research articles on dengue fever in pakistan

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• Ann Med Surg (Lond)
• v.85(4); 2023 Apr
• PMC10129218

Year-round dengue fever in Pakistan, highlighting the surge amidst ongoing flood havoc and the COVID-19 pandemic: a comprehensive review

Shehroze tabassum.

a King Edward Medical University, Lahore

Aroma Naeem

Abubakar nazir, farhan naeem, shehram tabassum.

b Faisalabad Medical University, Faisalabad, Pakistan

Dengue fever (DF) is an arthropod-borne viral infection caused by four serotypes of dengue virus (DENV 1–4) transmitted to the host by the vector mosquito Aedes , which causes fever, vomiting, headache, joint pain, muscle pain, and a distinctive itching and skin rash, ultimately leading to dengue hemorrhagic fever and dengue shock syndrome. The first case of DF in Pakistan was documented in 1994, but outbreak patterns began in 2005. As of 20 August 2022, Pakistan has 875 confirmed cases, raising alarming concerns. Misdiagnosis due to mutual symptoms, lack of an effective vaccine, the weakened and overburdened health system of Pakistan, irrational urbanization, climate change in Pakistan, insufficient waste management system, and a lack of awareness are the significant challenges Pakistan faces and result in recurrent dengue outbreaks every year. The recent flood in Pakistan has caused massive destruction, and stagnant dirty water has facilitated mosquito breeding. Sanitization and spraying, proper waste management, an adequate and advanced diagnostic system, control of population size, public awareness, and promotion of medical research and global collaboration, especially amidst flood devastation, are recommended to combat this deadly infection in Pakistan. This article aims to comprehensively review the year-round DF in Pakistan, highlighting the surge amidst ongoing flood havoc and the coronavirus disease 2019 pandemic.

Introduction

• Dengue fever is an arthropod-borne viral infection transmitted to the host by the vector mosquito Aedes , which can lead to death when complicated by dengue hemorrhagic fever and dengue shock syndrome.
• The Pattern outburst began in 2005, and since then it has become endemic to Pakistan. This year’s massive floods in Pakistan are aggravating the already worsening dengue situation in Pakistan
• Our article provides a comprehensive review of the past and present status of dengue, the past and present hurdles faced by Pakistan, the efforts made by the government to mitigate the situation in the past, and the counteractive measures taken to control this deadly infection.

Dengue fever (DF) is an arthropod-borne viral disease caused by four serotypes of dengue virus (DENV 1–4), transmitted to the host by the vector mosquito Aedes 1 . Symptoms include fever, vomiting, headache, joint pain, muscle pain, and a distinctive itching and skin rash that usually begin 3–4 days after infection. In rare cases, the disease develops into a severe dengue hemorrhagic fever, resulting in bleeding, a low platelet count, and blood plasma leakage, or a dengue shock syndrome in which blood pressure becomes critically low 2 , 3 . The bite of a mosquito vector bearing dengue virus facilitates dengue virus entry white blood cells by binding to them, causing the production of interferons and cytokines, which are responsible for many of the disease symptoms. Due to increased capillary permeability, blood leaks from the blood vessels into the body cavities, causing a decrease in blood flow and ultimately decreasing blood pressure, due to which vital organs suffer. The platelet count also decreases, increasing the bleeding risk 4 .

Direct and indirect methods are used for diagnostic purposes. Direct methods include virus isolation, RT-PCR, and dengue nonstructural protein one antigen detection. Indirect methods include serological tests, that is, immunoglobulin (Ig)G and IgM detection. Direct methods are preferred during the first 7 days after the onset of fever. Virus isolation and RT-PCR have largely been replaced by the rapid diagnostic detection of nonstructural protein one antigen 2 . If more than 7 days have passed, serologic tests are used to detect IgM. The presence of IgM confirms a recent infection. The detection of IgG can be due to a recent or past infection. Therefore, serial titers are required to confirm the diagnosis 5 .

Comparing the past and current status of dengue in Pakistan

The earliest outbreak of dengue dates from 1779, but the details about its viral cause, spread, and complications were comprehended in the early 20th century. DF has become an international issue since the Second World War. It is prevalent in 120 countries, especially in Southeast Asia and South America 6 . Approximately 390 million cases of DF are reported annually, but only 96 million are clinically evident. A population of more than 3 billion is at risk of getting this viral infection 7 . Every year, Pakistan reports hundreds of cases of DF. Most of the cases are reported from the southeast of the country. Lahore and the twin cities (Rawalpindi and Islamabad) are significantly affected by it. As of 20 August 2022, Pakistan has reported 1807 suspected cases with 875 confirmed cases. There had been an increase of 932 suspected cases during the past 1.5 months 8 , raising alarming concerns. A DF outbreak occurs every year in Pakistan. It has become a national risk amidst the coronavirus disease 2019 (COVID-19) and monkeypox pandemics. According to the WHO, the first case of DF in Pakistan was registered in 1994. However, the yearly outburst pattern started in Karachi in November 2005. Before 2006, dengue was limited to certain areas of Pakistan. Since 2010, Pakistan has been affected by annual dengue outbreaks, which peak in the postmonsoon season 9 . According to the National Institute of Health, about 22 938 DF cases were reported in 2017. More than 3200 in 2018, 24 547 cases in 2019, and 3442 cases were reported in 2020. In 2021, a significant rise in cases was seen in Lahore and the twin cities (Rawalpindi and Islamabad), where the confirmed cases were reported to be 48 906. The outbreak came to its seasonal end in the winter, though some cases were reported until December 10 . This year, Pakistan is again facing a dengue outbreak, and cases are increasing daily, with a total of 41 746 confirmed cases reported as of 11 October 2022 8 . Figures ​ Figures1 1 and ​ and2 2 show the number of confirmed dengue cases and the trend of dengue cases in Pakistan, respectively, during recent years in Pakistan 8 , 10 .

Illustrates the number of confirmed dengue cases in Pakistan.

Illustrates the trend of dengue cases in Pakistan.

Past and present obstacles in battling dengue in Pakistan

Misdiagnosis due to mutual symptoms.

Since the symptoms of DF are similar to those of other febrile viral diseases, it becomes difficult to accurately diagnose dengue clinically. Patients presenting with complaints of fatigue, fever, skin rashes, muscle aches, and petechiae with unremarkable chest radiographs, suggesting severe viral diseases, make it quite difficult to distinguish between dengue and COVID-19 11 . A comprehensive comparison between dengue and COVID-19 is written in Table ​ Table1 1 12 . Similarly, Zika and Chikungunya also have similar signs and symptoms and are strong differentials of dengue. Overlapping symptoms of Dengue, COVID-19, Chikungunya, and Zika are illustrated in Figure ​ Figure3 3 .

Comparison between dengue and COVID-19.

COVID-19, coronavirus disease 2019; SARS-CoV-2, severe acute respiratory syndrome coronavirus-2.

Illustrates overlapping symptoms of dengue with other febrile diseases. COVID-19, coronavirus disease 2019.

Lack of effective vaccine

There has yet to be an effective vaccine developed for dengue, one of the significant challenges developing countries like Pakistan face, resulting in thousands of dengue cases each year. Sanof-Pasteur developed a tetravalent dengue vaccine that has been allowed for patient usage, but its efficacy has put a question mark on it 13 . The disease is treated mainly by managing the symptoms that occur during its course. Moreover, the health system of Pakistan lacks adequate funds for research to develop a vaccine for such diseases.

Susceptibility to all serotypes and secondary infections

There are four different serotypes of dengue virus (DENV 1–4). An infection with one serotype provides long-lasting immunity to the homologous serotype but not to other serotypes. DF is endemic in Pakistan, with widespread distribution of all serotypes, and the population is at risk of re-infection. Due to secondary infections, people are more susceptible to developing severe dengue that requires hospital admissions. Consequently, catastrophic sequelae can occur if such cases are not promptly and effectively treated 14 .

The overburdened health system of Pakistan amidst the COVID-19

The health care system is overburdened and facing a financial crisis as well. The health system is not strong enough to deal with outbreaks like dengue amidst COVID-19. Most cases in remote areas of Pakistan remain unreported due to a lack of testing facilities. Moreover, health care facilities are more oriented toward fighting COVID-19, which may cause many dengue cases to go unreported 9 .

Irrational urbanization

Unplanned urbanization is associated with dengue spread through different socioeconomic factors, including population growth, sewage issues, and access to reliable water sources 2 .

Climate changes in Pakistan

The spread of the dengue virus is inversely proportional to the rise in temperature. The majority of cases in Pakistan are reported from July to September. Heavy rainfall, ideal temperature, and humidity during this period provide convenient circumstances for the survival, growth, and breeding of Aedes mosquitoes. The climate of Pakistan is a major factor contributing to the recurrent outbreaks of dengue in Pakistan 15 , 16 .

Insufficient waste management system

Waste management authorities fail to fulfill their responsibilities by adequately managing the waste, thus polluting the environment. Sewage waste and open drainage systems can act as a habitat for the dengue virus, thus catalyzing the spread of the virus 17 .

Lack of awareness

There is a lack of understanding of the causes and complications of DF in the general population of Pakistan. Children are not appropriately educated in schools regarding its symptoms and preventive measures. Moreover, most people in endemic areas do not use mosquito nets or mosquito repellants for protection.

Massive floods aggravating the dengue situation in Pakistan

As of June 2022, rainfall in Pakistan was 2.9 times higher than the previous 30-year average. Since 1961, Pakistan saw its wettest August in August 2022. The most severely affected province was Sindh. With 33 million people affected, the ensuing floods have injured 13 000 people and claimed about 2000 lives 18 . Thirteen million homes were damaged, and 800 000 houses were completely destroyed. More than 2 million individuals were left without a place to live 19 . Tentative analyses show that the current level of destruction is significantly worse than that brought on by previous floods, including the devastating floods of 2010 20 .

Before the heavy rain and ensuing floods, Pakistan had already documented a considerable number of dengue cases. The condition is worsened by the flood, especially in camps and places where water and sanitation infrastructure has been devastated. Standing water serves as an ideal breeding place for mosquitoes that spread dengue 20 . The correlation between record-breaking rainfall in August 2022, followed by the highest number of dengue cases in October 2022 nationwide, seems obvious. The incidence of dengue infection in Pakistan appears to be directly correlated with the amount of precipitation, and dengue infections were most prevalent in the areas that experienced flooding 21 . Pakistan is already afflicted with waterborne disease outbreaks recently 22 , 23 ; the present dengue situation, exacerbated by floods, can prove a threat to Pakistan’s public health and safety.

Efforts done by the Government of Pakistan for dengue control in past years

Punjab province.

In Punjab province, Aedes larvae surveillance and space spraying operations are being carried out as part of integrated vector management (IVM). Rawalpindi and Islamabad city have undergone fumigation and spot checks since a field hospital in Lahore opened. To contain the dengue outbreak in Islamabad, multisectoral coordinated activities have been started, including vector surveillance, breeding site destruction, the active finding of cases and contacts, patient management, waste management, and space and indoor residual spraying 14 .

Sindh and KPK province

In Sindh province and 10 Union Councils of the Peshawar district in the Khyber Pakhtunkhwa (KPK) province, control activities and vector surveillance are now being conducted as part of a special campaign 14 .

Balochistan province

In Balochistan province, some districts underwent selective indoor residual spraying operations. At specific hotspots in the Kech District, space spraying operations and breeding site management are conducted ad hoc 14 .

WHO and other international organizations are helping Pakistan by strengthening surveillance and reporting systems, ensuring the availability of logistics required for diagnosis, treatment, and control (pesticides, nets, etc.) of dengue, and training health care providers and surveillance teams, including entomologists 14 .

Counteracting measures needed to eradicate dengue in Pakistan

Although it is commendable that the Government of Pakistan has taken practical steps to prevent and control dengue. But there is still a dire need for specific measures to be taken to alleviate the burden of DF in Pakistan.

