Research in Veterinary Science 131 (2020) 104–116

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Research in Veterinary Science

journal homepage: www.elsevier.com/locate/rvsc

The global status of Dirofilaria immitis in dogs: a systematic review and meta- T
analysis based on published articles
⁎⁎
Davood Anvaria,b,c,1, , Elahe Naroueid, Ahmad Daryanib, Shahabeddin Sarvib,
Mahmood Moosazadehe, Hajar Ziaei Hezarjaribib, Mohammad Reza Naroueid,
⁎
Shirzad Gholamib,1,
a
Student Research Committee, Mazandaran University of Medical Science, Sari, Iran
b
Toxoplasmosis Research Center, Department of Parasitology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
c
School of Medicine, Iranshahr University of Medical Sciences, Iranshahr, Iran
d
Faculty of Veterinary Medicine, University of Zabol, Zabol, Iran
e
Health Science Research Center, Addiction Institute, Mazandaran University of Medical Sciences, Sari, Iran

A R T I C LE I N FO A B S T R A C T

Keywords: Dirofilaria immitis is a parasitic filarial nematode responsible for heartworm disease in domestic as well as wild
Dirofilaria immitis canines and felines and pulmonary or cutaneous infections in humans. This systematic review and meta-analysis
Dirofilariasis aimed to evaluate the status of D. immitis in dogs based on available literature. Four English language databases
Dogs (ISI Web of Science, Scopus, PubMed and Science Direct) containing data on D. immitis prevalence in dogs were
Systematic review
thoroughly searched resulting in the inclusion of 193 studies. The findings revealed that the pooled and
Meta-analysis
weighted prevalence of D. immitis infection in dog population based on published papers throughout the world
was 10.91% (95% CI=10.18–11.65). In addition, subgroup analysis based on meta-regression revealed that a
significant difference between the pooled and weighted prevalence of D. immitis in dogs and country (β =0.14,
P=0.049). Given the relatively high prevalence of D. immitis infection in dogs and its adverse effects, it is
suggested that to perform more research on the prevention and control of dirofilariasis infection in dogs
worldwide.

1. Introduction
Dirofilariasis is a common disease between human and animals,
caused by Dirofilaria immitis (D. immitis), a nematode that can be
transmitted by insects and spread worldwide. Many domestic animals,
especially dogs and cats play the role of main hosts for this parasite
(Atkins, 2003). Human may be infected with the larval stage as an
aberrant host, and several human cases have so far been detected in
Iran, Japan and the United States (Ettinger and Feldman, 2005). Adult
worm resides in the pulmonary artery of dogs which can produce blood-
circulating microfilariae in dogs. On the other hand, the preadult worm
is responsible for pulmonary dirofilariasis in humans since the worm
cannot reach full maturity, (Taylor et al., 2016). The infective third-
stage larvae can be transmitted to the vertebrate hosts, such as humans
and animals through mosquito bite (Anopheles and Culex). Dirofilariasis
in dogs can cause clinical symptoms, such as persistent cough, dyspnea,
congestive heart failure, physical activity intolerance, intravascular
hemolysis, hemoptysis, ascites, pulmonary thromboembolism, and loss
of appetite and weight. In tropical and subtropical regions of the world,
dirofilariasis is considered one of the most important zoonotic diseases
transmitted between humans and carnivores (Vieira et al., 2014) and
deadly in dogs if not treated (Taylor et al., 2016). The presence of dogs
infected with microfilariae-producing adult worms determines the
prevalence and transmission of D. immitis in dogs and cats. The pre-
valence tends to vary dramatically among different regions of the world
on account of certain epidemiological factors, such as the distribution
of the mosquito species (vector), mosquito fertility, mosquito popula-
tion density, animal behavior, environmental temperature, living con-
ditions, and the average age of the susceptible host (Anvari et al.,
2019a; Omar et al., 2018; Taylor et al., 2016).

⁎
Corresponding author at: S. Gholami, Department of Parasitology, Toxoplasmosis Research Center (TRC), School of Medicine, Mazandaran University of Medical
Sciences, 18th Km of Khazar abad Road, Sari, Mazandaran Province, Iran. P.O.Box: 48175-1665. Fax: +98 151 3543088.
⁎⁎
Correspondence to: D. Anvari, Department of Parasitology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran.
E-mail addresses: davood_anvari@live.com (D. Anvari), sgholami200@gmail.com (S. Gholami).
1
Contributed equally.

https://doi.org/10.1016/j.rvsc.2020.04.002
Received 23 March 2019; Received in revised form 1 April 2020; Accepted 2 April 2020
0034-5288/ © 2020 Elsevier Ltd. All rights reserved.
D. Anvari, et al. Research in Veterinary Science 131 (2020) 104–116

Fig. 1. Flow diagram of systematic review and meta-analysis process.

