Rajatonirina, Rakotomanana, Randrianasolo, Razanajatovo, Andriamandimby, Ravolomanana, Randrianarivo-Solofoniaina, Reynes, Piola, Finlay-Vickers, Heraud, and Richard: Early-warning health and process indicators for sentinel surveillance in Madagascar 2007-2011
Introduction

The concept of surveillance was developed principally for control of the transmission of infections and for the early detection of outbreaks. The main elements of surveillance methods have been described elsewhere. Surveillance is a continuous, systematic process of descriptive information collection, validation, analysis, interpretation, and dissemination for use in planning, and in the implementation and evaluation of public health policies and strategies for the prevention and control of diseases or disease outbreaks [1-3]. The public health problems approached in this way, including acute and chronic diseases and environmental hazards, are diverse, necessitating the development of tools for the timely monitoring of disease trends. Furthermore, surveillance systems must be evaluated regularly, to ensure that they provide valuable information in an efficient manner [4,5].

Efficient disease surveillance systems are the key to the timely detection of early-warning signs potentially signalling the occurrence of disease outbreaks or epidemics. The World Health Organisation (WHO) has highlighted the importance of improving national epidemic surveillance capacities [6,7]. Recently developed innovative tools, such as mobile telephone technology and electronic systems, have facilitated the improvement of surveillance systems, by reducing data processing [8]. However, these systems are mostly implemented in high-income countries [9], as most developing countries are faced with logistic and budgetary constraints, resulting in low-quality surveillance systems based on pen-and-paper methods. In many cases, these low-tech systems provide health institutions with inadequate support, resulting in frequent “health crises” [10]. Moreover, the healthcare infrastructure, laboratory diagnostic capacity, skills and number of physicians in these countries are generally insufficient to deal with emerging diseases likely to cause epidemics. Consequently, delays in raising the alarm often limit the possibility of an effective early response to new, emerging public health problems.

The need for an efficient sentinel surveillance network in Madagascar was highlighted by worldwide infectious disease threats to public health, such as severe acute respiratory syndrome (SARS) in 2003, avian influenza A H5N1 in 2005 and the Chikungunya epidemics observed in the Indian Ocean region in 2006. In addition, the 2005 International Health Regulations stressed the importance of commitment to the goal of global security and asked all member states to establish and implement effective surveillance and response systems, making it possible to detect and contain public health threats of national and international importance. As a result, the government of Madagascar, in partnership with the Institut Pasteur de Madagascar, established 13 fever sentinel sites in 2007, expanding the network to 34 sites by 2011, to improve the timely detection and management of febrile disease outbreaks. Two key attributes of the sentinel surveillance system are monitored continuously: timeliness and data quality. This system was designed to identify outbreaks for which public health interventions may be required early enough for such interventions to be effective.

We report here the indicators, for 2007 to 2011, of the syndromic sentinel surveillance network, presenting spatiotemporal trends, alert detection capability and evaluations of the process on the basis of timeliness and quality data.

Methods

The sentinel surveillance network in Madagascar has been described elsewhere [11,12]. Briefly, it includes primary healthcare centres (sentinel sites) from across the country (Figure 1) and is managed by a national steering committee. The network was expanded from 13 influenza-like illness (ILI) sentinel sites in 2007 to 34 sentinel sites in 2011, with the aim of improving geographic coverage and representativeness of the country as a whole (4 sites are located in Antananarivo) (Figure 1). The sentinel surveillance system makes use of syndromic indicators to monitor the occurrence of selected diseases of importance for the country. The main criterion for the inclusion of cases or patients is fever or diarrhoea. For patients with fever, additional screening criteria (based on syndromic case definitions) are used to identify specific syndromes: malaria, ILI, dengue-like syndromes. Standard WHO case definitions are used, to ensure comparability [11,12]. Malaria diagnosis requires biologic confirmation with a positive rapid diagnostic test in patients with fever syndromes.