Vector control measures

WHO encourages IVM, which is a strategic method to manage mosquito vectors. To eliminate potential breeding places, lower vector populations, and reduce personal exposure, IVM actions should be effectively implemented. This should include methods for protecting individuals and homes and tactics for controlling vector larvae and adults (such as source reduction, chemical control measures, and environmental management). All sites where there is human-vector contact (places of residence, workplaces, schools, and hospitals) should be the focus of vector control initiatives. Weekly draining, cleaning, and covering of household water storage containers must be done in this regard. If mosquito bites occur indoors, skin creams or mosquito repellant sprays should be, and household insecticide aerosol products should be encouraged 14 . The municipal committee must be vigilant in the rainy seasons to avoid stagnant water, which can provide a medium for vector growth. District management must prioritize filling stagnant water reservoirs and demoralize the concept of open water containers. The government must dispose of the garbage and wastes properly to maintain a healthy environment and control the spread of dengue in the community.

An adequate and advanced diagnostic system

Although diagnostic facilities are available in the country’s main areas, the facilities are not uniformly distributed and are lacking in various underprivileged areas. The government must organize a proper diagnostic system for testing dengue in remote areas to keep the viral load in check before it gets too late to handle the case with limited resources. Moreover, the laboratory testing facilities should be equipped with advanced technologies like PCR and antibody testing to distinguish between dengue and related diseases. Similar to other infectious diseases, there must be early case detection, prompt case isolation, quick traceback, close monitoring of those at risk, appropriate personal protection, and safe burial, especially in underprivileged areas.

Control in population size

The population size must be controlled as it will lower the burden on Pakistan’s already weakened health care system, enabling it to provide better and extraordinary services to the people affected by DF. This is crucial for a developing country like Pakistan where massive population size and irrational urbanization have already crippled the country.

Public awareness

Health education is a fundamental part of any infectious disease control program. People can better comprehend the dengue virus by being aware of the vector’s life cycle, ecology, and biology, which encourages healthy behaviors 10 . Awareness sessions must be conducted throughout the country to make people aware of their responsibilities as citizens to combat recurrent dengue outbreaks. The teachers, elders, and influential people should be sensitized about the severity of the virus 24 . Both electronic and print media should be engaged to play their part.

Promotion of medical research and global collaboration

Extensive research should be carried out in the area of vaccine and antiviral development for dengue. The development of an effective vaccine can work wonders in eradicating dengue not only from Pakistan but from the whole world. Therefore, international collaboration is also essential in this cause.

Emergency preventive measures in recent flood-affected areas

The current floods in Pakistan have posed severe health risks for the affected population. The current situation provides favorable conditions for dengue to spread. The situation should be controlled by an appropriate and immediate action plan. Prevention at this stage should be taken before things get out of hand. Restoration of the drainage system would help decrease mosquitoes’ breeding places. People should have access to safe drinking water and health care facilities. Other priorities include strengthening and expanding disease surveillance, preventing and controlling outbreaks, and ensuring a well-coordinated response at the national and subnational levels, with the coordination of all relevant partners. The government should allocate an appropriate budget for this cause. National and international nongovernment organizations can also contribute to the motivation to make it more effective.

Dengue is a significant challenge for the health care system of many under-developed countries, especially Pakistan, affecting many people each year. Pakistan is experiencing major public health threats in the face of the current massive flood that facilitates the transmission of this deadly disease. Almost one-third of Pakistan’s population is suffering from life-threatening infections, including cholera, malaria, typhoid, etc., due to flood consequences. Although the government of Pakistan has initiated plans to tackle the problem, there is still a need for improvement. Diagnostic and treatment facilities should be extended in far-flung rural areas, and measures should be taken to destroy breeding places for mosquitoes that transmit the disease. Strict standard operating procedures must be formed and implemented effectively to prevent this year-round fatal disease in Pakistan.

Ethical approval

Not required.

Not applicable.

Source of funding

Author contribution.

S.T.: conceptualization. S.T., A.N., A.N., F.N., S.G., and S.T.: writing. S.T. and S.G.: review with critical comments. S.T. and S.G.: editing.

Conflicts of interest disclosure

None declared by any authors involved in the manuscript.

Research registration unique identifying number (UIN)

Shehroze Tabassum.

Provenance and peer review

Not commissioned, externally peer reviewed.

Acknowledgments

Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article

Published online ■ ■

• Research article
• Open access
• Published: 25 June 2020

A spatial-temporal study for the spread of dengue depending on climate factors in Pakistan (2006–2017)

• Waqas Shabbir   ORCID: orcid.org/0000-0002-0753-7850 1 ,
• Juergen Pilz 1 &
• Amna Naeem 2  

BMC Public Health volume  20 , Article number:  995 ( 2020 ) Cite this article

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In Pakistan, dengue fever has become a major concerning factor, given that it is a relatively new disease compared to malaria. The number of people affected by dengue fever has increased at least 10-fold in the last 15 years in specific areas of Pakistan. Therefore, it is necessary to analyse this disease to reduce or prevent the effects of dengue fever in the region.

Geographical information system (GIS) maps are used to identify the intensity of the spread according to the count of affected people in our study area. Generalised linear modelling (GLM) is used to study the significance of factors associated with dengue fever.

The dengue virus is present throughout the year in specific areas of Pakistan. Karachi and Lahore are most significantly affected with cases in these two most populous cities of Pakistan reported every year. In the study period (2006–2017), 2011 was the most devastating year for Pakistan. Lahore recorded more than 17,000 confirmed cases with 290 deaths in a single year. The GLM analysis shows rainfall, the average maximum temperature, and hospitals to be significant factors in the prevalence of dengue fever.

This study finds that Sindh and Khyber Pakhtunkhwa are two of the primarily vulnerable provinces for the spread of dengue fever. Punjab has observed sporadic increases in dengue fever cases. In Pakistan, dengue cases increase in the rainfall season, especially during monsoon season. Lack of proper hospitals and clinics are another major factor, and mobile hospitals are needed in remote hotspot regions often affected by dengue fever. Finally, improved sanitation systems in metropoles would facilitate reducing breeding grounds for Aedes Aegypti larvae.

Peer Review reports

The dengue virus is spread through the bite of a mosquito into the bodies of mammals including humans. This virus is spread from the mosquitos of the family Aedes Aegypti, and the dengue virus is transmitted through the bite of female mosquitos [ 1 ]. The lifespan of a dengue mosquito is short, but after the larvae emerge from the eggs, they spread the dengue virus from 4 to 10 days on average during their lifespan [ 2 , 3 , 4 ]. The most suitable temperature for the eggs is 30°C. The combination of high temperatures and rainfall provides a substantial rise in dengue outbreaks [ 5 ]. The symptoms of dengue fever include nausea, pain in the limbs and joints, severe headache, vomiting, and so on [ 1 , 6 ]. The early symptoms of dengue are similar to common fever and headaches, becoming increasingly intense over time. Different types of dengue viruses exist, and four types have been identified so far, namely DENV1, DENV2, DENV3, and DENV4 [ 2 ].

The World Health Organization has projected that 2.5 billion people across the globe are at risk of becoming affected with dengue fever in all continents except Antarctica [ 1 ]. The incidence of dengue fever has increased by 30 times worldwide, in the last 50 years alone in more than 100 countries. South-East Asia and southwestern America are two primary hotspots where the dengue virus has affected substantial populations [ 7 , 8 ]. Rapid globalisation in the trade and tourism sectors and mass displacements (migration) have had major implications on human lives because globalisation has the potential to spread the disease to other parts of the world. Climate change effects are found in multiple parts of the globe and are responsible for making temperatures in particular regions more suitable for breeding mosquito-borne diseases, such as dengue fever [ 9 , 10 , 11 , 12 ]. Although the dengue virus is a noncontagious disease, it can be imported by different means, including air transportation. A viraemic person can carry the virus from one region or country to another because it can be transmitted via other mosquitos who are infected by the viraemic person [ 13 , 14 , 15 ]. The rise in global travel patterns is also a cause of the spread of new dengue virus serotypes and genotypes along with the spread of existing ones [ 16 , 17 , 18 ].

Recent climate-based research and projections put Pakistan in the top 10 list of countries affected by climate change, and numerous research articles have linked climate change and dengue fever [ 19 , 20 ]. Studies have found that rainfall, temperature, and humidity are associated with the prevalence of dengue fever [ 21 , 22 , 23 , 24 ]. In Pakistan, all types of climates can be found: tropical to semi-tropical areas, deserts, and relatively cold areas in the north. Dengue fever in Pakistan has changed in terms of survivability against multiple factors, and the data in more recent years have suggested that the intensity of dengue fever has shifted from mild to severe [ 25 ].

Pakistan comprises a total area of 796,095 km 2 and has four provinces (Sindh, Khyber Pakhtunkhwa, Punjab, and Balochistan) and two federally administrated regions (Gilgit-Baltistan and Kashmir). Our study is focused on the three provinces of Sindh, Khyber Pakhtunkhwa, and Punjab. We investigate the spread of dengue in 41 cities across these three provinces. The study area is illustrated in Fig. 2 . Punjab is the biggest province in terms of population in Pakistan, and Lahore is its capital. Lahore has a population of 12 million people. Karachi is by far the biggest city in Pakistan and is the capital of the province of Sindh. It has a total population of 20 million people. It also generates most of the revenue for Pakistan. Big cities have major complexities in terms of managing various departments, which is observed in Karachi where pollution (air and land) is the norm. Karachi has experienced regular power outages and the lack of proper waste disposal. Moreover, excess rainfall water and poor sanitation make it one of the worst maintained metropolitan areas in the world, and it is a breeding ground for mosquitos. Except for a few hospitals, not many have the capacity to cope with emergencies, as in the case of dengue fever. Peshawar is the capital of Khyber Pakhtunkhwa and has a population of 4 million people. Islamabad is the capital of Pakistan and has a population of one million inhabitants.

Pakistan is 30.37° north and 69.34° east in South Asia with a population of over 210 million. The dengue virus is present in tropical and subtropical regions of Pakistan because it is a hospitable environment for the virus [ 26 , 27 , 28 ]. Pakistan experiences heavy rainfalls in the monsoon season and an increase in dengue cases in that period [ 29 ]. Dengue cases in Pakistan first surfaced in 1994; however, it only gained attention in the mid-2000s when the number of cases began to rise to large numbers in the coastal city of Karachi [ 30 ].

In this paper, we discuss the data and methods used to conduct the analysis. In the later part of our study, we plot the data spatiotemporally for 2006 to 2017 in three provinces of Pakistan. Finally, in the last section, we present the conclusions and suitable suggestions.

In this study, we mapped the intensity of dengue fever in 41 regions of Pakistan over a 12-year period using the choropleth (intensity) mapping technique. Our study is conducted in three provinces: Sindh, Khyber Pakhtunkhwa, and Punjab. The regions under study differ in terms of climate, elevation, population densities, and so on.

Area Selection

The regions were selected based on their population densities and importance in terms of economic growth. The climates of the regions vary to a high extent. The province of Sindh is mostly hot, humid, and dry. In contrast, Punjab has a very cold winter with a hot summer but receives heavy precipitation in the monsoon season. Khyber Pakhtunkhwa has a mild climate compared to the other two provinces; it includes regions with significantly higher elevations.

Data Collection

The data on dengue were collected through news publishing agencies and published articles [ 31 , 32 , 33 , 34 , 35 ]. Dengue case data were collected yearly for the period 2006 to 2017. Climate data were collected through NOAA, USA, and online weather monitoring service providers [ 36 , 37 ]. The climatic factors include maximum temperature, minimum temperature, and rainfall. The data on literacy, population, sanitation, and hospitals were collected through the World Wide Web and published reports from nongovernmental organisations (NGOs) [ 38 , 39 ].