Over the past 20 years, the geographic range of canine heartworm Analyses (PRISMA) guideline and its checklist (Moher et al., 2009).
infection has increased significantly. In addition, an increasing number
of D. immitis infection cases in dogs has been reported in many countries
2.1. Strategy for literature search
(Hou et al., 2011). However, there still exists a gap in our knowledge
concerning the status of this parasite throughout the world and across
For the purpose of the study, four English language databases, in-
different continents.
cluding ISI Web of Science, Scopus, PubMed and Science Direct, were
With this background in mind, the present systematic review and
searched for every article related to infection with D. immitis in dogs
meta-analysis aimed to update and broaden our knowledge on the
published until September 2019. The search process was performed
status of Dirofilaria immitis infections in dogs based on published arti-
using Medical Subject Heading terms including “Dirofilariasis”,
cles, provide and compile information on the status and distribution of
“Dirofilaria immitis”, “D. immitis”, “dog”, “prevalence” and “ser-
Dirofilaria immitis infections in dogs around the world, assess the risk
oprevalence”.
factors of heartworm infection, and establish the worldwide status of
this parasite for the first time according to so far published studies.
2.2. Inclusion and exclusion criteria

2. Methods The inclusion criteria entailed: 1) cross-sectional papers that esti-

mated the prevalence of D. immitis in dogs with detailed data, 2) re-
This systematic literature review and meta-analysis is strictly sub- search that performed only on dogs and 3) English language papers.
ject to the Preferred Reporting Items for Systematic Reviews and Meta- Furthermore, the excluded papers were: 1) review papers, 2)

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Table 1
Characteristics of abstracted studiesa.
Study Author, Year Total Sample No. of Positive Diagnostic method Country Continent Q.A

1 (Ward, 1965) 543 239 Knott's test USA America 5

2 (Sengbusch et al., 1975) 100 2 Knott's test USA America 6
3 (Streitel et al., 1977) 500 24 Knott's test USA America 5
4 (Kazacos, 1978) 112 17 Necropsy USA America 6
5 (Walters et al., 1981) 97 2 Knott's test USA America 7
6 (Pratt et al., 1981) 11823 447 Knott's test USA America 7
7 (Falls and Platt, 1982) 100 19 Knott's test USA America 6
8 (Blake and Overend, 1982) 734 15 Necropsy Australia Australia 6
9 (Martin and Collins, 1985) 331 36 Filtration test Wales Europe 6
10 (Hesselink, 1988) 631 66 Knott's test Curaçao America 7
11 (Foreyt and Lagerquist, 1991) 601 3 ELISA USA America 7
12 (Patton and McCracken, 1991) 3608 213 ELISA USA America 6
13 (Patton and Faulkner, 1992) 6977 430 Knott's test USA America 7
14 (Copland et al., 1992) 1428 18 Knott's test Australia Australia 6
15 (Bidgood and Collins, 1996) 304 19 Acid phosphatase test Australia Australia 7
16 (Jafari et al., 1996) 114 11 Knott's test Iran Asia 7
17 (Montoya et al., 1998) 2034 1198 Haemagglutination test Spain Europe 7
18 (Wang, 1998) 100 47 ELISA Taiwan Asia 6
19 (Fan et al., 2001) 664 89 ELISA Taiwan Asia 6
20 (Theis et al., 2001) 788 6 ELISA USA America 7
21 (Cringoli et al., 2001) 351 2 Knott's test Italy Europe 6
