test Exploring Temporal Patterns of American Foulbrood Disease in Türkiye Through the Seasonal-Trend Decomposition (STL) Method|Journal of the Hellenic Veterinary Medical Society

Exploring Temporal Patterns of American Foulbrood Disease in Türkiye Through the Seasonal-Trend Decomposition (STL) Method


Publiée : нояб. 5, 2025
T Bayir
İS Gürcan
Résumé

American Foulbrood (AFB), a highly dangerous and fatal disease of honey bees, is accountable for significant economic losses in harvesting of honey. This study analyzes temporal changes in reported numbers of AFB outbreaks and cases using a new analytical tool, STL decomposition. Time-series analyses were carried out using data supplied over an 18-year period beginning in January 2005 to uncover trends and the existence of seasonal fluctuations to enable beeking industry strategies to track and manage this significant bee diseases. STL, a seasonal-trend decomposition method developed using locally weighted regression, was used for visual statistical analysis to model the monthly number for AFB outbreaks and cases. To investigate the importance of the seasonality, a logistic regression model was employed. A total of 18483 AFB cases were recorded in Türkiye from January 1, 2005 to December 31, 2022, with a mean of 86 cases per month. STL decomposition demonstrated that the outbreak trend cycle was more flexible, whereas the case trend cycle abruptly rose and fell between 2018 and 2019. The STL decompositon revealed that the highest seasonal peaks of AFB incidence occurred in the spring and summer. This disease was more likely to occur throughout these two seasons (OR = 1.66, 95% CI: 1.16–2.37 and OR = 1.93, 95% CI: 1.36–2.75, respectively, with autumn regarded as reference). These findings can make significant contributions to the fight against the disease, further increasing regional competitiveness in honey production, better use of existing resources and meeting the increasing demand for honey products. 


Keywords: American Foulbrood; Honey bee diseases; Seasonal trend; STL method;  Time-series analysis.