Geographical Information Systems

Geographical information systems (GIS) are used for mapping quantitative data and are easy and well-defined tools to use when the aim is to demonstrate the intensity of an effect in specific areas to compare the area visibly because it is easier to observe which location exhibits more influence. ArcMap 10.5 is used as the GIS mapping tool for the dengue cases, population density, maximum and minimum temperatures, and elevation. Figure 1 illustrates the map of Pakistan, and the study area is depicted in Fig. 2 .

Provinces and administrated regions of Pakistan

Study area: 41 cities selected from three provinces

Data Analysis

The data were analysed using a GIS mapping technique. Approximately 86,000 dengue casualties (both deaths and number of cases) were observed in our preselected spatial units under study throughout the 12-year period. Most cases were reported in Lahore cumulatively, but this is primarily because of the anomaly observed in 2011 with the highest number of cases reported. The choropleth maps show the hotspots and areas that are less affected. We used different levels of intensities depending on the number of dengue fever cases in a given year. Generalised linear modelling (GLM) was applied to our climatic, social, and geographical factors involved in our dengue study. In addition, R-studio was used for the GLM analysis.

In this study, GIS was used to map the spatial and temporal intensity of dengue fever. In the figures depicted below, we mapped dengue fever cases according to different spatial units in our study area (Fig. 3 a-l).

a Dengue incidences recorded in 2006. b Dengue incidences recorded in 2007. c Dengue incidences recorded in 2008. d Dengue incidences recorded in 2009. e Dengue incidences recorded in 2010. f Dengue incidences recorded in 2011. g Dengue incidences recorded in 2012. h Dengue incidences recorded in 2013. i Dengue incidences recorded in 2014. j Dengue incidences recorded in 2015. k Dengue incidences recorded in 2016. l Dengue incidences recorded in 2017

The most affected years regarding dengue cases were 2011 and 2013 (for the study period 2006–2017) (Fig. 3 a-l). One possible reason that 2011 was the most devastating year is because of the heavy rainfall in the country causing heavy flooding; however, an increase in the number of dengue cases started to emerge prior to this in 2010. The study found that the main cause for higher than usual cases of dengue in Lahore could be attributed to the import of automobile tyres from Thailand (one of the hotspots for dengue in Asia) in 2011, and the tyres were infested with larvae contaminated with the dengue virus. Hence, the spread was massive [ 40 ].

The average temperatures in north-western Pakistan are mild, and these areas also record high amounts of rainfall. Northern Pakistan has several regions with high-altitude populations. However, the GLM estimates did not find elevation to be a significant factor affecting dengue fever cases, although we know that elevation influences the temperature. Our results using GLM indicate that the rainfall, average maximum temperature, and hospitals are also significant factors in the spread of dengue fever.

The availability of hospitals specifically equipped for dealing with dengue disease is a concern. People from remote areas in Sindh, Punjab, and Khyber Pakhtunkhwa usually must travel to big cities to be treated for this disease. The dengue virus inflicts additional stress on the existing healthcare system in specific seasons (anomalies such as higher than average rainfall, lower than average maximum temperatures, etc.). Therefore, it is necessary to provide mobile health facilities in remote areas.

Figures 4 and 5 illustrate the elevation map population densities in Pakistan. A high density of population lives in the lower elevation regions in the north-eastern region. Studies have found that a high risk of dengue incidence is associated with the population density (but not in all cases because the dengue virus is noncontagious), urbanisation, and the climate [ 41 , 42 ].

Elevation map of Pakistan

Population spread across Pakistan

We observed that numerous cases have arisen in cities with larger populations. The spread of dengue fever is attributed to several factors. Rainfall, average maximum temperature, and hospitals play a significant role in the prevalence of this disease, which was confirmed using GLM analysis. Figures 6 and 7 illustrate the annual average maximum and minimum temperatures in our study area.

Annual average maximum temperature

Annual average minimum temperature

We observed that southeast Pakistan is warmer compared to the northern and north-western regions of Pakistan and that temperature plays a key role in the spread of dengue fever because suitable temperatures for breeding larvae with the dengue virus are around 30°C. The southern cities of the provinces have the highest average minimum temperature, making these regions more vulnerable in the rainfall season, although the cycle of Aedes Aegypti is short-lived.

In Fig. 8 , the number of cases and amount of rainfall are displayed. However, this does not conclusively (for all regions simultaneously) indicate that rainfall is the only factor causing the hike in dengue cases because some regions (in our study area) received more rainfall in the monsoon season than other regions in the same period. Our findings suggest that dengue cases tend to increase in erratic and increased rainfall seasons, along with other significant factors associated with the dengue virus.

Dengue incidences and precipitation pattern

In Table 1 , an increase in the number of dengue cases occurred after an increase in rainfall. The historical annual average precipitation for the 41 cities is 424 mm. In the years 2010 and 2011, an accumulative increase of 54.38% in precipitation was recorded, compared to the historical average rainfall in this study, which was also the cause of major flooding across the country. Furthermore, in 2010, 2011, and 2013, significantly large numbers of dengue cases occurred. A decrease of more than 9% in the annual average rainfall in the study area occurred from 2006 to 2017; however, the provinces of Khyber Pakhtunkhwa and Sindh recorded heavier than average monsoon rains that killed or displaced hundreds of people in these two regions due to flooding. The excessive water in these regions is considered one reason for the numerous dengue fever cases. Other potential factors can be studied for a possible explanation of the spread of dengue from hot and humid locations (Sindh) to cold and mild locations (Khyber Pakhtunkhwa). Studies have shown that, regardless of dengue fever being directly noncontagious, it can spread from viraemic subjects from one place to another through infection by mosquitos [ 13 , 16 ].

The variables included in the dengue study are rainfall, maximum temperature, minimum temperature, elevation, sanitation, population density, hospitals, and literacy. These variables were analysed using GLM to search for significant factors. The model is stated as follows:

where y is the number of dengue cases, and the GLM estimates are given in Table 2 . A more detailed study can be found in [ 43 ].

Conclusions

This study found that Sindh and Khyber Pakhtunkhwa are two main vulnerable areas for the spread of dengue fever. Punjab experienced the worst spread in 2011. Multiple factors are responsible for the spread and prevalence of dengue fever. Climate factors, such as rainfall and average maximum temperatures, play a significant role along with hospitals. The lack of proper hospital units is a highly significant factor in the spread of dengue fever. Areas most affected in Pakistan include areas that have large populations and higher population densities. The sanitation situation must be improved. Furthermore, awareness programmes are needed to help understand the dengue epidemic in remote and less developed regions of metropolitans. Preventive measures are needed that can be undertaken by the local governments in monsoon and rainy seasons to eradicate the breeding grounds for Aedes Aegypti larvae.

This manuscript has not been submitted in any other publishing source.

Availability of data and materials

All the data and material for this study are included in the manuscript, and additional data are provided in the supplementary material.

Abbreviations

Geographical information systems

Generalised linear model

Non-governmental organisations

National Oceanic and Atmospheric Agency

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This study was funded by the Institute of Statistics Klagenfurt, Alpen-Adria University of Klagenfurt, Austria and Higher Education Commission of Pakistan. There was no role of funding partners in the study design, interpretation, or conclusions.

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Shabbir, W., Pilz, J. & Naeem, A. A spatial-temporal study for the spread of dengue depending on climate factors in Pakistan (2006–2017). BMC Public Health 20 , 995 (2020). https://doi.org/10.1186/s12889-020-08846-8

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Epidemiological study of dengue fever in District Swabi, Khyber Pakhtunkhwa, Pakistan

Estudo epidemiológico da dengue no distrito swabi, khyber pakhtunkhwa, paquistão.

Dengue is a viral disease which is serious health concern from last few decades and the infection transmitted through mosquito bite into human. This study was conducted to carry out prevalence of dengue fever in District Swabi. A total of 196 blood sample were collected from patients with age ranges (0-80 years) having dengue fever on the basis of physical symptoms from Bacha Khan Medical Complex Swabi during August to October 2017. Serological test were performed for detection of IgM, IgG and NS1 (Non structural protein antigen of virus) against dengue. Out of total 196 confirmed dengue cases the most prone gender was male 123(62%) while 73(38%) were female. Among the age groups; 21-30 years group 62 (31.6%) was found the most predominated age group. The higly affected areas in district Swabi were Topi (40.8%) followed by Main Swabi (27%), Maneri (8.2%), Marghuz (6%), Shawa Ada (5.1%), Shah Mansoor (5.1%), Gohati (4.1%), and Chota Lahore (3.6%). Therefore, the health department should take actions by educating the public about basic cleanliness of the environment. The community should be encouraged to participate in the control of such vector based diseases/infections.

Keywords: dengue fever; prevalence; NS1; serological test

A dengue é uma doença viral que é um sério problema de saúde das últimas décadas e a infecção transmitida através da picada de mosquito em humanos. Este estudo foi realizado para realizar a prevalência da dengue no distrito de Swabi. Foram coletadas 196 amostras de sangue de pacientes com faixa etária (0 a 80 anos) com dengue com base nos sintomas físicos do Complexo Médico Bacha Khan de Swabi, no período de agosto a outubro de 2017. Foram realizados testes sorológicos para detecção de IgM, IgG e NS1 (antígeno proteico não estrutural do vírus) contra a dengue. Do total de 196 casos confirmados de dengue, o sexo mais propenso foi o masculino 123 (62%), enquanto 73 (38%) eram do sexo feminino. Entre as faixas etárias; A faixa etária de 21 a 30 anos 62 (31,6%) foi a faixa etária mais predominante. As áreas altamente afetadas no distrito de Swabi foram Topi (40,8%), seguidas por Main Swabi (27%), Maneri (8,2%), Marghuz (6%), Shawa Ada (5,1%), Shah Mansoor (5,1%), Gohati (4,1%) e Chota Lahore (3,6%). Portanto, o departamento de saúde deve tomar ações educando o público sobre a limpeza básica do meio ambiente. A comunidade deve ser incentivada a participar do controle de tais doenças / infecções baseadas em vetores.

Palavras-chave: dengue; prevalência; NS1; teste sorológico

1. Introduction

Dengue is a viral disease spread through mosquito bite into human. It may be caused by any of four serotypes of dengue virus (DEN1, DEN2, DEN3, DEN4) belonging to the genus Flavi virus which are RNA viruses transmitted to human by Aedes aegypti ( Munir et al., 2014 MUNIR, M.A., ALAM, S.E., KHAN, Z.U., SAEED, Q., ARIF, A., IQBAL, R. and QURESHI, H., 2014. Dengue fever in patients admitted in tertiary care hospitals in Pakistan. Journal of the Pakistan Medical Association, vol. 64, no. 5, pp. 553‐559. PMID: 25272543. ; Khanani et al., 2011 KHANANI, M.R., ARIF, A. and SHAIKH, R., 2011. Dengue in Pakistan: journey from a disease free to a hyper endemic nation. Journal of the Dow University of Health Sciences Karachi, vol. 5, no. 3, pp. 81-94. ). Environmental changes such as climate and weather can affect the dengue virus in which temperature is the most important climatic factor, strongly affects the survival of dengue virus. Dengue Fever appears as a febrile serious illness and presents an ample clinical condition varying from oligo-symptomatic forms to several clinical cases with bleeding and shock, which can leads to death ( Ebi and Nealon, 2016 EBI, K.L. and NEALON, J., 2016. Dengue in a changing climate. Environmental Research, vol. 151, pp. 115-123. http://dx.doi.org/10.1016/j.envres.2016.07.026. PMid:27475051. http://dx.doi.org/10.1016/j.envres.2016.... ; Rocha and Tauil, 2009 ROCHA, L.A. and TAUIL, P.L., 2009. Dengue em criança: aspectos clínicos e epidemiológicos, Manaus, Estado do Amazonas, no período de 2006 e 2007. Revista da Sociedade Brasileira de Medicina Tropical, vol. 42, no. 1, pp. 18-22. http://dx.doi.org/10.1590/S0037-86822009000100005. PMid:19287930. http://dx.doi.org/10.1590/S0037-86822009... ).