22 (Yoon et al., 2002) 17644 263 ELISA South Korea Asia 7
23 (Öge et al., 2003) 280 26 ELISA Turkey Europe 6
24 (Labarthe et al., 2003) 2553 51 ELISA Brazil America 6
25 (Kaiser and Williams, 2004) 176 170 Necropsy USA America 6
26 (Reifur et al., 2004) 256 10 Filtration test Brazil America 6
27 (Voyvoda et al., 2004) 158 22 Knott's test Turkey Europe 7
28 (Yabsley et al., 2004) 611 68 Knott's test USA America 7
29 (Duran-Struuck et al., 2005) 104 19 WITNESS HW Test Dominican Republic America 7
30 (Kim and Huh, 2005) 500 50 Necropsy South Korea Asia 7
31 (Svobodova and Mišoňova, 2005) 36 11 ELISA Czech Republic Europe 7
32 (Oncel and Vural, 2005) 380 4 ELISA Turkey Europe 6
33 (Montoya et al., 2006) 823 172 Antigen detection Spain Europe 7
34 (Svobodová et al., 2006) 77 5 ELISA Czech Republic Europe 6
35 (Solano-Gallego et al., 2006) 460 3 IFAT Spain Europe 6
36 (Bolio-Gonzalez et al., 2007) 676 56 Knott's test Mexico America 7
37 (Byeon et al., 2007) 294 19 Blood Smear South Korea Asia 7
38 (Yildirim et al., 2007) 280 27 ELISA Turkey Europe 6
39 (Notarnicola and Navone, 2007) 265 6 Knott's test Argentina America 7
40 (Levy et al., 2007) 1958 956 Antigen detection USA America 7
41 (Boonyapakorn et al., 2008) 589 107 Microhematocrit tube technique Thailand Asia 6
42 (Simsek et al., 2008) 211 27 ELISA Turkey Europe 6
43 (Yildiz et al., 2008) 142 49 ELISA Turkey Europe 6
44 (Vezzani et al., 2008) 4934 88 Antigen detection Argentina America 6
45 (Levy et al., 2008) 95 32 Antigen detection Galapagos America 7
46 (Lazri et al., 2008) 272 19 Antigen detection Kosovo and Albania Europe 7
47 (Hoff et al., 2008) 187 67 ELISA Turks and Caicos Islands America 7
48 (Gadahi et al., 2008) 300 16 Knott's test Pakistan Asia 7
49 (Beall et al., 2008) 731 11 ELISA USA America 7
50 (Hirsch and Pantchev, 2008) 5483 65 ELISA Germany Europe 7
51 (Bowman et al., 2009) 3182301 43500 ELISA USA America 7
52 (Meriem-Hind and Mohamed, 2009) 184 45 ELISA Algeria Africa 7
53 (Yaman et al., 2009) 269 70 ELISA Turkey Europe 7
54 (Pantchev et al., 2009b) 919 2 Antigen detection France Europe 6
55 (Pantchev et al., 2009a) 44 3 PCR Germany Europe 7
56 (Hamel et al., 2009) 30 1 IFAT Albania Europe 7
57 (Furtado et al., 2009) 188 61 Knott's test Brazil America 7
58 (Kim et al., 2010) 252 5 ELISA South Korea Asia 7
59 (Lefkaditis et al., 2010) 341 61 ELISA Greece Europe 6
60 (Miterpakova et al., 2010) 591 118 Knott's test Slovakia Europe 6
61 (Morchón et al., 2010) 100 12 Antigen detection Spain Europe 7
62 (Nematollahi and Barazandeh, 2010) 100 30 Knott's test Iran Asia 7
63 (Jalali et al., 2010) 100 5 Knott's test Iran Asia 7
64 (Song et al., 2010) 81 17 ELISA South Korea Asia 6
65 (Tzipory et al., 2010) 1500 81 ELISA USA America 7
66 (Montoya-Alonso et al., 2010) 697 290 ELISA Spain Europe 7
67 (Montoya-Alonso et al., 2010) 697 135 Antigen detection Spain Europe 7
68 (Tiawsirisup et al., 2010) 500 50 Blood Smear Thailand Asia 6
69 (Lim et al., 2010) 229 51 Antigen detection South Korea Asia 6
70 (Chandrashekar et al., 2010) 846 113 ELISA USA America 7
71 (Caro-Gonzalez et al., 2011) 279 167 PCR Mexico America 6
72 (Carrade et al., 2011) 2431 17 ELISA USA America 7
73 (Hou et al., 2011) 886 147 PCR China Asia 7
74 (Icen et al., 2011) 82 2 ELISA Turkey Europe 7
(continued on next page)