Figure 1

Surrounding climate and location of the health centres participating in the sentinel surveillance system in Madagascar

ojphi-06-e197-g001

Cases and patients at the participating sites are identified by trained healthcare personnel participating in the surveillance network on a voluntary basis. One of the key features of the system is the timely transmission of syndromic data, on a daily basis, by coded short message service (SMS) messages sent from mobile phones. Upon reception at the IPM, the data transmitted in this manner are input daily into a specifically designed MS Access® database and analysed as soon as possible after the patients’ initial visit. This results in a turnaround time of 24 hours, from data collection to reception at the IPM, even for data sent from the most remote areas of the country. The data received by SMS include: sentinel site code, date of data collection, total number of outpatient consultations, total number of confirmed malaria cases, total number of ILI cases, total number of dengue-like cases, total number of diarrhoea cases, and the number of consultations by age group. The age groups were those commonly used by the Ministry of Health in Madagascar: less than 1 year, 1-4 years, 5-14 years, 15-24 years, 25 years and over.

Surveillance data are analysed and presented in easy-to-interpret tables and graphs providing the number of cases for each syndrome monitored. In addition, daily and weekly baselines (mean number of cases in the corresponding period of previous years) are calculated for each syndrome and plotted against current observations, to identify early signs of outbreaks triggering alerts. The information is disseminated on a weekly and monthly basis to healthcare staff involved in the network and to the staff of the Ministry of Health (MoH) in Madagascar.

Ethics clearance

The surveillance protocol was approved by the MoH and the National Ethics Committee of Madagascar.

Results

Description of the epidemiological indicators

From January 2007 to December 2011, the data collected on a daily basis corresponded to 917,798 visits (Table 1). The age distribution of the patients concerned, as a function of the total numbers of visits and febrile syndromes, is indicated in Table 1. In total, 102,200 cases (11.1%) of fever were reported. Fever syndromes accounted for 12.1% of visits in 2007, 12.2% in 2008, 11.8% in 2009, 10.8% in 2010 and 10.0% in 2011 (p<0.01, Table 2).

Table 1

Annual distribution of visits by age group, according to SMS data

Age group All visits (n=917,798)

2007
2008
2009
2010
2011

n
(%)
n
(%)
n
(%)
n
(%)
n
(%)
<1 year 7,663 (9.6) 13,794 (10.0) 22,748 (10.4) 24,405 (10.8) 28,607 (11.2)
1-4 years 12,564 (15.7) 20,967 (15.2) 35,652 (16.3) 38,074 (16.8) 44,382 (17.4)
5-14 years 10,092 (12.6) 17,836 (13.0) 34,911 (15.9) 32,230 (14.2) 37,695 (14.8)
15-24 years 16,096 (20.2) 27,569 (20.1) 39,421 (18.0) 42,254 (18.7) 49,340 (19.3)
≥25 years
33,456
(41.9)
57,356
(41.7)
86,259
(39.4)
89,196
(39.4)
95,231
(37.3)
Total 79,871 (8.7) 137,522 (15.0) 218,991 (23.9) 226,159 (24.6) 255,255 (27.8)
Table 2

