Article  Google Scholar 

  • Kalkowska DA, Tebbens RJD, Thompson KM (2012) The probability of undetected wild poliovirus circulation after apparent global interruption of transmission. Am J Epidemiol 175(9):936–949

    Article  Google Scholar 

  • Kalkowska DA, Duintjer Tebbens RJ, Pallansch MA, Thompson KM (2018) Modeling undetected live poliovirus circulation after apparent interruption of transmission: Pakistan and Afghanistan. Risk Anal 39(2):402–413. https://doi.org/10.1111/risa.13214

    Article  Google Scholar 

  • Kalkowska DA, Tebbens RJD, Thompson KM (2018) Another look at silent circulation of poliovirus in small populations. Infectious Disease Modelling 3:107–117

    Article  Google Scholar 

  • Kalkowska D, Duintjer Tebbens R, Thompson K (2019) Environmental surveillance system characteristics and impacts on confidence about no undetected serotype 1 wild poliovirus circulation. Risk Anal 39(2):414–425. https://doi.org/10.1111/risa.13193

    Article  Google Scholar 

  • Kalkowska D, Pallansch M, Wassilak S, Cochi S, Thompson K (2021) Global transmission of live polioviruses: updated dynamic modeling of the polio endgame. Risk Anal 41(2):248–265. https://doi.org/10.1111/risa.13447

    Article  Google Scholar 

  • Koopman J, Henry CJ, Park JH, Eisenberg MC, Ionides EL, Eisenberg JN (2017) Dynamics affecting the risk of silent circulation when oral polio vaccination is stopped. Epidemics 20:21–36. https://doi.org/10.1016/j.epidem.2017.02.013

    Article  Google Scholar 

  • Kuschminder K, Dora M (2009) Migration in Afghanistan: History, Current Trends and Future prospects. Ph.D. thesis

  • Martinez-Bakker M, King AA, Rohani P (2015) Unraveling the transmission ecology of polio. PLoS Biol 13(6):1–21. https://doi.org/10.1371/journal.pbio.1002172

    Article  Google Scholar 

  • Mbaeyi C, Ryan MJ, Smith P, Mahamud A, Farag N, Haithami S, Sharaf M, Jorba JC, Ehrhardt D (2017) Response to a large polio outbreak in a setting of conflict - middle east, 2013–2017. Morbidity and mortality weekly report, Centers for Disease Control and Prevention

  • Naeem M, Adil M, Abbas S, Khan M, Naz M, Khan A, Khan M (2013) Coverage and causes of missed oral polio vaccine in urban and rural areas of Peshawar. J Ayub Med College, Abbottabad : JAMC 23:98–102

    Google Scholar 

  • Naqvi A, Naqvi S, Yazdani N, Ahmad R, Ahmad N, Zehra F (2017) Understanding the dynamics of poliomyelitis spread in Pakistan. Iran J Public Health 46(7):997–998

    Google Scholar 

  • Nnadi C, Damisa E, Esapa L, Braka F, Waziri N, Siddique A, Jorba J, wa Nganda G, Ohuabunwo C, Bolu O, Wiesen E, Adamu U (2017) Continued endemic wild poliovirus transmission in security-compromised areas – Nigeria, 2016. Morbidity and mortality weekly report, Centers for Disease Control and Prevention

  • O’Reilly KM, Durry E, ul Islam O, Quddus A, Abid N, Mir TP, Tangermann RH, Aylward RB, Grassly NC (2012) The effect of mass immunisation campaigns and new oral poliovirus vaccines on the incidence of poliomyelitis in Pakistan and Afghanistan, 2001–11: a retrospective analysis. The Lancet 380(9840):491–498. https://doi.org/10.1016/S0140-6736(12)60648-5

    Article  Google Scholar 

  • Saleem M, Haider I, Ajmal F, Khan A (2016) Audit and evaluation of the acute flaccid paralysis surveillance system in Khyber Pakhtunkhwa, Pakistan. Khyber Med Univ J 8(1), 22–26. https://www.kmuj.kmu.edu.pk/article/view/14602

  • The world bank: population, total - Afghanistan, Pakistan (2020). Data retrieved from https://data.worldbank.org/indicator/SP.POP.TOTL?end=2008 &locations=AF-PK &start=2008