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Table 1 (continued)

Study Author, Year Total Sample No. of Positive Diagnostic method Country Continent Q.A

75 (Miller and Crosbie, 2011) 519 18 ELISA USA America 7

76 (Montoya-Alonso et al., 2011) 547 105 ELISA Spain Europe 7
77 (Simsek et al., 2011) 123 10 PCR Turkey Europe 7
78 (Theis et al., 2011) 1822 134 ELISA USA America 6
79 (Villeneuve et al., 2011) 86251 187 ELISA Canada America 7
80 (Kartashev et al., 2011) 76 23 Knott's test Russia Europe 7
81 (Venco et al., 2011) 608 181 Knott's test Italy Europe 7
82 (Scorza et al., 2011) 84 2 ELISA Costa Rica America 7
83 (Levy et al., 2011) 400 195 Antigen detection USA America 7
84 (Gholami et al., 2011) 50 3 Necropsy Iran Asia 6
85 (Cantó et al., 2011) 378 5 Necropsy Mexico America 7
86 (Cardoso et al., 2012) 557 20 ELISA Portugal Europe 7
87 (Mircean et al., 2012) 1146 38 ELISA Romania Europe 7
88 (Ng et al., 2012) 150 2 Antigen detection Malaysia Asia 6
89 (Yuasa et al., 2012) 344 71 dot-ELISA Taiwan Asia 7
90 (Schnyder and Deplazes, 2012) 16 5 ELISA Switzerland Europe 7
91 (Salinas-Melendez et al., 2012) 391 28 ELISA Mexico America 7
92 (Jung et al., 2012) 418 29 ELISA South Korea Asia 7
93 (Hamel et al., 2012) 78 2 ELISA Hungary Europe 7
94 (Altas et al., 2013) 50 31 ELISA Turkey Europe 7
95 (Adanir et al., 2013) 142 31 ELISA Turkey Europe 7
96 (Liu et al., 2013) 528 67 Antigen detection China Asia 6
97 (Razi Jalali et al., 2013) 200 19 Counterimmunoelectrophoresis test Iran Asia 6
98 (Sari et al., 2013) 100 40 Antigen detection Turkey Europe 6
99 (Volgina et al., 2013) 440 36 Antigen detection Russia Europe 7
100 (Tabar et al., 2013) 49 7 PCR Spain Europe 7
101 (Hamel et al., 2013) 23 2 PCR Ukraine Europe 7
102 (Eberts, 2013) 72 65 Antigen detection USA America 7
103 (Bhattacharjee and Sarmah, 2013) 468 24 Blood Smear India Asia 6
104 (Bhattacharjee and Sarmah, 2014) 468 36 Antigen detection India Asia 7
105 (Kramer et al., 2014) 3094 5 Antigen detection Poland Europe 7
106 (Labarthe et al., 2014) 1531 354 Antigen detection Brazil America 7
107 (Landum et al., 2014) 308 47 Knott's test Portugal Europe 7
108 (McCown et al., 2014) 498 8 Antigen detection Colombia America 7
109 (Méndez et al., 2014) 194 156 Antigen detection Spain Europe 6
110 (Oi et al., 2014) 100 23 Antigen detection Japan Asia 6
111 (Velasquez et al., 2014) 165 103 Antigen detection USA America 7
112 (Vieira et al., 2014) 304 78 Antigen detection Portugal Europe 6
113 (Khedri et al., 2014) 87 24 Knott's test Iran Asia 7
114 (Víchová et al., 2014) 366 8 PCR Slovakia Europe 7
115 (Ural et al., 2014) 307 7 ELISA Turkey Europe 7
116 (Stillman et al., 2014) 366 94 ELISA USA America 7
117 (Farkas et al., 2014) 1305 31 ELISA Hungary Europe 7
118 (Chou et al., 2014) 720 52 PCR Taiwan Asia 7
119 (Borthakur et al., 2014) 191 34 Antigen detection India Asia 5
120 (Bhattacharjee et al., 2014) 58 8 Antigen detection India Asia 5
121 (Balakrishnan et al., 2014) 71 8 Antigen detection USA America 7
122 (Aroch et al., 2015) 48 14 Antigen detection Israel Asia 7
123 (Borthakur et al., 2015) 782 141 Antigen detection India Asia 7
124 (Ionica et al., 2015) 390 24 PCR Romania Europe 7
125 (Montoya-Alonso et al., 2015) 1511 37 Antigen detection Spain Europe 7
126 (Pantchev et al., 2015) 167 27 Antigen detection Bulgaria Europe 7
127 (Vieira et al., 2015) 386 8 ELISA Portugal Europe 7
128 (Willi et al., 2015) 15 4 PCR Hungary Europe 7
129 (Wei et al., 2015) 40 9 PCR Costa Rica America 7
130 (Siwila et al., 2015) 251 10 Antigen detection Zambia Africa 7
131 (Schüle et al., 2015) 116 13 ELISA Albania Europe 7
132 (Rojas et al., 2015) 146 16 Antigen detection Costa Rica America 7
133 (Maia et al., 2015) 170 16 DAT Portugal Europe 7
134 (Feng et al., 2015) 1440 102 PCR Taiwan Asia 7
135 (Bacsadi et al., 2016) 2622 27 Necropsy Hungary Europe 6
136 (Ciucă et al., 2016a) 108 24 Knott's test Romania Europe 7
137 (Ciucă et al., 2016b) 458 41 ELISA Romania Europe 6
138 (Diakou et al., 2016) 750 31 Knott's test Greece Europe 7
139 (Moraes-da-Silva Mde et al., 2016) 204 44 Antigen detection Brazil America 6
140 (Movilla et al., 2016) 1706 91 Antigen detection Mexico America 7
141 (Nguyen et al., 2016) 39 36 real-time PCR Australia Australia 7
142 (Ogbaje and Abel, 2016) 186 4 Knott's test Nigeria Africa 7
143 (Radev et al., 2016) 33 5 Knott's test Bulgaria Europe 6
144 (Ugochukwu et al., 2016) 119 4 Blood Smear Nigeria Africa 7
145 (Hosseinzadeh Varjoy et al., 2016) 121 14 PCR Iran Asia 7
146 (Wang et al., 2016) 1176 155 Antigen detection China Asia 7
147 (Montoya-Alonso et al., 2016) 1643 258 Antigen detection Spain Europe 7
148 (Vascellari et al., 2016) 330 19 IFAT Italy Europe 7
149 (Starkey et al., 2016) 210 67 Antigen detection Haiti America 7
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Table 1 (continued)

Study Author, Year Total Sample No. of Positive Diagnostic method Country Continent Q.A