Process indicators by sentinel site and year

2007 2008 2009 2010 2011
Sentinel site
Opening date

Fever
Forms
Forms / Fever
%
SMS delay
%

Fever
Forms
Forms / Fever
%
SMS delay
%

Fever
Forms
Forms / Fever
%
SMS delay
%

Fever
Forms
Forms / Fever
%
SMS Delay
%

Fever
Forms
Forms / Fever
%
SMS Delay
%
Ambatondrazaka 2009-05-11 -- -- -- -- -- 297 200 67.3 37 211 185 87.7 38 276 154 55.8 25
Ambato Boeny 2010-09-01 -- -- -- -- -- -- -- -- -- 363 53 14.6 51 1094 4 0.4 28
Ambovombe 2009-06-02 -- -- -- -- -- 111 111 100.0 34 171 53 31.0 53 190 73 38.4 45
Ambositra 2011-08-25 -- -- -- -- -- -- -- -- -- -- -- -- -- 212 195 92.0 6
AntananarivoBHK 2009-01-26 -- -- -- -- -- 412 412 100.0 18 331 180 54.4 22 273 124 45.4 39
Antananarivo CDA 2009-04-01 -- -- -- -- -- 132 111 84.1 18 240 172 71.7 23 308 198 64.3 43
Antananarivo MJR 2009-02-02 -- -- -- -- -- 441 144 32.7 24 292 215 73.6 2 480 235 49.0 7
Antananarivo TSL 2009-02-09 -- -- -- -- -- 143 134 93.7 26 44 44 100.0 25 38 28 73.7 10
Antsirabe 2008-09-08 -- -- -- -- 258 256 99.2 20 1304 1304 100.0 7 576 550 95.5 4 1025 653 63.7 4
Antsiranana 2007-04-19 1652 1650 99.8 NA 2215 2215 100.0 10 2579 2148 83.3 5 1995 1968 98.6 10 1577 1252 79.4 11
Antsohihy 2007-05-02 263 263 100.0 NA 1172 1172 100.0 19 611 565 92.5 29 585 558 95.4 35 248 180 72.6 23
Anjozorobe 2010-07-29 -- -- -- -- -- -- -- -- -- -- -- 49 38 77.6 45 158 153 96.8 38
Belo sur Tsiribina 2010-10-11 -- -- -- -- -- -- -- -- -- -- -- 183 182 99.5 48 529 419 79.2 50
Ejeda 2007-12-10 5 5 100.0 NA 63 63 100.0 12 76 76 100.0 10 113 113 100.0 20 137 137 100.0 24
Farafangana 2007-06-07 473 473 100.0 NA 929 929 100.0 6 970 961 99.1 8 1102 925 83.9 14 1710 1609 94.1 17
Fianarantsoa 2008-08-04 -- -- -- -- 250 250 100.0 9 427 427 100.0 10 162 145 89.5 11 302 186 61.6 11
Ihosy 2007-12-10 71 71 100.0 NA 793 793 100.0 9 552 525 95.1 16 350 350 100.0 19 745 538 72.2 11
Maevatanana 2007-04-23 1639 1639 100.0 NA 1906 1906 100.0 9 2736 2223 81.3 5 3414 3311 97.0 20 2582 1668 64.6 29
Mahajanga 2007-04-23 519 518 99.8 NA 597 467 78.2 10 851 829 97.4 8 943 922 97.8 11 891 730 81.9 20
Maintirano 2010-07-19 -- -- -- -- -- -- -- -- -- -- -- -- 354 311 87.9 25 675 467 69.2 50
Mananjara 2010-02-18 -- -- -- -- -- -- -- -- -- -- -- -- 853 822 96.4 27 409 299 73.1 35
Mandritsara 2011-09-26 -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- 391 391 100.0 37
Maroantsetra 2010-09-02 -- -- -- -- -- -- -- -- -- -- -- -- 158 158 100.0 18 433 240 55.4 28
Miandrivaza 2010-05-07 -- -- -- -- -- -- -- -- -- -- -- -- 875 875 100.0 37 582 493 84.7 46
Moramanga 2007-04-12 1436 1436 100.0 NA 2227 2196 98.6 18 3213 2964 92.3 15 1454 1396 96.0 23 1730 1010 58.4 20
Morombe 2011-09-12 -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- 158 130 82.3 21
Morondava 2007-04-10 623 623 100.0 NA 1163 1163 100.0 5 1182 1182 100.0 8 707 707 100.0 21 617 426 69.0 37
Nosy Be 2009-06-02 -- -- -- -- -- -- -- -- 2402 18 0.7 28 2645 1100 41.6 54 2542 791 31.1 68
Sainte Marie 2010-03-04 -- -- -- -- -- -- -- -- -- -- -- -- 71 35 49.3 46 61 6 9.8 41
Sambava 2009-01-21 -- -- -- -- -- -- -- -- 1125 574 51.0 25 1515 279 18.4 40 934 242 25.9 50
Taolagnara 2007-04-24 407 407 100.0 NA 709 709 100.0 15 742 636 85.7 17 464 427 92.0 23 383 320 83.6 35
Toamasina 2007-04-16 1140 1140 100.0 NA 2602 2602 100.0 14 3803 2727 71.7 11 2428 2159 88.9 24 2116 1713 81.0 24
Tsiroanamandidy 2007-04-30 1056 1056 100.0 NA 1152 1152 100.0 13 1199 1199 100.0 36 1093 1048 95.9 48 1024 602 58.8 45
Tulear 2007-04-30 352 352 100.0 NA 706 706 100.0 15 576 499 86.6 26 714 711 99.6 25 653 494 75.7 33



























Total


9,636
9,633
99.9


16,742
16,579
99.0


25,884
19,969
77.1


24,455
19,992
81.7


25,483
16,160
63.4

Fever= number of febrile syndrome cases declared by SMS, Forms= number of fever forms received, % forms = percentage of forms for patients with febrile syndromes, NA=not available

