Epidemic waves of HPAI H5N1 outbreaks in Egypt

In Egypt, six epidemic waves (EW1–6) of HPAI H5N1 outbreaks were identified over the study period, Fig. 1. The 1st EW began in February 2006, peaked in March 2006, and ended in July 2006. This was the first introduction of the disease in Egypt with 1627 outbreaks, Fig. 1. The highest numbers of outbreaks were in Sharkia, Giza, Qalyobiya, Dakahlia, Gharbia, Menia, and Menofia governorates, respectively, Fig. 2A. The 2nd EW began in October 2006, peaked in March 2007, and ended in August 2007; with 571 outbreaks, Fig. 1. Unlike the 1st EW, the highest numbers of outbreaks were in Gharbia, Menofia, Damietta, Menia, Giza, Alexandria, Dakahlia Qalyobiya, Qena, Aswan, and Luxor governorates respectively, Fig. 2B. The 3rd EW began in November 2007, peaked in January 2008, and ended in July 2008; with 309 outbreaks, Fig. 1. The highest numbers of outbreaks were in Gharbia, Qalyobiya, Sharkia, and Menofia governorates respectively, Fig. 2C. The 4th EW began in November 2008 and ended in July 2012 with three successive peaks in March 2009, March 2010, and March 2011. This was the longest EW with three epidemic cycles; from January 2009 to August 2009, January 2010 to August 2010, and from January 2011 to August 2011, respectively. All cycles peaked in March with outbreaks observed all over the year. The total number of recorded outbreaks during the 4th EW was 2280, Fig. 1. The highest numbers of outbreaks were recorded in Menofia, Dakahlia, Qalyobiya, Fayoum, Gharbia, and Giza governorates respectively, Fig. 2D.

Fig. 1
figure 1

Epidemic curves of outbreaks of highly pathogenic avian influenza subtype H5N1 in Egypt (January 2006 to December 2017), illustrating A) daily, B) weekly, and C) monthly frequency of outbreaks as a function of time. Vertical lines delineate the six epidemic waves

Fig. 2
figure 2

Spatial distribution of HPAI H5N1 outbreaks in Egyptian governorates in the six epidemic waves

The 5th EW began in October 2012, peaked in March 2013, and ended in June 2013 with no significant outbreak until December 2013 in which 255 outbreaks were reported. The highest numbers of outbreaks were in Menofia, Giza, Gharbia, Behera, and Dakahlia, governorates respectively Fig. 2E. While, the 6th EW began in December 2013, with a significant number (2391) of outbreaks over the whole period until 2017; successive peaks were observed without specific patterns with alteration in the usual epidemic cycles. Unlike all EWs, the highest numbers of outbreaks were in Menia, Sharkia, Suhag, Giza, and Dakahlia governorates respectively, Fig. 2F.

The spatial pattern of outbreak density

The outbreaks are represented by black dots and the density from the adaptive kernel density estimation is highlighted in monochromatic grey (the higher the density, the darker the color) and Fig. 3.

Fig. 3
figure 3

Adaptive kernel density estimation of highly pathogenic avian influenza subtype H5N1 outbreaks in Egypt in six epidemic waves (Highlighted in monochromatic grey: the higher the density, the darker the color)

The spatial distribution of outbreaks in the 1st EW was confined to the Delta region with low density in Upper Egypt. The highest density was observed in Sharkia, Giza, Qalyobiya, Dakahlia, and Gharbia governorates. In the 2nd EW, outbreak density covers all Delta governorates besides, Alexandria and Damietta with outbreaks beginning to increase toward upper Egypt covering Fayoum, Menia, Qena, Luxor, Aswan with a significant density. The 3rd EW almost has the same distribution as the 2nd EW but with lower sharpness.

In the 4th EW, the outbreaks seem to be connected from Damietta, Behera, Alexandria passing through all delta governorates to Giza, Fayoum, Beni Suef with a lower density in Lower Egypt compared to Upper Egypt. The spatial distribution of outbreaks in the 5th EW was confined to the Delta region with two separate spots of high density in the new valley and Luxor. By the 6th EW, all governorates along the delta region and Nile valley suffered from the highest density of outbreaks.