The Dengue infection was spread epidemically to south, Central and North America, Africa, China and Australia in 1980, and was expected to continue in well exposed region containing Aedes aegypti ( Monath, 1994 MONATH, T.P., 1994. Dengue: the risk to developed and developing countries. Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 7, pp. 2395-2400. http://dx.doi.org/10.1073/pnas.91.7.2395. PMid:8146129. http://dx.doi.org/10.1073/pnas.91.7.2395... ). In the South East Asia region, the dengue cases are reported in many countries including India, Sri Lanka and Thailand ( Garg et al., 2011 GARG, A., GARG, J., RAO, Y. K., UPADHYAY, G.C. and SAKHUJA, S., 2011. Prevalence of dengue among clinically suspected febrile episodes at a teaching hospital in North India. Journal of Infectious Diseases and Immunity, vol. 3, no. 5, pp. 85-89. ). In the year of 2012, 44,456 cases were registered in Sri Lanka while 10,000 cases were registered in the city of Colombo ( Ocwieja et al., 2014 OCWIEJA, K.E., SUNDARARAMAN, S.A., FERNANDO, A.N., DE SILVA, A.D., KRISHNANANTHASIVAM, S., SHERRILL-MIX, S., TENNEKOON, R.N., PREMAWANSA, G., TIPPALAGAMA, R. and PREMAWANSA, S., 2014. Phylogeography and Molecular epidemiology of an epidemic strain of dengue virus type 1 in Sri Lanka. The American Journal of Tropical Medicine and Hygiene, vol. 91, no. 2, pp. 225-234. http://dx.doi.org/10.4269/ajtmh.13-0523. PMid:24799375. http://dx.doi.org/10.4269/ajtmh.13-0523... ). In the year of 2000 and 2012, 5000 people were affected and 93 deaths and in year 2002 there were 6104 cases with 58 deaths were registered in Bangladesh ( Rahman et al., 2002 RAHMAN, M., RAHMAN, K., SIDDQUE, A.K., SHOMA, S., KAMAL, A.H., ALI, K.S., NISALUK, A. and BREIMAN, R.F., 2002. First outbreak of denguehemorrhagic fever, Bangladesh. Emerging Infectious Diseases, vol. 8, no. 7, pp. 738-740. http://dx.doi.org/10.3201/eid0807.010398. PMid:12095447. http://dx.doi.org/10.3201/eid0807.010398... ).

Dengue viral disease has caused many outbreaks in Pakistan in 1994 to 2011.In Pakistan Dengue fever first time reported in 1982 in which out of 174 patients, 12 were the affected patients ( Atif et al., 2016 ATIF, M., RAHEEL, U., ALAM, F., ARSHAD, H.U., BALOCH, F. H., IMRAN, M., ZAIDI, N. S. S. and WAQAR, A. B., 2016. Serotyping of dengue virus from deadly outbreaks of Pakistan. Journal of Human Virology & Retro-virology, vol. 3, no. 3, pp. 00092. http://dx.doi.org/10.15406/jhvrv.2016.03.00092. http://dx.doi.org/... ). The symptoms of dengue fever first time seen in 1994 in Karachi, while in Khyber Pakhtunkhwa the dengue fever case was initially registered in swat in August 2013, Dengue infection spread from one place to another through travellers. According to 2013 data, Khyber Pakhtunkhwa was on the top of dengue infected people, 3177 cases were registered ( Haider and Iqbal, 2016 HAIDER, N. and IQBAL, A., 2016. Dengue prevalence and diagnosis in Pakistan. International Journal of TROPICAL DISEASE & Health, vol. 19, no. 2, pp. 1-14. ). In Swat from August 2013 to November 2016, and 5569 patients were affected from dengue fever in which 37 patients were died ( Khan et al., 2017 KHAN, W., KHAN, B.A., KHAN, Z., REHMAN, A., AKBAR, M. and KHAN, I.A., 2017. Dengue fever; the clinical pattern and mortality in epidemic and post epidemic years in Swat. The Professional Medical Journal, vol. 24, no. 10, pp. 1466-1470. http://dx.doi.org/10.17957/TPMJ/17.3947. http://dx.doi.org/10.17957/TPMJ/17.3947... ).

During 2013 to 2015 individuals aged 16-30 year of age were the main victims of Dengue fever infection, followed by individuals between 31-45 year of age. The infection rate in males was double as compared to female, with a male to female ratio of 2:1, an observation that corresponds with previous results from studies of the Khyber Paktunkhwa province ( Suleman et al., 2016 SULEMAN, M., FARYAL, R., ALAM, M. M., SHARIF, S., SHAUKAT, S., KHURSHID, A., ANGEZ, M., UMAIR, M. and S. Z. Z. SYED, 2016. Identification of concurrent infection by multiple dengue virus serotypes during an epidemic in 2011 in Pakistan. Journal Microbiology & Experimentation, vol. 3, no. 3, pp. 00088. http://dx.doi.org/10.15406/jmen.2016.03.00088. http://dx.doi.org/10.15406/jmen.2016.03.... ). This epidemic disease transferred from Swat to nearby areas including the Malakand, Kohat, Mansehra districts, lower and upper Dir, Peshawar ( Suleman et al., 2017 SULEMAN, M., FARYAL, R., ALAM, M.M., SHARIF, S., SHAUKAT, S., AAMIR, U.B., KHURSHID, A., ANGEZ, M., UMAIR, M., SUFIAN, M.M., ARSHAD, Y. and ZAIDI, S.S., 2017. Dengue virus serotypes circulating in Khyber Pakhtunkhwa Province, Pakistan, 2013-2015. Annals of Laboratory Medicine, vol. 37, no. 2, pp. 151-154. http://dx.doi.org/10.3343/alm.2017.37.2.151. PMid:28029002. http://dx.doi.org/10.3343/alm.2017.37.2.... ) and then other districts like Mardan, Nowshera and Swabi. In Peshawar 11,685 infected people’s cases were registered till to 7 November 2017 ( Gubler, 1998 GUBLER, D.J., 1998. The global pandemic of dengue/dengue haemorrhagic fever: current status and prospects for the future. Annals of the Academy of Medicine, vol. 27, no. 2, pp. 227-234. PMid:9663316. ) and 7 deaths were recorded till to 22 August according to the Dawn News. In Mardan total number of dengue patients 12 till to 25 August 2017 ( Hasan Khan et al., 2013 HASAN KHAN, M.I., ANWAR, E., AGHA, A., SALEH, N., ULLAH, E., SYED, I.A. and RAJA, A., 2013. Factors predicting severe dengue in patients with dengue Fever. Mediterranean Journal of Hematology and Infectious Diseases, vol. 5, no. 1, pp. e2013014. http://dx.doi.org/10.4084/mjhid.2013.014. PMid:23505602. http://dx.doi.org/10.4084/mjhid.2013.014... ). In Nowshera 18 cases were reported till to 22 August 2017 ( Shahid, 2017 SHAHID, S., 2017 [viewed 8 November 2018]. Uncontrollable dengue continues to test mettle of Peshawar health officials [online]. Lahore: PakistanToday. Available from: https://www.pakistantoday.com.pk/2017/10/07/uncontrollable-dengue-continues-to-test-mettle-of-peshawar-health-officials/ https://www.pakistantoday.com.pk/2017/10... ).

Keeping in view the current scenario of dengue fever in Khyber Pakhtunkhwa this study was conducted to find out average prevalence in different areas of Swabi and the causing factors of dengue infection.

2. Methods and Materials

2.1. study design.

Proper consent was taken before conducting this study from authorities and patients enrolled for this study, data from patients were collected through questionnaire. A total of 196 blood samples were collected from suspected dengue fever patients from Bacha Khan Medical Complex Swabi from August to October 2017, to check the prevalence of dengue fever in Swabi on the basis of serological test.

2.2. Identification of dengue

For Identification of Dengue virus STANDARD Q Dengue Duo test (SD Biosensor, Republic of Korea) was used, which is an immune-chromato-graphic assay for the detection of NS1 antigen and Dengue virus-specific IgM and IgG antibodies in human serum, plasma and whole blood. By detecting the NS1 antigen, not only the initial infection was detected, but also Dengue virus-specific IgM and IgG were detected at the same time. Screening test results were obtained within 15 minutes with high sensitivity and specificity. All the suspected blood samples were collected in 2 mL sterile Eppendorf tubes for the dengue identification. The entire sample tubes were carefully transferred to the centrifuge and centrifuged for 1 minute. For NS1Antigen rapid test, 100µl of the test serum was put on the NS1 rapid test strip and 1 drop of NS1 buffer was added, after 15 minutes the red colour of the test line was considered as positive. For IgM, IgG Antibody test, 100µl of the test serum was put on IgM, IgGAntibody rapid test strip and 2 drops of IgM, IgG buffer were added, after 15 minutes the red colour of the test line was considered as positive (As per manufacturer protocol CAT No: 09DEN30A 09DEN30A)

Data analysis: Data was analysed on Microsoft excel version 2010 and data was presented in number and percentages (n %). Chi- Square (χ 2 ) and Kruskal Wallis test p-value was applied.

Out of confirmed 196 dengue cases, 123 (62.8%) were male and 73 (37.2%) were female. The highly affected age group was 21-30 years, 62(31.6%) followed age group11-20years, 28(14.3%), 31-40 years, 27 (13.8%), 41-50 years, 26(13.3%), 51-60 years 20 (10.2%), 71-80 years, 15 (7.7%), 0-10 years and 61-70 years, 9(4.6%). The highly affected area in District Swabi was Topi 80 (40.8%) followed by Swabi 53 (27.0%), Maneri 16(8.2%), Marghuz 12(6.1%), Shawa Adda and Shah Mansoor 10 (5.1%), Gohati 8(4.1%) and Chota Lahor 7(3.6%) as shown in ( Table 1 )