ILI accounted for 14.7% of fever cases in 2007, 8.5% in 2008, 21.3% in 2009, 20.2% in 2010 and 32.8% in 2011 (p<0.01), according to the data transmitted by SMS (Table 3). Dengue-like syndromes (Table 3) accounted for 18.6% of fever cases in 2007, 8.7% in 2008, 10.2% in 2009, 11.5% in 2010 and 4.2% in 2011 (p<0.01). Confirmed cases of malaria (Table 3) accounted for 12.0% of fever cases in 2007, 8.3% in 2008, 10.6% in 2009, 16.8% in 2010 and 12.4% in 2011 (p<0.01). From January 2008 to December 2011, 40,510 cases (4.8%) of diarrhoea were reported in the 837,881 visits (Table 3). Diarrhoea cases accounted for 3.1% of visits in 2008, 4.9% in 2009, 5.5% in 2010 and 5.1% in 2011 (p<0.01).

Table 3

Number of declared syndromes by sentinel site and year

2007 2008 2009 2010 2011
Sentinel site
Opening date

ILI
DLS
Malr
Diarr

ILI
DLS
Malr
Diarr

ILI
DLS
Malr
Diarr

ILI
DLS
Malr
Diarr

ILI
DLS
Malr
Diarr
Ambatondrazaka 2009-05-11 -- -- -- -- -- -- -- -- 129 19 7 337 39 4 7 160 122 1 7 234
Ambato Boeny 2010-09-01 -- -- -- -- -- -- -- -- -- -- -- -- 195 1 156 156 828 18 197 491
Ambovombe 2009-06-02 -- -- -- -- -- -- -- -- 4 0 7 61 3 2 16 114 6 0 9 137
Ambositra 2011-08-25 -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- 68 12 8 118
AntananarivoBHK 2009-01-26 -- -- -- -- -- -- -- -- 381 0 6 1365 160 9 4 1093 193 4 9 826
Antananarivo CDA 2009-04-01 -- -- -- -- -- -- -- -- 34 0 3 298 68 7 3 393 67 6 2 216
Antananarivo MJR 2009-02-02 -- -- -- -- -- -- -- -- 289 2 2 255 185 4 5 188 239 2 11 175
Antananarivo TSL 2009-02-09 -- -- -- -- -- -- -- -- 125 0 2 396 41 0 0 569 29 0 2 513
Antsirabe 2008-09-08 -- -- -- -- 150 22 8 288 860 12 7 539 311 1 2 535 765 1 7 467
Antsiranana 2007-04-19 236 678 10 -- 121 201 3 274 471 180 30 1136 394 210 54 1050 130 115 28 985
Antsohihy 2007-05-02 6 22 10 -- 0 0 14 1 1 1 40 4 4 9 215 128 64 31 34 179
Anjozorobe 2010-07-29 -- -- -- -- -- -- -- -- -- -- -- 36 4 4 24 141 0 4 53
Belo sur Tsiribina 2010-10-11 -- -- -- -- -- -- -- -- -- -- -- 52 33 68 82 159 97 63 483
Ejeda 2007-12-10 0 0 0 -- 5 3 7 43 0 4 3 36 0 0 7 39 0 0 30 56
Farafangana 2007-06-07 285 33 23 -- 424 45 83 169 289 27 174 322 379 230 59 375 485 37 661 414
Fianarantsoa 2008-08-04 -- -- -- -- 13 0 0 113 37 0 12 212 24 2 1 193 70 0 14 178
Ihosy 2007-12-10 0 12 7 -- 11 90 63 253 30 63 47 219 72 8 37 131 303 10 33 189
Maevatanana 2007-04-23 127 152 628 -- 76 60 644 620 472 146 1158 805 269 126 1681 1301 96 11 631 1173
Mahajanga 2007-04-23 25 142 50 -- 11 56 13 505 98 37 30 285 163 23 56 324 381 41 20 293
Maintirano 2010-07-19 -- -- -- -- -- -- -- -- -- -- -- -- 97 0 128 106 346 0 109 248
Mananjara 2010-02-18 -- -- -- -- -- -- -- -- -- -- -- -- 143 441 6 888 0 115 67 782
Mandritsara 2011-09-26 -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- 90 0 20 212
Maroantsetra 2010-09-02 -- -- -- -- -- -- -- -- -- -- -- -- 96 20 18 93 363 2 30 468
Miandrivazo 2010-05-07 -- -- -- -- -- -- -- -- -- -- -- -- 266 0 265 142 263 0 39 218
Moramanga 2007-04-12 222 12 59 -- 2196 9 77 557 2964 63 66 881 203 30 30 667 573 42 55 628
Morombe 2011-09-12 -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- 61 0 21 48
Morondava 2007-04-10 153 82 139 -- 176 15 39 284 117 27 16 575 25 1 62 545 23 0 27 497
Nosy Be 2009-06-02 -- -- -- -- -- -- -- -- 18 205 99 501 783 321 306 991 983 147 135 902
Sainte Marie 2010-03-04 -- -- -- -- -- -- -- -- -- -- -- -- 32 10 25 5 30 5 25 60
Sambava 2009-01-21 -- -- -- -- -- -- -- -- 331 16 120 487 306 52 220 272 464 20 44 218
Taolagnara 2007-04-24 29 15 8 -- 34 32 9 249 93 6 29 331 54 1 90 168 57 2 49 105
Toamasina 2007-04-16 53 583 64 -- 123 847 315 267 272 1683 782 352 194 1072 468 237 111 260 734 160
Tsiroanamandidy 2007-04-30 250 15 150 200 12 112 276 299 99 94 583 249 109 104 693 570 51 42 545
Tulear 2007-04-30 34 43 13 17 74 1 395 23 62 3 731 105 80 7 734 266 25 3 838



