150 (Simsek and Ciftci, 2016) 161 3 PCR Turkey Europe 7

151 (Ramos et al., 2016) 104 12 Knott's test Brazil America 6
152 (Maia et al., 2016) 230 24 PCR Portugal Europe 7
153 (Liesner et al., 2016) 1023 2 PCR Germany Europe 6
154 (Inpankaew et al., 2016) 101 16 PCR Cambodia Asia 6
155 (Hamel et al., 2016) 602 13 ELISA Albania Europe 7
156 (Cetinkaya et al., 2016) 402 27 Antigen detection Turkey Europe 7
157 (Cetinkaya et al., 2016) 402 11 PCR Turkey Europe 7
158 (Cannon et al., 2016) 196 23 ELISA USA America 7
159 (Borthakur et al., 2016) 782 141 ELISA India Asia 6
160 (Borthakur et al., 2016) 782 109 PCR India Asia 6
161 (Barrett and Little, 2016) 105 11 Antigen detection USA America 7
162 (Alvåsen et al., 2016) 100 4 ELISA Malawi Africa 6
163 (Conan et al., 2017) 115 8 Antigen detection Saint Kitts and Nevis America 6
164 (DiGangi et al., 2017) 616 45 Antigen detection USA America 7
165 (Elhamiani Khatat et al., 2017) 217 35 Antigen detection Morocco Africa 7
166 (Kamyingkird et al., 2017) 394 95 PCR Thailand Asia 7
167 (Montenegro et al., 2017) 314 25 Antigen detection Costa Rica America 7
168 (Rjeibi et al., 2017) 200 29 PCR Tunisia Africa 7
169 (Tahir et al., 2017b) 209 3 PCR Algeria Africa 7
170 (Montoya-Alonso et al., 2017) 1716 52 Antigen detection Spain Europe 7
171 (Tahir et al., 2017a) 94 20 PCR France Europe 7
172 (Piantedosi et al., 2017) 1335 3 ELISA Italy Europe 7
173 (Mrljak et al., 2017) 435 2 IFAT Croatia Europe 6
174 (Moraes et al., 2017) 50 8 Knott's test Brazil America 7
175 (Lau et al., 2017) 90 9 Antigen detection Malaysia Asia 5
176 (Guven et al., 2017) 133 2 PCR Turkey Europe 7
177 (Figueredo et al., 2017) 300 32 Antigen detection Brazil America 7
178 (Carslake et al., 2017) 237 111 Antigen detection Samoa Australia 7
179 (Bamorovat et al., 2017) 149 8 ELISA Iran Asia 6
180 (Bamorovat et al., 2017) 149 6 PCR Iran Asia 6
181 (Atas et al., 2018) 306 9 PCR Turkey Europe 7
182 (Diosdado et al., 2018) 191 11 Antigen detection Spain Europe 7
183 (Omar et al., 2018) 294 40 ELISA Saudi Arabia Asia 6
184 (Sauda et al., 2018) 639 1 Antigen detection Italy Europe 7
185 (Torres-Chable et al., 2018) 1050 84 PCR Mexico America 7
186 (Dahmani et al., 2018) 65 11 PCR France Europe 7
187 (Wang et al., 2018) 637 1 Antigen detection China Asia 7
188 (Hodo et al., 2019) 608 97 Antigen detection USA America 7
189 (Anvari et al., 2019a) 99 30 Knott's test Iran Asia 7
190 (Evason et al., 2019) 753468 1263 Antigen detection Canada America 7
191 (McGill et al., 2019) 660946 762 Antigen detection Canada America 7
192 (Pedram et al., 2019) 311 7 PCR Iran Asia 6
193 (Silva et al., 2019) 33 2 PCR Brazil America 7

PCR: Polymerase chain reaction, ELISA: The enzyme-linked immunosorbent assay, IFAT: The immunofluorescence antibody test, DAT: Direct agglutination test, QA:
Quality assessment.
a
Type of studies were cross-sectional study.

presentation of the final result, rather than the raw data, 3) non-English
language articles and 4) absence of dogs in the study.
2.3. Study selection and data extraction
Each paper was separately evaluated by two authors. Then, the
eligible full-text papers were downloaded, and their data were recorded
in an excel file. The recorded data included the first author, year of
publication, geographic location, total sample size, number of positive
cases, and diagnostic methods.
2.4. Quality assessment
Quality of the included studies was determined using the Newcastle
Ottawa Scale (Low quality articles score less than 3.5, moderate quality
articles score 3.6–5.25 and high-quality articles score 5–5.26) (Modesti
et al., 2016). Accordingly, the papers with appropriate and acceptable
quality (> 3.5) were entered into the meta-analysis.
2.5. Meta-analysis
In the present study, the visual summary of the data was obtained
using forest plots to evaluate effect size and effect of each survey
(prevalence of Dirofilaria immitis among dogs in all included studies)
with their 95% confidence interval (CI). For the purpose of meta-ana-
lysis, a random effect model was selected to account for the study effect
to account for the expected variation on the underlying prevalence of
infection depending on the study.
Heterogeneity between studies was assessed using Cochran's Q test
and I2 index. The amount of heterogeneity varies from 0 to 100% ranges
and indicates the percentage of the difference in the point estimate that
can be attributed to study heterogeneity rather than chance. I2 values
of < 25%, 25 - 50%, and > 50% considered to indicate low, moderate,
and high heterogeneity, respectively. When moderate to high hetero-
geneity was present, data sets were sub-grouped to investigate possible
sources of heterogeneity. For this review, we determined that I2 values
above 75 % were indicative of significant heterogeneity warranting
analysis with a random effects model as opposed to the fixed effects
model to adjust for the observed variability. This heterogeneity was
further explored through subgroup analyses and meta-regression.
Multivariate approach was employed to assess the causes of hetero-
geneity among the selected studies. Furthermore, based on Egger's re-
gression test, a funnel plot was designed to check for the existence of
publication bias (Rothstein et al., 2005). The meta-analysis was

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performed using Stata software, version 14 (StataCorp, College Station,

TX, USA). P-value less than 0.05 was considered statistically significant
(Higgins and Thompson, 2002).

3. Results

3.1. Qualified studies

The search of four databases resulted in the inclusion of 2031 ar-

ticles, 1446 articles of which were excluded due to duplication and 585
papers were screened after this exclusion. A total of 379 papers were
excluded after a preliminary screening based on titles and abstracts and
206 studies were extracted. Thereafter, 17 articles were ruled out by
considering the inclusion and exclusion criteria of the full texts of the
articles. Finally, a number of 189 eligible papers (includes 193 dataset)
were qualified for systematic literature review and meta-analysis. Fig. 1
demonstrates the process of study selection and Table 1 presents the
baseline characteristics of all studies entered into the meta-analysis.

