Evidence of Coxiella burnetii in Punjab province, Pakistan

Muhammad Zubair Shabbir, Sidra Akram, Zia ul Hassan, Kashif Hanif, Masood Rabbani, Javed Muhammad, Muhammad Hamid Chaudhary, Tariq Abbas, Muhammad Taslim Ghori, Haroon Rashid, Tariq Jamil, Zia ul Islam, Haisem Rasool, Asghari Bano, Arfan Ahmad, Muhammad Asad Ali, Tahir Yaqub, Walter Roland McVey, Jr., Bhushan M. Jayarao

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

Coxiella burnetii causes query (Q) fever, an important zoonotic disease with worldwide significance. The role of environment in the ecology of C. burnetti, and its influence on seroconversion in animals has not been elucidated in Pakistan. We carried out a cross-sectional study in Punjab province to (1) determine the prevalence and distribution of C. burnetii in soil using an ISIIII gene-based real time-polymerase chain reaction (RT-PCR) assay, (2) analyze association between the occurrence of C. burnetii in soil and its predictors i.e. soil characteristics (macro- and micro-nutrients) and several likely risk factors including the seroconversion in small ruminants at places where its genome had or had not been detected, and (3) predict homology and genetic diversity of the identified strains using sequences originated from different hosts worldwide. A total of 2425 soil samples from nine districts of Punjab province were processed. C. burnetii DNA was detected in 47 samples (1.94%, 95% CI: ±0.55) originating from 35 villages of studied districts (7.22%, 95% CI: ±2.30). The highest prevalence was found in Attock (7.11%, 95% CI: ±3.36), followed by Lahore (4.83%, 95% CI: ±3.49), Sahiwal (4.70%, 95% CI: ±2.6), Dera Ghazi Khan (2.33%, 95% CI: ±2.02), Faisalabad (1.35%, 95% CI: ±1.18) and Sheikhupura (0.68%, 95% CI: ±0.94). The odds of detecting bacterial DNA in soil was increased with a unit increase in organic matter [2.511 (95% CI: 1.453–4.340), p = 0.001] and sodium [1.013 (95% CI: 1.005–1.022), p = 0.001], whereas, calcium [0.984 (95% CI: 0.975–0.994), p = 0.002] and potassium [0.994 (95% CI: 0.990–0.999), p = 0.011] had protective effect where a unit increase in each analyte decreased odds for its occurrence by 1.0% approximately. Likewise, for categorical variables (risk factors), the odds of detecting C. burnetii were higher at locations >500 m away from a main road [1.95 (95% CI: 1.06–3.78), p = 0.04]. The enzyme-linked immunosorbent assay (ELISA) revealed an increased prevalence of antibodies in sheep (17.9%, 95% CI: ±5.54) compared with goats (16.4%, 95% CI: ±4.34). When determining the association between soil DNA and C. burnetii antibodies in small ruminants, the odds of detecting these antibodies were significant in sheep at the livestock barns [2.81 (95% CI: 1.20–7.37), p = 0.02]. The IS1111 gene-based sequence analysis revealed a clustering of the DNA into two distinct groups with much genetic divergence (0.76–68.70%): the first group that contained sequences from Lahore district clustered with human and buffalo origin isolates, whereas the second group that contained the sequences from the remaining study districts clustered with goat-, rodent- and human-origin isolates. This study provides the first evidence of the presence of C. burnetii in the environment in Punjab province, Pakistan. Future studies are needed to ascertain the bacteria's molecular epidemiology over a wide geographical area, type the isolates, and evaluates the potential risks to human populations, particularly farmers and veterinarians.

Original languageEnglish (US)
Pages (from-to)61-69
Number of pages9
JournalActa Tropica
Volume163
DOIs
StatePublished - Nov 1 2016

Fingerprint

Coxiella burnetii
Pakistan
Soil
Q Fever
Ruminants
small ruminants
seroconversion
DNA
soil
Goats
Antibodies
Sheep
risk factors
goats
Q fever
sheep
Food
Sahiwal
Bacterial DNA
genetic variation

All Science Journal Classification (ASJC) codes

  • Parasitology
  • veterinary (miscalleneous)
  • Insect Science
  • Infectious Diseases