4. Discussion

The data obtained in this study showed that Dengue fever in 2017 was highly prevalent in district Swabi. This study showed that the arboviral pathogen is affecting both rural and urban areas in the world ( Suleman et al., 2017 SULEMAN, M., FARYAL, R., ALAM, M.M., SHARIF, S., SHAUKAT, S., AAMIR, U.B., KHURSHID, A., ANGEZ, M., UMAIR, M., SUFIAN, M.M., ARSHAD, Y. and ZAIDI, S.S., 2017. Dengue virus serotypes circulating in Khyber Pakhtunkhwa Province, Pakistan, 2013-2015. Annals of Laboratory Medicine, vol. 37, no. 2, pp. 151-154. http://dx.doi.org/10.3343/alm.2017.37.2.151. PMid:28029002. http://dx.doi.org/10.3343/alm.2017.37.2.... ). The total population of district Swabi is 1,624,616 according to city population and the dengue fever affected patient ratio is 0.012%. The current study showed that the percentage of male (62.8%) is higher than female (37.2%). Similar study was conducted in district Mardan 2011, the male patient were 13 (52%) and female were 12 (48%) ( Shahid, 2017 SHAHID, S., 2017 [viewed 8 November 2018]. Uncontrollable dengue continues to test mettle of Peshawar health officials [online]. Lahore: PakistanToday. Available from: https://www.pakistantoday.com.pk/2017/10/07/uncontrollable-dengue-continues-to-test-mettle-of-peshawar-health-officials/ https://www.pakistantoday.com.pk/2017/10... ). Another similar study was conducted in district Nowshera, in which affected male percentage was recorded high 16 (77%) whereas female were 5 (23%) in 2011 ( TNS World, 2017 TIMES INTERNATIONAL NEWS SERVICE – TNS WORLD, 2017. [viewed 8 November 2018]. Dengue tally in Mardan reaches 12 [online]. Islamabad: TNS. Available from: https://tns.world/dengue-tally-in-mardan-reaches-12/ https://tns.world/dengue-tally-in-mardan... ; Dawn Today’s Paper, 2017). Similar study was conducted in Swat in August 2013 to November 2016, 5569 patients were affected by dengue fever in which out of 5569 patients, 3834 (68.85%) were male and 1735 (31.15%) were female ( WHO, 2015 WORLD HEALTH ORGANIZATION – WHO, 2015. Dengue and severe dengue. Geneva: WHO. Fact sheet, No. 117. ), which is similar to the findings of current study. Male mobility rate is higher than the female mobility rate. Because in Pakistan most of the females spend their time in homes whereas male do their jobs and travel from place to place to fulfil their needs. In the current study the highly affected age groups were 21-30 years, 62 (31.6%) and age group 11-20 years, 28 (14.3%). Similar study was conducted in the years of 2013, 2015 and 2016 where age group 16-30 years was found the most predominated age group ( Suleman et al., 2017 SULEMAN, M., FARYAL, R., ALAM, M.M., SHARIF, S., SHAUKAT, S., AAMIR, U.B., KHURSHID, A., ANGEZ, M., UMAIR, M., SUFIAN, M.M., ARSHAD, Y. and ZAIDI, S.S., 2017. Dengue virus serotypes circulating in Khyber Pakhtunkhwa Province, Pakistan, 2013-2015. Annals of Laboratory Medicine, vol. 37, no. 2, pp. 151-154. http://dx.doi.org/10.3343/alm.2017.37.2.151. PMid:28029002. http://dx.doi.org/10.3343/alm.2017.37.2.... ). The occurrence of dengue fever in the highly affected age group is due to the involvement of individual in activities outside their residences especially in morning and evening. In the present study, the high occurrence of dengue fever was recorded in Topi 80 (40.8%) and Swabi 53 (27.0%). In these areas, the poor sanitation system, poor water supply and drainage, inappropriate clean water storage system in living areas, improper collection and disposal of wastes contribute in the breeding of vector mosquito ( WHO, 2015 WORLD HEALTH ORGANIZATION – WHO, 2015. Dengue and severe dengue. Geneva: WHO. Fact sheet, No. 117. ).

5. Conclusion

In this study the prevalence of dengue fever was found more in male than female. The most predominated age group was 21-30 years. Furthermore, the highly affected area in district Swabi was found Topi. Therefore, the health department should take actions by educating the public about basic cleanliness of the environment. The community should be encouraged to participate in the control of such vector based diseases/infections.

6. Disclaimer

This manuscript has been prepared from BS Thesis and the abstract is accepted in International conference on Microbiology and Molecular Genetics (MMG2018) organised by University of the Punjab, Lahore Department of Microbiology and Molecular Genetics.

Acknowledgements

Bacha Khan Medical Complex Swabi for blood sampling. Department of Microbiology, University of Swabi, for providing lab Facility for this Study.

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Publication Dates

• Publication in this collection 20 July 2020
• Date of issue Mar-May 2021
• Received 08 Nov 2018
• Accepted 12 Nov 2019

• http://orcid.org/0000-0002-2633-6018
• * e-mail: [email protected] ; [email protected]

SCIMAGO INSTITUTIONS RANKINGS

Table 1   distribution of confirmed dengue virus cases gender, age and area wise..

• χ 2 -p Value and also kruskal wallis test p-value is same 0.000 which is highly significantly associated with each other.

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Original research article, a cross-sectional study to assess the epidemiological situation and associated risk factors of dengue fever; knowledge, attitudes, and practices about dengue prevention in khyber pakhtunkhwa province, pakistan.

• 1 Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, China
• 2 Key Laboratory of Tropical Disease Control of the Ministry of Education, Sun Yat-sen University-Michigan State University Joint Center of Vector Control for Tropical Disease, Zhongshan School of Medicine, Guangzhou, China
• 3 Chinese Atomic Energy Agency Center of Excellence on Nuclear Technology Applications for Insect Control, Sun Yat-sen University, Guangzhou, China
• 4 Department of Zoology, Abdul Wali Khan University Mardan, Mardan, Pakistan
• 5 Pakistan Bureau of Statistics, Islamabad, Pakistan
• 6 Department of Global Health, Research School of Population Health, College of Health and Medicine, Australian National University, Canberra, ACT, Australia
• 7 Royal Centre for Disease Control, Ministry of Health, Thimphu, Bhutan
• 8 Guangzhou SYSU Nuclear and Insect Biotechnology Co., Ltd., Guangzhou, China
• 9 Medical Unit, Khyber Teaching Hospital Peshawar, Peshawar, Pakistan
• 10 Department of Pharmacy, Abdul Wali Khan University Mardan, Mardan, Pakistan

Background: Dengue fever has been responsible for around 12 countrywide large outbreaks in Pakistan, resulting in 286,262 morbidities and 1,108 deaths. Khyber Pakhtunkhwa (KP) is the most recently impacted province. This study aimed to investigate the molecular, epidemiological, and potential elements that contribute to increasing dengue transmission patterns, and knowledge, attitude, and practice (KAP) toward dengue in KP province.

Method: This cross-sectional community-based study was conducted (June-December, 2021) in two phases. Phase I involved the epidemiological ( n = 5,242) and molecular analysis of DENV in 500 randomly collected blood samples of the 2021 dengue outbreak in KP. Phase II focused on assessing dengue-KAP levels in healthy communities ( n = 14,745, aged > 18 years), adopting a cross-sectional clustered multistage sampling in eight districts (dengue-hotspot vs. non-hotspot) of KP. Chi-square tests and logistic regression analysis were applied.

Results: Peshawar district had the highest dengue cases (60.0%) associated with the predominant co-circulation of DENV-2 (45.8%) and DENV-3 (50.4%) serotypes. A rise in cases was reported in October (41.8%) followed by September (27.9%) and August (14.4%; p < 0.001). Males (63.7%, p < 0.001) and individuals aged 16–30 years (37.0%, p < 0.001) were highly affected. General workers (18.0%), families with a monthly income of 10,000–20,000 Pak rupees (50.5%), unmarried (71.0%), uneducated (31%), families with higher human density (>10 individuals per household), and those (29.0%) who faced power outages for more than 7/24 h were the most affected. Moreover, co-morbidities like renal failure and bronchial asthma were associated with disease severity. A community survey on KAP revealed that an average of 74, 60, and 43% of the participants demonstrated good knowledge, attitudes, and dengue preventive practices, respectively.

Conclusion: Multiple poor socioeconomic elements are influencing dengue fever transmission in the province. Higher KAP levels may explain the low frequency of dengue in non-hotspot districts. Our study emphasizes the need for effective and long-term public health education, strengthened vector surveillance, and expanded laboratory capacity for better diagnosis and management of dengue cases to better predict the burden and seasonality of disease in the country.

Introduction

Dengue fever (DF) is a vector-borne disease caused by one or more serotypes of dengue virus (DENV). Four DENV serotypes (DENV1-4) are currently identified to cause dengue in humans. Transmission occurs through the bites of Aedes aegypti and Ae. albopictus , a daytime biting mosquito species that reproduce in a variety of water-holding containers (both natural and manmade) and environments (rural, urban, and semi-urban) ( 1 , 2 ).

Dengue has been constantly expanding (30-times increase over the past 50 years) to new areas and resurging in parts where it had recently been controlled ( 1 ). At present, dengue is widespread in over 129 countries and cases are rising constantly over the course of time: 0.51 million in 2000, 2.4 million in 2010, and 4.2 million in 2019. Asia represents about 70% of the world dengue disease burden ( 2 ). In particular, countries in the world health organization South-East Asia Region (WHO-SEAR) are severely affected with an estimated 1.3 billion people at risk, accounting for almost 52% of the world population at risk of contracting dengue virus ( 3 ). Dengue has significant negative financial and sociological consequences with a potential to considerably impede the development of economies, politics, and society ( 4 ).

Globally, transmission of dengue has been linked to a variety of social factors, including education level, household characteristics, overcrowding, water supply (i.e., poor sanitation and water-storing practices), electricity availability, vegetation cover, human behavior, and the abundance of Aedes mosquitoes ( 5 , 6 ). To achieve effective disease control, communities should be empowered with right knowledge on dengue preventive strategies because human behaviors play a key role in facilitating dengue vectors (providing a favorable environment for breeding and blood meals) and disease transmission ( 5 ). Communities with higher socioeconomic status (SES) and a better understanding of dengue (in relation to knowledge, attitude, and prevention practices) have resulted in more successful disease control ( 5 , 7 ). For example, in the Malaysian state of Selangor, human behavior has a significant impact on the spread and transmission of dengue ( 5 , 7 ).

Dengue in Pakistan is also spreading at an alarming rate due to the wide range dispersion and adaptation of Ae . aegypti and Ae. albopictus ( 1 ). Dengue epidemics have been observed on a cyclical (2-to 3-year) basis, with an 8-fold increase in cases over the last decade. For example, a severe first dengue outbreak hit Peshawar (the country's third most populated city in KP) in 2017 that resulted in 24,938 cases and 70 deaths ( 8 ), followed by a second outbreak in 2021 that claimed over 10,000 cases and 10 deaths ( 9 ).

The public health intervention strategy for dengue relies heavily on massive insecticide spray in emergency and outbreak scenarios in Pakistan ( 10 ). A limited vector surveillance is also conducted including ovitraps, immature sampling for larva/pupae, and adult traps in various dengue prone districts ( 11 , 12 ). Recently, an android based application named “Mosquito Alert Pakistan (MAP)” has been launched in Pakistan by the National Institute of Health (NIH), Islamabad. The application provides an early warning system for the risk of dengue transmission and other mosquito-borne diseases ( 13 ). Other control measures such as integrated vector management (IVM), with emphasis on habitat management, disposal of discarded tires, urban trash, and community awareness has been worked out very recently ( 14 ).

Previous studies have primarily focused on the epidemiology of dengue in the Peshawar district ( 8 , 15 ). This is the first study to investigate the potential elements that contribute to increasing dengue transmission patterns and to assess the KAP on dengue in the KP province. Consequently, comprehensive epidemiological and molecular studies were carried out during the dengue outbreak to determine: (i) socio-demographic and clinical determinants of dengue fever; (ii) molecular analysis of DENV circulating; (iii) other societal variables like living standards, household type, power outages, impact of water storing practices, etc. that could be risk factors for dengue transmission; and (v) knowledge, attitude, and practice (KAP) about dengue prevention among general communities in dengue-hotspot and non-hotspot districts across the province. These findings will eventually provide a conceptual framework for building evidence-based, community-friendly, and long-term dengue preventive measures in Pakistan and elsewhere.

Methodology

Study settings.

KP: 34.9526°N, 72.3311°E, formerly known as the North-West Frontier Province (NWFP), is the country's third-largest province by population and economy ( Figure 1 ). It comprises of 17.9% (35.53 million) of Pakistan's overall population (2017 census) ( 16 ). Dengue transmission has increased in the province due to a variety of climatic settings, multiple tourist sites, rising urbanization, and increased travel and trade ( 17 ). Peshawar, the largest metropolitan city in KP with a population density of 1,612.5 per sq.km, has reported two massive dengue outbreaks in recent years (2017 and 2021). Peshawar is regarded as a hotspot for disease transmission ( 18 ). No dengue outbreaks had previously been documented in the other districts of the province except Swat, which observed an outbreak in 2013. KP can be divided into two zones: a dengue-endemic zone with only one district (Peshawar) and a non-endemic zone with seven districts (Mardan, Haripur, Nowshera, Swabi, Buner, Khyber, and Mansehra) ( Figure 1 ). Thus, Peshawar is used as a reference for the rest (seven) of the surveyed districts according to set criteria ( 7 ).