3.2. Prevalence rate of D. immitis in dogs worldwide based on published

papers

The result of the current meta-analysis revealed that the pooled and
weighted prevalence of D. immitis in dogs across the world using
random-effects models was 10.91% (95% CI=10.18–11.65) (Fig. 2).

3.2.1. D. immitis infection in dogs based on continent

On the basis of the meta-analysis, the prevalence of D. immitis in
dogs based on continent was in the following way: Australia 22.68 %
(95% CI: 6.30-45.37), Asia 12.07 % (95% CI: 9.12-15.37), America
11.60 % (95% CI: 10.47-12.77), Europe 10.45 % (95% CI: 7.51-13.82)
and Africa 7.57 % (95% CI: 3.09-13.80) (Figure 3). Furthermore, the
total heterogeneity in the continent subgroup was 99.23% and the
highest heterogeneity was observed in America continent (I2=99.99%).

3.2.2. D. immitis infection in dogs based on country

Based on the random-effects models, the highest and lowest pre-
valence of D. immitis in dogs based on the country was as follows: Spain
19.25 % (95% CI: 8.27-33.45) and Canada 0.16 % (95% CI: 0.11-0.21)
(Table 2). Moreover, the total heterogeneity in the country subgroup
was 99.82% and the highest heterogeneity was observed in USA
(I2=99.77%).

3.2.3. D. immitis infection in dogs based on year

The prevalence of D. immitis in dogs based on year was as listed
below: 2011 – 2015 year 14.05 % (95% CI: 10.51-18.00), 2006 – 2010
year 12.65 % (95% CI: 8.80-17.09), 2001 – 2005 year 11.44 % (95% CI:
5.99-18.36), < 2000 (1965-1998) year 10.76 % (95% CI: 5.46-17.58)
and ≥2016 year 7.60 % (95% CI: 6.84-8.41). Also, the total hetero-
geneity in the year subgroup was 99.62% and the highest heterogeneity
was observed in > 2000 years (I2=99.60%).

3.2.4. D. immitis infection in dogs based on diagnostic method

In this regard, the prevalence of D. immitis in dogs based on diag-
nostic method was as follows: necropsy 14.49 % (95% CI: 2.37-34.36),
antigen detection 13.57 % (95% CI: 12.16-15.05), Knott's test 11.99 %
(95% CI: 8.97-15.39), PCR 11.44 % (95% CI: 7.75-15.74), ELISA 8.56 %
(95% CI: 7.37-9.82), blood smear 6.51 % (95% CI: 4.10-9.42) and IFAT
2.14 % (95% CI: 0.30-5.60). In addition, the total heterogeneity in the
method subgroup was 98.12% and the highest heterogeneity was ob-
served in antigen detection method (I2=99.77%).

3.2.5. Publication bias and meta regression

Fig. 2. Forest plot of the worldwide prevalence of Dirofilaria immitis in dogs. Subgroup analysis based on meta-regression revealed that a sig-
nificant difference between the pooled prevalence of D. immitis in dogs
and country (β =0.14, P=0.049) (Table 2).