Cite this

Shabbir, M. Z., Akram, S., Hassan, Z. U., Hanif, K., Rabbani, M., Muhammad, J., ... Jayarao, B. M. (2016). Evidence of Coxiella burnetii in Punjab province, Pakistan. Acta Tropica, 163, 61-69. https://doi.org/10.1016/j.actatropica.2016.07.017
Shabbir, Muhammad Zubair ; Akram, Sidra ; Hassan, Zia ul ; Hanif, Kashif ; Rabbani, Masood ; Muhammad, Javed ; Chaudhary, Muhammad Hamid ; Abbas, Tariq ; Ghori, Muhammad Taslim ; Rashid, Haroon ; Jamil, Tariq ; Islam, Zia ul ; Rasool, Haisem ; Bano, Asghari ; Ahmad, Arfan ; Ali, Muhammad Asad ; Yaqub, Tahir ; McVey, Jr., Walter Roland ; Jayarao, Bhushan M. / Evidence of Coxiella burnetii in Punjab province, Pakistan. In: Acta Tropica. 2016 ; Vol. 163. pp. 61-69.
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abstract = "Coxiella burnetii causes query (Q) fever, an important zoonotic disease with worldwide significance. The role of environment in the ecology of C. burnetti, and its influence on seroconversion in animals has not been elucidated in Pakistan. We carried out a cross-sectional study in Punjab province to (1) determine the prevalence and distribution of C. burnetii in soil using an ISIIII gene-based real time-polymerase chain reaction (RT-PCR) assay, (2) analyze association between the occurrence of C. burnetii in soil and its predictors i.e. soil characteristics (macro- and micro-nutrients) and several likely risk factors including the seroconversion in small ruminants at places where its genome had or had not been detected, and (3) predict homology and genetic diversity of the identified strains using sequences originated from different hosts worldwide. A total of 2425 soil samples from nine districts of Punjab province were processed. C. burnetii DNA was detected in 47 samples (1.94{\%}, 95{\%} CI: ±0.55) originating from 35 villages of studied districts (7.22{\%}, 95{\%} CI: ±2.30). The highest prevalence was found in Attock (7.11{\%}, 95{\%} CI: ±3.36), followed by Lahore (4.83{\%}, 95{\%} CI: ±3.49), Sahiwal (4.70{\%}, 95{\%} CI: ±2.6), Dera Ghazi Khan (2.33{\%}, 95{\%} CI: ±2.02), Faisalabad (1.35{\%}, 95{\%} CI: ±1.18) and Sheikhupura (0.68{\%}, 95{\%} CI: ±0.94). The odds of detecting bacterial DNA in soil was increased with a unit increase in organic matter [2.511 (95{\%} CI: 1.453–4.340), p = 0.001] and sodium [1.013 (95{\%} CI: 1.005–1.022), p = 0.001], whereas, calcium [0.984 (95{\%} CI: 0.975–0.994), p = 0.002] and potassium [0.994 (95{\%} CI: 0.990–0.999), p = 0.011] had protective effect where a unit increase in each analyte decreased odds for its occurrence by 1.0{\%} approximately. Likewise, for categorical variables (risk factors), the odds of detecting C. burnetii were higher at locations >500 m away from a main road [1.95 (95{\%} CI: 1.06–3.78), p = 0.04]. The enzyme-linked immunosorbent assay (ELISA) revealed an increased prevalence of antibodies in sheep (17.9{\%}, 95{\%} CI: ±5.54) compared with goats (16.4{\%}, 95{\%} CI: ±4.34). When determining the association between soil DNA and C. burnetii antibodies in small ruminants, the odds of detecting these antibodies were significant in sheep at the livestock barns [2.81 (95{\%} CI: 1.20–7.37), p = 0.02]. The IS1111 gene-based sequence analysis revealed a clustering of the DNA into two distinct groups with much genetic divergence (0.76–68.70{\%}): the first group that contained sequences from Lahore district clustered with human and buffalo origin isolates, whereas the second group that contained the sequences from the remaining study districts clustered with goat-, rodent- and human-origin isolates. This study provides the first evidence of the presence of C. burnetii in the environment in Punjab province, Pakistan. Future studies are needed to ascertain the bacteria's molecular epidemiology over a wide geographical area, type the isolates, and evaluates the potential risks to human populations, particularly farmers and veterinarians.",
author = "Shabbir, {Muhammad Zubair} and Sidra Akram and Hassan, {Zia ul} and Kashif Hanif and Masood Rabbani and Javed Muhammad and Chaudhary, {Muhammad Hamid} and Tariq Abbas and Ghori, {Muhammad Taslim} and Haroon Rashid and Tariq Jamil and Islam, {Zia ul} and Haisem Rasool and Asghari Bano and Arfan Ahmad and Ali, {Muhammad Asad} and Tahir Yaqub and {McVey, Jr.}, {Walter Roland} and Jayarao, {Bhushan M.}",
year = "2016",
month = "11",
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doi = "10.1016/j.actatropica.2016.07.017",
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Shabbir, MZ, Akram, S, Hassan, ZU, Hanif, K, Rabbani, M, Muhammad, J, Chaudhary, MH, Abbas, T, Ghori, MT, Rashid, H, Jamil, T, Islam, ZU, Rasool, H, Bano, A, Ahmad, A, Ali, MA, Yaqub, T, McVey, Jr., WR & Jayarao, BM 2016, 'Evidence of Coxiella burnetii in Punjab province, Pakistan', Acta Tropica, vol. 163, pp. 61-69. https://doi.org/10.1016/j.actatropica.2016.07.017