Figure 1 . Map of Khyber Pakhtunkhwa province.

Study design

This cross-sectional community-based study took place during June-December, 2021 (dengue season) in two phases (independently) in dengue-hotspot and non-hotspot districts of KP province (mentioned above; Figure 1 ). The molecular (analytical), clinical, and epidemiological investigation of dengue patients (admitted in the dengue specified district headquarter hospital; DHQ) in each district throughout the outbreak was the focus of Phase I. Whereas, Phase II evaluated KAP on dengue among healthy communities, adopting a cross-sectional clustered multistage sampling in these eight districts. This study followed the STROBE principles for cross-sectional epidemiological studies ( 19 ) in terms of design, setting, analysis, and reporting.

Sampling and sample size

In phase I, non-structural protein (NS1) or immunoglobulin IgG/IgM positive (active) patients across the province (having WHO defined dengue symptoms of dengue) ( 20 ) were considered for random blood sampling (4 ml of blood in EDTA tubes) during the initial days (0–5) of the disease ( 21 ) to isolate and characterize the DENV. The blood samples were immediately shifted to the dengue diagnostic laboratory in Peshawar and processed for further investigations ( 1 ). Following blood sampling, these patients were given a self-administered questionnaire adopted from previous studies ( 1 , 22 ) ( Supplementary Material 1 ) to fill out information about dengue disease clinical symptoms, duration, diagnostic results (i.e., platelet counts, etc.), and travel history to dengue endemic locations in the 5–10 days prior to the onset of symptoms, socioeconomic details like monthly income, household characteristics, power outages, other related information, and demographic details such as age and gender. The asset index developed by ( 23 ) was assumed to measure and classify participants' socioeconomic level (SES).

KAP measurements in phase II

In phase II, we tested the hypothesis that good dengue KAP in healthy communities in non-dengue hotspot districts across the province could be the explanation for low dengue cases. Thus, an additional cross-sectional clustered multistage sampling approach ( Figure 2 ) was undertaken to compare dengue-KAP levels in different communities (in hotspot and non-hotspot districts) and its subsequent impact on disease transmission according to Selvarajoo et al. ( 5 ). A dengue hotspot is defined as an area where a dengue outbreak has lasted longer than 30 days, whereas a non-hotspot is characterized as a place where there has been no dengue epidemic for longer than 30 days ( 7 ). A community's understanding of dengue, including its vectors and symptoms, is referred to as its knowledge. The methods people exhibit their knowledge and attitude via their actions are referred to as practices ( 5 ). For this, a questionnaire ( Supplementary Material 2 ) was designed, in light of the 2009 WHO guidelines on dengue fever, which have been previously verified ( 5 , 7 ). The questionnaire was comprised of two sections: (i) eight questions about knowledge and attitude (KA); and (ii) eight questions about dengue prevention practices (P). The study included participants who were over the age of 18, had lived in the selected district for at least 3 months, and could read and communicate ( 5 , 7 ). Thus, a sample size of 14,745 participants was necessary to meet the study's objectives ( 24 ). Notably, the sample size from each district was based on population size together with the population density of the concerned district. The rationale for a large sample size was justified in order to ensure that enough respondents from across the province (eight districts) were included in the results, allowing the findings to be applied to a wide range of community contexts. Previous studies selected small sample size without taking into consideration the actual target population size. Here, in our study, the larger sample size is based on the previous dengue prevalence rates and the actual human population density in each target district. Therefore, the sample size was not uniform in each target district ( Supplementary Material 3 ). The study participants were reached (weekdays during office hours) and interviews were requested after obtaining the written consent. Individuals who did not answer all of the questions, were unwilling to participate in the interview, or left prior to the interview were excluded. The data was subsequently entered (day wise) in the Microsoft Excel sheets (2010 version) and double-checked and validated for accuracy according to quality control protocols ( 21 ).

Figure 2 . A conceptual framework diagram for a KAP-based (Phase II) study.

Individual characteristics like age, gender, education level, socioeconomic status, and household characteristics, etc., were considered the independent variables in this study, while KAP scores (good vs. bad) and dengue incidence or DENV seropositivity (NS1/IgG) were considered as the dependent variable ( 25 ).

Molecular identification of DENV serotypes

Reverse Transcription Polymerase Chain Reaction (RT-PCR) was used to identify the circulating DENV serotypes in the blood samples taken (randomly) from 500 NS1-positive hospitalized patients with dengue symptoms across the province (each district with 50 samples). The RNA extraction and PCR procedures were followed as described in recently published papers ( 1 , 22 ). RNA was extracted using a Favorgine RNA extraction kit (CAT # FAVNKOO1-2) in line with the manufacturer's instructions. To identify the serotypes, the extracted RNA was processed using dengue virus type specific primers (TS1–TS4, plus D1) ( 26 ), in addition to positive (DENV-1, 2, 3, and 4) and negative controls. The amplified fragments were visualized in 2% agarose gels stained with Gel Red (Biotium Inc., USA).

Statistical analysis and data interpretation/management

For the data (like epidemiological and socio-demographic and other associated risk factors etc.,) collected in Phases-I, we used the Chi-Square test, while for the data (KAP) collected in Phase-II, we adopted univariate and multivariate logistic regression analysis. Odds Ratios (ORs) were computed in the KAP survey to assess the magnitude of association between the outputs of a given category/district with a reference category/district ( 27 ). Given category is also known as the exposed category (non-hot spot area) while the one mentioned in reference category is considered as a control case/category (hot spot area). The statistical significance of the association was assessed using the 95% confidence interval. In this analysis Peshawar is chosen as a reference category due to highest dengue case load (hotspot). OR values less than or equal to one suggested similar attitude of the comparative non hotspot district to hotspot district, while a value >1 suggested that the odds of exposure among non-hot spot districts are greater than the odds of exposure among hot spot district. The predictors of each KAP domain were determined using logistic regression analysis. KAP responses as, “Yes” vs. “No,” were used as the outcome variables in the logistic regressions. Significant predictor factors from univariate analysis ( p ≤ 0.25) were entered into the multivariate analysis. Confounding factors were explored by comparing the difference between the adjusted odds ratio (aOR) in multivariate analyses and the crude odds ratio (OR) in univariate analyses, of a particular predictor variable on the KAP domain. The correlation values among KAP scores and between KAP score and asset index were calculated using Spearman's rank correlation (rs) ( 28 ). SPSS and R softwares were used for the analysis. Ggplot in R was used to obtain boxplot which gave a five-point summary measure of the available data. The summary points are lower and upper quartiles, median, minimum and maximum values.

Ethical considerations

The study and associated protocols were developed in accordance with national ethical legislation and as endorsed by the Ethic Board of the Zoology Faculty, Abdul Wali Khan University. In line with the latest version of the Declaration of Helsinki ( 29 ), all samples were obtained after the participants' written consent.

Socio-demographic determinants of dengue fever

Figure 3 shows the demographic details of the 5,242 dengue patients reported in 2021, including their socioeconomic status (SES) and other associated risk factors. Dengue fever was more common in males (65%) and in people aged 16–30 years (37%) ( p < 0.001). About 69% patients belonged to the general community (with little or no knowledge of dengue). In terms of occupation, general workers (working in various private organizations) had the highest dengue positive rates (18%), followed by the labor community (working on daily pay) (16%) ( p < 0.000). Moreover, the majority (50.5%) of the patients had a monthly income of 10,000–20,000 Pakistan rupees (PKR) ( p < 0.000). Single (unmarried) people had a higher rate of dengue fever (71%) than married people (11%). About 59% of the dengue patients belonged to rural areas. In terms of qualification, the highest frequency was identified in uneducated (31%) and primary-level educated (23%) communities ( p < 0.000). About 29% of dengue fever was observed in areas with >7 h of power outages ( p < 0.000). Surprisingly, families with a higher human density per household and communities living in multi-story houses had higher dengue prevalence rates of 35 and 45%, respectively ( Figure 3 ).

Figure 3 . Socio-demographic determinants and other risk factors for dengue fever in the KP dengue outbreak (2021). Chi-square test was performed; p < 0.05 was considered statistically significant.

Seasonal characteristics of dengue fever

The month-wise hospitalization of dengue patients revealed October with highest hospitalization rates (2,149; 41%) followed by September (1,468; 28%), whereas lowest rates were documented in June (63; 1.2%) and December (252; 4.8%; p < 0.001; Figure 3 ). Overall, the month and age wise data details of dengue occurrence in KP suggested significant association between the dengue occurrence and season (months).

Dengue highly affected districts in KP during 2021

Figure 1 demonstrates the number of dengue cases reported in each district. Among the reported confirmed dengue cases (5,242) and 10 deaths, Peshawar alone faced a load of 3,139 (60) cases, with three deaths only ( p < 0.001). Nowshera and Mardan districts, adjacent to Peshawar, reported 404 (7.7%) and 327 (6.2%) incidences with one death each, respectively. Thus, Peshawar is considered the dengue hot-spot district ( p < 0.001). Districts Khyber (4.2%) and Buner (5%), with one death each, reported a low number of dengue cases ( p < 0.001). Surprisingly, the majority of these patients had visited dengue-endemic sites both within and outside the province (data not shown), showing that positive dengue cases were imported rather than locally acquired, which requires further investigations.

Clinical characteristics of dengue fever

Table 1 shows the clinical characteristics of dengue fever. About 95% of cases were NS1+, and 15% of patients had blood platelets below 20,000. Among the dengue associated symptoms, 100% patients had fever and bone/muscles pain. About 97 and 93% of patients develop headaches and body aches, respectively. Abdominal pain was the second common symptom (84%) while bleeding was reported only in 8% patients. Dengue shock syndrome (DSS; 53.7%) and dengue hemorrhagic fever (DHF; 21%) were reported during the study ( Table 1 ).

Table 1 . Clinical characteristics of dengue fever during 2021.

Distribution of DENV serotypes

Out of the total blood samples tested ( n = 500), only 260 (52%) samples were DENV positive ( Figure 4 ). The dengue infection rates remained higher in district Peshawar (62%), whereas, Nowshera, Haripur, Mansehra, and Khyber had the similar infection rates (56%). Comparatively, the lowest infection rates were observed in districts Shangla (38%) and Kohat (40%). Regarding serotype distribution, DENV-3 (50.4%) and 2 (45.8%) were the predominant serotypes.

Figure 4 . Molecular investigation of DENV among dengue patients across the province.

Socio-demographic characteristics of KAP-study population

In Phase-II, the data was collected from 14,745 healthy participants from different eight districts across the province. Males constituted 88% of the total population, and half of the participants (50%) were 18–30 years old. Almost 29% of respondents had a higher secondary education certificate, and the majority (31%) was entrepreneurs ( Figure 5 ). The majority of the residents (60%) belonged to rural areas, and nearly half of the participants (48%) had a monthly income of 10,000–20,000 Pakistan rupees (PKR). About 60% of the study subjects were married, and only 12% of the respondents had a history of dengue ( Figure 5 ).

Figure 5 . Socio-demographic characteristics of KAP-study participants in Phase II. Values are presented: n (%).

KAP levels among communities

Knowledge about dengue fever.

We developed a series of logistic regression analyses to determine the factors independently associated with knowledge, attitude, and practice score for dengue prevention. Out of seven readily available parameters that had p -values < 0.25 in the univariate analysis, all factors were independently associated with knowledge, attitude and practice score for dengue. The findings showed that the odds of a knowledge score regarding dengue is 1.10 times higher for males as compared to females with (OR = 1.01, p < 0.001; Table 2 ). The odds of a knowledge score were 1.24 times higher in non-hot spot districts than in hot spot districts (OR = 1.24, p < 0.001). Regarding the education status, participants having education of middle and above had an odd knowledge score of 4.71 times higher than those with a lower education (OR = 4.71, p < 0.001). Similarly, the participants living in urban areas had an odd knowledge score that was 2.33 times higher as compared to rural areas (OR = 2.33, p < 0.001) as shown in Table 2 . Similarly, those who had a history of dengue were more (OR = 1.4, p < 0.001) aware of the disease. The knowledge scores for married couples were 1.07 times higher than unmarried individuals (K; OR = 1.07, p < 0.05). However, there was no significant association between KAP, age, and SES.