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Fig. 3. World map showing the prevalence of Dirofilaria immitis in dogs based on continent.
According to Egger regression test revealed that publication bias
may not have a substantial impact on the total prevalence estimate
(Egger bias = 6.9, P = 0.0751) (Figure 4).
4. Discussion
Cardiopulmonary dirofilariasis is a worldwide distributed vector-
borne transmitted disease caused by Dirofilaria immitis mainly affecting
dogs and cats. Different species of culicid mosquitoes mainly belonging
to Culex, Anopheles, and Aedes genera have been implicated in the
transmission of this parasite. Since some of these mosquito species in-
discriminately feed on both humans and animal reservoirs, D. immitis
can be transmitted to humans residing in endemic areas, causing benign
pulmonary nodules frequently mistaken with pulmonary carcinomas
(Montoya-Alonso et al., 2011; Simón et al., 2009).
To the best of our knowledge, the current review is the first study
that investigated the overall prevalence of D. immitis infection among
dogs worldwide. The results reported that the global prevalence of D.
immitis infection in dogs based on published articles as 10.91 % with the
95% confidence interval of 10.18 % - 11.65 % within 1965 - 2019.
Furthermore, the obtained result revealed that the prevalence of D.
immitis in dog population based on the continent was as listed: Australia
22.68 %, Asia 12.07 %, America 11.60 %, Europe 10.45 %, and Africa
7.57 %. One of the main vectors of D. immitis is the Culex mosquito
which has worldwide distribution (Taylor et al., 2016). A higher pre-
valence of D. immitis in dogs was observed in Australia which can be
attributed to the high prevalence of Culex mosquitoes in this region (Shi
et al., 2017). Also, the humidity and mild seasonal variations on this
continent contribute to the survival and development of the vector
mosquitoes (Dearsley et al., 2019). Moreover, according to the obtained
results of the random-effects models, the highest and lowest outbreak of
D. immitis in dog population based on the country were detected in
Spain 19.25 % and Canada 0.16 %, respectively. As the results show,
the prevalence of D. immitis varies widely across different countries and
continents. Hence, according to the results of sub-analysis of this re-
view, heterogeneity of included studies was very high in the year
subgroup (I2= 99.62%), diagnostic method (I2= 98.12%), country
(I2= 99.82%) and continent (I2= 99.23%). On the other hand, for
110
Research in Veterinary Science 131 (2020) 104–116
evaluate the reasons of heterogeneity among the selected studies, meta-
regression was performed. The results of the meta-regression showed
that the country subgroup had the greatest impact on the heterogeneity
(P= 0.049). In general, it can be concluded that the geographical fac-
tors of each country or area are the most important reason for the
discrepancy between studies. Dirofilariasis is a serious disease long
been known to spread from tropical and subtropical regions to tempe-
rate-zone countries. The geographical distribution of the disease is es-
sential for the biological cycle of D. immitis (Rosa et al., 2002) and the
weather is a critical factor affecting the prevalence of this disease.
Mosquitoes need hot weather and suitable temperatures to produce
third-stage larval development in the intermediate host since the worms
require temperatures higher than 18°C for nearly 1 month (Montoya
et al., 1998). In Europe, dirofilariasis in animals and humans is endemic
in the Mediterranean countries (Simón et al., 2005) and being detected
more frequently in central and eastern areas of the European continent
(Simón et al., 2009). In addition to the geographical factors, i) high
density of dogs in areas where vectors are present, ii) seasonal changes
in the development and survival rates of both parasite and vector, iii)
diurnal periodicity of microfilaraemia (ensures that high numbers of
microfilariae are circulating in the peripheral blood during the period
of mosquito activity), iv) distribution of mosquito fauna and v) age of
dogs (the infection commonly occurs in dogs older than one year) play
an important role in the distribution and epidemiology of the disease.
These factors, along with reasons such as type of diagnostic method
with different sensitivity and specificity, number of samples examined,
type of climate affecting mosquito presence and type of breeding system
of dogs, have led to the highly variable (high heterogeneity) prevalence
of D. immitis in dogs around the world (Brooks and Hoberg, 2007;
Montoya-Alonso et al., 2010; Morchón et al., 2012; Taylor et al., 2016).
According to the results of meta-analysis, the prevalence of D. im-
mitis in dogs based on the year from highest to lowest was followed:
2011 – 2015 year 14.05 %, 2006 – 2010 year 12.65 %, 2001 – 2005
year 11.44 %, < 2000 (1965-1998) year 10.76 % and ≥2016 year 7.60
%. In recent years (≥2016), the prevalence of D. immitis parasite in
dogs has been declining throughout the world. This apparent reduction
of dirofilariasis can be attributed to effective measures to control the
population of mosquitoes carrying the disease, and regular preventive
D. Anvari, et al. Research in Veterinary Science 131 (2020) 104–116

Table 2
Subgroup analysis of global prevalence of Dirofilaria immitis in dogs
Stratification group Weighted prevalence (%) 95%CI Heterogeneity test Publication bias Meta Regression

Q P 2
I % 2
Total I % t P β P

Continent
Africa 7.57 3.09-13.80 110.07 < 0.001 93.6 99.23 7.5 0.744 -0.30 0.741
America 11.60 10.47-12.77 39412.34 < 0.001 99.9 9.7 0.571
Asia 12.07 9.12-15.37 2443.59 < 0.001 98.2 5.7 0.591
Australia 22.68 6.30-45.37 529.12 < 0.001 99.2 34.8 0.060
Europe 10.45 7.51-13.82 8273.74 < 0.001 99.1 4.8 0.130

Country
Albania 5.49 0.83-13.85 15.27 < 0.001 86.9 99.82 3.2 0.614 0.14 0.049
Australia 16.49 4.90-33.12 221.39 < 0.001 98.6 12.9 0.149
Brazil 13.03 5.17-23.75 617.58 < 0.001 98.7 5.9 0.060
Canada 0.16 0.11-0.21 94.83 < 0.001 97.9 7.7 0.668
China 8.81 2.06-19.61 241.63 < 0.001 98.8 13.7 0.545
Costa Rica 9.53 4.66-15.91 13.49 0.003 77.8 2.7 0.375
Germany 1.15 0.19-2.89 18.47 < 0.001 89.2 1.75 0.751
Hungary 2.62 0.97-5.05 23.13 < 0.001 87 1.9 0.209
India 13.11 9.05-17.78 84.02 < 0.001 92.9 3.8 0.416
Iran 11.45 632-17.85 123.73 < 0.001 91.9 9.1 0.085
Italy 3.98 0.00-15.72 536.20 < 0.001 99.3 8.9 0.118
Mexico 11.60 3.94-22.57 461.19 < 0.001 98.9 22.4 0.268
Portugal 9.90 3.97-18.10 140.88 < 0.001 96.5 12.3 0.390
Romania 8.78 4.06-15.07 50.48 < 0.001 94.1 5.2 0.083
South Korea 8.49 3.43-15.52 285.99 < 0.001 97.9 4.5 0.136
Spain 19.25 8.27-33.45 3309.42 < 0.001 99.6 -1.0 0.930
Taiwan 16.65 9.44-25.41 136.85 < 0.001 97.1 17.1 0.112
Thailand 17.04 9.91-25.63 33.83 < 0.001 94.1 18.1 0.704
Turkey 11.32 6.70-16.96 449.03 < 0.001 96.2 14.0 0.100
USA 15.06 10.86-19.81 9124.54 < 0.001 99.7 10.3 0.117