  • Thompson K, Kalkowska D (2020) Review of poliovirus modeling performed from 2000 to 2019 to support global polio eradication. Expert Rev Vaccines 19(7):661–686. https://doi.org/10.1080/14760584.2020.1791093

    Article  Google Scholar 

  • Vallejo C, Pearson C, Koopman J, Hladish TJ (2019) Evaluating the probability of silent circulation of polio in small populations using the silent circulation statistic. Infect Dis Model 4:239–250. https://doi.org/10.1016/j.idm.2019.06.003

    Article  Google Scholar 

  • Wesolowski A, Qureshi T, Boni MF, Sundsøy PR, Johansson MA, Rasheed SB, Engø-Monsen K, Buckee CO (2015) Impact of human mobility on the emergence of dengue epidemics in Pakistan. Proc Natl Acad Sci 38:11887–11892. https://doi.org/10.1073/pnas.1504964112

    Article  Google Scholar 

Download references

Acknowledgements

This research was partially supported by a National Science Foundation Grant Number DMS 1440386 (CV) and by NIH/National Institute of General Medical Sciences Grant U54 GM111274 (TJH).

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5 Appendix

5 Appendix

1.1 5.1 Intercase Interval Definition

The initial intercase interval has been defined as either the time between the start of the simulation and the first simulated paralytic case (referred to as the initial case assumption (ICA) in Vallejo et al. (2019)) (Eichner and Dietz 1996; Kalkowska et al. 2012) or as the time between the first two explicitly simulated paralytic cases (referred to as the non-initial case assumption (NICA)) (Vallejo et al. 2019). Vallejo et al. (2019) explored the consequence of the ICA in small populations (25000 and smaller). They determined that defining the first interparalytic case interval as the time between the start of the simulation and the first paralytic case had the effect (in most cases) of estimating a higher probability of silent circulation when compared to the NICA. This effect decreased with an increase in population size. In this paper the population size considered is large enough such that either definition of the first interparalytic case interval is appropriate (see Fig. 9). In any case, we believe it is more realistic for observation of the system to begin after a paralytic case had been detected, rather than at the exact moment of detection. Therefore, we define all interparalytic case intervals as between two explicitly simulated paralytic cases (or the NICA).

Fig. 10
figure 10

Box plots demonstrating the distribution of starting values for each compartment after the 50-year burn-in period compared to the endemic equilibrium value obtained by solving the related system of differential equation represented by the solid red horizontal line. Note that the extinction dynamics are highly influential in determining the starting conditions. Even the 64k population is not large enough to reproduce equilibrium-like conditions (Color figure online)

1.2 5.2 Initial Patch Population Distribution

See Fig. 10.

1.3 5.3 Intercase and Extinction Interval Distribution in Single Populations

See Fig. 11.

Fig. 11
figure 11

Cumulative distribution function (CDF) of intercase (time between detected paralytic cases, (A) and extinction (time between the last detected paralytic case and extinction, (B) intervals for single populations

1.4 5.4 Intercase and Extinction Interval Distribution for the Multi-patch Model with Interpatch Movement

See Fig. 12.

Fig. 12
figure 12

Cumulative distribution function (CDF) of intercase (time between paralytic cases, (A) and extinction (time between the last detected case and extinction, (B) intervals for the multi-patch model with an interpatch movement rate of 0.1 per year. Lighter, more transparent, lines represent the value of the quantity in the absence of movement to use for comparison

1.5 5.5 The Probability of Silent Circulation in Heterogeneous Patches

See Fig. 13.

Fig. 13
figure 13

Comparison of the probability of silent circulation between evenly distributed patch populations and heterogeneous patch distributions visualized using the silent circulation statistic (A), the differential comparison to the 1 \(\times \) 64k population (B), and the odds ratio (C). The probability differential (B) is calculated by subtracting the probability of silent circulation in the partitioned populations from that of the large 64k population. Negative values indicate that the partitioned populations have a higher probability of silent circulation. Values less than one in the odds ratio plot (C) indicate that the 64k population is less likely to have continued silent circulation compared to the partitioned populations. The inset plot shows the curves restricted to between 2.5 and 3.5 years since a paralytic case. The mixed population distributions are represented by dashed lines.

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Vallejo, C., Pearson, C.A.B., Koopman, J.S. et al. Effect of Population Partitioning on the Probability of Silent Circulation of Poliovirus. Bull Math Biol 84, 62 (2022). https://doi.org/10.1007/s11538-022-01014-6

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