Table 2 . Predictors of KAP levels (good vs. poor) in univariate and multivariate analysis ( n = 14,745).

Overall, an average of 74% of participants demonstrated good knowledge of dengue and its symptoms ( Supplementary Material 3 ). A district-wide analysis of dengue KAP levels revealed a considerable disparity in responses between communities in various districts ( Supplementary Material 3 , Figures 6A,B ). All these districts were found to have statistically significant positive associations except the case of Peshawar vs. Mansehra ( Supplementary Material 3 ). People in Peshawar, Mansehra, and Haripur districts were more aware of dengue fever, possibly as a result of a previous dengue outbreak in Peshawar and a few dengue cases reported in Mansehra and Haripur during 2004. It was also discovered that residents of district Khyber had a higher risk of exposure (odds for KAP) than residents of Peshawar.

Figure 6. (A) District wise response of communities for questions mentioned in Supplementary Table 1 . The above boxplot revealed significant relationship between the response of KAP for different questions for eight districts considered for study ( p < 0.05). (B) Collective response of communities in the form of Yes and No for all districts to our questionnaires ( Supplementary Table 1 ). Boxplot revealed significant association between collective responses of KAP questionnaire for different questions asked from eight districts considered for study. P -value was statistically significant at 5% level of significance, which was based on Chi Square test of independence.

Attitude toward dengue fever

Regarding the attitude score, the findings revealed that the odds of the attitude score regarding dengue was 2.68 times higher for males as compared to the attitude score regarding dengue in females (OR = 2.68, p < 0.001; Table 2 ). The odds of an attitude score were 0.829 times higher in non-hot spot districts than in hot spot districts (OR = 0.829, p < 0.004). In terms of education, participants having a middle and above had an odd attitude score that was 2.45 times higher than those having a lower middle (OR = 2.45, p < 0.001). Similarly, the participants living in urban areas have an average attitude score that is 1.50 times higher as compared to those in rural areas (OR = 1.50, p < 0.001) as shown in Table 2 . The individuals with previous dengue history showed good attitude score (OR = 1.1, p < 0.001). The odd attitude scores for married subjects were 1.29 times higher than unmarried (OR = 1.29, p < 0.001). Overall, in terms of attitude, about 40% (average) of participants gave an unsatisfactory response ( Supplementary Material 3 ).

Dengue prevention practices

Regarding the practice score, the findings demonstrated that the odds of the prevention practice score were 1.2 times higher for males as compared females (OR = 1.12, p < 0.010; Table 2 ). The odds of a practice score were 0.85 times higher in non-hotspot districts than in hotspot districts (OR = 0.85, p < 0.001). In terms of education, participants having a middle and above had an odd practice score that was 2.28 times higher than those having a lower middle (OR = 2.28, p < 0.001). Similarly, the participants living in urban areas have an odd practice score that is 1.29 times higher as compared to those in rural areas (OR = 1.29, p < 0.001) as shown in Table 2 . Those who had dengue history demonstrated good practices (OR = 1.4, p < 0.001). The married subjects had 1.13 times practice odd practice score as compared to unmarried participants (OR = 1.13, p < 0.001).

Dengue preventative practices were indicated by roughly 43% of the respondents, with an emphasis on avoiding adult mosquito bites. Among the prevention practices, contact administration for fogging (29–68%) and the use of mosquito spray (48–63%) were most preferred strategies ( Supplementary Material 3 , Figures 6A,B ). The widely used larval annihilation procedures include discarding stagnant water and scrub the container (~40%). In terms of opinions on different mosquito protection strategies, the most efficient option were full clothing (~37%) followed by chemical fogging (~25%) ( Supplementary Material 3 ). The common approaches to self-protection were using mosquito repellent (~59%), followed by using mosquito nets (~53%). Interestingly, we observed two new methods, including burning dung cake (fumigation) and killing vector mosquito larvae with hot water (at 90–100°C). In general, our findings demonstrated that adult mosquito control approaches were prioritized over larvae/habitat destruction (source elimination). Finally, a strong correlation coefficient ( r = 0.96) was found between the responses of those districts that had good knowledge and had taken adequate precautions to avoid dengue infection. However, a negative association ( r = −0.287) was found for some districts (particularly Peshawar, Mardan, and Haripur) where people had good knowledge but were severely affected by dengue, possibly due to their failure to adopt the strict dengue prevention strategies.

This is the first study in the province to offer a comprehensive analysis of dengue epidemiology, risk factors, and the dengue-KAP. The current research (during sampling period) has documented a total of 5,242 confirmed dengue cases with 10 deaths across the province during 2021, with Peshawar being the hotspot reporting highest dengue cases (60%; Figure 1 ). Dengue fever is on the rise in the province, affecting people from all walks of life, particularly those with a poor standard of living. However, a substantial association between KAP levels and dengue control was found. Moreover, high education level, gender, marital status, dengue history, and living in the urban areas were all linked to good dengue-KAP ( p < 0.001).

Demographic and seasonal characteristics of dengue fever

Our result of dengue affecting more males than females is in congruent with the results obtained from Ahmad et al. ( 30 ) and other six Asian countries ( 31 ). However, the current finding is in contrast to research in South America that has reported either similar proportions of males and females or a larger ratio of female dengue patients ( 31 ). The higher prevalence of infection in male individuals may reflect their greater tendency to seek medical assistance and visit health facilities, resulting in more reporting, in contrast to females who choose traditional (at home) remedies for treatment ( 32 ). The other reasons might be attributed to a local cultural habit in which males often take off their shirts during the hot summer months and spend the entire night exposed to mosquito bites and disease transmission. Also, males are more exposed to mosquito bites (DENV-infected) during the daylight hours, either at work or on their way to and from work, at school, colleges, and universities ( 30 , 33 , 34 ). Secondly, females have a lower prevalence of dengue because they cover their bodies with full clothing (a cultural trait) and stay at home (with no free movement), limiting their exposure to mosquito bites and subsequent dengue transmission, an observation that agrees with ( 22 , 35 ). The pattern of males being more infected with dengue is consistent across the country over time. For example, comparable outcomes were observed in a study conducted in two Pakistani metropolitan cities, Lahore and Multan ( 36 ). To target preventive strategies to lower the disease burden in the region, more studies are needed to determine the reasons for such sex-specific disparities.

The higher incidence of dengue in the economically productive age group in the current study ( 16 – 45 ) is consistent with other national and South Asian studies ( 1 , 30 , 32 , 37 – 40 ). Contrary to our findings, others ( 22 , 31 ) have reported higher dengue infection rates in the age group below 16 years, while others have reported higher incidence in older age groups ( 41 ). Such difference might be related to different local socio-demographic characteristics and warrants further research.

Our findings of higher dengue incidence in August, September and October might be related to higher temperatures and humidity that favors vector mosquito breeding. Similar finding was reported by ( 1 , 12 , 22 , 32 , 42 ). A severe power outage (particularly in August-October; Figure 3 ) exacerbates the dengue spread scenario by providing opportunities for mosquitoes to stay (on exposed human bodies), bite, and transmit DENV. Also, due to frequent power outages, local residents store water in various containers that serve as larval breeding habitats, resulting in an increase in mosquito population density. This promotes mosquito-human interaction, potentially resulting in DENV transmission, an observation similar to ( 44 , 45 ). These observations are backed up by the fact that locations with > 7/24 h power outages reported maximum (29%) dengue cases ( Figure 3 ). This indicates that energy crises hastened the spread of dengue fever in the region.

Socio-economic status and dengue fever transmission

Individuals with lower or no education and low monthly income had greater dengue occurrences than those with higher education and higher SES ( Figure 3 ), similar to other Malaysian studies ( 13 , 44 – 46 ). Firstly, individuals with a higher education and SES can have easy and frequent access to a variety of dengue-related information, allowing them to be aware of it and stay away from mosquito bites and disease transmission ( 25 , 37 , 47 ). Secondly, they can easily take advantage of all financial options to be safe, whereas a poor person or family cannot. For example, during hot seasons, when mosquito density is higher and human interaction is more likely, individuals with a better SES can stay safe (to avoid DENV infected mosquito bites) in air-conditioned rooms. Thirdly, they use alternative resources such as UPS (uninterrupted power supply) machines and electric generators (frequent power outage is a serious issue in Pakistan as discussed above). Poor families, on the other hand, are more exposed to mosquito bites (and disease transmission) due to lack of these resources, observations in line with ( 1 , 22 ). Moreover, people with low SES and limited knowledge (about dengue) were less likely to take precautionary measures, including using mosquito nets, covering water containers, and changing water containers weekly, in line with others ( 18 , 48 – 50 ). This could further explain the higher prevalence (59%) of dengue in rural areas (with limited resources) as compared to urban areas (49%; Figure 3 ). Likewise, residents of multi-story buildings and families with higher human densities were more vulnerable to dengue infection. This may suggest that vector-to-host ratios can explain epidemics in a given location, similar to studies ( 1 , 22 ). Regarding employment, a large number of people infected with dengue belonged to education departments (513; 9.8%) and police department ( n = 351; 6.7%; Figure 3 ). It's possible that these employees are more exposed to mosquito bites (infected with DENV) during work hours because they're in a crowded setting (as usually) in the workplace, which facilitates human-mosquito interactions and, subsequently, disease transmission, an observation in agreement with others ( 1 , 22 , 30 ).

Household characteristics and dengue occurrence

Families with low human population densities (2–4 individuals per household) had a low dengue prevalence rate (17%) compared to higher densities (>10 individuals per household) which had a 35% prevalence rate ( Figure 3 ). A household with more individuals offers more opportunities for female mosquitoes to have regular/frequent human-contacts, increasing the risk of virus transmission. Our hypothesis is supported by previous national and international studies ( 1 , 12 , 22 , 47 , 51 ). Interestingly, we noted higher dengue prevalence (71%) in unmarried (single) individuals than in married people (11%). This finding is in concordance with that of a Singapore study that linked living alone to a higher risk of dengue fever ( 52 ). This could be owing to a greater sense of obligation in married couples for their families than in single individuals. For example, married couples are more likely to use resources to provide a comfortable and safe environment (free of Aedes habitats) for their children at home and in the surroundings ( 50 ).

Clinical symptoms and disease severity of dengue fever

WHO-defined clinical symptoms of dengue act as a significant tool in diagnosing and managing dengue fever ( 1 ). Rapid diagnosis of severe cases and effective clinical care are the mainstays of avoiding dengue-related case mortality ( 3 ). In our study, fever and bone/muscle pain was present in 100% of patients followed by headache (97%) and body aches (93%), with abdominal pain in 84% of patients and bleeding in only 8% of them ( Table 1 ). Such milder symptoms are common for dengue infections across other countries in the Southeast Asia region (reviewed in Tsheten et al.) ( 3 ). Taken together, there is variation across studies regarding the severity of dengue. Vomiting and dehydration, as well as haematocrit with concurrent reduction in platelet count, were the most common (warning indicators) reasons for hospitalization in our study, which is consistent with studies from India ( 53 ), Thailand ( 54 , 55 ), Bangladesh ( 56 ), and others ( 57 ). Here, severe dengue and case fatalities was associated with reduced platelet count, which is also reported in other studies ( 57 – 60 ). In our study, pulmonary infection, renal failure, and secondary infections were also associated with DHF and DSS, consistent with those of a study ( 3 ) that examined data from countries in the WHO-SEA region. This suggests that patients with renal and pulmonary infections should be given extra care in detecting the severity of their illness and receiving timely treatment. These characteristics, however, must be interpreted in conjunction with other lab tests (both recent and past). Furthermore, severe dengue was found to be a significant cause of morbidity and mortality in the country's older population in our study, in contrast to studies that found DHF and DSS to be a significant cause of hospitalization and death in children from Southeast Asia ( 61 ) and tropical regions ( 3 , 62 , 63 ). Thus, it recommends that elderly people and children should be given extra care during dengue epidemics and be prioritized for medical therapies to reduce the impact of dengue disease. Certain DENV serotypes, on the other hand, may have an impact on disease severity, such as secondary infection with DENV-1, 2, and 3 ( 64 ). Likewise, DENV-2 and DENV-4 have been highly associated with DSS, while DENV-3 and DENV-4 have been linked to DHF in the SEA region ( 65 ). Consistently, disease severity in our study can be attributed to the predominant serotypes 2 and 3, as very limited samples were diagnosed with DENV-1, DENV-4, and mix infection ( Figure 4 ). It would be interesting if further detailed studies are conducted to explore the association between disease severity, DENV serotypes and age-related factors.