Evidence of Coxiella burnetii in Punjab province, Pakistan. / Shabbir, Muhammad Zubair; Akram, Sidra; Hassan, Zia ul; Hanif, Kashif; Rabbani, Masood; Muhammad, Javed; Chaudhary, Muhammad Hamid; Abbas, Tariq; Ghori, Muhammad Taslim; Rashid, Haroon; Jamil, Tariq; Islam, Zia ul; Rasool, Haisem; Bano, Asghari; Ahmad, Arfan; Ali, Muhammad Asad; Yaqub, Tahir; McVey, Jr., Walter Roland; Jayarao, Bhushan M.

In: Acta Tropica, Vol. 163, 01.11.2016, p. 61-69.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Evidence of Coxiella burnetii in Punjab province, Pakistan

AU - Shabbir, Muhammad Zubair

AU - Akram, Sidra

AU - Hassan, Zia ul

AU - Hanif, Kashif

AU - Rabbani, Masood

AU - Muhammad, Javed

AU - Chaudhary, Muhammad Hamid

AU - Abbas, Tariq

AU - Ghori, Muhammad Taslim

AU - Rashid, Haroon

AU - Jamil, Tariq

AU - Islam, Zia ul

AU - Rasool, Haisem

AU - Bano, Asghari

AU - Ahmad, Arfan

AU - Ali, Muhammad Asad

AU - Yaqub, Tahir

AU - McVey, Jr., Walter Roland

AU - Jayarao, Bhushan M.

PY - 2016/11/1

Y1 - 2016/11/1

N2 - Coxiella burnetii causes query (Q) fever, an important zoonotic disease with worldwide significance. The role of environment in the ecology of C. burnetti, and its influence on seroconversion in animals has not been elucidated in Pakistan. We carried out a cross-sectional study in Punjab province to (1) determine the prevalence and distribution of C. burnetii in soil using an ISIIII gene-based real time-polymerase chain reaction (RT-PCR) assay, (2) analyze association between the occurrence of C. burnetii in soil and its predictors i.e. soil characteristics (macro- and micro-nutrients) and several likely risk factors including the seroconversion in small ruminants at places where its genome had or had not been detected, and (3) predict homology and genetic diversity of the identified strains using sequences originated from different hosts worldwide. A total of 2425 soil samples from nine districts of Punjab province were processed. C. burnetii DNA was detected in 47 samples (1.94%, 95% CI: ±0.55) originating from 35 villages of studied districts (7.22%, 95% CI: ±2.30). The highest prevalence was found in Attock (7.11%, 95% CI: ±3.36), followed by Lahore (4.83%, 95% CI: ±3.49), Sahiwal (4.70%, 95% CI: ±2.6), Dera Ghazi Khan (2.33%, 95% CI: ±2.02), Faisalabad (1.35%, 95% CI: ±1.18) and Sheikhupura (0.68%, 95% CI: ±0.94). The odds of detecting bacterial DNA in soil was increased with a unit increase in organic matter [2.511 (95% CI: 1.453–4.340), p = 0.001] and sodium [1.013 (95% CI: 1.005–1.022), p = 0.001], whereas, calcium [0.984 (95% CI: 0.975–0.994), p = 0.002] and potassium [0.994 (95% CI: 0.990–0.999), p = 0.011] had protective effect where a unit increase in each analyte decreased odds for its occurrence by 1.0% approximately. Likewise, for categorical variables (risk factors), the odds of detecting C. burnetii were higher at locations >500 m away from a main road [1.95 (95% CI: 1.06–3.78), p = 0.04]. The enzyme-linked immunosorbent assay (ELISA) revealed an increased prevalence of antibodies in sheep (17.9%, 95% CI: ±5.54) compared with goats (16.4%, 95% CI: ±4.34). When determining the association between soil DNA and C. burnetii antibodies in small ruminants, the odds of detecting these antibodies were significant in sheep at the livestock barns [2.81 (95% CI: 1.20–7.37), p = 0.02]. The IS1111 gene-based sequence analysis revealed a clustering of the DNA into two distinct groups with much genetic divergence (0.76–68.70%): the first group that contained sequences from Lahore district clustered with human and buffalo origin isolates, whereas the second group that contained the sequences from the remaining study districts clustered with goat-, rodent- and human-origin isolates. This study provides the first evidence of the presence of C. burnetii in the environment in Punjab province, Pakistan. Future studies are needed to ascertain the bacteria's molecular epidemiology over a wide geographical area, type the isolates, and evaluates the potential risks to human populations, particularly farmers and veterinarians.