Total


1,418
1,789
1,161
--

1,420
1,466
1,388
4,294

5,503
2,652
2,736
10,711

4,948
2,810
4,104
12,396

8,346
1,055
3,171
13,109
ILI= number of influenza-like illness cases, DLS=number of dengue-like syndromes, Malaria=number of confirmed malaria confirmed cases, Diarr=number of diarrhoea cases declared by SMS

The epidemiological characteristics of groups with fever-related syndromes, such as those with ILI, identified by the sentinel surveillance system, were investigated by the plotting of daily count data on a graph (Figure 2). Daily and weekly counts, as a function of the regional pattern, were also plotted and analysed for each sentinel centre (data not shown). Figure 2 shows a peak in the number of daily visits in November 2009 corresponding to an increase in the number of febrile syndromes and ILI cases.

Figure 2

Mean daily visit counts, by centre, in the sentinel surveillance system in Madagascar and daily sentinel surveillance time series plots (%) of fever, total visits and the ILI cases among total fever cases, with the moving average (over 10 days – red curve) for daily visit counts, April 14, 2007 – December 31, 2011.

ojphi-06-e197-g002

A plot of the distribution of febrile and other syndromes over the various years (Figures 2-5) showed that ILI was the dominant cause of fever in most of the country, from 2009 onwards. A subanalysis of the longitudinal data, using only the first 13 sentinel sites established in 2007-2011, yielded similar trends (Figure 4).

Figure 3

Weekly syndromic data from all sentinel centres in 2011.

ojphi-06-e197-g003
Figure 4

Weekly syndromic data from the first 13 sentinel centres in 2011

ojphi-06-e197-g004
Figure 5

Annual percentage of fever-related syndromes, by centre, based on data collected from sentinel centres by SMS, from 2007 to 2011.

ojphi-06-e197-g005

Alerts

From 2007 to 2011, 21 alerts resulting from syndromic surveillance were confirmed by biological surveillance and led to a response and epidemiological investigations to assess the risk.

In October 2008, in Morondava, on the west coast of Madagascar, an increase in the percentage of febrile syndromes and the percentage of ILI cases was recorded. Samples were requested and influenza virus A (H3N2) was detected.

In January 2009, an increase in the percentage of febrile syndromes and in the number of confirmed malaria cases was identified, leading to an investigation of factors potentially associated with an increase in malaria transmission.

In 2010, excess cases of dengue-like syndromes were declared in Mananjary health district, which is located on the southeast coast. The Chikungunya virus was identified and the epidemic confirmed.

None of these events were detected by the routine surveillance system. However, there was no organised response to any of these outbreaks because the MoH lacked the means to deal with these large events.

Process indicators

Relevant process indicators have been identified for the monitoring of the network. These indicators are presented in Table 2 and concern principally the data transmission and data validation processes.

Overall, 85% of the data were transmitted within the 24-hour time frame. This indicator was introduced in 2008. The percentage of data for which transmission was delayed increased from 2008 (12.3%) to 2011 (32.6%), and considerable differences between sentinel sites were observed for this indicator (Table 3).