Year
< 2000 10.76 5.46-17.58 4131.32 < 0.001 99.6 99.62 7.9 0.816 -0.24 0.816
2001 – 2005 11.44 5.99-18.36 1557.16 < 0.001 99.2 9.3 0.103
2006 – 2010 12.65 8.80-17.09 7641.05 < 0.001 99.5 6.4 0.070
2011 – 2015 14.05 10.51-18.00 9485.51 < 0.001 99.3 6.7 0.340
≥2016 7.60 6.84-8.41 6917.82 < 0.001 99.2 5.2 0.183

Diagnostic method
Antigen detection 13.57 12.16-15.05 15630.83 < 0.001 99.7 98.12 8.4 0.379 -0.29 0.564
Blood Smear 6.51 4.10-9.42 11.36 0.009 73.6 -0.4 0.938
ELISA 8.56 7.37-9.82 6404.93 < 0.001 99.2 3.9 0.087
IFAT 2.14 0.30-5.60 27.10 < 0.001 88.9 2.4 0.281
Knott's test 11.99 8.97-15.39 1569.52 < 0.001 98.1 4.5 0.164
Necropsy 14.49 2.37-34.36 1149.83 < 0.001 99.5 16.2 0.253
PCR 11.44 7.75-15.74 1151.85 < 0.001 97.4 3.6 0.204

chemotherapy to dogs and vector control seems more plausible for the
apparent reduction of dirofilariasis at least in domestic reservoirs
(Alphey and Andreasen, 2002; Benelli et al., 2016; Bowman and Atkins,
2009; Pates and Curtis, 2005).
As reported by results of the meta-analysis, the prevalence of D.
immitis in dogs based on diagnostic method was as follows: necropsy
14.49 %, antigen detection 13.57 %, Knott’s test 11.99 %, PCR 11.44 %,
ELISA 8.56 %, blood smear 6.51 % and IFAT 2.14 %. There can be no
doubt that infection with adult nematode worm of D. immitis in dogs
can be detected in the pulmonary arteries and the heart of dogs by
necropsy method (Taylor et al., 2016). However, the necropsy is not
approved and accepted on the basis of the ethical principles in scientific
studies on animals (Fraser, 1999; Touitou et al., 2004, 2006). There-
fore, molecular methods, such as antigen detection are more acceptable
owing to high sensitivity and specificity of blood samples (Tahir et al.,
2017b; Torres-Chable et al., 2018; Anvari et al., 2019b). According to
meta-analysis, knott's test, and PCR are the next priorities. However,
microscopic methods, such as the knott's test, are still used to detect
microfilariae of D. immitis (Anvari et al., 2019a; Hou et al., 2011);
nonetheless, using molecular methods, such as PCR, will give more
accurate and reliable results (Siyadatpanah et al., 2019).
The limitations of the current systematic review included 1) variant
diagnostic laboratory tests without equal specificities and sensitivities
used in researches, 2) variable factors influencing dirofilariasis infec-
tion evaluated in few papers, 3) there is insufficient data about the si-
tuation or intensity of dirofilariasis infection, and 4) we only had access
to English-language papers.
The overall prevalence rate of D. immitis in dogs in the current study
may have been affected by the abovementioned items. For example,
variant diagnostic laboratory tests without equal specificities and sen-
sitivities exert a profound effect on the obtained outcomes.
Accordingly, it is recommended to use a reliable method, such as an-
tigen detection, with a high level of specificity and sensitivity to
achieve true and trustworthy results in various geographic regions.
Moreover, the correct interpretation of the results of the studies on
dirofilariasis in dogs would be the beneficial effects of this precise
method. Hence, the researchers are suggested to use antigen detection
tests with the appropriate sample size and evaluate the influential
factors on the epidemiology of dirofilariasis, including seasons of the
year, type of dog maintenance system, age of dogs and study on mos-
quito fauna in the survey area.
5. Conclusion
The results of the current review determined a relatively significant
prevalence of dirofilariasis in dog population worldwide. In addition, a

111
D. Anvari, et al.
Fig. 4. Bias assessment plot from Egger for the prevalence of Dirofilaria immitis in dog population across the world.
significant difference was detected between prevalence of D. immitis
and geographical region. Hence, it is recommended that a routine and
reliable screening test be conducted onD. immitis infection among dogs
in endemic regions. Moreover, veterinarians should pay more attention
to this zoonotic disease and take appropriate measures to prevent it,
such as the using of antiparasitic drugs with both preventive and
treatment purposes.
Acknowledgements
The authors would like to thank all members of the parasitology
department at the medical school of Mazandaran University of Medical
Sciences. Also, authors are grateful to Dr. Seyed Abdollah Hosseini for
his helpful comments. This study was approved by the deputy of re-
search and ethics committee, Mazandaran University of Medical
Sciences, Sari, Iran (Grant No: 5468; Code of Ethics:
IR.MAZUMS.REC.1398.5468).
Authors' contributions
DA, SG, AD, and SS conceived and designed the study, and SG cri-
tically revised the manuscript. DA, EN, HZH and MRN searched the
literature; DA and EN extracted the data. DA wrote the manuscript. DA
and MM performed the statistical analysis. All authors have read and
approved the final version of manuscript.
Declaration of Competing Interest Statement
The authors have no conflicts of interest to declare.
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