AB - Coxiella burnetii causes query (Q) fever, an important zoonotic disease with worldwide significance. The role of environment in the ecology of C. burnetti, and its influence on seroconversion in animals has not been elucidated in Pakistan. We carried out a cross-sectional study in Punjab province to (1) determine the prevalence and distribution of C. burnetii in soil using an ISIIII gene-based real time-polymerase chain reaction (RT-PCR) assay, (2) analyze association between the occurrence of C. burnetii in soil and its predictors i.e. soil characteristics (macro- and micro-nutrients) and several likely risk factors including the seroconversion in small ruminants at places where its genome had or had not been detected, and (3) predict homology and genetic diversity of the identified strains using sequences originated from different hosts worldwide. A total of 2425 soil samples from nine districts of Punjab province were processed. C. burnetii DNA was detected in 47 samples (1.94%, 95% CI: ±0.55) originating from 35 villages of studied districts (7.22%, 95% CI: ±2.30). The highest prevalence was found in Attock (7.11%, 95% CI: ±3.36), followed by Lahore (4.83%, 95% CI: ±3.49), Sahiwal (4.70%, 95% CI: ±2.6), Dera Ghazi Khan (2.33%, 95% CI: ±2.02), Faisalabad (1.35%, 95% CI: ±1.18) and Sheikhupura (0.68%, 95% CI: ±0.94). The odds of detecting bacterial DNA in soil was increased with a unit increase in organic matter [2.511 (95% CI: 1.453–4.340), p = 0.001] and sodium [1.013 (95% CI: 1.005–1.022), p = 0.001], whereas, calcium [0.984 (95% CI: 0.975–0.994), p = 0.002] and potassium [0.994 (95% CI: 0.990–0.999), p = 0.011] had protective effect where a unit increase in each analyte decreased odds for its occurrence by 1.0% approximately. Likewise, for categorical variables (risk factors), the odds of detecting C. burnetii were higher at locations >500 m away from a main road [1.95 (95% CI: 1.06–3.78), p = 0.04]. The enzyme-linked immunosorbent assay (ELISA) revealed an increased prevalence of antibodies in sheep (17.9%, 95% CI: ±5.54) compared with goats (16.4%, 95% CI: ±4.34). When determining the association between soil DNA and C. burnetii antibodies in small ruminants, the odds of detecting these antibodies were significant in sheep at the livestock barns [2.81 (95% CI: 1.20–7.37), p = 0.02]. The IS1111 gene-based sequence analysis revealed a clustering of the DNA into two distinct groups with much genetic divergence (0.76–68.70%): the first group that contained sequences from Lahore district clustered with human and buffalo origin isolates, whereas the second group that contained the sequences from the remaining study districts clustered with goat-, rodent- and human-origin isolates. This study provides the first evidence of the presence of C. burnetii in the environment in Punjab province, Pakistan. Future studies are needed to ascertain the bacteria's molecular epidemiology over a wide geographical area, type the isolates, and evaluates the potential risks to human populations, particularly farmers and veterinarians.

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Shabbir MZ, Akram S, Hassan ZU, Hanif K, Rabbani M, Muhammad J et al. Evidence of Coxiella burnetii in Punjab province, Pakistan. Acta Tropica. 2016 Nov 1;163:61-69. https://doi.org/10.1016/j.actatropica.2016.07.017