As previously described [11,12], an individual fever form had to be completed and sent to the IPM for each declared case of febrile syndrome. The fever forms were used to validate the syndrome data transmitted by SMS. Specific forms relating to fever were completed for 82,333 of the patients presenting fever (80.6%). In 2007, 99.9% of the febrile syndromes were documented on a fever form, but this percentage had fallen to 63.4% by 2011.

The sex ratio (male/female) for those with febrile syndromes was 0.88. Age was known for 81,981 patients (99.5%), and the mean age of the patients was 12.5 years (CI 95%: [12.4-12.7]). The age-group distribution is presented in Table 4. ILI, defined on the basis of the symptoms noted on the fever forms (fever and cough, or fever and sore throat), accounted for 49.4% (40,709) of all cases of febrile illness, but significant differences in these percentages (p<0.01) were found between years: 49.2% (4,739/9,633) in 2007, 53.6% (8,884/16,579) in 2008, 55.6% (11,102/19,969) in 2009, 42.8% (8,563/19,992) in 2010 and 45.9% (7,421/16,160) in 2011.

Table 4

Annual distribution of febrile illnesses by age group, according to data from individual fever forms

Age group Febrile syndromes (81,981 data available from 82,222 individuals forms)

2007
2008
2009
2010
2011

n
(%)
n
(%)
n
(%)
n
(%)
n
(%)
<1 year 1,601 (16.6) 2,887 (17.1) 2,916 (14.5) 2,923 (14.4) 2,375 (14.7)
1-4 years 3,122 (32.3) 5,391 (31.9) 5,396 (26.9) 6,096 (30.0) 4,864 (30.1)
5-14 years 1,775 (18.4) 3,110 (18.4) 4,905 (24.4) 4,529 (22.3) 3,743 (23.1)
15-24 years 1,156 (12.0) 2,177 (12.9) 3,057 (15.2) 2,983 (14.7) 2,253 (13.9)
≥25 years
1,837
(19.0)
3,145
(18.6)
3,563
(17.7)
3,542
(17.4)
2,635
(16.3)
Total 9,491 (11.6) 16,710 (20.4) 19,837 (24.2) 20,073 (24.5) 15870 (19.3)
Discussion

The sentinel surveillance system in Madagascar has two key functions: it provides an early warning of potential threats to public health and it can be used to manage public health programmes, by providing data for malaria indicators, for example. It can rapidly detect unexpected increases in the incidence of fever or diarrhoea syndromes and the biological surveillance associated with the syndromic surveillance programme can then identify the causes of these syndromes.

This system has been described in terms of the methods used [11] and in relation to aspects of influenza surveillance [12,13], such as the spread of the influenza A(H1N1)pdm09 virus [14,15]. During the influenza A(H1N1)pdm09 pandemic, the circulation of this virus in Madagascar was detected and the spread of the virus was followed from October 2009 to March 2010 [14]. We have already highlighted the weaknesses of the routine disease surveillance system in Madagascar, which is based on passive collection and limited capacities for diagnosis outside the capital city. None of the early-warning signs was identified by routine surveillance. Routine surveillance is useful for monitoring long-term programmes, but inappropriate for the timely detection of aberrant patterns. By contrast, syndrome-based near-real time surveillance can detect unusual events more rapidly [15-18]. This timeliness is a key element of the surveillance system and should be evaluated periodically [19].

The evaluation of surveillance systems should promote the most effective use of public health resources, by ensuring that surveillance systems operate efficiently [20]. The sentinel system in Madagascar was clearly simple and rapid, but we found that some process indicators tended to decline over time, due to high staff turnover. The decrease in the number of fever forms received annually, between 2007 and 2011, is one of the weaknesses of this system. The increase in the number of sentinel sites increased the workload of central staff managing the different activities. A lack of co-ordination hindered the training of new healthcare workers entering the network, and changes in practices were discovered only during supervision in the field. Challenges resulting from high staff turnover have also been identified in other countries [6,8]. The indicators used for the continuous assessment of the sentinel network in Madagascar are useful for a rapid, basic internal evaluation, but an external evaluation approach is also required, using CDC guidelines [21], for example, and including economic indicators as an integral part of the surveillance evaluation process [4].