Spatiotemporal clusters

The extent and location of clusters are fully described in (Tables 1 and 2, Fig. 4). The results from daily, weekly, and monthly outbreaks were very similar, therefore only weekly results were reported. Significantly detected Spatiotemporal clusters, from the space-time permutation scan statistics, are illustrated by the most likely cluster (red circle) and by a secondary cluster (light, green-dashed circles) in (Tables 1 and 2, Fig. 4). In the 1st EW, clusters were covering the whole country. The primary clusters with the highest number of locations were stopover sites for wild birds in Fayoum “Lake Qarun, Wadi El Rayan”, and in Behera “Wadi El Naturn”. Also, in Menofia, Qalyobiya, Cairo, Giza, Menia, and Benisuef of 119.7 Km radius. The highest relative risk (RR) clusters were observed in Dakahlia, Qalyobiya, and one cluster in Upper Egypt involving (Menia, Qena, Suhag, Assuit, Luxor, Aswan, New_valley).

Table 1 Clusters of HPAI H5N1 outbreaks detected by space-time permutation scan statistic for six epidemic waves in Egypt
Table 2 Spatial distribution of significant clusters of HPAI H5N1 outbreaks detected by space-time permutation scan statistic for six epidemic waves in Egypt
Fig. 4
figure 4

Spatial patterns and Spatiotemporal clusters of weekly outbreaks of highly pathogenic avian influenza subtype H5N1 over six epidemic waves in Egypt. Outbreaks represented by black dots and Outbreak density from adaptive kernel density estimation are highlighted in monochromatic grey (the higher the density, the darker the color). Significant spatiotemporal clusters detected from the space–time permutation scan statistics are illustrated by the most likely cluster (red circle) and by a secondary cluster (light green-dashed circles)

In the 2nd EW, the primary cluster of the first outbreak with the highest number of locations and cases of radius 28.9 km was located only in the delta governorates-Menofia, Gharbia, Qalyobiya, Dakahlia, Sharkia, and KafrElsheikh. It is near the migratory bird stopover site “Wadi El Naturn”. Clusters of high RR were also detected in Kafr_Elsheikh, Damietta, Dakahlia, Behera, and Menia governorates (the same governorates appear to have the highest outbreak density).

In the 3rd EW, the primary cluster was detected at the end in the Menia governorate with a 44.9 Km radius. Outbreak clusters continued to appear in the same governorates except for Damietta. The highest RR clusters were in Fayoum, Cairo, Giza governorates. Other clusters with relatively high RR were noticed in the delta region, specifically in Sharkia, Dakahlia, Qalyobiya, Kafr_Elsheikh, Gharbia governorates. It is worth mentioning that no clusters were detected in Upper Egypt.

In the 4th EW, 30 clusters were detected and characterized by small radius size, all confined to the Delta region and Nile valley, with a noticed cluster in Damietta. The primary cluster, the first occurring cluster in the 4th EW, was located in Alexandria and Behera of a 33.7 Km radius. It was including migratory bird stopover sites “Lake Maryut” in Behera and “Lake ldku” in Alexandria. However, lowered density observed in upper Egypt, several clusters in all upper Egypt governorates were detected-unlike the 3rd EW- in Menia, BeniSuef, Assuit, Luxor, Suhag, and Aswan governorates. The highest RR clusters were observed in Qalyobiya, Luxor, Menofia, BeniSuef, Assuit, Aswan, Behera, Sharkia, and Fayoum governorates.

In the 5th EW, newly hot spots with clusters in Ismailia, Suez, and New Vally governorates were detected. With only one cluster conjoin Suhag, Qena, and Luxor governorates of a radius of 91 Km. The primary cluster was detected at the end of the wave of 57.5 Km radius with the highest number of locations in Menofia, Gharbia, Qalyobiya, Dakahlia, Sharkia, Kafr_Elsheikh- besides Cairo, Suez, and Ismailia governorates. It included two migratory bird stopover sites in Ismailia “Bitter Lakes” and Suez. The highest RR clusters were detected in Fayoum, Giza, BeniSuef, Suez, Suhag, Qena, Luxor, and Alexandria governorates.

In the 6th EW, clusters previously detected in Ismailia and Suez continued to be detected with clustering in all delta regions and Nile valley governorates. A special primary dislodged cluster was detected in Menia, Suhag, Assuit, Qena, and BeniSuef. The Primary cluster occurred as the fifth cluster in the first 4 months of the beginning of the wave and lasted 8 months to the end of 2014 with the highest number of cases and of 183.7 Km radius. Clusters of high RR in Giza, Cairo, Qalyobiya, Menofia, Sharkia, Fayoum, Benisuef, Dakahlia, Damietta, Kafr_Elsheikh, and Gharbia governorates were identified.

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