Circulating DENV serotypes and dengue fever severity

DENV detection in human blood could be very effective in predicting impending epidemics. The current study observed 52% DENV positivity in blood ( Figure 4 ). In Peshawar, however, higher DENV infection rates were found in blood samples. According to our findings, the predominant serotypes were DENV-2 (45.8%) and DENV-3 (50.4%), with DENV-1 (1.9%) and DENV-4 (0.4%) the least common serotypes ( Figure 4 ), suggesting this outbreak is a continuation of the previous outbreak (2017). Our hypothesis is confirmed by recent studies conducted in the area (Peshawar) ( 66 , 67 ). The epidemiological dynamics of dengue disease in a region are influenced by multiple serotypes ( 64 ). Previously, DENV-1, 2, 3, and 4 were identified as the primary cause of dengue epidemics in Pakistan ( 68 – 71 ). The severity of the disease in terms of high infection rates and pervasiveness in our study area is likely attributable to the serotypes DENV-2 and 3 and emergence of a new clade of DENV2 (cosmopolitan genotype IV: A1 lineage) ( 71 ) in 2017 dengue outbreak, an observation similar to other national and international studies ( 1 , 3 , 22 , 51 , 64 , 69 , 71 , 72 ). Our claim is endorsed by ( 73 ), who mentioned that there are repeated extinctions of serotypes 2 and 3, which are replaced by new variants (more virulent) in the country, similar to others ( 65 , 69 , 72 , 73 ). Different serotypes have been associated with different severity of dengue infections ( 64 , 74 ). In the current study, both serotype 2 and 3 were associated with severe infections whereas previously DENV-2 was associated with almost 100 dengue infections in 2011 ( 69 ). Similar to our finding, Soo et al. ( 64 ) reported DENV-3 to have maximum percentage of primary infections (severity) in Southeast Asia (SEA) region whereas DENV-2 caused a larger percentage of severe dengue illnesses in non-SEA regions. In Thailand, all the severe primary infections were caused by serotype-1. Whereas, DENV-4 had the fewest cases in both SEA and non-SEA regions ( 64 ) and has been shown to be less immunogenic ( 75 ). Together, because DENV-2 and DENV-3 are more closely linked to dengue infection, serotype-specific antiviral medications may be customized to target these serotypes. Concurrent and secondary infections, on the other hand, were shown to be more severe than primary infections caused by any particular serotype ( 64 ). Thus, this demonstrates that while evaluating clinical outcomes and the severity of the illness, these serotypes should be given special attention. However, further studies (with increased sample size) determining serotype-specific disease severity and clinical symptoms will be fascinating and crucial to understanding epidemiological dynamics and evolutionary changes (genotypes/clades) in multi-strain disease systems in a given area.

This is the first study to illustrate a possible link between KAP and dengue prevalence during a dengue outbreak in the province. Although good knowledge and attitude was observed among the communities, the dengue prevention practices were not much effective ( Table 2 and Supplementary Material 3 ). However, communities with previous dengue exposure (i.e., Haripur, Masnsehra, and Peshawar) had a better level of awareness and attitudes toward dengue, with Khyber, Swabi, Buner, and Nowshera districts being significantly exposed to dengue infection based on low dengue-KAP ( Supplementary Material 3 ). Fascinatingly, despite being aware of the disease's seriousness, having better SES, and having previously been exposed to dengue, residents of Peshawar, Mardan, Haripur, and Nowshera exhibited very limited interest in adopting strict preventive measures, which contradicts earlier findings ( 5 , 7 , 48 – 50 ). Despite the fact that males revealed higher KAP than females in our study ( Table 2 ), the epidemiological investigation discovered a higher prevalence of dengue in males ( Figure 3 ), possibly due to males' frequent exposure to mosquito bites and females' full clothing (a culturing trait) as discussed earlier. This requires further investigation. Taking together, this suggests that only knowledge is ineffective unless and until an individual's self-efficacy in adopting strict relevant precautions is strong, an observation similar to ( 7 , 76 ). Consequently, the effective operation of dengue prevention measures requires good local government-community partnership.

Furthermore, very limited (~50%) knowledge regarding vector mosquitoes, their habits, and behavior was observed. For example, most communities confused Aedes mosquito species (which bite during dusk and dawn) with Anopheles and Culex species (night biters). Consequently, this increases the likelihood of Aedes mosquitoes breeding, biting, and transmitting DENV in human populations, similar to other national ( 37 ) and international studies ( 7 , 48 , 77 ). Taken together, this reveals a low level of KAP in the region when it comes to dengue prevention. Therefore, a nationwide survey is recommended to analyze the general public's knowledge and attitudes toward dengue fever, as well as any misunderstandings.

Likewise, among various options for dengue prevention, fogging and mosquito spray were the highly practiced methods ( Supplementary Material 3 ). Self-protection methods included using mosquito repellent, bed nets, and full clothing. Vector control methods relied on discarding the larvae-infested water. Our findings on dengue prevention practices are in line with national ( 37 , 78 – 80 ) and those of studies in India ( 81 ) and Nepal ( 82 ), but contradict with those of Malaysia ( 5 , 7 , 83 , 84 ), Thailand ( 85 ), the Philippines ( 86 ), Yemen ( 87 ), and Jamaica ( 88 ), which revealed the participants had good and appropriate knowledge of dengue and dengue vectors. The disparity in outcomes could be due to differing governments' education and awareness initiatives in dengue-endemic countries, as indicated by the level of knowledge in communities. However, due to methodological discrepancies (for example, question type, community type, dissimilarity in respondents' background, scoring method, etc.), conclusions drawn from these studies must be interpreted with caution ( 5 ).

Notably, the current study observed that dengue prevention is predominantly focused on mosquito bite avoidance instead of mosquito eradication (through breeding site destruction and covering water containers, etc.), similar to other national report ( 37 ). It's crucial to note that discarding larvae-infested water near residences (as found in this study) is not a remedy for eradicating vector mosquitoes; rather, it allows mosquito populations to expand unnoticed in nature. Whereas, in the area, larvicidal spraying mostly targets homes, field sites for larval elimination are rarely inspected and treated. Subsequently, adult mosquitoes will reinvade homes in quest of a human host for blood, resulting in increased DENV transmission. Thus, antiseptics should be used to clean the larvae positive containers. The decreasing trend of dengue incidences in communities with adequate dengue knowledge ( 5 , 17 , 83 ) encourages measures to raise public awareness about dengue fever using a variety of information sharing approaches. The greater public awareness and motivation to eliminate mosquito breeding sites ( via physical and chemical approaches), and the practice of using mosquito nets and complete clothing, will be critical in vector and disease management.

Strengths and limitations of this study

Finally, our study has some limitations. First, some questions in the attitude domain may have a desirability bias. Second, since participants' KAP levels were only assessed once, the overall dynamic could shift over time. In contrast, one of our study's key strengths is that subjects (with a huge sample size) were recruited from all around the province, implying that the findings can be extended to a wide range of community settings. Determining a correlation between community-KAP-level and disease prevalence (based on epidemiological and molecular analysis) in each district further strengthens our study. The eligibility criteria further added to the quality of our results.

We observed an increasing trend in DF caused by DENV serotypes 2 and 3, together with a high level of public attitude. However, there is still a profound ignorance and insensitivity regarding DF and proactive efforts for vector control. Individuals with low socioeconomic standing, and those with a lack of adequate information (dengue fever) and prevention measures, were particularly vulnerable to the disease. Moreover, the risk of dengue was higher in rural than in urban areas, largely explained by a lack of adequate resources and a poor level of KAP on dengue. Peshawar, Nowshera, and Mardan were among the most dengue-affected districts, with higher human population densities more frequently falling under the critical range. Our findings add to the body of knowledge that policymakers can use to develop guidelines aimed at addressing the root causes of the rising trend of dengue fever in KP province, in particular, and Pakistan in general. Moreover, it is strongly recommended that information concerning DF be disseminated by mass media, such as television, etc., in order to influence people's behavior and stop the impending outbreaks. The inclusion of DF preventive programmes into university and school curricula is highly recommended, particularly in places with a dearth of both high-quality healthcare resources and adequate health education.

Data availability statement

The original contributions presented in the study are included in the article/ Supplementary material , further inquiries can be directed to the corresponding authors.

Ethics statement

The study and associated protocols were developed in accordance with National Ethical Legislation and as endorsed by the Ethic Board of the Zoology Faculty, Abdul Wali Khan University. In line with the latest version of the Declaration of Helsinki ( 29 ), all samples were obtained after the participants' written consent. The patients/participants provided their written informed consent to participate in this study.

Author contributions

JK, ZW, XZ, and YW conceived and designed the experiments. JK, MA, GW, and IR analyzed the data. XZ, ZW, YW, DZ, GW, WP, and MA contributed reagents, materials, and analysis tools. TT critically revised the manuscript and provided suggestions and comments on the manuscript. MA formatted the figures. JK and MA interpreted and adjusted the figures in the manuscript. JK wrote the manuscript. All authors read and approved the final manuscript.

This study was supported by the National Key R&D Program of China (no. 2020YFC1200100), National Natural Science Foundation of China (nos. 82002168 and 82072308), the 6th Nuclear Energy R&D Project (no. 20201192), and 111 project (no. B12003).

Acknowledgments

The authors thank the individuals who directly or indirectly helped us in collecting field data.

Conflict of interest

Author WP was employed by Guangzhou SYSU Nuclear and Insect biotechnology Co., Ltd.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpubh.2022.923277/full#supplementary-material

Supplementary material 1. Questionnaire 1.

Supplementary material 2. Questionnaire 2.

Supplementary material 3. The levels of knowledge, attitude, and practices (KAP) among people ( n = 14,745) from various districts (KP) in 2021.

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Keywords: epidemiology, serology, DENV, SES, KAP

Citation: Khan J, Adil M, Wang G, Tsheten T, Zhang D, Pan W, Khan MA, Rehman Iu, Zheng X, Wu Z and Wu Y (2022) A cross-sectional study to assess the epidemiological situation and associated risk factors of dengue fever; knowledge, attitudes, and practices about dengue prevention in Khyber Pakhtunkhwa Province, Pakistan. Front. Public Health 10:923277. doi: 10.3389/fpubh.2022.923277

Received: 19 April 2022; Accepted: 04 July 2022; Published: 29 July 2022.

Reviewed by:

Copyright © 2022 Khan, Adil, Wang, Tsheten, Zhang, Pan, Khan, Rehman, Zheng, Wu and Wu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Zhongdao Wu, wuzhd@mail.sysu.edu.cn ; Yu Wu, wuyu@mail.sysu.edu.cn

† These authors have contributed equally to this work