The choice of methods used in the sentinel surveillance system in Madagascar was based on the capabilities of the volunteer healthcare providers and the financial resources available. The Madagascan network has grown over the years and its expansion is probably now limited by the human resources required to manage the network and data analysis. We have found that progressive step-by-step implementation is best, with assessment of the various processes, evaluations of network management capacity and the training of healthcare workers, to make the processes more acceptable.

Despite the results obtained to date, the sustainability of this system remains unclear, although data transmission costs amount to only about 2 US dollars per sentinel site per month. The Madagascan network has been supported by funding from various sources over the years, focusing on different health topics. Self-sustainability is another challenge, as already described [8], and has already been identified as a weakness of this network. We therefore need to focus on the first steps of surveillance system implementation and all system changes. Initial funds targeted arbovirosis, because of the spread of Chikungunya epidemics in Indian Ocean countries in 2006, and influenza, due to the threat posed by avian flu. However, the steering committee subsequently decided to include other diseases associated with febrile syndromes. This policy has been tremendously successful, making it possible for the network to provide epidemiological information not only about arboviruses, but also about malaria and influenza, throughout the country. In 2008, the first human case of Rift Valley fever was detected, by this network, at Taolognaro (in the south of the country), a site used for both syndromic and biological surveillance. For malaria, the network has monitored the shift from control to elimination following the strengthening of malaria prevention and control measures. The usefulness of sentinel networks for influenza detection is well documented and was assessed in the last pandemic period in 2009 [15]. Funding for work on these diseases has improved geographical coverage and made it possible to extend the network over the last five years. This network has become an additional tool for public health decision-making. The syndromic surveillance has been shown to be an effective approach to surveillance and, thanks to the availability of large mobile phone networks throughout Madagascar, the cost of real-time data transmission is low. This surveillance method may also facilitate compliance with the revised International Health Regulations for low-income countries and the aim of the Global Outbreak Alert and Response Network (GOARN) [22].

Limitations

However, the rapidity with which the system can identify unexpected events, which is seen as an advantage [23], must be weighed against delays in the response. For instance, the time required to conduct investigations and retrieve diagnostic and epidemiological information might negate the advantage of rapid data acquisition, particularly in developing countries, in which it can be hard to find the resources necessary for investigations.

The lack of historical data made it difficult to interpret the syndromic trends at each sentinel centre. One of the challenges in our system is determining epidemiological baselines for each centre, to facilitate the development of better statistical methods and more sensitive alert thresholds, as suggested by several authors [24-28]. Indeed, five years after the establishment of this network, large amounts of data are already available and data analysis methods have identified trends for ILI, malaria and dengue-like syndromes in areas of Madagascar with different climates. We now need to develop spatiotemporal models to increase the sensitivity of the alert detection process. However, limited geographical coverage and limited resources may prevent the detection of some epidemic events by this network.

Conclusion

It is clear that the greatest advantage of this system is the ease with which it can be implemented, thanks to the availability of mobile phones and mobile phone networks. Furthermore the quality of the homogeneous data collected will make it possible to improve the system relative to its principal objective: identifying epidemic events early. We recommend this solution for other African countries, because it performs very well and provides rapid benefits in terms of public health decision-making.

Notes

[1] This work was made feasible by the setting up of a sentinel network supported by WHO Geneva (APW/Ref. OD/AP-08-02451), the French Ministry of Health, the Madagascan Ministry of Health through “projet CRESAN” (crédit IDA – 3302-1-MAG (CRESAN-2)), the US Centers for Disease Control and Prevention (Cooperative Agreement Number: U51/IP000327-01), the US Department of Health and Human Service (Grant Number 6 IDSEP060001-01-01) via the International Network of Pasteur Institutes and the President’s Malaria Initiative program (USAIDS). We would like to thank Kathleen Victoir and Marc Jouan from the International Network of Pasteur Institutes.

[2] The authors have no competing interests to declare.

Acknowledgements

We thank all the staff from the Madagascan National Influenza Centre for influenza testing (Julia Guillebaud, Arnaud Orelle, Girard Razafitrimo and Vololoniaina Raharinosy), and the National Laboratory for Arbovirus (Jean Théophile Rafisandrantantsoa, Jean-Pierre Ravalohery and Josette Razainirina) for all laboratory tests.

We would like to express our gratitude to Dr Yolande Nirina Raoelina, who was one of the key people involved in setting up the sentinel network, and all the staff from the MoH. We are deeply indebted to all the doctors and nurses involved in sentinel surveillance on a daily basis in Madagascar.

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