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Références
Akpınar R, Bozdeveci A, Çelik S (2023) Orta ve Doğu Karadeniz
Bölgesindeki Bal Arılarında ve Temel Petekte Amerikan Yavru
Çürüklüğünün Teşhisi. F Ü Sağ Bil Vet Derg 37: 245-250.
Barros LV, Paulino MF, Moraes EHBK, Valadares Filho S, Martins LS,
Almeida DM, Valente EE, Cabral CHA, Lopes SA, Silva AG (2015)
Increasing levels of crude protein in multiple supplements for grazing
beef heifers in rainy season. Semin Cienc Agrar 36:1583-1598.
Balkaya İ (2016) Türkiye’de Görülen Bal Arısı (Apis mellifera) Hastalıkları.
Atatürk Üniversitesi Veteriner Bilimleri Dergisi 11:339-
Bayir T, and Gürcan İS (2023) Assessment of Peste Des Petits Ruminants
(PPR) in Turkey Between 2017-2019. Journal of the Hellenic
Veterinary Medical Society 74:5771–5780.
Bikaun JM, Bates T, Bollen M, Flematti GR, Melonek J, Praveen P,
Grassl J (2022) Volatile biomarkers for non-invasive detection of
American foulbrood, a threat to honey bee pollination services. Sci
Total Environ 845:157123
Chaloupka M (2001) Historical trends, seasonality and spatial synchrony
in green sea turtle egg production. Biological Conservation
:263-279.
Cleveland R, Cleveland WS, McRae JE, Terpenning IJ (1990) STL:
A seasonal-trend decomposition procedure based on loess (with
discussion). Journal of Official Statistics 6:3-73.
Cleveland WS, and Devlin SJ (1988) Locally weighted regression: an
approach to regression analysis by local fitting. JSTOR 83:596-610.
Dickel F, Bos NMP, Hughes H, Martín-Hernández R, Higes M, Kleiser
A, Freitak D (2022) The oral vaccination with Paenibacillus
larvae bacterin can decrease susceptibility to American Foulbrood
infection in honey bees-A safety and efficacy study. Front Vet Sci
:946237.
Diggle PJ (1990) Time series: a biostatistical introduction. Oxford
University Press.
Donkersley P, Rhodes G, Pickup RW, Jones KC, Power EF, Wright GA,
Wilson K (2017) Nutritional composition of honey bee food stores
vary with floral composition. Oecologia 185:749-761.
Gallai N, Salles JM, Settele J, Vaissiere BE (2009) Economic valuation
of the vulnerability of world agriculture confronted with pollinator
decline. Ecol Econ 68:810–821.
Genersch E (2010) American foulbrood in honeybees and its causative
agent, paenibacillus larvae. J Invertebr Pathol 103:S10–S9.
Graaf DC, Alippi AM, Brown ME, vans JD, Feldlaufer MF, Gregorc
A, Hornitzky M, Pernal SF, Schuch DM, Titěra D, Tomkies V,
Ritter WD (2006) Diagnosis of American foulbrood in honey bees:
a synthesis and proposed analytical protocols Letters in Applied
Microbiology 43:583-590
Hafen RP, Anderson DE, Cleveland WS, Maciejewski R, Ebert DS,
Abusalah A, Yakout M, Ouzzani M, Grannis SJ (2009) Syndromic
surveillance: STL for modeling, visualizing, and monitoring disease
counts. BMC Med Inform Decis Mak 9:21
Haseman L (1961) How long can spores of American foulbrood live. Am
Bee J 101:298–299.
Hitchcock JD, Stoner A, Wilson WT, Menapace DM (1979) Pathogenicity
of Bacillus pulvifaciens to hone bee larvae of various ages
(hymenoptera: apidae). J Kans Entomol Soc 52:238–246.
Jacques A, Laurent M, EPILOBEE Consortium, Ribière-Chabert M,
Saussac M, Bougeard S, Budge GE, Hendrikx P, Chauzat MP (2017)
A pan-European epidemiological study reveals honey bee colony
survival depends on beekeeper education and disease control. PloS
one 12:e0172591.
Jordan A, Patch HM, Grozinger CM, Khanna V (2021) Economic
dependence and vulnerability of United States agricultural sector
on insect-mediated pollination service. Environ Sci Technol
:2242–2253.
Jore S, Viljugrein H, Brun E, Heier BT, Borck B, Ethelberg S, Hakkinen
M, Kuusi M, Reiersen J, Hansson I, Olsson Engval E, Løfdahl
M, Wagenaar JA, van Pelt W, Hofshagen M (2010) Trends in
Campylobacter incidence in broilers and humans in six European
countries, 1997–2007. Prev Vet Med 93(1):33-41.
Karahan A, Zengin E, Kutlu MA, Karaca İ (2022) Afyonkarahisar İli
Arıcılarının Arı Hastalık ve Zararlılarını Tanıma Oranları. Uluslararası
Anadolu Ziraat Mühendisliği Bilimleri Dergisi 4:1-9.
Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham
SA, Kremen CT (2007) Tscharntke: importance of pollinators in
changing landscapes for world crops. R Soc 274:303–313.
Laurino D, Lioy S, Carisio L, Manino A, Porporato M (2019) Vespa
velutina: An Alien Driver of Honey Bee Colony Losses. Diversity
:5.
Mao Y, Zhang N, Zhu B, Liu J, He R (2019) A descriptive analysis of
the Spatio-temporal distribution of intestinal infectious diseases in
China. BMC Infect Dis 19(1):766.
McGregor SE (1976) Insect Pollination of Cultivated Crop-Plants. Agriculture
Handbook, Washington: pp 93–98.
Moretti LDA, Dias RA, Telles EO, de Carvalho Balian S (2010) Time
series evaluation of traumatic lesions and airsacculitis at one poultry
abattoir in the state of São Paulo, Brazil (1996–2005). Prev Vet
Med 94(3-4):231-239.
Özden (2017) Balarılarındaki Amerikan Yavru Çürüklüğü hastalığı
etkeni olan Paenibacillus larvae’nın larvalı petek ve bal örneklerinden
konvansiyonel ve moleküler biyolojik yöntemlerle teşhisi.
Ege Üniversitesi Fen Bilimleri Enstitüsü (PhD Thesis).
Roubik DW (2002) The value of bees to the coffee harvest. Nature
:708.
Rusenova N, and Parvanov P (2016) Prevalence of American Foulbrood
and Paenibacillus Larvae Genotypes in Bulgaria İstanbul Üniversitesi
Veteriner Fakültesi Dergisi 42(1):98-102.
Sanchez-Vazquez MJ, Nielen M, Gunn GJ, Lewis FI (2012) Using seasonal-
trend decomposition based on loess (STL) to explore temporal
patterns of pneumonic lesions in finishing pigs slaughtered in England,
-2011. Preventive veterinary medicine 104(1-2):65–73.
Sık Z, Atıcı EG, Altıntas O, Elitok Y, Sen S (2022) Frequency of American
Foulbrood in Honeybees: 2015-2020 Data of the Veterinary
Control Central Research Institute in Turkey. Etlik Veteriner Mikrobiyoloji
Dergisi 33(2): 15-20
Silawan T, Singhasivanon P, Kaewkungwal J, Nimmanitya S, Suwonkerd
W (2008) Temporal patterns and forecast of dengue infection
in Northeastern Thailand. The Southeast Asian journal of tropical
medicine and public health 39(1):90–98.
Steinhauer N, Kulhanek K, Antúnez K, Human H, Chantawannakul
P, Chauzat MP, vanEngelsdorp D (2018) Drivers of colony losses.
Current opinion in insect science 26:142–148.
Stephan JG, de Miranda JR, Forsgren E (2020) American foulbrood
in a honeybee colony: spore-symptom relationship and feedbacks
between disease and colony development. BMC Ecol 20:15
TEPGE (2023) Beekeeping product report http://www.tepge.gov.tr [accessed
August 2023].
Walton A, Dolezal AG, Bakken MA, Toth AL (2018) Hungry for the
queen: honey bee nutritional environment affects worker pheromone
response in a life-stage dependent manner. Funct Ecol 32:2699-
Ward MP (2002) Seasonality of canine leptospirosis in the United
States and Canada and its association with rainfall. Prev Vet
Med 56(3):203-213.
Xiong T, Li C, Bao Y (2018) Seasonal forecasting of agricultural commodity
price using a hybrid STL and ELM method: Evidence from
the vegetable market in China. Neurocomputing 275:2831-2844.
Yalcinkaya A, Keskin N, Özkirim A (2009) After Colony Losses in
Hatay and Adana Region of Turkey the Investigation of Honey Bee
Diseases. Montpellier, France: Abstract API mondia.
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